Hgc1-Cdc28–how much does a single protein kinase do in the regulation of hyphal development in Candida albicans?
详细信息    查看全文
  • 作者:Yue Wang
  • 关键词:Candida albicans ; yeast ; to ; hyphae growth transition ; cyclin ; dependent kinase ; polarized growth ; protein phosphorylation
  • 刊名:Journal of Microbiology
  • 出版年:2016
  • 出版时间:March 2016
  • 年:2016
  • 卷:54
  • 期:3
  • 页码:170-177
  • 全文大小:394 KB
  • 参考文献:Banerjee, M., Uppuluri, P., Zhao, X.R., Carlisle, P.L., Vipulanandan, G., Villar, C.C., López-Ribot, J.L., and Kadosh, D. 2013. Expression of UME6, a key regulator of Candida albicans hyphal development, enhances biofilm formation via Hgc1- and Sun41-dependent mechanisms. Eukaryot. Cell 12, 224–232.PubMedCentral CrossRef PubMed
    Bassetti, M., Mikulska, M., and Viscoli, C. 2010. Bench-to-bedside review: therapeutic management of invasive candidiasis in the intensive care unit. Crit. Care 14, 244.PubMedCentral CrossRef PubMed
    Bassilana, M., Hopkins, J., and Arkowitz, R.A. 2005. Regulation of the Cdc42/Cdc24 GTPase module during Candida albicans hyphal growth. Eukaryot. Cell 4, 588–603.PubMedCentral CrossRef PubMed
    Bishop, A., Lane, R., Beniston, R., Chapa-y-Lazo, B., Smythe, C., and Sudbery, E. 2010. Hyphal growth in Candida albicans requires the phosphorylation of Sec2 by the Cdc28-Ccn1/Hgc1 kinase. EMBO J. 29, 2930–2942.PubMedCentral CrossRef PubMed
    Bonhomme, J. and d’Enfert, C. 2013. Candida albicans biofilms: building a heterogeneous, drug-tolerant environment. Curr. Opin. Microbiol. 16, 398–403.CrossRef PubMed
    Braun, B.R. and Johnson, A.D. 1997. Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277, 105–109.CrossRef PubMed
    Braun, B.R., Kadosh, D., and Johnson, A.D. 2001. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20, 4753–4761.PubMedCentral CrossRef PubMed
    Brown, G.D., Denning, D.W., Gow, N.A.R., Stuart, M., Levitz, S.M., Netea, M.G., and White, T.C. 2012. Hidden killers: human fungal infections. Sci. Transl. Med. 4, 1–9.CrossRef
    Bruno, V.M., Wang, Z., Marjani, S.L., Euskirchen, G.M., Martin, J., Sherlock, G., and Snyder, M. 2010. Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res. 20, 1451–1458.PubMedCentral CrossRef PubMed
    Buffo, J., Herman, M.A., and Soll, D.R. 1984. A characterization of pH-regulated dimorphism in Candida albicans. Mycopathologia 85, 21–30.CrossRef PubMed
    Caballero-Lima, D. and Sudbery, P.E. 2014. In Candida albicans, phosphorylation of Exo84 by Cdk1-Hgc1 is necessary for efficient hyphal extension. Mol. Biol. Cell 25, 1097–1110.PubMedCentral CrossRef PubMed
    Calderón-Noreña, D.M., González-Novo, A., Orellana-Muñoz, S., Gutiérrez-Escribano, P., Arnáiz-Pita, Y., Dueñas-Santero, E., Suárez, M.B., Bougnoux, M.E., Del Rey, F., Sherlock, G., et al. 2015. A single nucleotide polymorphism uncovers a novel function for the transcription factor Ace2 during Candida albicans hyphal development. PLoS Genet. 11, e1005152.PubMedCentral CrossRef PubMed
    Carlisle, P.L. and Kadosh, D. 2010. Candida albicans Ume6, a filament- specific transcriptional regulator, directs hyphal growth via a pathway involving Hgc1 cyclin-related protein. Eukaryot. Cell 9, 1320–1328.PubMedCentral CrossRef PubMed
    Chao, C.C., Hsu, P.C., Jen, C.F., Chen, I.H., Wang, C.H., Chan, H.C., Tsai, P.W., Tung, K.C., Wang, C.H., Lan, C.Y., et al. 2010. Zebrafish as a model host for Candida albicans infection. Infect. Immun. 78, 2512–2521.PubMedCentral CrossRef PubMed
    Court, H. and Sudbery, P.E. 2007. Regulation of Cdc42 GTPase activity in the formation of hyphae in Candida albicans. Mol. Biol. Cell 18, 265–281.PubMedCentral CrossRef PubMed
    Crampin, H., Finley, K., Gerami-Nejad, M., Court, H., Gale, C., Berman, J., and Sudbery, P. 2005. Candida albicans hyphae have a Spitzenkörper that is distinct from the polarisome found in yeast and pseudohyphae. J. Cell Sci. 118, 2935–2947.CrossRef PubMed
