Development of oxidative stress tolerance resulted in reduced ability to undergo morphologic transitions and decreased pathogenicity in a t-butylhydroperoxide-tolerant mutant of Candida albicans

FEMS Yeast Research

Volumn 7, Issue 6, 2007, Pages 834-847

  Fekete, Andrea ^a,b   Emri, Tamás ^a   Gyetvai, Ágnes ^a   Gazdag, Zoltán ^c   Pesti, Miklós ^c   Varga, Zsuzsa ^b   Balla, József ^b   Cserháti, Csaba ^a   Emody, Levente ^d   Gergely, Lajos ^b   Pócsi, István ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF PÉCS   (Hungary)

^d UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Antimycotics; Candida albicans; Oxidative stress; Respiration; t butylhydroperoxide; Virulence attributes

Indexed keywords

AGAR; AMPHOTERICIN B; CYTOCHROME C; FATTY ACID; FLUCONAZOLE; FLUCYTOSINE; HYDROGEN PEROXIDE; LIPID; MENADIONE SODIUM BISULFITE; MONOUNSATURATED FATTY ACID; PHOSPHOLIPASE; POLYUNSATURATED FATTY ACID; REACTIVE OXYGEN METABOLITE; TERT BUTYL HYDROPEROXIDE; VORICONAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; BACTERIAL CELL; BREATHING; CANDIDA ALBICANS; CANDIDIASIS; CELL INVASION; CELL ISOLATION; CELL SIZE; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; ENZYME RELEASE; FEMALE; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; FUNGUS MUTANT; GROWTH RATE; LIPID COMPOSITION; LIPID PEROXIDATION; MITOCHONDRION; MORPHOLOGICAL ADAPTATION; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PATHOGENICITY; VIRULENCE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; CELL SIZE; DNA, FUNGAL; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; HYPHAE; LIPID PEROXIDATION; MICE; MUTATION; OXIDATIVE STRESS; TERT-BUTYLHYDROPEROXIDE; VIRULENCE FACTORS;

ARANEAE; CANDIDA; CANDIDA ALBICANS; FUNGI; MUS;

EID: 34547895079     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2007.00244.x     Document Type: Article

References (70)

