Differential Response of Candida albicans and Candida glabrata to Oxidative and Nitrosative Stresses

Current Microbiology

Volumn 69, Issue 5, 2014, Pages 733-739

  Cuéllar Cruz, Mayra ^a   López Romero, Everardo ^a   Ruiz Baca, Estela ^b   Zazueta Sandoval, Roberto ^a  

^a UNIVERSITY OF GUANAJUATO   (Mexico)

^b UNIVERSIDAD JUÁREZ DEL ESTADO DE DURANGO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

NITROSO DERIVATIVE; OXIDIZING AGENT;

CANDIDA ALBICANS; CANDIDA GLABRATA; COMPARATIVE STUDY; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

CANDIDA ALBICANS; CANDIDA GLABRATA; METABOLIC NETWORKS AND PATHWAYS; NITROSO COMPOUNDS; OXIDANTS; STRESS, PHYSIOLOGICAL;

EID: 84930983010     PISSN: 03438651     EISSN: 14320991     Source Type: Journal    
DOI: 10.1007/s00284-014-0651-3     Document Type: Review

References (64)

1. Alarco AM, Raymond M (1999) The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J Bacteriol 181:700–708
2. Bhattacharjee A, Majumdar U, Maity D, Sarkar TS, Goswami AM, Sahoo R, Ghosh S (2010) Characterizing the effect of nitrosative stress in Saccharomyces cerevisiae. Arch Biochem Biophys 496:109–116
3. Brown JP, Haynes K, Quinn J (2009) Nitrosative and oxidative stress responses in fungal pathogenicity. Curr Opin Microbiol 12:384–391
4. Calderone RA (2002) Candida and candidiasis. ASM Press, Washington, DC
5. Chauhan N, Latge JP, Calderone R (2006) Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat Rev Microbiol 4:435–444
6. Chaves GM, Bates S, MacCallum DM, Odds FC (2007) Candida albicans GRX2, encoding a putative glutaredoxin, is required for virulence in a murine model. Genet Mol Res 6:1051–1063
7. Chaves GM, da Silva WP (2012) Superoxide dismutases and glutaredoxins have a distinct role in the response of Candida albicans to oxidative stress generated by the chemical compounds menadione and diamide. Mem Inst Oswaldo Cruz 107:998–1005
8. Chiranand W, McLeod I, Zhou H, Lynn JJ, Vega LA, Myers H, Yates JR 3rd, Lorenz MC, Gustin MC (2008) CTA4 transcription factor mediates induction of nitrosative stress response in Candida albicans. Eukaryot Cell 7:268–278
9. Cuéllar-Cruz M, Briones-Martin-del-Campo M, Cañas-Villamar I, Montalvo-Arredondo J, Riego-Ruiz L, Castaño I, De Las Peñas A (2008) 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 7:814–825
10. Cuéllar-Cruz M, Castaño I, Arroyo-Helguera O, De Las Peñas A (2009) Oxidative stress response to menadione and cumene hydroperoxide in the opportunistic fungal pathogen Candida glabrata. Mem Inst Oswaldo Cruz 104:649–654
11. Cuéllar-Cruz M, Gutiérrez-Sánchez G, López-Romero E, Ruiz-Baca E, Villagómez-Castro JC, Rodríguez-Sifuentes L (2013) Identification of heat shock proteins in Candida albicans and enolases in Candida glabrata and Candida krusei involved in the response to oxidative stress. Cent Eur J Biol 8:337–345
12. Enjalbert B, Nantel A, Whiteway M (2003) Stress-induced gene expression in Candida albicans: absence of a general stress response. Mol Biol Cell 14:1460–1467
13. Estruch F, Carlson M (1993) Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol Cell Biol 13:3872–3881
14. Fernández-Arenas E, Cabezón V, Bermejo C, Arroyo J, Nombela C, Diez-Orejas R, Gil C (2007) Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol Cell Proteomics 6:460–478
15. Ferrari CK, Souto PC, França EL, Honorio-França AC (2011) Oxidative and nitrosative stress on phagocytes’ function: from effective defense to immunity evasion mechanisms. Arch Immunol Ther Exp 59:441–448
16. Fradin C, De Groot P, MacCallum D, Schaller M, Klis F, Odds FC, Hube B (2005) Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 56:397–415
17. Frohner IE, Bourgeois C, Yatsyk K, Majer O, Kuchler K (2009) Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol Microbiol 71:240–252
18. Gardner PR, Gardner AM, Martin LA, Salzman AL (1998) Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc Natl Acad Sci USA 95:10378–10383
