铜绿假单胞菌T6SS效应蛋白Tse3和人天然免疫蛋白STING结构和功能研究
|
摘要
细菌六型分泌系统(T6SS)利用自身注射器样的分泌装置,以直接接触的方式注射多种效应蛋白到与其比邻的同种或者异种的细胞中,导致异种受体细胞死亡或生长停滞。同时为了使自身细胞免受这些效应分子的毒害,T6SS+细菌同时表达与各种效应分子对应的同宗免疫蛋白(cognate immunity protein)而使其失活。这种效应蛋白和免疫蛋白对(E-I pair)使拥有T6SS的细菌在与其它细菌竞争中保持了优势。通过分泌组学和质谱的方法,在铜绿假单胞菌中鉴定出三种受H1-T6SS控制的效应蛋白Tse1、Tse2和Tse3。其中Tsel和Tse3分别降解敌对细菌中细胞壁成分的肽侧链和糖主链部分。本文利用X-射线晶体学技术研究了效应因子Tse3和Tse3-Tsi3复合物的三维结构,揭示了Tse3除含有一个C端的溶菌酶结构域以外,N端还含有一个annexin repeat-like结构域；来源于N端结构域的loop12和C端结构域的螺旋α9在钙离子存在下把Tse3和Tse3-Tsi3锚定到膜上；膜锚定对于Tse3的活性是必需的；Tse3可以利用Tsel的产物作为底物,首次发现了T6SS效应蛋白之间的协同效应；发现在Tse3催化中心和底物结合位点分别含有一个钙结合基序,它们对催化活性也是必需的。另外,Tse3-Tsi3复合物的结构揭示了Tsi3通过三个功能性loop结合到Tse3的活性中心而使其失去结合底物的能力,并发现Tsi3对Yse3的抑制也是钙依赖的,即Tsi3是一种新颖的G-型溶菌酶抑制剂。Tse3和Tsi3结构与功能的研究丰富了我们对T6SS效应蛋白的认识,并为控制病原菌感染提供了必要的结构基础。
在高等生物天然免疫系统中,STING蛋白是细胞内对双链DNA (dsDNA)免疫应答的重要接头分子。细胞内的DNA感受器能把dsDNA信号传递给STING蛋白,STING招募下游的激酶分子TBK1,使其磷酸化转录因子IRF3,磷酸化的IRF3二聚化而进入核内,使INF-β表达上调,继而激活病原菌入侵应答。最近发现的CDNs信号通路使我们对STING介导的dsDNA信号通路的认识更加深入。我们借助X-射线晶体学的方法解析了人源STING蛋白的C端结构域(CTD)及其与细菌第二信使c-di-GMP复合物的三维空间结构。我们的晶体学结构显示h-STINGCTD以二体发挥功能,c-di-GMP的结合并没有使h-STINGCTD构象变化,而人细胞内第二信使2'5'-cGAMP则可引起h-STINGCTD构象从open到close的变化,位于β2-β3的loop变为了反平行的β片层盖子结构把CDNs封闭在二体形成的口袋内；同时体内实验显示h-STING并不对c-di-GMP的刺激产生免疫应答,鉴于I型干扰素可能有利于细菌的侵染,推测细菌很有可能通过模拟真核细胞的第二信使来劫持宿主的天然免疫系统。人的STING蛋白则通过对c-di-GMP不响应,成功地逃避了细菌的劫持,这在进化上对人类是有利的。而小鼠的STING蛋白则对所有的CDNs应答,并且其构象始终保持close的状态,这提示了STING蛋白在天然免疫中的物种间的差异性。总之,STING结构的解析,为我们治疗病原侵染和自身免疫疾病提供了重要的结构基础。
Gram negative bacteria using a syringe-like tool of Type VI secretion system (T6SS) inject the effector proteins into the rival cells in a cell-contact manner leading to their death. Concurrently, bacteria employ cognate immunity proteins neutralizing these effector proteins to prevent self-intoxition. This effector-immunity pairs (E-I pairs) of T6SS endow the bacteria with great advantage in the fierce niche competiton. Three effector proteins (Tsel, Tse2and Tse3) controlled by H1-T6SS from Pseudomonas aeruginosa have been identified by Secretome and Mass spectrum analysis. Tsel and Tse3were demonstrated to be the amidase and muramidase degrading the peptide and glycan moiety of peptidoglycan (PG) respectively. In this thesis, X-ray crystallography method was performed to elucidate the mechanism used by Tse3and Tsi3in details. Tse3has an annexin repeat-like fold at the N-terminus and a G-type lysozyme fold at the C-terminus. Interestingly, one loop (loop12) at the N-terminal domain, together with one helix (a9) from the C-terminal domain, anchors Tse3or the Tse3-Tsi3complex to membrane in a calcium-dependent manner in vitro. Moreover, the membrane-binding ability is shown to be essential for Tse3's activity. In the C-terminal domain, a Y-shaped groove occurs on the surface probably serving as the PG-binding site. Two calcium-binding motifs are also observed in the groove and they are necessary for Tse3's activity. In the Tse3-Tsi3structure, three loops of Tsi3insert into the substrate-binding groove of Tse3. Three calcium ions found in the interface of the complex are demonstrated to be indispensable for the formation of Tse3-Tsi3complex. These findings further our perspective on the T6SS effector proteins and provide the structural basis for eliminating and combating the pathogenic infection.
STING protein plays an essential role in the double strands DNA sensing pathway in the cytosol for innate immunity. The DNA sensors relayed the signal to STING which recruited the kinase TBK1and transcript factor IRF3. Then, IRF3was phosphated by TBK1, which leaded to its dimerization. Dimerized IRF3was transferred to the nucleus and promote the transcription of type I INF which initialized the anti-pathogen process by innate immunity. Recently, the cyclic dinucleotides (CDNs) pathway was discovered making adaptor protein STING more fascinating. In this thesis, we solved the crystal structures of h-STINGCTD domain and its complex with c-di-GMP. The h-STINGCTD and c-di-GMP-h-STINGCTD complex behaves as a dimmer in the solution and crystal indicating it may function as a dimmer. The c-di-GMP was found in the dimmer interface of two STING protomer with a moderate binding affinity. Comparing to the apo form structure, c-di-GMP binding did not induce significant conformation change occurring in h-STINGCTD. However, the metazoan second messenger2'5'-cGAMP binded to h-STINGCTD resulting in drastic structural changes:The open state h-STINGCTD became close state; Loops between β2and β3became anti-parallel β sheet capping the CDNs in the pocket formed by two STING protomers. At the same time, the c-di-GMP did not induce significant immune response mediated by h-STING in vivo. Considering the complicated results of type I INF for the infection of bacteria, they may hijack the CDNs pathway for their purpose by mimcing the metazoan second messenger and human STING protein may evade this bacterial strategy in the evolution process. As for the mouse STING protein, it always adopts the close form and strongly responses to stimulates of CDNs, which indicates the functional differences of STING protein among species. All in all, our structural information of h-STINGCTD provides the molecular basis for the therapy of infection and autoimmune diseases such as systemic lupus erythematosus, SLE.
在高等生物天然免疫系统中,STING蛋白是细胞内对双链DNA (dsDNA)免疫应答的重要接头分子。细胞内的DNA感受器能把dsDNA信号传递给STING蛋白,STING招募下游的激酶分子TBK1,使其磷酸化转录因子IRF3,磷酸化的IRF3二聚化而进入核内,使INF-β表达上调,继而激活病原菌入侵应答。最近发现的CDNs信号通路使我们对STING介导的dsDNA信号通路的认识更加深入。我们借助X-射线晶体学的方法解析了人源STING蛋白的C端结构域(CTD)及其与细菌第二信使c-di-GMP复合物的三维空间结构。我们的晶体学结构显示h-STINGCTD以二体发挥功能,c-di-GMP的结合并没有使h-STINGCTD构象变化,而人细胞内第二信使2'5'-cGAMP则可引起h-STINGCTD构象从open到close的变化,位于β2-β3的loop变为了反平行的β片层盖子结构把CDNs封闭在二体形成的口袋内；同时体内实验显示h-STING并不对c-di-GMP的刺激产生免疫应答,鉴于I型干扰素可能有利于细菌的侵染,推测细菌很有可能通过模拟真核细胞的第二信使来劫持宿主的天然免疫系统。人的STING蛋白则通过对c-di-GMP不响应,成功地逃避了细菌的劫持,这在进化上对人类是有利的。而小鼠的STING蛋白则对所有的CDNs应答,并且其构象始终保持close的状态,这提示了STING蛋白在天然免疫中的物种间的差异性。总之,STING结构的解析,为我们治疗病原侵染和自身免疫疾病提供了重要的结构基础。
Gram negative bacteria using a syringe-like tool of Type VI secretion system (T6SS) inject the effector proteins into the rival cells in a cell-contact manner leading to their death. Concurrently, bacteria employ cognate immunity proteins neutralizing these effector proteins to prevent self-intoxition. This effector-immunity pairs (E-I pairs) of T6SS endow the bacteria with great advantage in the fierce niche competiton. Three effector proteins (Tsel, Tse2and Tse3) controlled by H1-T6SS from Pseudomonas aeruginosa have been identified by Secretome and Mass spectrum analysis. Tsel and Tse3were demonstrated to be the amidase and muramidase degrading the peptide and glycan moiety of peptidoglycan (PG) respectively. In this thesis, X-ray crystallography method was performed to elucidate the mechanism used by Tse3and Tsi3in details. Tse3has an annexin repeat-like fold at the N-terminus and a G-type lysozyme fold at the C-terminus. Interestingly, one loop (loop12) at the N-terminal domain, together with one helix (a9) from the C-terminal domain, anchors Tse3or the Tse3-Tsi3complex to membrane in a calcium-dependent manner in vitro. Moreover, the membrane-binding ability is shown to be essential for Tse3's activity. In the C-terminal domain, a Y-shaped groove occurs on the surface probably serving as the PG-binding site. Two calcium-binding motifs are also observed in the groove and they are necessary for Tse3's activity. In the Tse3-Tsi3structure, three loops of Tsi3insert into the substrate-binding groove of Tse3. Three calcium ions found in the interface of the complex are demonstrated to be indispensable for the formation of Tse3-Tsi3complex. These findings further our perspective on the T6SS effector proteins and provide the structural basis for eliminating and combating the pathogenic infection.
STING protein plays an essential role in the double strands DNA sensing pathway in the cytosol for innate immunity. The DNA sensors relayed the signal to STING which recruited the kinase TBK1and transcript factor IRF3. Then, IRF3was phosphated by TBK1, which leaded to its dimerization. Dimerized IRF3was transferred to the nucleus and promote the transcription of type I INF which initialized the anti-pathogen process by innate immunity. Recently, the cyclic dinucleotides (CDNs) pathway was discovered making adaptor protein STING more fascinating. In this thesis, we solved the crystal structures of h-STINGCTD domain and its complex with c-di-GMP. The h-STINGCTD and c-di-GMP-h-STINGCTD complex behaves as a dimmer in the solution and crystal indicating it may function as a dimmer. The c-di-GMP was found in the dimmer interface of two STING protomer with a moderate binding affinity. Comparing to the apo form structure, c-di-GMP binding did not induce significant conformation change occurring in h-STINGCTD. However, the metazoan second messenger2'5'-cGAMP binded to h-STINGCTD resulting in drastic structural changes:The open state h-STINGCTD became close state; Loops between β2and β3became anti-parallel β sheet capping the CDNs in the pocket formed by two STING protomers. At the same time, the c-di-GMP did not induce significant immune response mediated by h-STING in vivo. Considering the complicated results of type I INF for the infection of bacteria, they may hijack the CDNs pathway for their purpose by mimcing the metazoan second messenger and human STING protein may evade this bacterial strategy in the evolution process. As for the mouse STING protein, it always adopts the close form and strongly responses to stimulates of CDNs, which indicates the functional differences of STING protein among species. All in all, our structural information of h-STINGCTD provides the molecular basis for the therapy of infection and autoimmune diseases such as systemic lupus erythematosus, SLE.
引文
Abdallah, A.M, T. Verboom, E.M. Weerdenburg, N.C. Gey van Pittius, P.W. Mahasha, C. Jimenez, M. Parra, N. Cadieux, M.J. Brennan, B J. Appelmelk & W. Bitter, (2009) PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol Microbiol 73:329-340.
