Stress response in Candida glabrata: Pieces of a fragmented picture

Future Microbiology

Volumn 6, Issue 12, 2011, Pages 1475-1484

  Jandric, Zeljkica ^a,b   Schüller, Christoph ^a,b  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Adhesion; Autophagy; Drug resistance; Fungal infections; Phagocytosis; Stress response

Indexed keywords

4 HYDROXYBENZOIC ACID ESTER; FLUCONAZOLE; GALACTOSE; NITROGEN; PHOSPHATE; PYRROLE DERIVATIVE; SORBIC ACID; TACROLIMUS; THIOREDOXIN PEROXIDASE; THIOREDOXIN REDUCTASE; TRANSCRIPTION FACTOR;

AEROBIC METABOLISM; ANTIFUNGAL RESISTANCE; AUTOPHAGY; AUXOTROPHY; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CANDIDA GLABRATA; CELL FUNCTION; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; DENDRITIC CELL; DRUG ACTIVITY; ENVIRONMENTAL STRESS; FATTY ACID OXIDATION; GENE MUTATION; GENETIC TRANSCRIPTION; GLUCONEOGENESIS; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; HYPEROSMOTIC STRESS; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; INTERNALIZATION; MACROPHAGE; MULTIDRUG RESISTANCE; NEUTROPHIL; NONHUMAN; OSMOLARITY; OXIDATIVE STRESS; PHAGOCYTE; PHAGOLYSOSOME; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; SACCHAROMYCES CEREVISIAE; STRESS; UPREGULATION;

CANDIDA GLABRATA; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 82455175441     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.11.131     Document Type: Review

References (84)

1. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20(1), 133-163 (2007).
2. Castano I, Pan SJ, Zupancic M, Hennequin C, Dujon B, Cormack BP. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol. Microbiol. 55(4), 1246-1258 (2005).
3. Caston-Osorio JJ, Rivero A, Torre-Cisneros J. Epidemiology of invasive fungal infection. Int. J. Antimicrob. Agents 32(Suppl. 2) S103-S109 (2008).
4. Perlroth J, Choi B, Spellberg B. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45(4), 321-346 (2007).
5. Kauffman CA, Vazquez JA, Sobel JD et al. Prospective multicenter surveillance study of funguria in hospitalized patients. The National Institute for Allergy and Infectious Diseases (NIAID) Mycoses Study Group. Clin. Infect. Dis. 30(1), 14-18 (2000).
6. Ruan SY, Hsueh PR. Invasive candidiasis: an overview from Taiwan. J. Formos. Med. Assoc. 108(6), 443-451 (2009).
7. Kaur R, Domergue R, Zupancic ML, Cormack BP. A yeast by any other name: Candida glabrata and its interaction with the host. Curr. Opin. Microbiol. 8(4), 378-384 (2005).
8. Filler SG. Candida-host cell receptor-ligand interactions. Curr. Opin. Microbiol. 9(4), 333-339 (2006).
9. Shahi P, Moye-Rowley WS. Coordinate control of lipid composition and drug transport activities is required for normal multidrug resistance in fungi. Biochim. Biophys. Acta 1794(5), 852-859 (2009).
10. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol. Rev. doi:10.1111/j.1574-6976.2011.00278.x (2011) (Epub ahead of print).
11. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. Adherence and biofilm formation of non-Candida albicans Candida species. Trends Microbiol. 19(5), 241-247 (2011).
12. Dujon B, Sherman D, Fischer G et al. Genome evolution in yeasts. Nature 430(6995), 35-44 (2004).
13. Marcet-Houben M, Gabaldon T. Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 26(1), 5-8 (2010).
14. Calderone RA. Candida and Candidiasis Calderone RA (Ed.). ASM Press Washington DC, USA (2002).
15. Jacobsen ID, Brunke S, Seider K et al. Candida glabrata persistence in mice does not depend on host immunosuppression and is unaffected by fungal amino acid auxotrophy. Infect. Immun. 78(3), 1066-1077 (2010).
16. Tsai HF, Krol AA, Sarti KE, Bennett JE. Candida glabrata PDR1, a transcriptional regulator of a pleiotropic drug resistance network, mediates azole resistance in clinical isolates and petite mutants. Antimicrob. Agents Chemother. 50(4), 1384-1392 (2006).
17. Gulshan K, Schmidt JA, Shahi P, Moye-Rowley WS. Evidence for the bifunctional nature of mitochondrial phosphatidylserine decarboxylase: role in Pdr3-dependent retrograde regulation of PDR5 expression. Mol. Cell Biol. 28(19), 5851-5864 (2008).
18. Paumi CM, Chuk M, Snider J, Stagljar I, Michaelis S. ABC transporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily. Microbiol. Mol. Biol. Rev. 73(4), 577-593 (2009).
19. Vermitsky JP, Edlind TD. Azole resistance in Candida glabrata: coordinate upregulation of multidrug transporters and evidence for a Pdr1-like transcription factor. Antimicrob. Agents Chemother. 48(10), 3773-3781 (2004).
20. Paul S, Schmidt JA, Moye-Rowley WS. Regulation of the CgPdr1 transcription factor from the pathogen Candida glabrata. Eukaryot. Cell 10(2), 187-197 (2011).
21. Caudle KE, Barker KS, Wiederhold NP, Xu L, Homayouni R, Rogers PD. Genomewide expression profile analysis of the Candida glabrata Pdr1 regulon. Eukaryot. Cell 10(3), 373-383 (2011).
22. Ferrari S, Ischer F, Calabrese D et al. Gain of function mutations in CgPDR1 of Candida glabrata not only mediate antifungal resistance but also enhance virulence. PLoS Pathog. 5(1), e1000268 (2009).
23. Ferrari S, Sanguinetti M, De Bernardis F et al. Loss of mitochondrial functions associated with azole resistance in Candida glabrata results in enhanced virulence in mice. Antimicrob. Agents Chemother. 55(5), 1852-1860 (2011).
24. Torelli R, Posteraro B, Ferrari S et al. The ATP-binding cassette transporter-encoding gene CgSNQ2 is contributing to the CgPDR1-dependent azole resistance of Candida glabrata. Mol. Microbiol. 68(1), 186-201 (2008).
25. Vermitsky JP, Earhart KD, Smith WL, Homayouni R, Edlind TD, Rogers PD. Pdr1 regulates multidrug resistance in Candida glabrata: gene disruption and genome-wide expression studies. Mol. Microbiol. 61(3), 704-722 (2006).
