细菌Lon蛋白酶研究进展
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摘要
Lon蛋白酶是首个被鉴定的ATP依赖蛋白酶家族成员,在原核生物中发挥着降解错误折叠蛋白、维持胞内蛋白质平衡的作用。最近研究表明Lon蛋白还可以作为压力应激蛋白,参与降解多种转录调控因子和二元调控系统,改变细菌胞内的生理代谢过程以适应环境的改变。本文从Lon蛋白酶的结构、功能与上下游调控网络作一综述,旨在更全面清楚地了解ATP依赖蛋白酶的生理功能,以期为其胞内调控机制研究提供参考。
Lon protease is the first identified ATP-dependent protease that plays critical role in degrading misfolded proteins and maintaining intracellular protein balance in prokaryotes. Recent studies have suggested that, as a pressure-stress protein, Lon was involved in the degradation of a variety of transcription regulators and two-component regulatory system in bacteria, resulting in altered physiologically metabolic process of bacteria cells to adapt to the environment change. In this paper, the structure, function, and up and down-stream regulatory network of bacterial Lon protease are reviewed, aiming at enhancing understanding in the physiological function of Lon, as well as providing basis for elucidating the mechanism of intracellular regulation.
Lon protease is the first identified ATP-dependent protease that plays critical role in degrading misfolded proteins and maintaining intracellular protein balance in prokaryotes. Recent studies have suggested that, as a pressure-stress protein, Lon was involved in the degradation of a variety of transcription regulators and two-component regulatory system in bacteria, resulting in altered physiologically metabolic process of bacteria cells to adapt to the environment change. In this paper, the structure, function, and up and down-stream regulatory network of bacterial Lon protease are reviewed, aiming at enhancing understanding in the physiological function of Lon, as well as providing basis for elucidating the mechanism of intracellular regulation.
引文
[1]Swamy KHS,Goldberg AL.E.coli contains eight soluble proteolytic activities,one being ATP dependent[J].Nature,1981,292(5824):652-654
[2]Gur E.The Lon AAA+protease[A]//Dougan D.Regulated Proteolysis in Microorganisms[M].Dordrecht:Springer,2013,66:35-51
[3]Tsilibaris V,Maenhaut-Michel G,van Melderen L.Biological roles of the Lon ATP-dependent protease[J].Research in Microbiology,2006,157(8):701-713
[4]van Melderen L,Aertsen A.Regulation and quality control by Lon-dependent proteolysis[J].Research in Microbiology,2009,160(9):645-651
[5]Lee JH,Ancona V,Zhao YF.Lon protease modulates virulence traits in Erwinia amylovora by direct monitoring of major regulators and indirectly through the Rcs and Gac-Csr regulatory systems[J].Molecular Plant Pathology,2018,19(4):827-840
[6]Nicoloff H,Andersson DI.Lon protease inactivation,or translocation of the lon gene,potentiate bacterial evolution to antibiotic resistance[J].Molecular Microbiology,2013,90(6):1233-1248
[7]Breidenstein EBM,Hancock REW.Armand-Frappier outstanding student award-role of ATP-dependent proteases in antibiotic resistance and virulence[J].Canadian Journal of Microbiology,2013,59(1):1-8
[8]Inoue M,Fukui K,Fujii Y,et al.The Lon protease-like domain in the bacterial RecA paralog RadA is required for DNA binding and repair[J].The Journal of Biological Chemistry,2017,292(23):9801-9814
[9]Vieux EF,Wohlever ML,Chen JZ,et al.Distinct quaternary structures of the AAA+Lon protease control substrate degradation[J].Proceedings of the National Academy of Sciences of the United States of America,2013,110(22):E2002-E2008
[10]Lin CC,Su SC,Su MY,et al.Structural insights into the allosteric operation of the lon AAA+protease[J].Structure,2016,24(5):667-675