Abergel, C., V. Monchois, D. Byrne, S. Chenivesse, F. Lembo, J.C. Lazzaroni & J.M. Claverie, (2007) Structure and evolution of the Ivy protein family, unexpected lysozyme inhibitors in Gram-negative bacteria. Proc Natl Acad Sci USA 104:6394-6399.
Ablasser, A., F. Bauernfeind, G Hartmann, E. Latz, K.A. Fitzgerald & V. Hornung, (2009) RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase Ⅲ-transcribed RNA intermediate. Nat Immunol 10:1065-1072.
Ablasser, A., M. Goldeck, T. Cavlar, T. Deimling, G. Witte, I. Rohl, K.P. Hopfner, J. Ludwig & V. Hornung, (2013a) cGAS produces a 2'-5'-linked cyclic dinucleotide second messenger that activates STING. Nature 498:380-384.
Ablasser, A., J.L. Schmid-Burgk, I. Hemmerling, G.L. Horvath, T. Schmidt, E. Latz & V. Hornung, (2013b) Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503:530-534.
Alvarez-Martinez, C.E. & P.J. Christie, (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73:775-808.
Archer, K.A., J. Durack & D.A. Portnoy, (2014) STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog 10:e1003861.
Aschtgen, M.S., M.S. Thomas & E. Cascales, (2010) Anchoring the type VI secretion system to the peptidoglycan:TssL, TagL, TagP... what else? Virulence 1:535-540.
Aubert, D., D.K. MacDonald & M.A. Valvano, (2010) BcsKC is an essential protein for the type VI secretion system activity in Burkholderia cenocepacia that forms an outer membrane complex with BcsLB. J Biol Chem 285:35988-35998.
Aubert, D.F., R.S. Flannagan & M.A. Valvano, (2008) A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76:1979-1991.
Auerbuch, V., D.G. Brockstedt, N. Meyer-Morse, M. O'Riordan & D.A. Portnoy, (2004) Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J Exp Med 200: 527-533.
Bartonickova, L., T. Sterzenbach, S. Nell, F. Kops, J. Schulze, A. Venzke, B. Brenneke, S. Bader, A.D. Gruber, S. Suerbaum & C. Josenhans, (2013) Hcp and VgrGl are secreted components of the Helicobacter hepaticus type VI secretion system and VgrGl increases the bacterial colitogenic potential. Cell Microbiol 15:992-1011.
Basler, M., B.T. Ho & J.J. Mekalanos, (2013) Tit-for-tat:type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152:884-894.
Basler, M. & J.J. Mekalanos, (2012) Type 6 secretion dynamics within and between bacterial cells. Science 337:815.
Battye, T.G, L. Kontogiannis, O. Johnson, H.R. Powell & A.G. Leslie, (2011) iMOSFLM:a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67:271-281.
Beck, T., A. Krasauskas, T. Gruene & GM. Sheldrick, (2008) A magic triangle for experimental phasing of macromolecules. Acta Crystallogr D Biol Crystallogr 64:1179-1182.
Benz, J., J. Reinstein & A. Meinhart, (2013) Structural Insights into the Effector-Immunity System Tae4/Tai4 from. PLoS One 8:e67362.
Benz, J., C. Sendlmeier, T.R. Barends & A. Meinhart, (2012) Structural insights into the effector-immunity system Tsel/Tsil from Pseudomonas aeruginosa. PLoS One 7:e40453.
Binet, R., S. Letoffe, J.M. Ghigo, P. Delepelaire & C. Wandersman, (1997) Protein secretion by Gram-negative bacterial ABC exporters-a review. Gene 192:7-11.
Bladergroen, M.R., K. Badelt & H.P. Spaink, (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 16:53-64.
Blander, J.M. & L.E. Sander, (2012) Beyond pattern recognition:five immune checkpoints for scaling the microbial threat. Nat Rev Immunol 12:215-225.
Bleves, S., V. Viarre, R. Salacha, G.P. Michel, A. Filloux & R. Voulhoux, (2010) Protein secretion systems in Pseudomonas aeruginosa:A wealth of pathogenic weapons. Int J Med Microbiol 300:534-543.
Blondel, C.J., J.C. Jimenez, I. Contreras & C.A. Santiviago, (2009) Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10:354.
Bonemann, G., A. Pietrosiuk, A. Diemand, H. Zentgraf & A. Mogk, (2009) Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 28: 315-325.
Boyer, F., G Fichant, J. Berthod, Y. Vandenbrouck & I. Attree, (2009) Dissecting the bacterial type VI secretion system by a genome wide in silico analysis:what can be learned from available microbial genomic resources? BMC Genomics 10:104.
Bricogne, G., C. Vonrhein, C. Flensburg, M. Schiltz & W. Paciorek, (2003) Generation, representation and flow of phase information in structure determination:recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 59:2023-2030.
Brooks, T.M., D. Unterweger, V. Bachmann, B. Kostiuk & S. Pukatzki, (2013) Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J Biol Chem 288:7618-7625.
Browder, H.P., W.A. Zygmunt, J.R. Young & P.A. Tavormina, (1965) Lysostaphin:Enzymatic Mode of Action. Biochem Biophys Res Commun 19:383-389.
Brunet, Y.R., C.S. Bernard, M. Gavioli, R. Lloubes & E. Cascales, (2011) An epigenetic switch involving overlapping fur and DNA methylation optimizes expression of a type VI secretion gene cluster. PLoS Genet 7:e1002205.
Burckstummer, T., C. Baumann, S. Bluml, E. Dixit, G. Durnberger, H. Jahn, M. Planyavsky, M. Bilban, J. Colinge, K.L. Bennett & G. Superti-Furga, (2009) An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10: 266-272.
Burdette, D.L., K.M. Monroe, K. Sotelo-Troha, J.S. Iwig, B. Eckert, M. Hyodo, Y. Hayakawa & R.E. Vance, (2011) STING is a direct innate immune sensor of cyclic di-GMP. Nature 478: 515-518.
Burdette, D.L. & R.E. Vance, (2013) STING and the innate immune response to nucleic acids in the cytosol. Nat Immunol 14:19-26.
Burtnick, M.N., D. DeShazer, V. Nair, F.C. Gherardini & P.J. Brett, (2010) Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages. Infect Immun 78:88-99.
Callewaert, L., A. Aertsen, D. Deckers, K.G. Vanoirbeek, L. Vanderkelen, J.M. Van Herreweghe, B. Masschalck, D. Nakimbugwe, J. Robben & C.W. Michiels, (2008) A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog 4: e1000019.
Callewaert, L. & C.W. Michiels, (2010) Lysozymes in the animal kingdom. JBiosci 35:127-160.
Campos, B., YD. Mo, T.R. Mealy, C.W. Li, M.A. Swairjo, C. Balch, J.F. Head, G Retzinger, J.R. Dedman & B.A. Seaton, (1998) Mutational and crystallographic analyses of interfacial residues in annexin V suggest direct interactions with phospholipid membrane components. Biochemistry 37:8004-8010.
Carrero, J.A., B. Calderon & E.R. Unanue, (2004) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. JExpMed 200:535-540.
Carrero, J.A.& E.R Unanue, (2006) Lymphocyte apoptosis as an immune subversion strategy of microbial pathogens. Trends Immunol 27:497-503.
Carruthers, M.D., P.A. Nicholson, E.N. Tracy & R.S. Munson, Jr., (2013) Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition. PLoS One 8:e59388.
Casabona, M.G., J.M. Silverman, K.M. Sall, F. Boyer, Y. Coute, J. Poirel, D. Grunwald, J.D. Mougous, S. Elsen & I. Attree, (2013) An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa. Environ Microbiol 15:471-486.
Cascales, E. & C. Cambillau, (2012) Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 367:1102-1111.
Chakraborty, S., J. Sivaraman, K.Y. Leung & Y.K. Mok, (2011) Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III and VI secretion systems of Edwardsiella tarda. J Biol Chem 286:39417-39430.
Chen, H., H. Sun, F. You, W. Sun, X. Zhou, L. Chen, J. Yang, Y. Wang, H. Tang, Y. Guan, W. Xia, J. Gu, H. Ishikawa, D. Gutman, G Barber, Z. Qin & Z. Jiang, (2011) Activation of STAT6 by STING is critical for antiviral innate immunity. Cell 147:436-446.
Chou, S., N.K. Bui, A.B. Russell, K.W. Lexa, T.E. Gardiner, M. LeRoux, W. Vollmer & J.D. Mougous, (2012) Structure of a peptidoglycan amidase effector targeted to Gram-negative bacteria by the type VI secretion system. Cell Rep 1:656-664.
Chow, J. & S.K. Mazmanian, (2010) A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 7:265-276.
Concha, N.O., J.F. Head, M.A. Kaetzel, J.R. Dedman & B.A. Seaton, (1993) Rat annexin V crystal structure:Ca(2+)-induced conformational changes. Science 261:1321-1324.
Cornelis, GR., (2006) The type III secretion injectisome. Nat Rev Microbiol 4:811-825.
Cornelis, G.R., (2010) The type III secretion injectisome, a complex nanomachine for intracellular 'toxin1 delivery. Biol Chem 391:745-751.
Corr, S.C., Y. Li, C.U. Riedel, P.W. OToole, C. Hill & C.G Gahan, (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci USA 104:7617-7621.
Cridland, J.A., E.Z. Curley, M.N. Wykes, K. Schroder, M.J. Sweet, T.L. Roberts, M.A. Ragan, K.S. Kassahn & K.J. Stacey, (2012) The mammalian PYHIN gene family:phylogeny, evolution and expression. BMC Evol Biol 12:140.
Cronan, J.E., (2003) Bacterial membrane lipids:where do we stand? Annu Rev Microbiol 57:203-224.
Das, S.& K. Chaudhuri, (2003) Identification of a unique IAHP (IcmF associated homologous proteins) cluster in Vibrio cholerae and other proteobacteria through in silico analysis. In Silico Biol 3: 287-300.
Dawid, S., A.M. Roche & J.N. Weiser, (2007) The blp bacteriocins of Streptococcus pneumoniae mediate intraspecies competition both in vitro and in vivo. Infect Immun 75:443-451.
DeFilippis, V.R., D. Alvarado, T. Sali, S. Rothenburg & K. Fruh, (2010) Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J Virol 84:585-598.
Delepelaire, P., (2004) Type I secretion in gram-negative bacteria. Biochim Biophys Acta 1694: 149-161.
Ding, J., W. Wang, H. Feng, Y. Zhang & D.C. Wang, (2012) Structural insights into the Pseudomonas aeruginosa type VI virulence effector Tsel bacteriolysis and self-protection mechanisms. J Biol Chem 287:26911-26920.
Dong, C., H. Zhang, Z.Q. Gao, W.J. Wang, Z. She, GF. Liu, Y.Q. Shen, X.D. Su & Y.H. Dong, (2013a) Structural insights into the inhibition of type VI effector Tae3 by its immunity protein Tai3. Biochem.J 454:59-68.
Dong, T.G., B.T. Ho, D.R. Yoder-Himes & J.J. Mekalanos, (2013b) Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc Natl Acad Sci U S A 110: 2623-2628.
Dudley, E.G., N.R. Thomson, J. Parkhill, N.P. Morin & J.P. Nataro, (2006) Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol 61:1267-1282.
Duong, F., A. Lazdunski & M. Murgier, (1996) Protein secretion by heterologous bacterial ABC-transporters:the C-terminus secretion signal of the secreted protein confers high recognition specificity. Mol Microbiol 21:459-470.
Economou, A., P.J. Christie, R.C. Fernandez, T. Palmer, G.V. Plano & A.P. Pugsley, (2006) Secretion by numbers:Protein traffic in prokaryotes. Mol Microbiol 62:308-319.
El Ghachi, M., A. Bouhss, H. Barreteau, T. Touze, G. Auger, D. Blanot & D. Mengin-Lecreulx, (2006) Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J Biol Chem 281:22761-22772.
Evans, P., (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
Fernandes-Alnemri, T, J.W. Yu, P. Datta, J. Wu & E.S. Alnemri, (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458:509-513.
Filloux, A., (2004) The underlying mechanisms of type Ⅱ protein secretion. Biochim Biophys Acta 1694:163-179.
Folkesson, A., S. Lofdahl & S. Normark, (2002) The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol 153:537-545.
Fritsch, M.J., K. Trunk, J.A. Diniz, M. Guo, M. Trost & S.J. Coulthurst, (2013) Proteomic identification of novel secreted antibacterial toxins of the Serratia marcescens type VI secretion system. Mol Cell Proteomics 12:2735-2749.
