Synergistic regulation of hyphal elongation by hypoxia, CO2, and nutrient conditions controls the virulence of Candida albicans

Cell Host and Microbe

Volumn 14, Issue 5, 2013, Pages 499-509

  Lu, Yang ^a   Su, Chang ^a   Solis, Norma V ^b   Filler, Scott G ^b,c   Liu, Haoping ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARBOR UCLA MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; OFD1 PROTEIN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UME6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANDIDA ALBICANS; CELL HYPOXIA; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMMENSAL; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE EXPRESSION; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR EVOLUTION; MUTANT; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION ELONGATION;

ANOXIA; CANDIDA ALBICANS; CARBON DIOXIDE; FOOD; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; SIGNAL TRANSDUCTION; VIRULENCE;

EID: 84887860497     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.10.008     Document Type: Article

References (42)

1. R.S. Almeida, S. Brunke, A. Albrecht, S. Thewes, M. Laue, J.E. Edwards, S.G. Filler, and B. Hube The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin PLoS Pathog. 4 2008 e1000217
2. M. Banerjee, D.S. Thompson, A. Lazzell, P.L. Carlisle, C. Pierce, C. Monteagudo, J.L. López-Ribot, and D. Kadosh UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence Mol. Biol. Cell 19 2008 1354 1365
3. F. Cao, S. Lane, P.P. Raniga, Y. Lu, Z. Zhou, K. Ramon, J. Chen, and H. Liu The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans Mol. Biol. Cell 17 2006 295 307
4. P.L. Carlisle, M. Banerjee, A. Lazzell, C. Monteagudo, J.L. López-Ribot, and D. Kadosh Expression levels of a filament-specific transcriptional regulator are sufficient to determine Candida albicans morphology and virulence Proc. Natl. Acad. Sci. USA 106 2009 599 604
5. Y.C. Chang, C.M. Bien, H. Lee, P.J. Espenshade, and K.J. Kwon-Chung Sre1p, a regulator of oxygen sensing and sterol homeostasis, is required for virulence in Cryptococcus neoformans Mol. Microbiol. 64 2007 614 629
6. C. Chen, K. Pande, S.D. French, B.B. Tuch, and S.M. Noble An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis Cell Host Microbe 10 2011 118 135
7. C.D. Chun, O.W. Liu, and H.D. Madhani A link between virulence and homeostatic responses to hypoxia during infection by the human fungal pathogen Cryptococcus neoformans PLoS Pathog. 3 2007 e22
8. I.A. Cleary, A.L. Lazzell, C. Monteagudo, D.P. Thomas, and S.P. Saville BRG1 and NRG1 form a novel feedback circuit regulating Candida albicans hypha formation and virulence Mol. Microbiol. 85 2012 557 573
9. 2 sensing pathway in yeast PLoS Pathog. 8 2012 e1002485
10. H. Du, G. Guan, J. Xie, F. Cottier, Y. Sun, W. Jia, F.A. Mühlschlegel, and G. Huang The transcription factor Flo8 mediates CO2 sensing in the human fungal pathogen Candida albicans Mol. Biol. Cell 23 2012 2692 2701
11. H. Du, G. Guan, J. Xie, Y. Sun, Y. Tong, L. Zhang, and G. Huang Roles of Candida albicans Gat2, a GATA-type zinc finger transcription factor, in biofilm formation, filamentous growth and virulence PLoS ONE 7 2012 e29707
12. R. Dumitru, J.M. Hornby, and K.W. Nickerson Defined anaerobic growth medium for studying Candida albicans basic biology and resistance to eight antifungal drugs Antimicrob. Agents Chemother. 48 2004 2350 2354
13. J.F. Ernst, and D. Tielker Responses to hypoxia in fungal pathogens Cell. Microbiol. 11 2009 183 190
14. N. Grahl, and R.A. Cramer Jr. Regulation of hypoxia adaptation: an overlooked virulence attribute of pathogenic fungi? Med. Mycol. 48 2010 1 15
15. N. Grahl, K.M. Shepardson, D. Chung, and R.A. Cramer Hypoxia and fungal pathogenesis: to air or not to air? Eukaryot. Cell 11 2012 560 570
16. J. Henri, D. Rispal, E. Bayart, H. van Tilbeurgh, B. Séraphin, and M. Graille Structural and functional insights into Saccharomyces cerevisiae Tpa1, a putative prolylhydroxylase influencing translation termination and transcription J. Biol. Chem. 285 2010 30767 30778
17. B.T. Hughes, and P.J. Espenshade Oxygen-regulated degradation of fission yeast SREBP by Ofd1, a prolyl hydroxylase family member EMBO J. 27 2008 1491 1501
18. A.L. Hughes, B.L. Todd, and P.J. Espenshade SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast Cell 120 2005 831 842
19. K.M. Keeling, J. Salas-Marco, L.Z. Osherovich, and D.M. Bedwell Tpa1p is part of an mRNP complex that influences translation termination, mRNA deadenylation, and mRNA turnover in Saccharomyces cerevisiae Mol. Cell. Biol. 26 2006 5237 5248