1. Alic N, Felder T, Temple MD, Gloeckner C, Higgins VJ, Briza P Dawes IW (2004) Genome-wide transcriptional responses to a lipid hydroperoxide: adaptation occurs without induction of oxidant defenses. Free Radic Biol Med 37 : 23 35.
2. Alviano WS, Mendoça-Filho RR, Alviano DS, Bizzo HR, Souto-Padrón T, Rodrigues ML, Bolognese AM, Alviano CS Souza MMG (2005) Antimicrobial activity of Croton cajucara Benth linalool-rich essential oil on artificial biofilms and planktonic microorganisms. Oral Microbiol Immunol 20 : 101 105.
3. Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113 : 548 555.
4. Aoki S Ito-Kuwa S (1987) Induction of petite mutation with acriflavine and elevated temperature in Candida albicans. J Med Vet Mycol 25 : 269 277.
5. Arancia G, Molinari A, Crateri P, Stringaro A, Ramoni C, Dupuis ML, Gomez MJ, Torosantucci A Cassone A (1995) Noninhibitory binding of human interleukin-2-activated natural killer cells to the germ tube forms of Candida albicans. Infect Immun 63 : 280 288.
6. Babior BM, Kipnes RS Curnutte JT (1973) Biological defence mechanism. The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest 52 : 741 744.
7. Bahr JT Bonner WD Jr. (1973) Cyanide-insensitive respiration. I. The steady states of skunk cabbage spadix and bean hypocotyl mitochondria. J Biol Chem 248 : 3441 3445.
8. Balla G, Jacob HS, Eaton JW, Belcher JD Vercellotti GM (1991) Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial injury. Arterioscler Thromb 11 : 1700 1711.
9. Bligh EG Dryer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37 : 911 917.
10. Braun BR Johnson AD (1997) Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277 : 105 109.
11. Brennan ML, Anderson MM, Shih DM et al 2001) Increased atherosclerosis in myeloperoxidase-deficient mice. J Clin Invest 107 : 419 430.
12. Brun S, Aubry C, Lima O, Filmon R, Bergès T, Chabasse D Bouchara JP (2003) Relationships between respiration and susceptibility to azole antifungals in Candida glabrata. Antimicrob Agents Chemother 47 : 847 853.
13. Brun S, Dalle F, Saulnier P, Renier G, Bonnin A, Chabasse D Bouchara JP (2005) Biological consequences of petite mutations in Candida glabrata. J Antimicrob Chemother 56 : 307 314.
14. Byun J, Mueller DM, Fabjan JS Heinecke JW (1999) Nitrogen dioxide radical generated by the myeloperoxidase-hydrogen peroxide-nitrite system promotes lipid peroxidation of low density lipoprotein. FEBS Lett 455 : 243 246.
15. Calderone RA Fonzi WA (2001) Virulence factors of Candida albicans. Trends Microbiol 9 : 327 335.
16. Cremer J, Vatou V Braveny I (1999) 2,4-(Hydroxyphenyl)-ethanol, an antioxidative agent produced by Candida spp., impairs neutrophilic yeast killing in vitro. FEMS Microbiol Lett 170 : 319 325.
17. Doudican NA, Song B, Shadel GS Doetsch PW (2005) Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol Cell Biol 25 : 5196 5204.
18. Emri T, Pócsi I Szentirmai A (1997) Glutathione metabolism and protection against oxidative stress caused by peroxides in Penicillium chrysogenum. Free Radic Biol Med 23 : 809 814.
19. Emri T, Pócsi I Szentirmai A (1999) Analysis of the oxidative stress response of Penicillium chrysogenum to menadione. Free Radic Res 30 : 125 132.
20. Emri T, Molnár Zs, Pusztahelyi T Pócsi I (2004) Physiological and morphological changes in autolysing Aspergillus nidulans cultures. Folia Microbiol 49 : 277 284.
21. 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.
22. Enjalbert B, Smith DA, Cornell MJ, Alam I, Nicholls S, Brown AJ Quinn J (2006) 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 : 1018 1032.
23. Evans MV, Turton HE, Grant CM Dawes IW (1998) Toxicity of linoleic acid hydroperoxide to Saccharomyces cerevisiae: involvement of a respiration-related process for maximal sensitivity and adaptive response. J Bacteriol 180 : 483 90.
24. Fradin C, Kretschmar M, Nichterlein T, Gaillardin C, d'Enfert C Hube B (2003) Stage-specific gene expression of Candida albicans in human blood. Mol Microbiol 47 : 1523 1543.
25. 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.
26. Frankel S, Reitman S Sonnenwirth AC (1970) Gradwohl's Clinical Laboratory Methods and Diagnosis. The C.V. Mosby Company, Saint Louis.
27. Fekete-Forgács K, Gyüre L Lenkey B (2000) Changes of virulence factors accompanying the phenomenon of induced fluconazole resistance in Candida albicans. Mycoses 43 : 273 279.
28. Genova ML, Pich MM, Bernacchia A, Bianchi C, Biondi A, Bovina C, Falasca AI, Formiggini G, Castelli GP Lenaz G (2004) The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann NY Acad Sci 1011 : 86 100.
29. Gow NA, Brown AJ Odds FC (2002) Fungal morphogenesis and host invasion. Curr Opin Microbiol 5 : 366 371.
30. Greenley TL Davies MJ (1992) Detection of radicals produced by reaction of hydroperoxides with rat liver microsomal fractions. Biochim Biophys Acta 1116 : 192 203.
31. Gyetvai Á, Emri T, Takács K, Dergez T, Fekete A, Pesti M, Pócsi I Lenkey B (2006) Lovastatin possesses a fungistatic effect against Candida albicans, but does not trigger apoptosis in this opportunistic human pathogen. FEMS Yeast Res 6 : 1140 1148.
32. Gyetvai Á, Emri T, Pusztahelyi T et al 2007) High-dose methylprednisolone influences the physiology and virulence of Candida albicans ambiguously and enhances the candidacidal activity of the polyene antibiotic amphotericin B and the superoxide generating agent menadione. FEMS Yeast Res 7 : 265 275.