Gan, L., S. Chen & G.J. Jensen, (2008) Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci USA 105:18953-18957.
Gao, D., J. Wu, Y.T. Wu, F. Du, C. Aroh, N. Yan, L. Sun & Z.J. Chen, (2013a) Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341:903-906.
Gao, P., M. Ascano, Y. Wu, W. Barchet, B.L. Gaffney, T. Zillinger, A.A. Serganov, Y. Liu, R.A. Jones, G. Hartmann, T. Tuschl & D.J. Patel, (2013b) Cyclic [G(2',5')pA(3',5')p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell153:1094-1107.
Gao, P., M. Ascano, T. Zillinger, W. Wang, P. Dai, A.A. Serganov, B.L. Gaffney, S. Shuman, R.A. Jones, L. Deng, G. Hartmann, W. Barchet, T. Tuschl & D.J. Patel, (2013c) Structure-function analysis of STING activation by c[G(2',5')pA(3',5')p] and targeting by antiviral DMXAA. Cell 154: 748-762.
Gerke, V, (1991) Identification of a homologue for annexin VII (synexin) in Dictyostelium discoideum. J Biol Chem 266:1697-1700.
Glauner, B., (1988) Separation and quantification of muropeptides with high-performance liquid chromatography. Anal Biochem 172:451-464.
Goto, T., Y. Abe, Y. Kakuta, K. Takeshita, T. Imoto & T. Ueda, (2007) Crystal structure of Tapes japonica Lysozyme with substrate analogue:structural basis of the catalytic mechanism and manifestation of its chitinase activity accompanied by quaternary structural change. J Biol Chem 282:27459-27467.
Gueguen, E. & E. Cascales, (2013) Promoter swapping unveils the role of the Citrobacter rodentium CTS1 type VI secretion system in interbacterial competition. Appl Environ Microbiol 79: 32-38.
Gurtler, C. & A.G. Bowie, (2013) Innate immune detection of microbial nucleic acids. Trends Microbiol 21:413-420.
Haapalainen, M., H. Mosorin, F. Dorati, R.F. Wu, E. Roine, S. Taira, R. Nissinen, L. Mattinen, R. Jackson, M. Pirhonen & N.C. Lin, (2012) Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J Bacteriol 194:4810-4822.
Hamada, S., M. Umemura, T. Shiono, K. Tanaka, A. Yahagi, M.D. Begum, K. Oshiro, Y. Okamoto, H. Watanabe, K. Kawakami, C. Roark, W.K. Born, R. O'Brien, K. Ikuta, H. Ishikawa, S. Nakae, Y. Iwakura, T. Ohta & G. Matsuzaki, (2008) IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J Immunol 181:3456-3463.
Henry, T., GS. Kirimanjeswara, T. Ruby, J.W. Jones, K. Peng, M. Perret, L. Ho, J.D. Sauer, Y. Iwakura, D.W. Metzger & D.M. Monack, (2010) Type IIFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J Immunol 184:3755-3767.
Hirakawa, H., A. Ochi, Y. Kawahara, S. Kawamura, T. Torikata & S. Kuhara, (2008) Catalytic reaction mechanism of goose egg-white lysozyme by molecular modelling of enzyme-substrate complex. J Biochem 144:753-761.
Ho, B.T., M. Basler & J.J. Mekalanos, (2013) Type 6 secretion system-mediated immunity to type 4 secretion system-mediated gene transfer. Science 342:250-253.
Ho, B.T., T.G Dong & J.J. Mekalanos, (2014) A view to a kill:the bacterial type VI secretion system. Cell Host Microbe 15:9-21.
Hofmann, A., J. Proust, A. Dorowski, R. Schantz & R. Huber, (2000) Annexin 24 from Capsicum annuum. X-ray structure and biochemical characterization. J Biol Chem 275:8072-8082.
Holland, I.B., L. Schmitt & J. Young, (2005) Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). Mol Membr Biol 22:29-39.
Holm, L. & C. Sander, (1994) Structural similarity of plant chitinase and lysozymes from animals and' phage. An evolutionary connection. FEBSLett 340:129-132.
Hood, R.D., P. Singh, F. Hsu, T. Guvener, M.A. Carl, R.R. Trinidad, J.M. Silverman, B.B. Ohlson, K.G Hicks, R.L. Plemel, M. Li, S. Schwarz, W.Y. Wang, A.J. Merz, D.R. Goodlett & J.D. Mougous, (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37.
Horan, K.A., K. Hansen, M.R. Jakobsen, C.K. Holm, S. Soby, L. Unterholzner, M. Thompson, J.A. West, M.B. Iversen, S.B. Rasmussen, S. Ellermann-Eriksen, E. Kurt-Jones, S. Landolfo, B. Damania, J. Melchjorsen, A.G. Bowie, K.A. Fitzgerald & S.R. Paludan, (2013) Proteasomal degradation of herpes simplex virus capsids in macrophages releases DNA to the cytosol for recognition by DNA sensors. J Immunol 190:2311-2319.
Hornung, V, A. Ablasser, M. Charrel-Dennis, F. Bauernfeind, G Horvath, D.R. Caffrey, E. Latz & K.A. Fitzgerald, (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-518.
Hsu, F., S. Schwarz & J.D. Mougous, (2009) TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol Microbiol 72:1111-1125.
Hu, N.J., A.M. Yusof, A. Winter, A. Osman, A.K. Reeve & A. Hofmann, (2008) The crystal structure of calcium-bound annexin Ghl from Gossypium hirsutum and its implications for membrane binding mechanisms of plant annexins. JBiol Chem 283:18314-18322.
Huang, Y.H., X.Y. Liu, X.X. Du, Z.F. Jiang & X.D. Su, (2012) The structural basis for the sensing and binding of cyclic di-GMP by STING. Nat Struct Mol Biol 19:728-730.
Huet, J., P. Rucktooa, B. Clantin, M. Azarkan, Y. Looze, V. Villeret & R. Wintjens, (2008) X-ray structure of papaya chitinase reveals the substrate binding mode of glycosyl hydrolase family 19 chitinases. Biochemistry 47:8283-8291.
Ishii, K.J., C. Coban, H. Kato, K. Takahashi, Y. Torii, F. Takeshita, H. Ludwig, G Sutter, K. Suzuki, H. Hemmi, S. Sato, M. Yamamoto, S. Uematsu, T. Kawai, O. Takeuchi & S. Akira, (2006) A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol 7:40-48.
Ishikawa, H., Z. Ma & G.N. Barber, (2009a) STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461:788-792.
Ishikawa, T., P.K. Rompikuntal, B. Lindmark, D.L. Milton & S.N. Wai, (2009b) Quorum sensing regulation of the two hcp alleles in Vibrio cholerae 01 strains. PLoS One 4:e6734.
Jin, L., K.K. Hill, H. Filak, J. Mogan, H. Knowles, B. Zhang, A.L. Perraud, J.C. Cambier & L.L. Lenz, (2011) MPYS is required for IFN response factor 3 activation and type IIFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J Immunol 187:2595-2601.
Johnston, P.A., M.S. Perin, GA. Reynolds, S.A. Wasserman & T.C. Sudhof, (1990) Two novel annexins from Drosophila melanogaster. Cloning, characterization, and differential expression in development. J Biol Chem 265:11382-11388.
Karaghiosoff, M., R. Steinborn, P. Kovarik, G Kriegshauser, M. Baccarini, B. Donabauer, U. Reichart, T. Kolbe, C. Bogdan, T. Leanderson, D. Levy, T. Decker & M. Muller, (2003) Central role for type I interferons and Tyk2 in lipopolysaccharide-induced endotoxin shock. Nat Immunol 4: 471-477.
Kato, H., K. Takahasi & T. Fujita, (2011) RIG-I-like receptors:cytoplasmic sensors for non-self RNA. Immunol Rev 243:91-98.
Keating, S.E., M. Baran & A.G Bowie, (2011) Cytosolic DNA sensors regulating type I interferon induction. Trends Immunol 32:574-581.
Kim, T., S. Pazhoor, M. Bao, Z. Zhang, S. Hanabuchi, V. Facchinetti, L. Bover, J. Plumas, L. Chaperot, J. Qin & Y.J. Liu, (2010) Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc Natl Acad Sci USA 107:15181-15186.
Kitaoka, M., S.T. Miyata, T.M. Brooks, D. Unterweger & S. Pukatzki, (2011) VasH is a transcriptional regulator of the type VI secretion system functional in endemic and pandemic Vibrio cholerae. JBacteriol 193:6471-6482.
Knapp, S., (2010) Update on the role of Toll-like receptors during bacterial infections and sepsis. Wien Med Wochenschr 160:107-111.
Kohler, R., K. Schafer, S. Muller, G. Vignon, K. Diederichs, A. Philippsen, P. Ringler, A.P. Pugsley, A. Engel & W. Welte, (2004) Structure and assembly of the pseudopilin PulG. Mol Microbiol 54: 647-664.
Kong, K.F., L. Schneper & K. Mathee, (2010) Beta-lactam antibiotics:from antibiosis to resistance and bacteriology. APMIS 118:1-36.
Konno, H., K. Konno & G.N. Barber, (2013) Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signaling. Cell 155:688-698.
Korotkov, K.V. & W.G. Hol, (2008) Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat Struct Mol Biol 15:462-468.
Koskiniemi, S., J.G Lamoureux, K.C. Nikolakakis, C. t'Kint de Roodenbeke, M.D. Kaplan, D.A. Low & C.S. Hayes, (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA 110:7032-7037.
Krissinel, E.& K. Henrick, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774-797.
Leiman, P.G., M. Basler, U.A. Ramagopal, J.B. Bonanno, J.M. Sauder, S. Pukatzki, S.K. Burley, S.C. Almo & J.J. Mekalanos, (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci U S A 106:4154-4159.
Lemaitre, B., E. Nicolas, L. Michaut, J.M. Reichhart & J.A. Hoffmann, (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973-983.
LeRoux, M., J.A. De Leon, N.J. Kuwada, A.B. Russell, D. Pinto-Santini, R.D. Hood, D.M. Agnello, S.M. Robertson, P.A. Wiggins & J.D. Mougous, (2012) Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword. Proc Natl Acad Sci USA 109:19804-19809.
Lertpiriyapong, K., E.R. Gamazon, Y. Feng, D.S. Park, J. Pang, G. Botka, M.E. Graffam, Z. Ge & J.G. Fox, (2012) Campylobacter jejuni type VI secretion system:roles in adaptation to deoxycholic acid, host cell adherence, invasion, and in vivo colonization. PLoS One 7:e42842.
Lesic, B., M. Starkey, J. He, R. Hazan & L.G. Rahme, (2009) Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155:2845-2855.
Leysen, S., J.M. Van Herreweghe, L. Callewaert, M. Heirbaut, P. Buntinx, C.W. Michiels & S.V. Strelkov, (2011) Molecular basis of bacterial defense against host lysozymes:X-ray structures of periplasmic lysozyme inhibitors Plil and PliC. JMol Biol 405:1233-1245.
Leysen, S., L. Vanderkelen, K. Van Asten, S. Vanheuverzwijn, V. Theuwis, C.W. Michiels & S.V. Strelkov, (2012) Structural characterization of the PliG lysozyme inhibitor family. J Struct Biol 180:235-242.
Leysen, S., L. Vanderkelen, S.D. Weeks, C.W. Michiels & S.V. Strelkov, (2013) Structural basis of bacterial defense against g-type lysozyme-based innate immunity. Cell Mol Life Sci 70: 1113-1122.
Li, M., I. Le Trong, M.A. Carl, E.T. Larson, S. Chou, J.A. De Leon, S.L. Dove, R.E. Stenkamp & J.D. Mougous, (2012) Structural basis for type VI secretion effector recognition by a cognate immunity protein. PLoS Pathog 8:e1002613.
Lossi, N.S., E. Manoli, A. Forster, R. Dajani, T. Pape, P. Freemont & A. Filloux, (2013) The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. JBiol Chem 288:7536-7548.
Ma, A.T., S. McAuley, S. Pukatzki & J.J. Mekalanos, (2009a) Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5: 234-243.
Ma, L.S., J.S. Lin & E.M. Lai, (2009b) An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and its walker a motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens. JBacteriol 191:4316-4329.
MacIntyre, D.L., ST. Miyata, M. Kitaoka & S. Pukatzki, (2010) The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci U S A 107:19520-19524.
Manzanillo, P.S., M.U. Shiloh, D.A. Portaoy & J.S. Cox, (2012) Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11:469-480.