    Etienne-Manneville, S. 2004. Cdc42—the centre of polarity. J. Cell Sci. 117, 1291–1300.CrossRef PubMed
    Evangelista, M., Blundell, K., Longtine, M.S., Chow, C.J., Adames, N., Pringle, J.R., Peter, M., and Boone, C. 1997. Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276, 118–122.CrossRef PubMed
    Fung, K.Y., Dai, L., and Trimble, W.S. 2014. Cell and molecular biology of septins. Int. Rev. Cell Mol. Biol. 310, 289–339.CrossRef PubMed
    González-Novo, A., Correa-Bordes, J., Labrador, L., Sánchez, M., Vázquez de Aldana, C.R., and Jiménez, J. 2008. Sep7 is essential to modify septin ring dynamics and inhibit cell separation during Candida albicans hyphal growth. Mol. Biol. Cell 19, 1509–1518.PubMedCentral CrossRef PubMed
    Guan, G., Xie, J., Tao, L., Nobile, C.J., Sun, Y., Cao, C., Tong, Y., and Huang, G. 2013. Bcr1 plays a central role in the regulation of opaque cell filamentation in Candida albicans. Mol. Microbiol. 89, 732–750.PubMedCentral CrossRef PubMed
    Hsu, S.C., Hazuka, C.D., Roth, R., Foletti, D.L., Heuser, J., and Scheller, R.H. 1998. Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments. Neuron 20, 1111–1122.CrossRef PubMed
    Huang, Z.X., Wang, H., Wang, Y.M., and Wang, Y. 2014. Novel mechanism coupling cyclic AMP-protein kinase A signaling and Golgi trafficking via Gyp1 phosphorylation in polarized growth. Eukaryot. Cell 13, 1548–1556.PubMedCentral CrossRef PubMed
    Hutagalung, A.H. and Novick, P.J. 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91, 119–149.PubMedCentral CrossRef PubMed
    Inglis D.O., Arnaud, M.B., Binkley, J., Shah, P., Skrzypek, M.S., Wymore, F., Binkley, G., Miyasato, S.R., Simison, M., and Sherlock, G. 2012. The Candida Genome Database incorporates multiple Candida species: multispecies search and analysis tools with curated gene and protein information for Candida albicans and Candida glabrata. Nucleic Acids Res. 40(Database issue), D667–674.PubMedCentral CrossRef PubMed
    Johnson, A. 2005. The biology of mating in Candida albicans. Nat. Rev. Microbiol. 1, 106–116.CrossRef
    Kadosh, D. and Johnson, A.D. 2005. Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16, 2903–2912.PubMedCentral CrossRef PubMed
    Klengel, T., Liang, W.J., Chaloupka, J., Ruoff, C., Schröppel, K., Naglik, J.R., Eckert, S.E., Mogensen, E.G., Haynes, K., Tuite, M.F., et al. 2005. Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr. Biol. 15, 2021–2026.PubMedCentral CrossRef PubMed
    Knaus, M., Pelli-Gulli, M.P., van Drogen, F., Springer, S., Jaquenoud, M., and Peter, M. 2007. Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence. EMBO J. 26, 4501–4513.PubMedCentral CrossRef PubMed
    Lew, D.J. and Reed, S. 1993. Morphogenesis in the yeast cell cycle, regulation by Cdc28 and cyclins. J. Cell Biol. 120, 1305–1320.CrossRef PubMed
    Lew, D.J. and Reed, S.I. 1995. Cell cycle control of morphogenesis in budding yeast. Curr. Opin. Genet. Dev. 5, 17–23.CrossRef PubMed
    Li, C.R., Lee, R.T., Wang, Y.M., Zheng, X.D., and Wang, Y. 2007. Candida albicans hyphal morphogenesis occurs in Sec3p-independent and Sec3p-dependent phases separated by septin ring formation. J. Cell Sci. 120, 1898–1907.CrossRef PubMed
    Li, C.R., Wang, Y.M., De Zheng, X., Liang, H.Y., Tang, J.C., and Wang, Y. 2005. The formin family protein CaBni1p has a role in cell polarity control during both yeast and hyphal growth in Candida albicans. J. Cell Sci. 118, 2637–2648.CrossRef PubMed
    Lin, C.H., Kabrawala, S., Fox, E.P., Nobile, C.J., Johnson, A.D., and Bennett, R.J. 2013. Genetic control of conventional and pheromone-stimulated biofilm formation in Candida albicans. PLoS Pathog. 9, e1003305.PubMedCentral CrossRef PubMed
    Lu, Y., Su, C., and Liu, H. 2014. Candida albicans hyphal initiation and elongation. Trends Microbiol. 22, 707–714.PubMedCentral CrossRef PubMed
    Lu, Y., Su, C., Wang, A., and Liu, H. 2011. Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance. PLoS Biol. 9, e1001105.PubMedCentral CrossRef PubMed