33. Gyurko C, Lendenmann U, Troxler RF Oppenheim FG (2000) Candida albicans mutants deficient in respiration are resistant to the small cationic salivary antimicrobial peptide histatin 5. Antimicrob Agents Chemother 44 : 348 354.
34. Hamilton AJ Holdom MD (1999) Antoxidant systems in the pathogenic fungi of man and their role in virulence. Med Mycol 37 : 375 389.
35. 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.
36. Hube B (2004) From commensal to pathogen: stage- and tissue-specific gene expression of Candida albicans. Curr Opin Microbiol 7 : 336 341.
37. Huh WK Kang SO (2001) Characterization of the gene family encoding alternative oxidase from Candida albicans. Biochem J 356 : 595 604.
38. Huh WK, Kim ST, Kim H, Jeong G Kang SO (2001) Deficiency of d-erythroascorbic acid attenuates hyphal growth and virulence of Candida albicans. Infect Immun 69 : 3939 3946.
39. 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.
40. Ibrahim AS, Mirbod F, Filler SG, Banno Y, Cole GT, Kitajima Y, Edwards JE Jr., Nozawa Y Ghannoum MA (1995) Evidence implicating phospholipase as a virulence factor of Candida albicans. Infect Immun 63 : 1993 1998.
41. Ito-Kuwa S, Aoki S, Watanabe T, Ehara T Osafune T (1988) Fluorescence microscopic studies on mitochondria and mitochondrial nucleoids in a wild-type strain and respiratory mutants of Candida albicans. J Med Vet Mycol 26 : 207 217.
42. Jamieson DJ, Stephen DWS Terrière EC (1996) Analysis of the adaptive oxidative stress response of Candida albicans. FEMS Microbiol Lett 138 : 83 88.
43. Johnson BE, Yoo BY Calleja GB (1973) Cell division in yeasts: movement of organelles associated with cell plate growth of Schizosaccharomyces pombe. J Bacteriol 115 : 358 366.
44. Kärber G (1931) Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Arch Exp Pathol Pharmakol 162 : 480 483.
45. Leidich SD, Ibrahim AS, Fu Y et al 1998) Cloning and disruption of caPLB1, a phospholipase B gene involved in the pathogenicity of Candida albicans. J Biol Chem 273 : 26078 26086.
46. Liu TT, Lee RE, Barker KS, Lee RE, Wei L, Homayouni R Rogers PD (2005) Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob Agents Chemother 49 : 2226 2236.
47. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A Fink GR (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90 : 939 949.
48. Lorenz MC Fink GR (2001) The glyoxylate cycle is required for fungal virulence. Nature 412 : 83 86.
49. Lorenz MC, Bender JA Fink GR (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3 : 1076 1087.
50. Macho A, Decaudin D, Castedo M, Hirsch T, Susin SA, Zamzami N Kroemer G (1996) Chloromethyl-X-rosamine is an aldehyde-fixable potential-sensitive fluorochrome for the detection of early apoptosis. Cytometry 25 : 333 340.
51. Mavor AL, Thewes S Hube B (2005) Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Curr Drug Targets 6 : 863 874.
52. Osiewacz HD Borghouts C (2000) Mitochondrial oxidative stress and ageing in the filamentous fungus Podospora anserina. Ann NY Acad Sci 908 : 31 39.
53. Paš M, Malačič R, Drašlar K, Pollak N Raspor P (2004) Uptake of chromium(III) and chromium(VI) compounds in the yeast cell structure. BioMetals 17 : 25 33.
54. Peterson GL (1983) Determination of total protein. Methods Enzymol 91 : 95 119.
55. Pócsi I, Prade EA Penninckx MJ (2004) Glutathione, altruistic metabolite in fungi. Adv Microb Physiol 49 : 1 76.
56. 2 and MSB exposed Aspergillus nidulans cultures - linking genome-wide transcriptional changes to cellular physiology. BMC Genomics 6, Article No: 182.
57. Savenkova MI, Mueller DM Heinecke JW (1994) Tyrosyl radical generated by myeloperoxidase is a physiological catalyst for the initiation of lipid peroxidation in low density lipoprotein. J Biol Chem 269 : 20394 20400.
58. 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.
59. Smith DA, Nicholls S, Morgan BA, Brown AJ Quinn J (2004) A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol Biol Cell 15 : 4179 4190.
60. Sokol-Anderson ML, Brajtburg J Medoff G (1986) Amphotericin B-induced oxidative damage and killing of Candida albicans. J Infect Dis 154 : 76 83.
61. Song JL, Lyons CN, Holleman S, Oliver BG White TC (2003) Antifungal activity of fluconazole in combination with Lovastatin and their effects on gene expression in the ergosterol and prenylation pathways in Candida albicans. Med Mycol 41 : 417 425.
62. 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.
63. Turton HE, Dawes IW Grant CM (1997) Saccharomyces cerevisiae exhibits a yAP-1-mediated adaptive response to malondialdehyde. J Bacteriol 179 : 1096 1101.
64. Varga Z, Kárpáti I, Paragh G, Buris L Kakuk G (1997) Relative abundance of some free fatty acids in plasma of uremic patients: relationship between fatty acids, lipid parameters, and diseases. Nephron 77 : 417 421.
65. Varga Z, Czompa A, Kakuk G Antus S (2001) Inhibition of superoxide anion release and hydrogen peroxide formation in PMNLs by flavonolignans. Phytother Res 15 : 608 612.
66. Vázquez-Torres A Balish E (1997) Macrophages in resistance to candidiasis. Microbiol Mol Biol Rev 61 : 170 192.
67. Wei YH Lee HC (2002) Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp Biol Med (Maywood) 227 : 671 682.
68. Wei YH, Lu CY, Lee HC, Pang CY Ma YS (1998) Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Ann NY Acad Sci 854 : 155 170.
69. 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.
70. Yang HC, Taguchi H, Nishimura K Miyaji M (1998) Imidazole-induced morphological abnormalities of mitochondria of Candida albicans. Mycoses 41 : 481 486.