McCoy, A.J., R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni & R.J. Read, (2007) Phaser crystallographic software. JAppl Crystallogr 40:658-674.
McWhirter, S.M., R. Barbalat, K.M. Monroe, M.F. Fontana, M. Hyodo, N.T. Joncker, K.J. Ishii, S. Akira, M. Colonna, Z.J. Chen, K.A. Fitzgerald, Y. Hayakawa & R.E. Vance, (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206:1899-1911.
Medzhitov, R., P. Preston-Hurlburt & C.A. Janeway, Jr., (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394-397.
Meeks, K.D., A.N. Sieve, J.K. Kolls, N. Ghilardi & R.E. Berg, (2009) IL-23 is required for protection against systemic infection with Listeria monocytogenes. J Immunol 183:8026-8034.
Miyata, S.T., D. Unterweger, S.P. Rudko & S. Pukatzki, (2013) Dual expression profile of type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathog 9: e1003752.
Monchois, V, C. Abergel, J. Sturgis, S. Jeudy & J.M. Claverie, (2001) Escherichia coli ykfE ORFan gene encodes a potent inhibitor of C-type lysozyme. J Biol Chem 276:18437-18441.
Mondini, M., S. Costa, S. Sponza, F. Gugliesi, M. Gariglio & S. Landolfo, (2010) The interferon-inducible HIN-200 gene family in apoptosis and inflammation:implication for autoimmunity. Autoimmunity 43:226-231.
Monzingo, A.F., E.M. Marcotte, P.J. Hart & J.D. Robertus, (1996) Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core. Nat Struct Biol 3:133-140.
Moscoso, J.A., H. Mikkelsen, S. Heeb, P. Williams & A. Filloux, (2011) The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol 13:3128-3138.
Mougous, J.D., M.E. Cuff, S. Raunser, A. Shen, M. Zhou, C.A. Gifford, A.L. Goodman, G Joachimiak, C.L. Ordonez, S. Lory, T. Walz, A. Joachimiak & J.J. Mekalanos, (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-1530.
Mougous, J.D., C.A. Gifford, T.L. Ramsdell & J.J. Mekalanos, (2007) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 9: 797-803.
Murdoch, S.L., K. Trunk, G English, M.J. Fritsch, E. Pourkarimi & S.J. Coulthurst, (2011) The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. JBacteriol 193:6057-6069.
Nagarajan, U.M., D. Prantner, J.D. Sikes, C.W. Andrews, Jr., A.M. Goodwin, S. Nagarajan & T. Darville, (2008) Type I interferon signaling exacerbates Chlamydia muridarum genital infection in a murine model. Infect Immun 76:4642-4648.
Nakayama, H., K. Kurokawa & B.L. Lee, (2012) Lipoproteins in bacteria:structures and biosynthetic pathways. FEBS J 219:4247-4268.
Nano, F.E., N. Zhang, S.C. Cowley, K.E. Klose, K.K. Cheung, M.J. Roberts, J.S. Ludu, G.W. Letendre, A. I. Meierovics, G Stephens & K.L. Elkins, (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186:6430-6436.
O'Connell, R.M., S.K. Saha, S.A. Vaidya, K.W. Bruhn, GA. Miranda, B. Zarnegar, A.K. Perry, B.O. Nguyen, T.F. Lane, T. Taniguchi, J.F. Miller & G Cheng, (2004) Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200:437-445.
Ordway, D., M. Henao-Tamayo, M. Harton, G. Palanisamy, J. Troudt, C. Shanley, R.J. Basaraba & I.M. Orme, (2007) The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 179:522-531.
Otwinowski, Z.& W. Minor, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol.276:307-326.
Ouyang, S., X. Song, Y. Wang, H. Ru, N. Shaw, Y. Jiang, F. Niu, Y. Zhu, W. Qiu, K. Parvatiyar, Y. Li, R. Zhang, G Cheng & Z.J. Liu, (2012) Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36:1073-1086.
Pallen, M., R. Chaudhuri & A. Khan, (2002) Bacterial FHA domains:neglected players in the phospho-threonine signalling game? Trends Microbiol 10:556-563.
Parvatiyar, K., Z. Zhang, R.M. Teles, S. Ouyang, Y. Jiang, S.S. Iyer, S.A. Zaver, M. Schenk, S. Zeng, W. Zhong, Z.J. Liu, R.L. Modlin, Y.J. Liu & G. Cheng, (2012) The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 13:1155-1161.
Peabody, C.R., Y.J. Chung, M.R. Yen, D. Vidal-Ingigliardi, A.P. Pugsley & M.H. Saier, Jr., (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051-3072.
Pell, L.G., V. Kanelis, L. W. Donaldson, P.L. Howell & A.R. Davidson, (2009) The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci USA 106:4160-4165.
Pieper, R., S.T. Huang, J.M. Robinson, D.J. Clark, H. Alami, P.P. Parmar, R.D. Perry, R.D. Fleischmann & S.N. Peterson, (2009) Temperature and growth phase influence the outer-membrane proteome and the expression of a type VI secretion system in Yersinia pestis. Microbiology 155:498-512.
Pigault, C., A. Follenius-Wund & M. Chabbert, (1999) Role of Trp-187 in the annexin V-membrane interaction:a molecular mechanics analysis. Biochem Biophys Res Commun 254:484-489.
Pincus, M.R., S.S. Zimmerman & H.A. Scheraga, (1976) Prediction of three-dimensional structures of enzyme-substrate and enzyme-inhibitor complexes of lysozyme. Proc Natl Acad Sci USA 73: 4261-4265.
Pincus, M.R., S.S. Zimmerman & H.A. Scheraga, (1977) Structures of enzyme-substrate complexes of lysozyme. Proc Natl Acad Sci USA 74:2629-2633.
Poole, S.J., E.J. Diner, S.K. Aoki, B.A. Braaten, C. t'Kint de Roodenbeke, D.A. Low & C.S. Hayes, (2011) Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 7:e1002217.
Pukatzki, S., A.T. Ma, A.T. Revel, D. Sturtevant & J.J. Mekalanos, (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 104:15508-15513.
Pukatzki, S., A.T. Ma, D. Sturtevant, B. Krastins, D. Sarracino, W.C. Nelson, J.F. Heidelberg & J.J. Mekalanos, (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103: 1528-1533.
Pukatzki, S., S.B. McAuley & S.T. Miyata, (2009) The type VI secretion system:translocation of effectors and effector-domains. Curr Opin Microbiol 12:11-17.
Rao, P.S., Y. Yamada, Y.P. Tan & K.Y. Leung, (2004) Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol Microbiol 53: 573-586.
Rasmussen, S.B., K.A. Horan, C.K. Holm, A.J. Stranks, T.C. Mettenleiter, A.K. Simon, S.B. Jensen, F.J. Rixon, B. He & S.R. Paludan, (2011) Activation of autophagy by alpha-herpesviruses in myeloid cells is mediated by cytoplasmic viral DNA through a mechanism dependent on stimulator of IFN genes. J Immunol 187:5268-5276.
Roberts, T.L., A. Idris, J.A. Dunn, GM. Kelly, C.M. Burnton, S. Hodgson, L.L. Hardy, V. Garceau, M.J. Sweet, I.L. Ross, D.A. Hume & K.J. Stacey, (2009) HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323:1057-1060.
Russell, A.B., R.D. Hood, N.K. Bui, M. LeRoux, W. Vollmer & J.D. Mougous, (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343-347.
Russell, A.B., M. LeRoux, K. Hathazi, D.M. Agnello, T. Ishikawa, P.A. Wiggins, S.N. Wai & J.D. Mougous, (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496:508-512.
Russell, A.B., S.B. Peterson & J.D. Mougous, (2014) Type VI secretion system effectors:poisons with a purpose. Nat Rev Microbiol 12:137-148.
Russell, A.B., P. Singh, M. Brittnacher, N.K. Bui, R.D. Hood, M.A. Carl, D.M. Agnello, S. Schwarz, D.R. Goodlett, W. Vollmer & J.D. Mougous, (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11:538-549.
Rye, C.S.& S.G. Withers, (2000) Glycosidase mechanisms. Curr Opin Chem Biol 4:573-580.
Saito, J., A. Kita, Y. Higuchi, Y. Nagata, A. Ando & K. Miki, (1999) Crystal structure of chitosanase from Bacillus circulans MH-K1 at 1.6-A resolution and its substrate recognition mechanism. J Biol Chem 274:30818-30825.
Saitoh, T., N. Fujita, T. Hayashi, K. Takahara, T. Satoh, H. Lee, K. Matsunaga, S. Kageyama, H. Omori, T. Noda, N. Yamamoto, T. Kawai, K. Ishii, O. Takeuchi, T. Yoshimori & S. Akira, (2009) Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc NatlAcadSci USA 106:20842-20846.
Salomon, D., H. Gonzalez, B.L. Updegraff & K. Orth, (2013) Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PLoS One 8:e61086.
Sauer, J.D., K. Sotelo-Troha, J. von Moltke, K.M. Monroe, C.S. Rae, S.W. Brubaker, M. Hyodo, Y. Hayakawa, J.J. Woodward, D.A. Portnoy & R.E. Vance, (2011) The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect Immun 79:688-694.
Sauvonnet, N., G Vignon, A.P. Pugsley & P. Gounon, (2000) Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J19:2221-2228.
Schell, M.A., R.L. Ulrich, W.J. Ribot, E.E. Brueggemann, H.B. Hines, D. Chen, L. Lipscomb, H.S. Kim, J. Mrazek, W.C. Nierman & D. Deshazer, (2007) Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol 64:1466-1485.
Schlieker, C., H. Zentgraf, P. Dersch & A. Mogk, (2005) ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol Chem 386:1115-1127.
Schwarz S, S.P., Robertson JD, Leroux M, Skerrett SJ, Goodlett DR, West TE, Mougous JD, (2014) VgrG-5 is a Burkholderia type VI secretion exported protein required for multinucleated giant cell formation and virulence. Infect Immun.
Schwarz, S., T.E. West, F. Boyer, W.C. Chiang, M.A. Carl, R.D. Hood, L. Rohmer, T. Tolker-Nielsen, S.J. Skerrett & J.D. Mougous, (2010) Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6:e1001068.
Shang, G., X. Liu, D. Lu, J. Zhang, N. Li, C. Zhu, S. Liu, Q. Yu, Y. Zhao, H. Zhang, J. Hu, H. Cang, S. Xu & L. Gu, (2012) Structural insight into how Pseudomonas aeruginosa peptidoglycanhydrolase Tse1 and its immunity protein Tsi1 function. Biochem J 448:201-211.
Sheldrick, G.M., (2010) Experimental phasing with SHELXC/D/E:combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66:479-485.
Shneider, M.M., S.A. Buth, B.T. Ho, M. Basler, J.J. Mekalanos & P.G. Leiman, (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500:350-353.
Shu, C., G. Yi, T. Watts, C.C. Kao & P. Li, (2012) Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat Struct Mol Biol 19:722-724.
Silverman, J.M., D.M. Agnello, H. Zheng, B.T. Andrews, M. Li, C.E. Catalano, T. Gonen & J.D. Mougous, (2013) Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol Cell 51:584-593.
Silverman, J.M., L.S. Austin, F. Hsu, K.G. Hicks, R.D. Hood & J.D. Mougous, (2011) Separate inputs modulate phosphorylation-dependent and-independent type VI secretion activation. Mol Microbiol 82:1277-1290.
Smallwood, M., J.N. Keen & D.J. Bowles, (1990) Purification and partial sequence analysis of plant annexins. Biochem J 270:157-161.
Stanley, S.A., J.E. Johndrow, P. Manzanillo & J.S. Cox, (2007) The Type ⅠIFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 178:3143-3152.
Stetson, D.B. & R. Medzhitov, (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24:93-103.
Suarez, G., J.C. Sierra, T.E. Erova, J. Sha, A.J. Horneman & A.K. Chopra, (2010) A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. JBacteriol 192:155-168.
Suarez, G, J.C. Sierra, J. Sha, S. Wang, T.E. Erova, A.A. Fadl, S.M. Foltz, A.J. Homeman & A.K. Chopra, (2008) Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb Pathog 44:344-361.
Sun, L., J. Wu, F. Du, X. Chen & Z.J. Chen, (2013) Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339:786-791.
Takaoka, A., Z. Wang, M.K. Choi, H. Yanai, H. Negishi, T. Ban, Y. Lu, M. Miyagishi, T. Kodama, K. Honda, Y. Ohba & T. Tanigucbi, (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448:501-505.