19. Gonzalez-Parraga P, Hernandez JÁ, Arguelles JC (2003) Role of antioxidant enzymatic defences against oxidative stress H(2)O(2) and the acquisition of oxidative tolerance in Candida albicans. Yeast 20:1161–1169
20. Herrero E (2005) Evolutionary relationships between Saccharomyces cerevisiae and other fungal species as determined from genome comparisons. Rev Iberoam Micol 22:217–222
21. Horan S, Bourges I, Meunier B (2006) Transcriptional response to nitrosative stress in Saccharomyces cerevisiae. Yeast 23:519–535
22. Hromatka BS, Noble SM, Johnson AD (2005) Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol Biol Cell 16:4814–4826
23. Hwang CS, Baek YU, Yim HS, Kang SO (2003) Protective roles of mitochondrial manganese-containing superoxide dismutase against various stresses in Candida albicans. Yeast 20:929–941
24. Hwang CS, Rhie GE, Oh JH, Huh WK, Yim HS, Kang SO (2002) Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148:3705–3713
25. Jong AY, Chen SH, Stins MF, Kim KS, Tuan TL, Huang SH (2003) Binding of Candida albicans enolase to plasmin(ogen) results in enhanced invasion of human brain microvascular endothelial cells. J Med Microbiol 52:615–622
26. Kaloriti D, Tillmann A, Cook E, Jacobsen M, You T, Lenardon M, Ames L, Barahona M, Chandrasekaran K, Coghill G, Goodman D, Gow NA, Grebogi C, Ho HL, Ingram P, McDonagh A, de Moura AP, Pang W, Puttnam M, Radmaneshfar E, Romano MC, Silk D, Stark J, Stumpf M, Thiel M, Thorne T, Usher J, Yin Z, Haynes K, Brown AJ (2012) Combinatorial stresses kill pathogenic Candida species. Med Mycol 50:699–709
27. Krems B, Charizanis C, Entian KD (1995) Mutants of Saccharomyces cerevisiae sensitive to oxidative and osmotic stress. Curr Genet 27:427–434
28. Kusch H, Engelmann S, Albrecht D, Morschhäuser J, Hecker M (2007) Proteomic analysis of the oxidative stress response in Candida albicans. Proteomics 7:686–697
29. Laín A, Elguezabal N, Amutio E, Fernández de Larrinoa I, Moragues MD, Pontón J (2008) Use of recombinant antigens for the diagnosis of invasive candidiasis. Clin Dev Immunol. doi:10.1155/2008/721950
30. Lushchak OV, Inoue Y, Lushchak VI (2010) Regulatory protein Yap1 is involved in response of yeast Saccharomyces cerevisiae to nitrosative stress. Biochemistry (Mosc) 75:629–664
31. Lushchak OV, Lushchak VI (2008) Catalase modifies yeast Saccharomyces cerevisiae response towards S-nitrosoglutathione-induced stress. Redox Rep 13:283–291
32. Martchenko M, Alarco AM, Harcus D, Whiteway M (2004) Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol Biol Cell 15:456–467
33. Martínez-Pastor MT, Marchler G, Schüller C, Marchler-Bauer A, Ruis H, Estruch F (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15:2227–2235
34. Miceli MH, Diaz JA, Lee SA (2011) Emerging opportunistic yeast infections. Lancet Infect Dis 11:142–151
35. Miramón P, Kasper L, Hube B (2013) Thriving within the host: Candida spp. interactions with phagocytic cells. Med Microbiol Immunol. doi:10.1007/s00430-013-0288-z
36. Moradas-Ferreira P, Costa V (2000) Adaptive response of the yeast Saccharomyces cerevisiae to reactive oxygen species: defences, damage and death. Redox Rep 5:277–285
37. Moreno I, Martinez-Esparza M, Laforet LC, Sentandreu R, Ernst JF, Valentin E (2010) Dosage-dependent roles of the Cwt1 transcription factor for cell wall architecture, morphogenesis, drug sensitivity and virulence in Candida albicans. Yeast 27:77–87
38. Murray WW, Rachubinski RA (1989) Nucleotide sequence of peroxisomal catalase from the yeast Candida tropicalis pK233: identification of an upstream BamHlI site polymorphism. Nucleic Acids Res 17:3600
39. Nakagawa Y, Kanbe T, Mizuguchi I (2003) 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 47:395–403
40. Nantel A, Dignard D, Bachewich C, Harcus D, Marcil A, Bouin AP, Sensen CW, Hogues H, van het Hoog M, Gordon P, Rigby T, Benoit F, Tessier DC, Thomas DY, Whiteway M (2002) Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol Biol Cell 13:3452–3465
41. Nathan C, Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97:8841–8848
