Antioxidant systems in the pathogenic fungi of man and their role in virulence

Medical Mycology

Volumn 37, Issue 6, 1999, Pages 375-389

  Hamilton, A J ^a   Holdom, M D ^a  

^a GUY S HOSPITAL   (United Kingdom)

Author keywords

Antioxidants; Fungi; Virulence

Indexed keywords

ANTIOXIDANT; CATALASE; MANNITOL; MELANIN; SCAVENGER; SUPEROXIDE DISMUTASE;

ANTIOXIDANT ACTIVITY; ASPERGILLUS FUMIGATUS; CRYPTOCOCCUS NEOFORMANS; FUNGUS; MELANOGENESIS; NONHUMAN; PATHOGENICITY; REVIEW; VIRULENCE;

ANTIOXIDANTS; CATALASE; FUNGI; HUMANS; MANNITOL; MELANINS; SUPEROXIDE DISMUTASE; VIRULENCE;

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; FUNGI;

EID: 0033454725     PISSN: 13693786     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-280X.1999.00208.x     Document Type: Review

References (190)

1. Franzon VL, Arondel J, Sansonetti PJ. Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun 1990; 58: 529-535.
2. Beaman BL, Beaman L. Nocardia species: host parasite relationships. Clin Microbiol Rev 1994; 7: 213-264.
3. Smith NC, Bryant C. The role of host generated free radicals in helminth infections: Nippostrongylus brasiliensis and Nematospiroides dubius compared. Inter J Parasite 1986; 16: 617-622.
4. Henkle KJ, Liebau E, Muller S, Bergmann B, Walter RD. Characterization and molecular cloning of a Cu/Zn superoxide dismutase from the human parasite Onchocerca volvulus. Infect Immun 1991; 59: 2063-2069.
5. Hill HZ. The function of melanin or six blind people examine an elephant. Bioessays 1992; 14: 49-56.
6. Perpetua NS, Kubo Y, Yasuda N, Takano Y, Furusawa I. Cloning and characterization of a melanin biosynthetic THR1 reductase gene essential for appressorial penetration of Colletotrichum lagenarium. Mol Plant Mic Interact 1996; 9: 323-329.
7. Lundqvist T, Rice J, Hodge CN, Basarab GS, Rice J, Pierce J. Crystal structure of scytalone dehydratase-the disease determinant of a rice pathogen, Magnaporthe grisea. Structure 1994; 15: 937-944.
8. Wheeler MH, Bell AA. Melanins and their importance in pathogenic fungi. Curr Top Med Mycol 1988; 2: 338-387.
9. Polak A. Melanin as a virulence factor in pathogenic fungi. Mycoses 1989; 33: 215-224.
10. Staib F. Cryptococcus neoformans und Guizotia abyssinica (Sn G.oleifera) Farbreaktion fur Cr. neoformans. Z Hyg Infektionskr 1962; 148: 466-475.
11. Shields AB, Ajello L. Medium for selective isolation of Cryptococcus neoformans. Science 1966; 151: 208-209.
12. Botard RW, Kelley DC. Modified Littman oxgall agar to isolate Cryptococcus neoformans. Appl Microbiol 1968; 16: 689-690.
13. Kapica L, Shaw CE. Improvement in laboratory diagnosis of pulmonary cryptococcosis. Can Med Ass J 1969; 101: 47-50.
14. Hopfer RL, Blank F. Caffeic acid-containing medium for identification of Cryptococcus neoformans. J Clin Microbiol 1976; 2: 115-120.
15. Hopfer RL, Groeschel D. Six-hour pigmentation test for the identification of Cryptococcus neoformans. J Clin Microbiol 1975; 2: 96-98.
16. Wang HS, Zeimis RT, Roberts GD. Evaluation of a caffeic acid ferric citrate test for rapid identification of Cryptococcus neoformans. J Clin Microbiol 1977; 6: 445-449.
17. Chaskes S, Tyndall RL. Pigment production by Cryptococcus neoformans from para- and ortho-diphenols: effect of the nitrogen source. J Clin Micro 1975; 1: 509-514.