Tanaka, Y. & Z.J. Chen, (2012) STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal 5:ra20.
Terwilliger, T.C., (2000) Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56:965-972.
Terwilliger, T.C., (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr D Biol Crystallogr 59:38-44.
Terwilliger, T.C.& J. Berendzen, (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55:849-861.
Toesca, I.J., C.T. French & J.F. Miller, (2014) The T6SS-5 VgrG spike protein mediates membrane fusion during intercellular spread by pseudomallei-group Burkholderia species. Infect Immun.
Traikia, M., D.E. Warschawski, M. Recouvreur, J. Cartaud & P.F. Devaux, (2000) Formation of unilamellar vesicles by repetitive freeze-thaw cycles:characterization by electron microscopy and 31P-nuclear magnetic resonance. Eur Biophys J 29:184-195.
Unterholzner, L., S.E. Keating, M. Baran, K.A. Horan, S.B. Jensen, S. Sharma, C.M. Sirois, T. Jin, E. Latz, T.S. Xiao, K.A. Fitzgerald, S.R. Paludan & A.G Bowie, (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11:997-1004.
Unterweger, D., M:Kitaoka, S.T. Miyata, V. Bachmann, T.M. Brooks, J. Moloney, O. Sosa, D. Silva, J. Duran-Gonzalez, D. Provenzano & S. Pukatzki, (2012) Constitutive type VI secretion system expression gives Vibrio cholerae intra-and interspecific competitive advantages. PLoS One 7: e48320.
Van Herreweghe, J.M. & C.W. Michiels, (2012) Invertebrate lysozymes:diversity and distribution, molecular mechanism and in vivo function. JBiosci 37:327-348.
Van Herreweghe, J.M., L. Vanderkelen, L. Callewaert, A. Aertsen, G Compernolle, P.J. Declerck & C.W. Michiels, (2010) Lysozyme inhibitor conferring bacterial tolerance to invertebrate type lysozyme. Cell Mol Life Sci 67:1177-1188.
Vanderkelen, L., J.M. Van Herreweghe, K.G Vanoirbeek, G Baggerman, B. Myrnes, P.J. Declerck, I.W. Nilsen, C.W. Michiels & L. Callewaert, (2011) Identification of a bacterial inhibitor against g-type lysozyme. Cell Mol Life Sci 68:1053-1064.
Vasella, A., G.J. Davies & M. Bohm, (2002) Glycosidase mechanisms. Curr Opin Chem Biol 6: 619-629.
Vollmer, W., H. Pilsl, K. Hantke, J.V. Holtje & V. Braun, (1997) Pesticin displays muramidase activity. J Bacteriol 179:1580-1583.
Vollmer, W. & S.J. Seligman, (2010) Architecture of peptidoglycan:more data and more models. Trends Microbiol 18:59-66.
Watson, R.O., P.S. Manzanillo & J.S. Cox, (2012) Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803-815.
Weaver, L.H.& B.W. Matthews, (1987) Structure of bacteriophage T4 lysozyme refined at 1.7 A resolution. J Mol Biol 193:189-199.
Whitney, J.C., C.M. Beck, Y.A. Goo, A.B. Russell, B. Harding, J.A. De Leon, D.A. Cunningham, B.Q. Tran, D.A. Low, D.R. Goodlett, C.S. Hayes & J.D. Mougous, (2014) Genetically distinct pathways guide effector export through the type VI secretion system. Mol Microbiol.
Whitney, J.C., S. Chou, A.B. Russell, J. Biboy, T.E. Gardiner, M.A. Ferrin, M. Brittnacher, W. Vollmer & J.D. Mougous, (2013) Identification, structure and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J Biol Chem.
Wilderman, P.J., A.I. Vasil, Z. Johnson & M.L. Vasil, (2001) Genetic and biochemical analyses of a eukaryotic-like phospholipase D of Pseudomonas aeruginosa suggest horizontal acquisition and a role for persistence in a chronic pulmonary infection model. Mol Microbiol 39:291-303.
Wohlkonig, A., J. Huet, Y. Looze & R. Wintjens, (2010) Structural relationships in the lysozyme superfamily:significant evidence for glycoside hydrolase signature motifs. PLoS One 5: el5388.
Woodward, J.J., A.T. Iavarone & D.A. Portnoy, (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703-1705.
Wu, H.Y., PC. Chung, H.W. Shin, S.R. Wen & E.M. Lai, (2008) Secretome analysis uncovers an Hep-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J Bacteriol 190:2841-2850.
Wu, J.X., L.J. Sun, X. Chen, F.H. Du, H.P. Shi, C. Chen & Z.J.J. Chen, (2013) Cyclic GMP-AMP Is an Endogenous Second Messenger in Innate Immune Signaling by Cytosolic DNA. Science 339: 826-830.
Yin, Q., Y. Tian, V. Kabaleeswaran, X. Jiang, D. Tu, M.J. Eck, Z.J. Chen & H. Wu, (2012) Cyclic di-GMP sensing via the innate immune signaling protein STING Mol Cell 46:735-745.
Yum, S., M.J. Kim, Y. Xu, X.L. Jin, H.Y. Yoo, J.W Park, J.H. Gong, K.M. Choe, B.L. Lee & N.C. Ha, (2009) Structural basis for the recognition of lysozyme by MliC, a periplasmic lysozyme inhibitor in Gram-negative bacteria. Biochem Biophys Res Commun 378:244-248.
Zechel, D.L.& S.G Withers, (2000) Glycosidase mechanisms:anatomy of a finely tuned catalyst. Ace Chem Res 33:11-18.
Zhang, H., Z.Q. Gao, W.J. Wang, GF. Liu, J.H. Xu, X.D. Su & Y.H. Dong, (2013a) Structure of the type VI effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein. JBiol Chem 288:5928-5939.
Zhang, X., H. Shi, J. Wu, L. Sun, C. Chen & Z.J. Chen, (2013b) Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell 51: 226-235.
Zhang, Z., B. Yuan, M. Bao, N. Lu, T. Kim & YJ. Liu, (2011) The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12:959-965.
Zheng, J., B. Ho & J.J. Mekalanos, (2011) Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS One 6:e23876.
Abergel, C., V. Monchois, D. Byrne, S. Chenivesse, F. Lembo, J.C. Lazzaroni & J.M. Claverie, (2007) Structure and evolution of the Ivy protein family, unexpected lysozyme inhibitors in Gram-negative bacteria. Proc Natl Acad Sci USA 104:6394-6399.
Ablasser, A., F. Bauernfeind, G Hartmann, E. Latz, K.A. Fitzgerald & V. Hornung, (2009) RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase Ⅲ-transcribed RNA intermediate. Nat Immunol 10:1065-1072.
Ablasser, A., M. Goldeck, T. Cavlar, T. Deimling, G. Witte, I. Rohl, K.P. Hopfner, J. Ludwig & V. Hornung, (2013a) cGAS produces a 2'-5'-linked cyclic dinucleotide second messenger that activates STING. Nature 498:380-384.
Ablasser, A., J.L. Schmid-Burgk, I. Hemmerling, G.L. Horvath, T. Schmidt, E. Latz & V. Hornung, (2013b) Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503:530-534.
Alvarez-Martinez, C.E. & P.J. Christie, (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73:775-808.
Archer, K.A., J. Durack & D.A. Portnoy, (2014) STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog 10:e1003861.
Aschtgen, M.S., M.S. Thomas & E. Cascales, (2010) Anchoring the type VI secretion system to the peptidoglycan:TssL, TagL, TagP... what else? Virulence 1:535-540.
Aubert, D., D.K. MacDonald & M.A. Valvano, (2010) BcsKC is an essential protein for the type VI secretion system activity in Burkholderia cenocepacia that forms an outer membrane complex with BcsLB. J Biol Chem 285:35988-35998.
Aubert, D.F., R.S. Flannagan & M.A. Valvano, (2008) A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76:1979-1991.
Auerbuch, V., D.G. Brockstedt, N. Meyer-Morse, M. O'Riordan & D.A. Portnoy, (2004) Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J Exp Med 200: 527-533.
Bartonickova, L., T. Sterzenbach, S. Nell, F. Kops, J. Schulze, A. Venzke, B. Brenneke, S. Bader, A.D. Gruber, S. Suerbaum & C. Josenhans, (2013) Hcp and VgrGl are secreted components of the Helicobacter hepaticus type VI secretion system and VgrGl increases the bacterial colitogenic potential. Cell Microbiol 15:992-1011.
Basler, M., B.T. Ho & J.J. Mekalanos, (2013) Tit-for-tat:type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152:884-894.
Basler, M. & J.J. Mekalanos, (2012) Type 6 secretion dynamics within and between bacterial cells. Science 337:815.
Battye, T.G, L. Kontogiannis, O. Johnson, H.R. Powell & A.G. Leslie, (2011) iMOSFLM:a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67:271-281.
Beck, T., A. Krasauskas, T. Gruene & GM. Sheldrick, (2008) A magic triangle for experimental phasing of macromolecules. Acta Crystallogr D Biol Crystallogr 64:1179-1182.
Benz, J., J. Reinstein & A. Meinhart, (2013) Structural Insights into the Effector-Immunity System Tae4/Tai4 from. PLoS One 8:e67362.
Benz, J., C. Sendlmeier, T.R. Barends & A. Meinhart, (2012) Structural insights into the effector-immunity system Tsel/Tsil from Pseudomonas aeruginosa. PLoS One 7:e40453.
Binet, R., S. Letoffe, J.M. Ghigo, P. Delepelaire & C. Wandersman, (1997) Protein secretion by Gram-negative bacterial ABC exporters-a review. Gene 192:7-11.
Bladergroen, M.R., K. Badelt & H.P. Spaink, (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 16:53-64.
Blander, J.M. & L.E. Sander, (2012) Beyond pattern recognition:five immune checkpoints for scaling the microbial threat. Nat Rev Immunol 12:215-225.
Bleves, S., V. Viarre, R. Salacha, G.P. Michel, A. Filloux & R. Voulhoux, (2010) Protein secretion systems in Pseudomonas aeruginosa:A wealth of pathogenic weapons. Int J Med Microbiol 300:534-543.
Blondel, C.J., J.C. Jimenez, I. Contreras & C.A. Santiviago, (2009) Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10:354.
Bonemann, G., A. Pietrosiuk, A. Diemand, H. Zentgraf & A. Mogk, (2009) Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 28: 315-325.
Boyer, F., G Fichant, J. Berthod, Y. Vandenbrouck & I. Attree, (2009) Dissecting the bacterial type VI secretion system by a genome wide in silico analysis:what can be learned from available microbial genomic resources? BMC Genomics 10:104.
Bricogne, G., C. Vonrhein, C. Flensburg, M. Schiltz & W. Paciorek, (2003) Generation, representation and flow of phase information in structure determination:recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 59:2023-2030.
Brooks, T.M., D. Unterweger, V. Bachmann, B. Kostiuk & S. Pukatzki, (2013) Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J Biol Chem 288:7618-7625.
Browder, H.P., W.A. Zygmunt, J.R. Young & P.A. Tavormina, (1965) Lysostaphin:Enzymatic Mode of Action. Biochem Biophys Res Commun 19:383-389.
Brunet, Y.R., C.S. Bernard, M. Gavioli, R. Lloubes & E. Cascales, (2011) An epigenetic switch involving overlapping fur and DNA methylation optimizes expression of a type VI secretion gene cluster. PLoS Genet 7:e1002205.
Burckstummer, T., C. Baumann, S. Bluml, E. Dixit, G. Durnberger, H. Jahn, M. Planyavsky, M. Bilban, J. Colinge, K.L. Bennett & G. Superti-Furga, (2009) An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10: 266-272.
Burdette, D.L., K.M. Monroe, K. Sotelo-Troha, J.S. Iwig, B. Eckert, M. Hyodo, Y. Hayakawa & R.E. Vance, (2011) STING is a direct innate immune sensor of cyclic di-GMP. Nature 478: 515-518.
Burdette, D.L. & R.E. Vance, (2013) STING and the innate immune response to nucleic acids in the cytosol. Nat Immunol 14:19-26.
Burtnick, M.N., D. DeShazer, V. Nair, F.C. Gherardini & P.J. Brett, (2010) Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages. Infect Immun 78:88-99.