[11]Wohlever ML,Baker TA,Sauer RT.Roles of the N domain of the AAA+Lon protease in substrate recognition,allosteric regulation and chaperone activity[J].Molecular Microbiology,2014,91(1):66-78
[12]Zhou XF,Teper D,Andrade MO,et al.A phosphorylation switch on Lon protease regulates bacterial type III secretion system in host[J].mBio,2018,9(1):e02146-17
[13]Su SC,Stephens BB,Alexandre G,et al.Lon protease of theα-proteobacterium Agrobacterium tumefaciens is required for normal growth,cellular morphology and full virulence[J].Microbiology,2006,152(4):1197-1207
[14]Tu IF,Liao JH,Yang FL,et al.Lon protease affects the RdxAnitroreductase activity and metronidazole susceptibility in Helicobacter pylori[J].Helicobacter,2014,19(5):356-366
[15]Breidenstein EBM,Janot L,Strehmel J,et al.The Lon protease is essential for full virulence in Pseudomonas aeruginosa[J].PLoSOne,2012,7(11):e49123
[16]Xie F,Li G,Zhang YH,et al.The Lon protease homologue LonA,not LonC,contributes to the stress tolerance and biofilm formation of Actinobacillus pleuropneumoniae[J].Microbial Pathogenesis,2016,93:38-43
[17]Pressler K,Vorkapic D,Lichtenegger S,et al.AAA+proteases and their role in distinct stages along the Vibrio cholerae lifecycle[J].International Journal of Medical Microbiology,2016,306(6):452-462
[18]Fernández L,Breidenstein EB,Taylor PK,et al.Interconnection of post-transcriptional regulation:The RNA-binding protein Hfq is a novel target of the Lon protease in Pseudomonas aeruginosa[J].Scientific Reports,2016,6:26811
[19]Mukherjee S,Bree AC,Liu J,et al.Adaptor-mediated Lon proteolysis restricts Bacillus subtilis hyperflagellation[J].Proceedings of the National Academy of Sciences of the United States of America,2015,112(1):250-255
[20]Lalsiamthara J,Lee JH.Virulence associated genes-deleted Salmonella montevideo is attenuated,highly immunogenic and confers protection against virulent challenge in chickens[J].Frontiers in Microbiology,2016,7:1634
[21]Rogers A,Townsley L,Gallego-Hernandez AL,et al.The LonAprotease regulates biofilm formation,motility,virulence,and the type VI secretion system in Vibrio cholerae[J].Journal of Bacteriology,2016,198(6):973-985
[22]Bhaskarla C,Das M,Verma T,et al.Roles of Lon protease and its substrate MarA during sodium salicylate-mediated growth reduction and antibiotic resistance in Escherichia coli[J].Microbiology,2016,162(5):764-776
[23]Nishii W,Maruyama T,Matsuoka R,et al.The unique sites in SulA protein preferentially cleaved by ATP-dependent Lon protease from Escherichia coli[J].European Journal of Biochemistry,2002,269(2):451-457
[24]Nazir A,Harinarayanan R.Inactivation of cell division protein FtsZ by SulA makes Lon indispensable for the viability of a ppGpp0 strain of Escherichia coli[J].Journal of Bacteriology,2015,198(4):688-700
[25]Heuveling J,Possling A,Hengge R.A role for Lon protease in the control of the acid resistance genes of Escherichia coli[J].Molecular Microbiology,2008,69(2):534-547
[26]Kim H,Lee H,Shin D.Lon-mediated proteolysis of the FeoCprotein prevents Salmonella enterica from accumulating the Fe(II)transporter FeoB under high-oxygen conditions[J].Journal of Bacteriology,2015,197(1):92-98
[27]Jonas K,Liu J,Chien P,et al.Proteotoxic stress induces a cell-cycle arrest by stimulating Lon to degrade the replication initiator DnaA[J].Cell,2013,154(3):623-636
[28]Arends J,Griego M,Thomanek N,et al.An integrated proteomic approach uncovers novel substrates and functions of the Lon protease in Escherichia coli[J].Proteomics,2018,18(13):1800080
[29]Riethdorf S,V?lker U,Gerth U,et al.Cloning,nucleotide sequence,and expression of the Bacillus subtilis lon gene[J].Journal of Bacteriology,1994,176(21):6518-6527