20. T. Klengel, W.J. Liang, J. Chaloupka, C. Ruoff, K. Schröppel, J.R. Naglik, S.E. Eckert, E.G. Mogensen, K. Haynes, and M.F. Tuite Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence Curr. Biol. 15 2005 2021 2026
21. H.-J. Lo, J.R. Köhler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G.R. Fink Nonfilamentous C. albicans mutants are avirulent Cell 90 1997 939 949
22. Y. Lu, C. Su, X. Mao, P.P. Raniga, H. Liu, and J. Chen Efg1-mediated recruitment of NuA4 to promoters is required for hypha-specific Swi/Snf binding and activation in Candida albicans Mol. Biol. Cell 19 2008 4260 4272
23. Y. Lu, C. Su, A. Wang, and H. Liu Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance PLoS Biol. 9 2011 e1001105
24. Y. Lu, C. Su, and H. Liu A GATA transcription factor recruits Hda1 in response to reduced Tor1 signaling to establish a hyphal chromatin state in Candida albicans PLoS Pathog. 8 2012 e1002663
25. S. MacPherson, B. Akache, S. Weber, X. De Deken, M. Raymond, and B. Turcotte Candida albicans zinc cluster protein Upc2p confers resistance to antifungal drugs and is an activator of ergosterol biosynthetic genes Antimicrob. Agents Chemother. 49 2005 1745 1752
26. C.J. Nobile, E.P. Fox, J.E. Nett, T.R. Sorrells, Q.M. Mitrovich, A.D. Hernday, B.B. Tuch, D.R. Andes, and A.D. Johnson A recently evolved transcriptional network controls biofilm development in Candida albicans Cell 148 2012 126 138
27. S.M. Noble, S. French, L.A. Kohn, V. Chen, and A.D. Johnson Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity Nat. Genet. 42 2010 590 598
28. A. Ozer, and R.K. Bruick Non-heme dioxygenases: cellular sensors and regulators jelly rolled into one? Nat. Chem. Biol. 3 2007 144 153
29. A.A. Sanchez, D.A. Johnston, C. Myers, J.E. Edwards Jr., A.P. Mitchell, and S.G. Filler Relationship between Candida albicans virulence during experimental hematogenously disseminated infection and endothelial cell damage in vitro Infect. Immun. 72 2004 598 601
30. S.P. Saville, A.L. Lazzell, C. Monteagudo, and J.L. Lopez-Ribot Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection Eukaryot. Cell 2 2003 1053 1060
31. C.J. Schofield, and P.J. Ratcliffe Signalling hypoxia by HIF hydroxylases Biochem. Biophys. Res. Commun. 338 2005 617 626
32. P.M. Silver, B.G. Oliver, and T.C. White Role of Candida albicans transcription factor Upc2p in drug resistance and sterol metabolism Eukaryot. Cell 3 2004 1391 1397
33. C. Stichternoth, A. Fraund, E. Setiadi, L. Giasson, A. Vecchiarelli, and J.F. Ernst Sch9 kinase integrates hypoxia and CO2 sensing to suppress hyphal morphogenesis in Candida albicans Eukaryot. Cell 10 2011 502 511
34. C. Su, Y. Lu, and H. Liu Reduced TOR signaling sustains hyphal development in Candida albicans by lowering Hog1 basal activity Mol. Biol. Cell 24 2013 385 397
35. J.N. Sun, N.V. Solis, Q.T. Phan, J.S. Bajwa, H. Kashleva, A. Thompson, Y. Liu, A. Dongari-Bagtzoglou, M. Edgerton, and S.G. Filler Host cell invasion and virulence mediated by Candida albicans Ssa1 PLoS Pathog. 6 2010 e1001181
36. J. Urban, A. Soulard, A. Huber, S. Lippman, D. Mukhopadhyay, O. Deloche, V. Wanke, D. Anrather, G. Ammerer, and H. Riezman Sch9 is a major target of TORC1 in Saccharomyces cerevisiae Mol. Cell 26 2007 663 674
37. A. Wang, S. Lane, Z. Tian, A. Sharon, I. Hazan, and H. Liu Temporal and spatial control of HGC1 expression results in Hgc1 localization to the apical cells of hyphae in Candida albicans Eukaryot. Cell 6 2007 253 261
38. Z. Weissman, and D. Kornitzer A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization Mol. Microbiol. 53 2004 1209 1220
39. S.D. Willger, S. Puttikamonkul, K.H. Kim, J.B. Burritt, N. Grahl, L.J. Metzler, R. Barbuch, M. Bard, C.B. Lawrence, and R.A. Cramer Jr. A sterol-regulatory element binding protein is required for cell polarity, hypoxia adaptation, azole drug resistance, and virulence in Aspergillus fumigatus PLoS Pathog. 4 2008 e1000200
40. U. Zeidler, T. Lettner, C. Lassnig, M. Müller, R. Lajko, H. Hintner, M. Breitenbach, and A. Bito UME6 is a crucial downstream target of other transcriptional regulators of true hyphal development in Candida albicans FEMS Yeast Res. 9 2009 126 142
41. X. Zheng, Y. Wang, and Y. Wang Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis EMBO J. 23 2004 1845 1856
42. C. Zhu, K.J. Byers, R.P. McCord, Z. Shi, M.F. Berger, D.E. Newburger, K. Saulrieta, Z. Smith, M.V. Shah, and M. Radhakrishnan High-resolution DNA-binding specificity analysis of yeast transcription factors Genome Res. 19 2009 556 566