Callewaert, L., A. Aertsen, D. Deckers, K.G. Vanoirbeek, L. Vanderkelen, J.M. Van Herreweghe, B. Masschalck, D. Nakimbugwe, J. Robben & C.W. Michiels, (2008) A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog 4: e1000019.
Callewaert, L. & C.W. Michiels, (2010) Lysozymes in the animal kingdom. JBiosci 35:127-160.
Campos, B., YD. Mo, T.R. Mealy, C.W. Li, M.A. Swairjo, C. Balch, J.F. Head, G Retzinger, J.R. Dedman & B.A. Seaton, (1998) Mutational and crystallographic analyses of interfacial residues in annexin V suggest direct interactions with phospholipid membrane components. Biochemistry 37:8004-8010.
Carrero, J.A., B. Calderon & E.R. Unanue, (2004) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. JExpMed 200:535-540.
Carrero, J.A.& E.R Unanue, (2006) Lymphocyte apoptosis as an immune subversion strategy of microbial pathogens. Trends Immunol 27:497-503.
Carruthers, M.D., P.A. Nicholson, E.N. Tracy & R.S. Munson, Jr., (2013) Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition. PLoS One 8:e59388.
Casabona, M.G., J.M. Silverman, K.M. Sall, F. Boyer, Y. Coute, J. Poirel, D. Grunwald, J.D. Mougous, S. Elsen & I. Attree, (2013) An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa. Environ Microbiol 15:471-486.
Cascales, E. & C. Cambillau, (2012) Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 367:1102-1111.
Chakraborty, S., J. Sivaraman, K.Y. Leung & Y.K. Mok, (2011) Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III and VI secretion systems of Edwardsiella tarda. J Biol Chem 286:39417-39430.
Chen, H., H. Sun, F. You, W. Sun, X. Zhou, L. Chen, J. Yang, Y. Wang, H. Tang, Y. Guan, W. Xia, J. Gu, H. Ishikawa, D. Gutman, G Barber, Z. Qin & Z. Jiang, (2011) Activation of STAT6 by STING is critical for antiviral innate immunity. Cell 147:436-446.
Chou, S., N.K. Bui, A.B. Russell, K.W. Lexa, T.E. Gardiner, M. LeRoux, W. Vollmer & J.D. Mougous, (2012) Structure of a peptidoglycan amidase effector targeted to Gram-negative bacteria by the type VI secretion system. Cell Rep 1:656-664.
Chow, J. & S.K. Mazmanian, (2010) A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 7:265-276.
Concha, N.O., J.F. Head, M.A. Kaetzel, J.R. Dedman & B.A. Seaton, (1993) Rat annexin V crystal structure:Ca(2+)-induced conformational changes. Science 261:1321-1324.
Cornelis, GR., (2006) The type III secretion injectisome. Nat Rev Microbiol 4:811-825.
Cornelis, G.R., (2010) The type III secretion injectisome, a complex nanomachine for intracellular 'toxin1 delivery. Biol Chem 391:745-751.
Corr, S.C., Y. Li, C.U. Riedel, P.W. OToole, C. Hill & C.G Gahan, (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci USA 104:7617-7621.
Cridland, J.A., E.Z. Curley, M.N. Wykes, K. Schroder, M.J. Sweet, T.L. Roberts, M.A. Ragan, K.S. Kassahn & K.J. Stacey, (2012) The mammalian PYHIN gene family:phylogeny, evolution and expression. BMC Evol Biol 12:140.
Cronan, J.E., (2003) Bacterial membrane lipids:where do we stand? Annu Rev Microbiol 57:203-224.
Das, S.& K. Chaudhuri, (2003) Identification of a unique IAHP (IcmF associated homologous proteins) cluster in Vibrio cholerae and other proteobacteria through in silico analysis. In Silico Biol 3: 287-300.
Dawid, S., A.M. Roche & J.N. Weiser, (2007) The blp bacteriocins of Streptococcus pneumoniae mediate intraspecies competition both in vitro and in vivo. Infect Immun 75:443-451.
DeFilippis, V.R., D. Alvarado, T. Sali, S. Rothenburg & K. Fruh, (2010) Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J Virol 84:585-598.
Delepelaire, P., (2004) Type I secretion in gram-negative bacteria. Biochim Biophys Acta 1694: 149-161.
Ding, J., W. Wang, H. Feng, Y. Zhang & D.C. Wang, (2012) Structural insights into the Pseudomonas aeruginosa type VI virulence effector Tsel bacteriolysis and self-protection mechanisms. J Biol Chem 287:26911-26920.
Dong, C., H. Zhang, Z.Q. Gao, W.J. Wang, Z. She, GF. Liu, Y.Q. Shen, X.D. Su & Y.H. Dong, (2013a) Structural insights into the inhibition of type VI effector Tae3 by its immunity protein Tai3. Biochem.J 454:59-68.
Dong, T.G., B.T. Ho, D.R. Yoder-Himes & J.J. Mekalanos, (2013b) Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc Natl Acad Sci U S A 110: 2623-2628.
Dudley, E.G., N.R. Thomson, J. Parkhill, N.P. Morin & J.P. Nataro, (2006) Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol 61:1267-1282.
Duong, F., A. Lazdunski & M. Murgier, (1996) Protein secretion by heterologous bacterial ABC-transporters:the C-terminus secretion signal of the secreted protein confers high recognition specificity. Mol Microbiol 21:459-470.
Economou, A., P.J. Christie, R.C. Fernandez, T. Palmer, G.V. Plano & A.P. Pugsley, (2006) Secretion by numbers:Protein traffic in prokaryotes. Mol Microbiol 62:308-319.
El Ghachi, M., A. Bouhss, H. Barreteau, T. Touze, G. Auger, D. Blanot & D. Mengin-Lecreulx, (2006) Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J Biol Chem 281:22761-22772.
Evans, P., (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
Fernandes-Alnemri, T, J.W. Yu, P. Datta, J. Wu & E.S. Alnemri, (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458:509-513.
Filloux, A., (2004) The underlying mechanisms of type Ⅱ protein secretion. Biochim Biophys Acta 1694:163-179.
Folkesson, A., S. Lofdahl & S. Normark, (2002) The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol 153:537-545.
Fritsch, M.J., K. Trunk, J.A. Diniz, M. Guo, M. Trost & S.J. Coulthurst, (2013) Proteomic identification of novel secreted antibacterial toxins of the Serratia marcescens type VI secretion system. Mol Cell Proteomics 12:2735-2749.
Gan, L., S. Chen & G.J. Jensen, (2008) Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci USA 105:18953-18957.
Gao, D., J. Wu, Y.T. Wu, F. Du, C. Aroh, N. Yan, L. Sun & Z.J. Chen, (2013a) Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341:903-906.
Gao, P., M. Ascano, Y. Wu, W. Barchet, B.L. Gaffney, T. Zillinger, A.A. Serganov, Y. Liu, R.A. Jones, G. Hartmann, T. Tuschl & D.J. Patel, (2013b) Cyclic [G(2',5')pA(3',5')p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell153:1094-1107.
Gao, P., M. Ascano, T. Zillinger, W. Wang, P. Dai, A.A. Serganov, B.L. Gaffney, S. Shuman, R.A. Jones, L. Deng, G. Hartmann, W. Barchet, T. Tuschl & D.J. Patel, (2013c) Structure-function analysis of STING activation by c[G(2',5')pA(3',5')p] and targeting by antiviral DMXAA. Cell 154: 748-762.
Gerke, V, (1991) Identification of a homologue for annexin VII (synexin) in Dictyostelium discoideum. J Biol Chem 266:1697-1700.
Glauner, B., (1988) Separation and quantification of muropeptides with high-performance liquid chromatography. Anal Biochem 172:451-464.
Goto, T., Y. Abe, Y. Kakuta, K. Takeshita, T. Imoto & T. Ueda, (2007) Crystal structure of Tapes japonica Lysozyme with substrate analogue:structural basis of the catalytic mechanism and manifestation of its chitinase activity accompanied by quaternary structural change. J Biol Chem 282:27459-27467.
Gueguen, E. & E. Cascales, (2013) Promoter swapping unveils the role of the Citrobacter rodentium CTS1 type VI secretion system in interbacterial competition. Appl Environ Microbiol 79: 32-38.
Gurtler, C. & A.G. Bowie, (2013) Innate immune detection of microbial nucleic acids. Trends Microbiol 21:413-420.
Haapalainen, M., H. Mosorin, F. Dorati, R.F. Wu, E. Roine, S. Taira, R. Nissinen, L. Mattinen, R. Jackson, M. Pirhonen & N.C. Lin, (2012) Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J Bacteriol 194:4810-4822.
Hamada, S., M. Umemura, T. Shiono, K. Tanaka, A. Yahagi, M.D. Begum, K. Oshiro, Y. Okamoto, H. Watanabe, K. Kawakami, C. Roark, W.K. Born, R. O'Brien, K. Ikuta, H. Ishikawa, S. Nakae, Y. Iwakura, T. Ohta & G. Matsuzaki, (2008) IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J Immunol 181:3456-3463.
Henry, T., GS. Kirimanjeswara, T. Ruby, J.W. Jones, K. Peng, M. Perret, L. Ho, J.D. Sauer, Y. Iwakura, D.W. Metzger & D.M. Monack, (2010) Type IIFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J Immunol 184:3755-3767.
Hirakawa, H., A. Ochi, Y. Kawahara, S. Kawamura, T. Torikata & S. Kuhara, (2008) Catalytic reaction mechanism of goose egg-white lysozyme by molecular modelling of enzyme-substrate complex. J Biochem 144:753-761.
Ho, B.T., M. Basler & J.J. Mekalanos, (2013) Type 6 secretion system-mediated immunity to type 4 secretion system-mediated gene transfer. Science 342:250-253.
Ho, B.T., T.G Dong & J.J. Mekalanos, (2014) A view to a kill:the bacterial type VI secretion system. Cell Host Microbe 15:9-21.
Hofmann, A., J. Proust, A. Dorowski, R. Schantz & R. Huber, (2000) Annexin 24 from Capsicum annuum. X-ray structure and biochemical characterization. J Biol Chem 275:8072-8082.
Holland, I.B., L. Schmitt & J. Young, (2005) Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). Mol Membr Biol 22:29-39.
Holm, L. & C. Sander, (1994) Structural similarity of plant chitinase and lysozymes from animals and' phage. An evolutionary connection. FEBSLett 340:129-132.
Hood, R.D., P. Singh, F. Hsu, T. Guvener, M.A. Carl, R.R. Trinidad, J.M. Silverman, B.B. Ohlson, K.G Hicks, R.L. Plemel, M. Li, S. Schwarz, W.Y. Wang, A.J. Merz, D.R. Goodlett & J.D. Mougous, (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37.
Horan, K.A., K. Hansen, M.R. Jakobsen, C.K. Holm, S. Soby, L. Unterholzner, M. Thompson, J.A. West, M.B. Iversen, S.B. Rasmussen, S. Ellermann-Eriksen, E. Kurt-Jones, S. Landolfo, B. Damania, J. Melchjorsen, A.G. Bowie, K.A. Fitzgerald & S.R. Paludan, (2013) Proteasomal degradation of herpes simplex virus capsids in macrophages releases DNA to the cytosol for recognition by DNA sensors. J Immunol 190:2311-2319.
Hornung, V, A. Ablasser, M. Charrel-Dennis, F. Bauernfeind, G Horvath, D.R. Caffrey, E. Latz & K.A. Fitzgerald, (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-518.
Hsu, F., S. Schwarz & J.D. Mougous, (2009) TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol Microbiol 72:1111-1125.
Hu, N.J., A.M. Yusof, A. Winter, A. Osman, A.K. Reeve & A. Hofmann, (2008) The crystal structure of calcium-bound annexin Ghl from Gossypium hirsutum and its implications for membrane binding mechanisms of plant annexins. JBiol Chem 283:18314-18322.
Huang, Y.H., X.Y. Liu, X.X. Du, Z.F. Jiang & X.D. Su, (2012) The structural basis for the sensing and binding of cyclic di-GMP by STING. Nat Struct Mol Biol 19:728-730.
Huet, J., P. Rucktooa, B. Clantin, M. Azarkan, Y. Looze, V. Villeret & R. Wintjens, (2008) X-ray structure of papaya chitinase reveals the substrate binding mode of glycosyl hydrolase family 19 chitinases. Biochemistry 47:8283-8291.