[30]Sobczyk A,Bellier A,Viala J,et al.The lon gene,encoding an ATP-dependent protease,is a novel member of the HAIR/HspRstress-response regulon in actinomycetes[J].Microbiology,2002,148(6):1931-1937
[31]Robertson GT,Kovach ME,Allen CA,et al.The Brucella abortus Lon functions as a generalized stress response protease and is required for wild-type virulence in BALB/c mice[J].Molecular Microbiology,2000,35(3):577-588
[32]Tojo N,Inouye S,Komano T.Cloning and nucleotide sequence of the Myxococcus xanthus lon gene:indispensability of lon for vegetative growth[J].Journal of Bacteriology,1993,175(8):2271-2277
[33]Schumann W.Regulation of bacterial heat shock stimulons[J].Cell Stress and Chaperones,2016,21(6):959-968
[34]Liu YF,Dong H,Peng XW,et al.RNA-seq reveals the critical role of Lon protease in stress response and Brucella virulence[J].Microbial Pathogenesis,2019,130:112-119
[2]Gur E.The Lon AAA+protease[A]//Dougan D.Regulated Proteolysis in Microorganisms[M].Dordrecht:Springer,2013,66:35-51
[3]Tsilibaris V,Maenhaut-Michel G,van Melderen L.Biological roles of the Lon ATP-dependent protease[J].Research in Microbiology,2006,157(8):701-713
[4]van Melderen L,Aertsen A.Regulation and quality control by Lon-dependent proteolysis[J].Research in Microbiology,2009,160(9):645-651
[5]Lee JH,Ancona V,Zhao YF.Lon protease modulates virulence traits in Erwinia amylovora by direct monitoring of major regulators and indirectly through the Rcs and Gac-Csr regulatory systems[J].Molecular Plant Pathology,2018,19(4):827-840
[6]Nicoloff H,Andersson DI.Lon protease inactivation,or translocation of the lon gene,potentiate bacterial evolution to antibiotic resistance[J].Molecular Microbiology,2013,90(6):1233-1248
[7]Breidenstein EBM,Hancock REW.Armand-Frappier outstanding student award-role of ATP-dependent proteases in antibiotic resistance and virulence[J].Canadian Journal of Microbiology,2013,59(1):1-8
[8]Inoue M,Fukui K,Fujii Y,et al.The Lon protease-like domain in the bacterial RecA paralog RadA is required for DNA binding and repair[J].The Journal of Biological Chemistry,2017,292(23):9801-9814
[9]Vieux EF,Wohlever ML,Chen JZ,et al.Distinct quaternary structures of the AAA+Lon protease control substrate degradation[J].Proceedings of the National Academy of Sciences of the United States of America,2013,110(22):E2002-E2008
[10]Lin CC,Su SC,Su MY,et al.Structural insights into the allosteric operation of the lon AAA+protease[J].Structure,2016,24(5):667-675
[11]Wohlever ML,Baker TA,Sauer RT.Roles of the N domain of the AAA+Lon protease in substrate recognition,allosteric regulation and chaperone activity[J].Molecular Microbiology,2014,91(1):66-78
[12]Zhou XF,Teper D,Andrade MO,et al.A phosphorylation switch on Lon protease regulates bacterial type III secretion system in host[J].mBio,2018,9(1):e02146-17
[13]Su SC,Stephens BB,Alexandre G,et al.Lon protease of theα-proteobacterium Agrobacterium tumefaciens is required for normal growth,cellular morphology and full virulence[J].Microbiology,2006,152(4):1197-1207
[14]Tu IF,Liao JH,Yang FL,et al.Lon protease affects the RdxAnitroreductase activity and metronidazole susceptibility in Helicobacter pylori[J].Helicobacter,2014,19(5):356-366
[15]Breidenstein EBM,Janot L,Strehmel J,et al.The Lon protease is essential for full virulence in Pseudomonas aeruginosa[J].PLoSOne,2012,7(11):e49123
[16]Xie F,Li G,Zhang YH,et al.The Lon protease homologue LonA,not LonC,contributes to the stress tolerance and biofilm formation of Actinobacillus pleuropneumoniae[J].Microbial Pathogenesis,2016,93:38-43