    Mathé, L. and Van Dijck, P. 2013. Recent insights into Candida albicans biofilm resistance mechanisms. Curr. Genet. 59, 251–264.PubMedCentral CrossRef PubMed
    Murad, A.M., d’Enfert, C., Gaillardin, C., Tournu, H., Tekaia, F., Talibi, D., Marechal, D., Marchais, V., Cottin, J., and Brown, A.J. 2001. Transcript profiling in Candida albicans reveals new cellular functions for the transcriptional repressors CaTup1, CaMig1 and CaNrg1. Mol. Microbiol. 42, 981–993.CrossRef PubMed
    Naglik, J.R., Challacombe, S.J., and Hube, B. 2003. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 67, 400–428.PubMedCentral CrossRef PubMed
    Nagy, G., Hennig, G.W., Petrenyi, K., Kovacs, L., Pocsi, I., Dombradi, V., and Banfalvi, G. 2014. Time-lapse video microscopy and image analysis of adherence and growth patterns of Candida albicans strains. Appl. Microbiol. Biotechnol. 98, 5185–5194.CrossRef PubMed
    Nantel, A., Dignard, D., Bachewich, C., Harcus, D., Marcil, A., Bouin, A.P., Sensen, C.W., Hogues, H., van het Hoog, M., Gordon, P., et al. 2002. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13, 3452–3465.PubMedCentral CrossRef PubMed
    Nurse, P. 2002. Cyclin dependent kinases and cell cycle control (Nobel lecture). Chembiochem 3, 596–603.CrossRef PubMed
    Ortiz, D., Medkova, M., Walch-Solimena, C., and Novick, P. 2002. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J. Cell Biol. 157, 1005–1015.PubMedCentral CrossRef PubMed
    Park, H.O. and Bi, E. 2007. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71, 48–96.PubMedCentral CrossRef PubMed
    Pulver, R., Heisel, T., Gonia, S., Robins, R., Norton, J., Haynes, P., and Gale, C.A. 2013. Rsr1 focuses Cdc42 activity at hyphal tips and promotes maintenance of hyphal development in Candida albicans. Eukaryot. Cell 12, 482–495.PubMedCentral CrossRef PubMed
    Ramanan, N. and Wang, Y. 2000. A High-affinity iron permease essential for Candida albicans virulence. Science 288, 1062–1064.CrossRef PubMed
    Schaekel, A., Desai, P.R., and Ernst, J.F. 2013. Morphogenesis-regulated localization of protein kinase A to genomic sites in Candida albicans. BMC Genomics 14, 842.PubMedCentral CrossRef PubMed
    Si, H., Hernday, A.D., Hirakawa, M.P., Johnson, A.D., and Bennett, R.J. 2013. Candida albicans white and opaque cells undergo distinct programs of filamentous growth. PLoS Pathog. 9, e1003210.PubMedCentral CrossRef PubMed
    Simonetti, N., Strippoli, V., and Cassone, A. 1974. Yeast-mycelial conversion induced by N-acetyl-D-glucosamine in Candida albicans. Nature 250, 344–346.CrossRef PubMed
    Sinha, I., Wang, Y.M., Philp, R., Li, C.R., Yap, W.H., and Wang, Y. 2007. Cyclin-dependent kinases control septin phosphorylation in Candida albicans hyphal development. Dev. Cell 13, 421–432.CrossRef PubMed
    Sopko, R., Huang, D., Smith, J.C., Figeys, D., and Andrews, B.J. 2007. Activation of the Cdc42p GTPase by cyclin-dependent protein kinases in budding yeast. EMBO J. 26, 4487–4500.PubMedCentral CrossRef PubMed
    Staab, J.F., Bradway, S.D., Fidel, P.L., and Sundstrom, P. 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283, 1535–1538.CrossRef PubMed
    Stoldt, V.R., Sonneborn, A., Leuker, C.E., and Ernst, J.F. 1997. Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J. 16, 1982–1991.PubMedCentral CrossRef PubMed
    Sudbery, P.E. 2001. The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localization. Mol. Microbiol. 41, 19–31.CrossRef PubMed
    Sudbery, P.E. 2011. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9, 737–748.CrossRef PubMed
    Sudbery, P., Gow, N., and Berman, J. 2004. The distinct morphogenic states of Candida albicans. Trends Microbiol. 12, 317–324.CrossRef PubMed
    Taschdjian, C.L., Burchall, J.J., and Kozinn, P.J. 1960. Rapid identification of Candida albicans by filamentation on serum and serum substitutes. AMA J. Dis. Child 99, 212–215.PubMed