Ishii, K.J., C. Coban, H. Kato, K. Takahashi, Y. Torii, F. Takeshita, H. Ludwig, G Sutter, K. Suzuki, H. Hemmi, S. Sato, M. Yamamoto, S. Uematsu, T. Kawai, O. Takeuchi & S. Akira, (2006) A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol 7:40-48.
Ishikawa, H., Z. Ma & G.N. Barber, (2009a) STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461:788-792.
Ishikawa, T., P.K. Rompikuntal, B. Lindmark, D.L. Milton & S.N. Wai, (2009b) Quorum sensing regulation of the two hcp alleles in Vibrio cholerae 01 strains. PLoS One 4:e6734.
Jin, L., K.K. Hill, H. Filak, J. Mogan, H. Knowles, B. Zhang, A.L. Perraud, J.C. Cambier & L.L. Lenz, (2011) MPYS is required for IFN response factor 3 activation and type IIFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J Immunol 187:2595-2601.
Johnston, P.A., M.S. Perin, GA. Reynolds, S.A. Wasserman & T.C. Sudhof, (1990) Two novel annexins from Drosophila melanogaster. Cloning, characterization, and differential expression in development. J Biol Chem 265:11382-11388.
Karaghiosoff, M., R. Steinborn, P. Kovarik, G Kriegshauser, M. Baccarini, B. Donabauer, U. Reichart, T. Kolbe, C. Bogdan, T. Leanderson, D. Levy, T. Decker & M. Muller, (2003) Central role for type I interferons and Tyk2 in lipopolysaccharide-induced endotoxin shock. Nat Immunol 4: 471-477.
Kato, H., K. Takahasi & T. Fujita, (2011) RIG-I-like receptors:cytoplasmic sensors for non-self RNA. Immunol Rev 243:91-98.
Keating, S.E., M. Baran & A.G Bowie, (2011) Cytosolic DNA sensors regulating type I interferon induction. Trends Immunol 32:574-581.
Kim, T., S. Pazhoor, M. Bao, Z. Zhang, S. Hanabuchi, V. Facchinetti, L. Bover, J. Plumas, L. Chaperot, J. Qin & Y.J. Liu, (2010) Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc Natl Acad Sci USA 107:15181-15186.
Kitaoka, M., S.T. Miyata, T.M. Brooks, D. Unterweger & S. Pukatzki, (2011) VasH is a transcriptional regulator of the type VI secretion system functional in endemic and pandemic Vibrio cholerae. JBacteriol 193:6471-6482.
Knapp, S., (2010) Update on the role of Toll-like receptors during bacterial infections and sepsis. Wien Med Wochenschr 160:107-111.
Kohler, R., K. Schafer, S. Muller, G. Vignon, K. Diederichs, A. Philippsen, P. Ringler, A.P. Pugsley, A. Engel & W. Welte, (2004) Structure and assembly of the pseudopilin PulG. Mol Microbiol 54: 647-664.
Kong, K.F., L. Schneper & K. Mathee, (2010) Beta-lactam antibiotics:from antibiosis to resistance and bacteriology. APMIS 118:1-36.
Konno, H., K. Konno & G.N. Barber, (2013) Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signaling. Cell 155:688-698.
Korotkov, K.V. & W.G. Hol, (2008) Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat Struct Mol Biol 15:462-468.
Koskiniemi, S., J.G Lamoureux, K.C. Nikolakakis, C. t'Kint de Roodenbeke, M.D. Kaplan, D.A. Low & C.S. Hayes, (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA 110:7032-7037.
Krissinel, E.& K. Henrick, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774-797.
Leiman, P.G., M. Basler, U.A. Ramagopal, J.B. Bonanno, J.M. Sauder, S. Pukatzki, S.K. Burley, S.C. Almo & J.J. Mekalanos, (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci U S A 106:4154-4159.
Lemaitre, B., E. Nicolas, L. Michaut, J.M. Reichhart & J.A. Hoffmann, (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973-983.
LeRoux, M., J.A. De Leon, N.J. Kuwada, A.B. Russell, D. Pinto-Santini, R.D. Hood, D.M. Agnello, S.M. Robertson, P.A. Wiggins & J.D. Mougous, (2012) Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword. Proc Natl Acad Sci USA 109:19804-19809.
Lertpiriyapong, K., E.R. Gamazon, Y. Feng, D.S. Park, J. Pang, G. Botka, M.E. Graffam, Z. Ge & J.G. Fox, (2012) Campylobacter jejuni type VI secretion system:roles in adaptation to deoxycholic acid, host cell adherence, invasion, and in vivo colonization. PLoS One 7:e42842.
Lesic, B., M. Starkey, J. He, R. Hazan & L.G. Rahme, (2009) Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155:2845-2855.
Leysen, S., J.M. Van Herreweghe, L. Callewaert, M. Heirbaut, P. Buntinx, C.W. Michiels & S.V. Strelkov, (2011) Molecular basis of bacterial defense against host lysozymes:X-ray structures of periplasmic lysozyme inhibitors Plil and PliC. JMol Biol 405:1233-1245.
Leysen, S., L. Vanderkelen, K. Van Asten, S. Vanheuverzwijn, V. Theuwis, C.W. Michiels & S.V. Strelkov, (2012) Structural characterization of the PliG lysozyme inhibitor family. J Struct Biol 180:235-242.
Leysen, S., L. Vanderkelen, S.D. Weeks, C.W. Michiels & S.V. Strelkov, (2013) Structural basis of bacterial defense against g-type lysozyme-based innate immunity. Cell Mol Life Sci 70: 1113-1122.
Li, M., I. Le Trong, M.A. Carl, E.T. Larson, S. Chou, J.A. De Leon, S.L. Dove, R.E. Stenkamp & J.D. Mougous, (2012) Structural basis for type VI secretion effector recognition by a cognate immunity protein. PLoS Pathog 8:e1002613.
Lossi, N.S., E. Manoli, A. Forster, R. Dajani, T. Pape, P. Freemont & A. Filloux, (2013) The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. JBiol Chem 288:7536-7548.
Ma, A.T., S. McAuley, S. Pukatzki & J.J. Mekalanos, (2009a) Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5: 234-243.
Ma, L.S., J.S. Lin & E.M. Lai, (2009b) An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and its walker a motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens. JBacteriol 191:4316-4329.
MacIntyre, D.L., ST. Miyata, M. Kitaoka & S. Pukatzki, (2010) The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci U S A 107:19520-19524.
Manzanillo, P.S., M.U. Shiloh, D.A. Portaoy & J.S. Cox, (2012) Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11:469-480.
McCoy, A.J., R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni & R.J. Read, (2007) Phaser crystallographic software. JAppl Crystallogr 40:658-674.
McWhirter, S.M., R. Barbalat, K.M. Monroe, M.F. Fontana, M. Hyodo, N.T. Joncker, K.J. Ishii, S. Akira, M. Colonna, Z.J. Chen, K.A. Fitzgerald, Y. Hayakawa & R.E. Vance, (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206:1899-1911.
Medzhitov, R., P. Preston-Hurlburt & C.A. Janeway, Jr., (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394-397.
Meeks, K.D., A.N. Sieve, J.K. Kolls, N. Ghilardi & R.E. Berg, (2009) IL-23 is required for protection against systemic infection with Listeria monocytogenes. J Immunol 183:8026-8034.
Miyata, S.T., D. Unterweger, S.P. Rudko & S. Pukatzki, (2013) Dual expression profile of type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathog 9: e1003752.
Monchois, V, C. Abergel, J. Sturgis, S. Jeudy & J.M. Claverie, (2001) Escherichia coli ykfE ORFan gene encodes a potent inhibitor of C-type lysozyme. J Biol Chem 276:18437-18441.
Mondini, M., S. Costa, S. Sponza, F. Gugliesi, M. Gariglio & S. Landolfo, (2010) The interferon-inducible HIN-200 gene family in apoptosis and inflammation:implication for autoimmunity. Autoimmunity 43:226-231.
Monzingo, A.F., E.M. Marcotte, P.J. Hart & J.D. Robertus, (1996) Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core. Nat Struct Biol 3:133-140.
Moscoso, J.A., H. Mikkelsen, S. Heeb, P. Williams & A. Filloux, (2011) The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol 13:3128-3138.
Mougous, J.D., M.E. Cuff, S. Raunser, A. Shen, M. Zhou, C.A. Gifford, A.L. Goodman, G Joachimiak, C.L. Ordonez, S. Lory, T. Walz, A. Joachimiak & J.J. Mekalanos, (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-1530.
Mougous, J.D., C.A. Gifford, T.L. Ramsdell & J.J. Mekalanos, (2007) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 9: 797-803.
Murdoch, S.L., K. Trunk, G English, M.J. Fritsch, E. Pourkarimi & S.J. Coulthurst, (2011) The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. JBacteriol 193:6057-6069.
Nagarajan, U.M., D. Prantner, J.D. Sikes, C.W. Andrews, Jr., A.M. Goodwin, S. Nagarajan & T. Darville, (2008) Type I interferon signaling exacerbates Chlamydia muridarum genital infection in a murine model. Infect Immun 76:4642-4648.
Nakayama, H., K. Kurokawa & B.L. Lee, (2012) Lipoproteins in bacteria:structures and biosynthetic pathways. FEBS J 219:4247-4268.
Nano, F.E., N. Zhang, S.C. Cowley, K.E. Klose, K.K. Cheung, M.J. Roberts, J.S. Ludu, G.W. Letendre, A. I. Meierovics, G Stephens & K.L. Elkins, (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186:6430-6436.
O'Connell, R.M., S.K. Saha, S.A. Vaidya, K.W. Bruhn, GA. Miranda, B. Zarnegar, A.K. Perry, B.O. Nguyen, T.F. Lane, T. Taniguchi, J.F. Miller & G Cheng, (2004) Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200:437-445.
Ordway, D., M. Henao-Tamayo, M. Harton, G. Palanisamy, J. Troudt, C. Shanley, R.J. Basaraba & I.M. Orme, (2007) The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 179:522-531.
Otwinowski, Z.& W. Minor, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol.276:307-326.
Ouyang, S., X. Song, Y. Wang, H. Ru, N. Shaw, Y. Jiang, F. Niu, Y. Zhu, W. Qiu, K. Parvatiyar, Y. Li, R. Zhang, G Cheng & Z.J. Liu, (2012) Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36:1073-1086.
Pallen, M., R. Chaudhuri & A. Khan, (2002) Bacterial FHA domains:neglected players in the phospho-threonine signalling game? Trends Microbiol 10:556-563.
Parvatiyar, K., Z. Zhang, R.M. Teles, S. Ouyang, Y. Jiang, S.S. Iyer, S.A. Zaver, M. Schenk, S. Zeng, W. Zhong, Z.J. Liu, R.L. Modlin, Y.J. Liu & G. Cheng, (2012) The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 13:1155-1161.
Peabody, C.R., Y.J. Chung, M.R. Yen, D. Vidal-Ingigliardi, A.P. Pugsley & M.H. Saier, Jr., (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051-3072.
Pell, L.G., V. Kanelis, L. W. Donaldson, P.L. Howell & A.R. Davidson, (2009) The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci USA 106:4160-4165.
Pieper, R., S.T. Huang, J.M. Robinson, D.J. Clark, H. Alami, P.P. Parmar, R.D. Perry, R.D. Fleischmann & S.N. Peterson, (2009) Temperature and growth phase influence the outer-membrane proteome and the expression of a type VI secretion system in Yersinia pestis. Microbiology 155:498-512.
Pigault, C., A. Follenius-Wund & M. Chabbert, (1999) Role of Trp-187 in the annexin V-membrane interaction:a molecular mechanics analysis. Biochem Biophys Res Commun 254:484-489.
Pincus, M.R., S.S. Zimmerman & H.A. Scheraga, (1976) Prediction of three-dimensional structures of enzyme-substrate and enzyme-inhibitor complexes of lysozyme. Proc Natl Acad Sci USA 73: 4261-4265.
Pincus, M.R., S.S. Zimmerman & H.A. Scheraga, (1977) Structures of enzyme-substrate complexes of lysozyme. Proc Natl Acad Sci USA 74:2629-2633.
Poole, S.J., E.J. Diner, S.K. Aoki, B.A. Braaten, C. t'Kint de Roodenbeke, D.A. Low & C.S. Hayes, (2011) Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 7:e1002217.
Pukatzki, S., A.T. Ma, A.T. Revel, D. Sturtevant & J.J. Mekalanos, (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 104:15508-15513.
Pukatzki, S., A.T. Ma, D. Sturtevant, B. Krastins, D. Sarracino, W.C. Nelson, J.F. Heidelberg & J.J. Mekalanos, (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103: 1528-1533.