26. Sanglard D, Ischer F, Bille J. Role of ATP-binding-cassette transporter genes in high-frequency acquisition of resistance to azole antifungals in Candida glabrata. Antimicrob. Agents Chemother. 45(4), 1174-1183 (2001).
27. Kaur R, Castano I, Cormack BP. Functional genomic analysis of fluconazole susceptibility in the pathogenic yeast Candida glabrata: roles of calcium signaling and mitochondria. Antimicrob Agents Chemother 48(5), 1600-1613 (2004).
28. Batova M, Borecka-Melkusova S, Simockova M, Dzugasova V, Goffa E, Subik J. Functional characterization of the CgPGS1 gene reveals a link between mitochondrial phospholipid homeostasis and drug resistance in Candida glabrata. Curr. Genet 53(5), 313-322 (2008).
29. Gasch AP, Spellman PT, Kao Cm et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11(12), 4241-4257 (2000).
30. Smith DA, Morgan BA, Quinn J. Stress signalling to fungal stress-activated protein kinase pathways. FEMS Microbiol. Lett. 306(1), 1-8 (2010).
31. Enjalbert B, Smith DA, Cornell Mj et al. Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol. Biol. Cell 17(2), 1018-1032 (2006).
32. Chen D, Toone WM, Mata J et al. Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell 14(1), 214-229 (2003).
33. Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, Brown AJ. Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol. Biol. 9, 44 (2009).
34. Chen RE, Thorner J. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1773(8), 1311-1340 (2007).
35. Gregori C, Schüller C, Roetzer A, Schwarzmüller T, Ammerer G, Kuchler K. The high-osmolarity glycerol response pathway in the human fungal pathogen Candida glabrata strain ATCC 2001 lacks a signaling branch that operates in baker's yeast. Eukaryot. Cell 6(9), 1635-1645 (2007).
36. Butler G. Fungal sex and pathogenesis. Clin. Microbiol. Rev. 23(1), 140-159 (2010).
37. Wong S, Fares MA, Zimmermann W, Butler G, Wolfe KH. Evidence from comparative genomics for a complete sexual cycle in the 'asexual' pathogenic yeast Candida glabrata. Genome Biol. 4(2), R10 (2003).
38. Muller H, Hennequin C, Gallaud J, Dujon B, Fairhead C. The asexual yeast Candida glabrata maintains distinct a and alpha haploid mating types. Eukaryot. Cell 7(5), 848-858 (2008).
39. Calcagno AM, Bignell E, Rogers TR, Canedo M, Muhlschlegel FA, Haynes K. Candida glabrata Ste20 is involved in maintaining cell wall integrity and adaptation to hypertonic stress, and is required for wild-type levels of virulence. Yeast 21(7), 557-568 (2004).
40. Görner W, Durchschlag E, Martinez-Pastor Mt et al. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12(4), 586-597 (1998).
41. Görner W, Durchschlag E, Wolf J et al. Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO J. 21(1-2), 135-144 (2002).
42. Durchschlag E, Reiter W, Ammerer G, Schüller C. Nuclear localization destabilizes the stress-regulated transcription factor Msn2. J. Biol. Chem. 279(53), 55425-55432 (2004).
43. Nicholls S, Straffon M, Enjalbert β et al. Msn2-and Msn4-like transcription factors play no obvious roles in the stress responses of the fungal pathogen Candida albicans. Eukaryot. Cell 3(5), 1111-1123 (2004).
44. Ramsdale M, Selway L, Stead D et al. MNL1 regulates weak acid-induced stress responses of the fungal pathogen Candida albicans. Mol. Biol. Cell 19(10), 4393-4403 (2008).
45. Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 6, 130 (2006).
46. Brown AJ, Haynes K, Quinn J. Nitrosative and oxidative stress responses in fungal pathogenicity. Curr. Opin. Microbiol. 12(4), 384-391 (2009).
47. Roos D, Van Bruggen R, Meischl C. Oxidative killing of microbes by neutrophils. Microbes Infect. 5(14), 1307-1315 (2003).
48. Cox GM, Harrison TS, Mcdade HC et al. Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect. Immun. 71(1), 173-180 (2003).
49. Nicola AM, Casadevall A, Goldman DL. Fungal killing by mammalian phagocytic cells. Curr. Opin. Microbiol. 11(4), 313-317 (2008).
50. Segal AW. How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197-223 (2005).
51. Nakagawa Y, Kanbe T, Mizuguchi I. Disruption of the human pathogenic yeast Candida albicans catalase gene decreases survival in mouse-model infection and elevates susceptibility to higher temperature and to detergents. Microbiol. Immunol. 47(6), 395-403 (2003).
52. Roetzer A, Gratz N, Kovarik P, Schüller C. Autophagy supports Candida glabrata survival during phagocytosis. Cell Microbiol. 12(2), 199-216 (2010).