    Wang, Y. 2009. CDKs and the yeast-hyphal decision. Curr. Opin. Microbiol. 12, 644–649.CrossRef PubMed
    Wang, Y. 2013. Fungal adenylyl cyclase acts as a signal sensor and integrator and plays a central role in interaction with bacteria. PLoS Pathog. 9, e1003612.PubMedCentral CrossRef PubMed
    Wang, A., Lane, S., Tian, Z., Sharon, A., Hazan, I., and Liu, H. 2007. Temporal and spatial control of HGC1 expression results in Hgc1 localization to the apical cells of hyphae in Candida albicans. Eukaryot. Cell 6, 253–261.PubMedCentral CrossRef PubMed
    Wang, A., Raniga, P.P., Lane, S., Lu, Y., and Liu, H. 2009. Hyphal chain formation in Candida albicans: Cdc28-Hgc1 phosphorylation of Efg1 represses cell separation genes. Mol. Biol. Cell 29, 4406–4416.CrossRef
    Wang, Y. and Xu, X.L. 2008. Bacterial peptidoglycan-derived molecules activate Candida albicans hyphal growth. Commun. Integr. Biol. 1, 137–139.PubMedCentral CrossRef PubMed
    Warenda, A.J. and Konopka, J.B. 2002. Septin function in Candida albicans morphogenesis. Mol. Biol. Cell 13, 2732–2746.PubMedCentral CrossRef PubMed
    Weiss, E.L. 2012. Mitotic exit and separation of mother and daughter cells. Genetics 192, 1165–1202.PubMedCentral CrossRef PubMed
    Whiteway, M. 2000. Transcriptional control of cell type and morphogenesis in Candida albicans. Curr. Opin. Microbiol. 3, 582–588.CrossRef PubMed
    Wilson, D. and Hube, B. 2010. Hgc1 mediates dynamic Candida albicans-endothelium adhesion events during circulation. Eukaryot. Cell 9, 278–287.PubMedCentral CrossRef PubMed
    Xu, X.L., Lee, R.T., Fang, H.M., Wang, Y.M., Li, R., Zou, H., Zhu, Y., and Wang, Y. 2008. Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host Microbe 4, 28–39.CrossRef PubMed
    Xue, J., Tsang, C.W., Gai, W.P., Malladi, C.S., Trimble, W.S., Rostas, J.A., and Robinson, P.J. 2004. Septin 3 (G-septin) is a developmentally regulated phosphoprotein enriched in presynaptic nerve terminals. J. Neurochem. 91, 579–590.CrossRef PubMed
    Zeng, G.S., Wang, Y.M., and Wang, Y. 2012. Cdc28–Cln3 regulates actin-mediated endocytosis by targeting Sla1 in different modes of fungal growth. Mol. Biol. Cell 23, 3485–3497.PubMedCentral CrossRef PubMed
    Zheng, X.D., Lee, R.T., Wang, Y.M., Lin, Q.S., and Wang, Y. 2007. Phosphorylation of Rga2, a Cdc42 GAP, by CDK/Hgc1 is crucial for Candida albicans hyphal growth. EMBO J. 26, 3760–3769.PubMedCentral CrossRef PubMed
    Zheng, X., Wang, Y., and Wang, Y. 2004. Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J. 23, 1845–1856.PubMedCentral CrossRef PubMed
  • 作者单位:Yue Wang (1)

    1. Candida albicans Biology Laboratory, Institute of Molecular and Cell Biology, Agency for Science, Technology, and Research, and Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
  • 刊物主题:Microbiology;
  • 出版者:Springer Netherlands
  • ISSN:1976-3794
文摘
The fungal human pathogen Candida albicans can cause invasive infection with high mortality rates. A key virulence factor is its ability to switch between three morphologies: yeast, pseudohyphae and hyphae. In contrast to the ovalshaped unicellular yeast cells, hyphae are highly elongated, tube-like, and multicellular. A long-standing question is what coordinates all the cellular machines to construct cells with distinct shapes. Hyphal-specific genes (HSGs) are thought to hold the answer. Among the numerous HSGs found, only UME6 and HGC1 are required for hyphal development. UME6 encodes a transcription factor that regulates many HSGs including HGC1. HGC1 encodes a G1 cyclin which partners with the Cdc28 cyclin-dependent kinase. Hgc1-Cdc28 simultaneously phosphorylates and regulates multiple substrates, thus controlling multiple cellular apparatuses for morphogenesis. This review is focused on major progresses made in the past decade on Hgc1’s roles and regulation in C. albicans hyphal development and other traits important for infection.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700