Pukatzki, S., S.B. McAuley & S.T. Miyata, (2009) The type VI secretion system:translocation of effectors and effector-domains. Curr Opin Microbiol 12:11-17.
Rao, P.S., Y. Yamada, Y.P. Tan & K.Y. Leung, (2004) Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol Microbiol 53: 573-586.
Rasmussen, S.B., K.A. Horan, C.K. Holm, A.J. Stranks, T.C. Mettenleiter, A.K. Simon, S.B. Jensen, F.J. Rixon, B. He & S.R. Paludan, (2011) Activation of autophagy by alpha-herpesviruses in myeloid cells is mediated by cytoplasmic viral DNA through a mechanism dependent on stimulator of IFN genes. J Immunol 187:5268-5276.
Roberts, T.L., A. Idris, J.A. Dunn, GM. Kelly, C.M. Burnton, S. Hodgson, L.L. Hardy, V. Garceau, M.J. Sweet, I.L. Ross, D.A. Hume & K.J. Stacey, (2009) HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323:1057-1060.
Russell, A.B., R.D. Hood, N.K. Bui, M. LeRoux, W. Vollmer & J.D. Mougous, (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343-347.
Russell, A.B., M. LeRoux, K. Hathazi, D.M. Agnello, T. Ishikawa, P.A. Wiggins, S.N. Wai & J.D. Mougous, (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496:508-512.
Russell, A.B., S.B. Peterson & J.D. Mougous, (2014) Type VI secretion system effectors:poisons with a purpose. Nat Rev Microbiol 12:137-148.
Russell, A.B., P. Singh, M. Brittnacher, N.K. Bui, R.D. Hood, M.A. Carl, D.M. Agnello, S. Schwarz, D.R. Goodlett, W. Vollmer & J.D. Mougous, (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11:538-549.
Rye, C.S.& S.G. Withers, (2000) Glycosidase mechanisms. Curr Opin Chem Biol 4:573-580.
Saito, J., A. Kita, Y. Higuchi, Y. Nagata, A. Ando & K. Miki, (1999) Crystal structure of chitosanase from Bacillus circulans MH-K1 at 1.6-A resolution and its substrate recognition mechanism. J Biol Chem 274:30818-30825.
Saitoh, T., N. Fujita, T. Hayashi, K. Takahara, T. Satoh, H. Lee, K. Matsunaga, S. Kageyama, H. Omori, T. Noda, N. Yamamoto, T. Kawai, K. Ishii, O. Takeuchi, T. Yoshimori & S. Akira, (2009) Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc NatlAcadSci USA 106:20842-20846.
Salomon, D., H. Gonzalez, B.L. Updegraff & K. Orth, (2013) Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PLoS One 8:e61086.
Sauer, J.D., K. Sotelo-Troha, J. von Moltke, K.M. Monroe, C.S. Rae, S.W. Brubaker, M. Hyodo, Y. Hayakawa, J.J. Woodward, D.A. Portnoy & R.E. Vance, (2011) The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect Immun 79:688-694.
Sauvonnet, N., G Vignon, A.P. Pugsley & P. Gounon, (2000) Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J19:2221-2228.
Schell, M.A., R.L. Ulrich, W.J. Ribot, E.E. Brueggemann, H.B. Hines, D. Chen, L. Lipscomb, H.S. Kim, J. Mrazek, W.C. Nierman & D. Deshazer, (2007) Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol 64:1466-1485.
Schlieker, C., H. Zentgraf, P. Dersch & A. Mogk, (2005) ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol Chem 386:1115-1127.
Schwarz S, S.P., Robertson JD, Leroux M, Skerrett SJ, Goodlett DR, West TE, Mougous JD, (2014) VgrG-5 is a Burkholderia type VI secretion exported protein required for multinucleated giant cell formation and virulence. Infect Immun.
Schwarz, S., T.E. West, F. Boyer, W.C. Chiang, M.A. Carl, R.D. Hood, L. Rohmer, T. Tolker-Nielsen, S.J. Skerrett & J.D. Mougous, (2010) Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6:e1001068.
Shang, G., X. Liu, D. Lu, J. Zhang, N. Li, C. Zhu, S. Liu, Q. Yu, Y. Zhao, H. Zhang, J. Hu, H. Cang, S. Xu & L. Gu, (2012) Structural insight into how Pseudomonas aeruginosa peptidoglycanhydrolase Tse1 and its immunity protein Tsi1 function. Biochem J 448:201-211.
Sheldrick, G.M., (2010) Experimental phasing with SHELXC/D/E:combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66:479-485.
Shneider, M.M., S.A. Buth, B.T. Ho, M. Basler, J.J. Mekalanos & P.G. Leiman, (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500:350-353.
Shu, C., G. Yi, T. Watts, C.C. Kao & P. Li, (2012) Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat Struct Mol Biol 19:722-724.
Silverman, J.M., D.M. Agnello, H. Zheng, B.T. Andrews, M. Li, C.E. Catalano, T. Gonen & J.D. Mougous, (2013) Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol Cell 51:584-593.
Silverman, J.M., L.S. Austin, F. Hsu, K.G. Hicks, R.D. Hood & J.D. Mougous, (2011) Separate inputs modulate phosphorylation-dependent and-independent type VI secretion activation. Mol Microbiol 82:1277-1290.
Smallwood, M., J.N. Keen & D.J. Bowles, (1990) Purification and partial sequence analysis of plant annexins. Biochem J 270:157-161.
Stanley, S.A., J.E. Johndrow, P. Manzanillo & J.S. Cox, (2007) The Type ⅠIFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 178:3143-3152.
Stetson, D.B. & R. Medzhitov, (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24:93-103.
Suarez, G., J.C. Sierra, T.E. Erova, J. Sha, A.J. Horneman & A.K. Chopra, (2010) A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. JBacteriol 192:155-168.
Suarez, G, J.C. Sierra, J. Sha, S. Wang, T.E. Erova, A.A. Fadl, S.M. Foltz, A.J. Homeman & A.K. Chopra, (2008) Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb Pathog 44:344-361.
Sun, L., J. Wu, F. Du, X. Chen & Z.J. Chen, (2013) Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339:786-791.
Takaoka, A., Z. Wang, M.K. Choi, H. Yanai, H. Negishi, T. Ban, Y. Lu, M. Miyagishi, T. Kodama, K. Honda, Y. Ohba & T. Tanigucbi, (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448:501-505.
Tanaka, Y. & Z.J. Chen, (2012) STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal 5:ra20.
Terwilliger, T.C., (2000) Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56:965-972.
Terwilliger, T.C., (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr D Biol Crystallogr 59:38-44.
Terwilliger, T.C.& J. Berendzen, (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55:849-861.
Toesca, I.J., C.T. French & J.F. Miller, (2014) The T6SS-5 VgrG spike protein mediates membrane fusion during intercellular spread by pseudomallei-group Burkholderia species. Infect Immun.
Traikia, M., D.E. Warschawski, M. Recouvreur, J. Cartaud & P.F. Devaux, (2000) Formation of unilamellar vesicles by repetitive freeze-thaw cycles:characterization by electron microscopy and 31P-nuclear magnetic resonance. Eur Biophys J 29:184-195.
Unterholzner, L., S.E. Keating, M. Baran, K.A. Horan, S.B. Jensen, S. Sharma, C.M. Sirois, T. Jin, E. Latz, T.S. Xiao, K.A. Fitzgerald, S.R. Paludan & A.G Bowie, (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11:997-1004.
Unterweger, D., M:Kitaoka, S.T. Miyata, V. Bachmann, T.M. Brooks, J. Moloney, O. Sosa, D. Silva, J. Duran-Gonzalez, D. Provenzano & S. Pukatzki, (2012) Constitutive type VI secretion system expression gives Vibrio cholerae intra-and interspecific competitive advantages. PLoS One 7: e48320.
Van Herreweghe, J.M. & C.W. Michiels, (2012) Invertebrate lysozymes:diversity and distribution, molecular mechanism and in vivo function. JBiosci 37:327-348.
Van Herreweghe, J.M., L. Vanderkelen, L. Callewaert, A. Aertsen, G Compernolle, P.J. Declerck & C.W. Michiels, (2010) Lysozyme inhibitor conferring bacterial tolerance to invertebrate type lysozyme. Cell Mol Life Sci 67:1177-1188.
Vanderkelen, L., J.M. Van Herreweghe, K.G Vanoirbeek, G Baggerman, B. Myrnes, P.J. Declerck, I.W. Nilsen, C.W. Michiels & L. Callewaert, (2011) Identification of a bacterial inhibitor against g-type lysozyme. Cell Mol Life Sci 68:1053-1064.
Vasella, A., G.J. Davies & M. Bohm, (2002) Glycosidase mechanisms. Curr Opin Chem Biol 6: 619-629.
Vollmer, W., H. Pilsl, K. Hantke, J.V. Holtje & V. Braun, (1997) Pesticin displays muramidase activity. J Bacteriol 179:1580-1583.
Vollmer, W. & S.J. Seligman, (2010) Architecture of peptidoglycan:more data and more models. Trends Microbiol 18:59-66.
Watson, R.O., P.S. Manzanillo & J.S. Cox, (2012) Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803-815.
Weaver, L.H.& B.W. Matthews, (1987) Structure of bacteriophage T4 lysozyme refined at 1.7 A resolution. J Mol Biol 193:189-199.
Whitney, J.C., C.M. Beck, Y.A. Goo, A.B. Russell, B. Harding, J.A. De Leon, D.A. Cunningham, B.Q. Tran, D.A. Low, D.R. Goodlett, C.S. Hayes & J.D. Mougous, (2014) Genetically distinct pathways guide effector export through the type VI secretion system. Mol Microbiol.
Whitney, J.C., S. Chou, A.B. Russell, J. Biboy, T.E. Gardiner, M.A. Ferrin, M. Brittnacher, W. Vollmer & J.D. Mougous, (2013) Identification, structure and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J Biol Chem.
Wilderman, P.J., A.I. Vasil, Z. Johnson & M.L. Vasil, (2001) Genetic and biochemical analyses of a eukaryotic-like phospholipase D of Pseudomonas aeruginosa suggest horizontal acquisition and a role for persistence in a chronic pulmonary infection model. Mol Microbiol 39:291-303.
Wohlkonig, A., J. Huet, Y. Looze & R. Wintjens, (2010) Structural relationships in the lysozyme superfamily:significant evidence for glycoside hydrolase signature motifs. PLoS One 5: el5388.
Woodward, J.J., A.T. Iavarone & D.A. Portnoy, (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703-1705.
Wu, H.Y., PC. Chung, H.W. Shin, S.R. Wen & E.M. Lai, (2008) Secretome analysis uncovers an Hep-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J Bacteriol 190:2841-2850.
Wu, J.X., L.J. Sun, X. Chen, F.H. Du, H.P. Shi, C. Chen & Z.J.J. Chen, (2013) Cyclic GMP-AMP Is an Endogenous Second Messenger in Innate Immune Signaling by Cytosolic DNA. Science 339: 826-830.
Yin, Q., Y. Tian, V. Kabaleeswaran, X. Jiang, D. Tu, M.J. Eck, Z.J. Chen & H. Wu, (2012) Cyclic di-GMP sensing via the innate immune signaling protein STING Mol Cell 46:735-745.
Yum, S., M.J. Kim, Y. Xu, X.L. Jin, H.Y. Yoo, J.W Park, J.H. Gong, K.M. Choe, B.L. Lee & N.C. Ha, (2009) Structural basis for the recognition of lysozyme by MliC, a periplasmic lysozyme inhibitor in Gram-negative bacteria. Biochem Biophys Res Commun 378:244-248.
Zechel, D.L.& S.G Withers, (2000) Glycosidase mechanisms:anatomy of a finely tuned catalyst. Ace Chem Res 33:11-18.
Zhang, H., Z.Q. Gao, W.J. Wang, GF. Liu, J.H. Xu, X.D. Su & Y.H. Dong, (2013a) Structure of the type VI effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein. JBiol Chem 288:5928-5939.
Zhang, X., H. Shi, J. Wu, L. Sun, C. Chen & Z.J. Chen, (2013b) Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell 51: 226-235.
Zhang, Z., B. Yuan, M. Bao, N. Lu, T. Kim & YJ. Liu, (2011) The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12:959-965.
Zheng, J., B. Ho & J.J. Mekalanos, (2011) Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS One 6:e23876.