18. Korth H, Pulverer G. Pigment formation for differentiating Cryptococcus neoformans from Candida albicans. Appl Microbiol 1971; 21: 541-542.
19. Lerner AB, Fitzpatrick TB. Biochemistry of melanin formation. Physiol Rev 1950; 30: 91-126.
20. Mason HS. Comparative biochemistry of the phenolase complex. Adv Enzymol 1955; 16: 105-184.
21. Shaw CE, Kapica L. Production of diagnostic pigment by phenoloxidase activity of Cryptococcus neoformans. Appl Microbiol 1972; 24: 824-830.
22. Hamilton AJ, Goodley J. Virulence factors of Cryptococcus neoformans. Curr Top Med Mycol 1996; 7: 19-42.
23. Polacheck I, Kwon-Chung KJ. Melanogenesis in Cryptococcus neoformans. J Gen Micro 1988; 134: 1037-1041.
24. Williamson PR, Wakamatsu K, Ito S. Melanin biosynthesis in Cryptococcus neoformans. J Bact 1998; 180: 1570-1572.
25. Taylor BE, Wheeler MH, Szaniszlo PJ. Evidence for pentaketide melanin biosynthesis in dermatiaceous human pathogenic fungi. Mycologia 1987; 79: 320-322.
26. Dixon DM, Polak A, Szaniszlo PJ. Pathogenicity and virulence of wild-type and melanin-deficient Wangiella dermatitidis. J Med Vet Mycol 1987; 25: 97-106.
27. Nurudeen TA, Ahearn DG. Regulation of melanin production by Cryptococcus neoformans. J Clin Micro 1979; 10: 724-729.
28. Kwon-Chung KJ. Tom WK, Costa JL. Utilization of indole compounds by Cryptococcus neoformans to produce a melanin-like pigment. J Clin Micro 1983; 18: 1419-1421.
29. Kwon-Chung KJ, Wickes BL, Stockman L, Roberts GD, Ellis D, Howard DH. Virulence, serotype and molecular characteristics of environmental strains of Cryptococcus neoformans var. gattii. Infect Immun 1992; 60: 1869-1874.
30. Wang Y, Aisen P, Casadevall A. Melanin, melanin "ghosts," and melanin composition in Cryptococcus neoformans. Infect Immun 1996; 64: 2420-2424.
31. Chaskes S, Tyndall RL. Pigment production by Cryptococcus neoformans and other Cryptococcus species from aminophenols and diaminobenzenes. J Clin Microbiol 1978; 7: 146-152.
32. Rodrigues de Miranda L. Cryptococcus Kutzing emend. phaff et Spencer. In: Kreger-van Rij NJW, ed. The Yeasts, a Taxonomic Study. Amsterdam: Elsevier, 1984; 845-872.
33. Melo JC, Srinivasan S, Scott ML, Raff MJ. Cryptococcus albidus meningitis. J Infect 1980; 2: 79-82.
34. Lynch JP, Schaberg DR, Kissner DG, Kauffman CA. Cryptococcus laurentii lung abscess. Am Rev Resp Dis 1981; 123: 135-138.
35. Kwon-Chung KJ, Polacheck I, Popkin TJ. Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice. J Bacteriol 1982; 150: 1414-1421.
36. Kwon-Chung KJ, Rhodes JC. Encapsulation and melanin formation as indicators of virulence in Cryptococcus neoformans. Infect Immun 1986; 51: 218-233.
37. Polacheck l, Hearing VJ, Kwon-Chung KJ. Biochemical studies of phenoloxidase and utilisation of catecholamines in Cryptococcus neoformans. J Bacteriol 1982; 150: 1212-1220.
38. Ikeda R, Jacobson ES. Heterogeneity of phenol oxidases in Cryptococcus neoformans. Infect Immun 1992; 60: 3552-3555.
39. Rhodes JC, Polacheck l, Kwon-Chung KJ. Phenoloxidase activity and virulence in isogenic strains of Cryptococcus neoformans. Infect Immun 1982; 36: 1175-1184.
40. Ikeda R, Shinoda T, Morita T, Jacobson ES. Characterization of a phenol oxidase from Cryptococcus neoformans var. neoformans. Microbiol Immunol 1993; 37: 759-764.