[17]Pressler K,Vorkapic D,Lichtenegger S,et al.AAA+proteases and their role in distinct stages along the Vibrio cholerae lifecycle[J].International Journal of Medical Microbiology,2016,306(6):452-462
[18]Fernández L,Breidenstein EB,Taylor PK,et al.Interconnection of post-transcriptional regulation:The RNA-binding protein Hfq is a novel target of the Lon protease in Pseudomonas aeruginosa[J].Scientific Reports,2016,6:26811
[19]Mukherjee S,Bree AC,Liu J,et al.Adaptor-mediated Lon proteolysis restricts Bacillus subtilis hyperflagellation[J].Proceedings of the National Academy of Sciences of the United States of America,2015,112(1):250-255
[20]Lalsiamthara J,Lee JH.Virulence associated genes-deleted Salmonella montevideo is attenuated,highly immunogenic and confers protection against virulent challenge in chickens[J].Frontiers in Microbiology,2016,7:1634
[21]Rogers A,Townsley L,Gallego-Hernandez AL,et al.The LonAprotease regulates biofilm formation,motility,virulence,and the type VI secretion system in Vibrio cholerae[J].Journal of Bacteriology,2016,198(6):973-985
[22]Bhaskarla C,Das M,Verma T,et al.Roles of Lon protease and its substrate MarA during sodium salicylate-mediated growth reduction and antibiotic resistance in Escherichia coli[J].Microbiology,2016,162(5):764-776
[23]Nishii W,Maruyama T,Matsuoka R,et al.The unique sites in SulA protein preferentially cleaved by ATP-dependent Lon protease from Escherichia coli[J].European Journal of Biochemistry,2002,269(2):451-457
[24]Nazir A,Harinarayanan R.Inactivation of cell division protein FtsZ by SulA makes Lon indispensable for the viability of a ppGpp0 strain of Escherichia coli[J].Journal of Bacteriology,2015,198(4):688-700
[25]Heuveling J,Possling A,Hengge R.A role for Lon protease in the control of the acid resistance genes of Escherichia coli[J].Molecular Microbiology,2008,69(2):534-547
[26]Kim H,Lee H,Shin D.Lon-mediated proteolysis of the FeoCprotein prevents Salmonella enterica from accumulating the Fe(II)transporter FeoB under high-oxygen conditions[J].Journal of Bacteriology,2015,197(1):92-98
[27]Jonas K,Liu J,Chien P,et al.Proteotoxic stress induces a cell-cycle arrest by stimulating Lon to degrade the replication initiator DnaA[J].Cell,2013,154(3):623-636
[28]Arends J,Griego M,Thomanek N,et al.An integrated proteomic approach uncovers novel substrates and functions of the Lon protease in Escherichia coli[J].Proteomics,2018,18(13):1800080
[29]Riethdorf S,V?lker U,Gerth U,et al.Cloning,nucleotide sequence,and expression of the Bacillus subtilis lon gene[J].Journal of Bacteriology,1994,176(21):6518-6527
[30]Sobczyk A,Bellier A,Viala J,et al.The lon gene,encoding an ATP-dependent protease,is a novel member of the HAIR/HspRstress-response regulon in actinomycetes[J].Microbiology,2002,148(6):1931-1937
[31]Robertson GT,Kovach ME,Allen CA,et al.The Brucella abortus Lon functions as a generalized stress response protease and is required for wild-type virulence in BALB/c mice[J].Molecular Microbiology,2000,35(3):577-588
[32]Tojo N,Inouye S,Komano T.Cloning and nucleotide sequence of the Myxococcus xanthus lon gene:indispensability of lon for vegetative growth[J].Journal of Bacteriology,1993,175(8):2271-2277
[33]Schumann W.Regulation of bacterial heat shock stimulons[J].Cell Stress and Chaperones,2016,21(6):959-968
[34]Liu YF,Dong H,Peng XW,et al.RNA-seq reveals the critical role of Lon protease in stress response and Brucella virulence[J].Microbial Pathogenesis,2019,130:112-119