53. Cuellar-Cruz M, Briones-Martin-Del-Campo M, Canas-Villamar I et al. High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot. Cell 7(5), 814-825 (2008).
54. Lee J, Godon C, Lagniel G et al. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem. 274(23), 16040-16046 (1999).
55. Gulshan K, Lee SS, Moye-Rowley WS. Differential oxidant tolerance determined by the key transcription factor Yap1 is controlled by levels of the Yap1-binding protein, Ybp1. J. Biol. Chem. 286(39), 34071-34081 (2011).
56. Delaunay A, Isnard AD, Toledano MB. H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J. 19(19), 5157-5166 (2000).
57. Delaunay A, Pflieger D, Barrault MB, Vinh J, Toledano MB. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111(4), 471-481 (2002).
58. Kuge S, Jones N, Nomoto A. Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J. 16(7), 1710-1720 (1997).
59. He XJ, Fassler JS. Identification of novel Yap1p and Skn7p binding sites involved in the oxidative stress response of Saccharomyces cerevisiae. Mol. Microbiol. 58(5), 1454-1467 (2005).
60. Morgan BA, Banks GR, Toone WM, Raitt D, Kuge S, Johnston LH. The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae. EMBO J. 16(5), 1035-1044 (1997).
61. Mulford KE, Fassler JS. Association of the Skn7 and Yap1 transcription factors in the Saccharomyces cerevisiae oxidative stress response. Eukaryot. Cell 10(6), 761-769 (2011).
62. Kuo D, Licon K, Bandyopadhyay S et al. Coevolution within a transcriptional network by compensatory trans and cis mutations. Genome Res. 20(12), 1672-1678 (2010).
63. Saijo T, Miyazaki T, Izumikawa K et al. Skn7p is involved in oxidative stress response and virulence of Candida glabrata. Mycopathologia 169(2), 81-90 (2010).
64. Roetzer A, Klopf E, Gratz N et al. Regulation of Candida glabrata oxidative stress resistance is adapted to host environment. FEBS Lett. 585(2), 319-327 (2011)
65. Kaur R, Ma B, Cormack BP. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl Acad. Sci. USA 104(18), 7628-7633 (2007).
66. Lorenz MC, Bender JA, Fink GR. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3(5), 1076-1087 (2004).
67. Carlson M. Glucose repression in yeast. Curr. Opin. Microbiol. 2(2), 202-207 (1999).
68. Petter R, Kwon-Chung KJ. Disruption of the SNF1 gene abolishes trehalose utilization in the pathogenic yeast Candida glabrata. Infect. Immun. 64(12), 5269-5273 (1996).
69. Orlova M, Barrett L, Kuchin S. Detection of endogenous Snf1 and its activation state: application to Saccharomyces and Candida species. Yeast 25(10), 745-754 (2008).
70. Roetzer A, Gregori C, Jennings Am et al. Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol. Microbiol. 69(3), 603-620 (2008).
71. Rodaki A, Bohovych IM, Enjalbert β et al. Glucose promotes stress resistance in the fungal pathogen Candida albicans. Mol. Biol. Cell 20(22), 4845-4855 (2009).
72. Calderone RA, Fonzi WA. Virulence factors of Candida albicans. Trends Microbiol. 9(7), 327-335 (2001).
73. Alvarez M, Casadevall A. Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16(21), 2161-2165 (2006).
74. Seider K, Brunke S, Schild L et al. The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J. Immunol. 187(6), 3072-3086 (2011).
75. Klionsky DJ. Cell biology: regulated self-cannibalism. Nature 431(7004), 31-32 (2004).
76. Klionsky DJ. Autophagy. Curr. Biol. 15(8), R282-283 (2005).
77. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9(10), 1102-1109 (2007).
78. Verstrepen KJ, Jansen A, Lewitter F, Fink GR. Intragenic tandem repeats generate functional variability. Nat. Genet. 37(9), 986-990 (2005).
79. Sundstrom P. Adhesion in Candida spp. Cell Microbiol. 4(8), 461-469 (2002).
80. De Groot PW, Kraneveld EA, Yin QY et al. The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot. Cell 7(11), 1951-1964 (2008).
81. Kraneveld EA, De Soet JJ, Deng DM et al. Identification and differential gene expression of adhesin-like wall proteins in Candida glabrata biofilms. Mycopathologia doi:10.1007/ s11046-011-9446-2 (2011) (Epub ahead of print).
82. Domergue R, Castano I, De Las Penas A et al. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308(5723), 866-870 (2005).
83. Mundy RD, Cormack B. Expression of Candida glabrata adhesins after exposure to chemical preservatives. J. Infect. Dis. 199(12), 1891-1898 (2009).
84. Schüller C, Mamnun YM, Mollapour M et al. Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. Mol. Biol. Cell 15(2), 706-720 (2004).