42. Nicholls S, Straffon M, Enjalbert B, Nantel A, Macaskill S, Whiteway M, Brown AJ (2004) Msn2- and Msn4-like transcription factors play no obvious roles in the stress responses of the fungal pathogen Candida albicans. Eukaryot Cell 3:1111–1123
43. Okada H, Ueda M, Sugaya T, Atomi H, Mozaffar S, Hishida T, Teranishi Y, Okazaki K, Takechi T, Kamiryo T, Tanaka A (1987) Catalase gene of the yeast Candida tropicalis. Sequence analysis and comparison with peroxisomal and cytosolic catalases from other sources. Eur J Biochem 170:105–110
44. Palmerini CA, Palombari R, Perito S, Arienti G (2003) NO synthesis in human saliva. Free Radic Res 37:29–31
45. Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163
46. Poole RK, Hughes MN (2000) New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol Microbiol 36:775–783
47. Rodríguez-Manzaneque MT, Ros J, Cabiscol E, Sorribas A, Herrero E (1999) Grx5 Glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae. Mol Cell Biol 19:8180–8190
48. Roetzer A, Gregori C, Jennings AM, Quintin J, Ferrandon D, Butler G, Kuchler K, Ammerer G, Schüller C (2008) Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol Microbiol 69:603–620
49. Roetzer A, Klopf E, Gratz N, Marcet-Houben M, Hiller E, Rupp S, Gabaldón T, Kovarik P, Schüller C (2011) Regulation of Candida glabrata oxidative stress resistance is adapted to host environment. FEBS Lett 585:319–327
50. Rogers PD, Vermitsky JP, Edlind TD, Hilliard GM (2006) Proteomic analysis of experimentally induced azole resistance in Candida glabrata. J Antimicrob Chemother 58:434–438
51. Schüller C, Brewster JL, Alexander MR, Gustin MC, Ruis H (1994) The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J 13:4382–4389
52. Sellam A, Tebbji F, Whiteway M, Nantel A (2012) A novel role for the transcription factor Cwt1p as a negative regulator of nitrosative stress in Candida albicans. PLoS ONE 7:e43956
53. Sen CK (1998) Redox signaling and the emerging therapeutic potential of thiol antioxidants. Biochem Pharmacol 55:1747–1758
54. Seneviratne CJ, Wang Y, Jin L, Abiko Y, Samaranayake LP (2008) Candida albicans biofilm formation is associated with increased anti-oxidative capacities. Proteomics 8:2936–2947
55. Shin DH, Jung S, Park SJ, Kim YJ, Ahn JM, Kim W, Choi W (2005) Characterization of thiol-specific antioxidant 1 (TSA1) of Candida albicans. Yeast 22:907–918
56. Singh P, Chauhan N, Ghosh A, Dixon F, Calderone R (2004) SKN7 of Candida albicans: mutant construction and phenotype analysis. Infect Immun 72:2390–2394
57. Sobko T, Reinders CI, Jansson E, Norin E, Midtvedt T, Lundberg JO (2005) Gastrointestinal bacteria generate nitric oxide from nitrate and nitrite. Nitric Oxide 13:272–278
58. Srikantha T, Zhao R, Daniels K, Radke J, Soll DR (2005) Phenotypic switching in Candida glabrata accompanied by changes in expression of genes with deduced functions in copper detoxification and stress. Eukaryot Cell 4:1434–1445
59. Srinivasa K, Kim NR, Kim J, Kim M, Bae JY, Jeong W, Kim W, Choi W (2012) Characterization of a putative thioredoxin peroxidase prx1 of Candida albicans. Mol Cells 33:301–307
60. Tillmann A, Gow NAR, Brown AJP (2011) Nitric oxide and nitrosative stress tolerance in yeast. Biochem Soc Trans 39:219–223
61. Ullmann BD, Myers H, Chiranand W, Lazzell AL, Zhao Q, Vega LA, Lopez-Ribot JL, Gardner PR, Gustin MC (2004) Inducible defense mechanism against nitric oxide in Candida albicans. Eukaryot Cell 3:715–723
62. Wysong DR, Christin L, Sugar AM, Robbins PW, Diamond RD (1998) Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect Immun 66:1953–1961
63. Zhang X, De Micheli M, Coleman ST, Sanglard D, Moye-Rowley WS (2000) Analysis of the oxidative stress regulation of the Candida albicans transcription factor, Cap1p. Mol Microbiol 36:618–629
64. Znaidi S, Barker KS, Weber S, Alarco AM, Liu TT, Boucher G, Rogers PD, Raymond M (2009) Identification of the Candida albicans Cap1p regulon. Eukaryot Cell 8:806–820