41. Williamson PR. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J Bacteriol 1994; 176: 656-664.
42. Reinhammer B. Laccase. In: Lontie R, ed. Copper Proteins and Copper Enzymes. Boca Raton, FL: CRC Press, 1984; 4-10.
43. Torres-Guererro H, Edman JC. Melanin deficient mutants of Cryptococcus neoformans. J Med Vet Mycol 1994; 32: 303-313.
44. Jacobson ES, Emery HS. Temperature regulation of the cryptococcal phenoloxidase. J Med Vet Mycol 1991; 29: 121-124.
45. Jacobson ES, Jenkins ND, Todd JM. Relationship between superoxide dismutase and melanin in a pathogenic fungus. Infect Immun 1994: 62: 4085-4086.
46. Jacobson ES, Compton GM. Discordant regulation of phenoloxidase and capsular polysaccharide in Cryptococcus neoformans. J Med Vet Mycol 1996; 34: 289-291.
47. Alspaugh JA, Perfect JR, Heitman J. Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Develop 1997; 11: 3206-3217.
48. Salas SD, Bennett JE, Kwon-Chung KJ, Perfect JR, Williamson PR. Effect of the laccase gene CNLACl. on virulence of Cryptococcus neoformans. J Exp Med 1996; 184: 377-386.
49. Kuo MJ, Alexander M. Inhibition of the lysis of fungi by melanins. J Bacteriol 1967; 94: 624-629.
50. Bloomfield BJ, Alexander M. Melanins and resitance of fungi to lysis. J Bacteriol 1967; 93: 1276-1280.
51. Potgeiter HJ, Alexander M. Susceptibility and resistance of several fungi to microbial lysis. J Bacteriol 1966; 91: 1526-1532.
52. Porebska-Budny M, Sakina NL, Stepien KB, Dontsov AE, Wilczok T. Antioxidative activity of synthetic melanins. Cardiolipin liposome model. Biochim Biophys Acta 1992; 1116: 11-16.
53. Babior BM. Oxygen-dependent microbial killing by phagocytes. N Eng J Med 1978; 298: 659-668.
54. Klebanoff SJ. Oxygen metabolism and the toxic properties of phagocytes. Ann Intern Med 1980; 93: 480-489.
55. Test ST, Weiss SJ. The generation and utilization of chlorinated oxidants by human neutrophils. Adv Free Rad Biol Med 1986; 2: 91-116.
56. Cohen G, Heikkila RE. In vivo scavenging of Superoxide radicals by catecholamines. In: Michelson AM, McCord JM, Fridovich I, eds. Superoxide and Superoxide Dismutases. New York: Academic Press Inc., 1977; 351-365.
57. Polacheck I, Platt Y, Aronovitch J. Catecholam nes and virulence of Cryptococcus neoformans. Infect Immun 1990; 58: 2919-2922.
58. Jacobson ES, Emery HS. Catecholamine uptake, melanization, and oxygen toxicity in Cryptococcus neoformans. J Bacteriol 1991; 173: 401-403.
59. Jacobson ES, Tinnell SB. Antioxidant function of fungal melanin. J Bacteriol 1993; 175: 7102-7104.
60. Jacobson ES, Hong JD. Redox buffering by melanin and Fe(II) in Cryptococcus neoformans. J Bact 1997; 179: 5340-5346.
61. Emery HS, Shelburne CP, Bowman JP, Fallon PG, Schulz CA, Jacobson ES. Genetic study of oxygen resistance and melanization in Cryptococcus neoformans. Infect Immun 1994; 62: 5694-5697.
62. Wang Y, Casadevall A. Susceptibility of melanized and non-melanized Cryptococcus neoformans to nitrogen- and oxygen-derived oxidants. Infect Immun 1994: 62: 3004-3007.
63. Nathan CF. Hibbs Jr JB. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr Opin Immunol 1991; 3: 65-70.
64. Yoshida K, Akaike T, Doi T, Sato K. Pronounced enhancement of NO'-dependent antimicrobial action by an NO'-oxidizing agent, imidazolineoxyl N-oxide. Infect Immun 1993; 61: 3552-3555.
65. Wang Y, Aisen P, Casadevall A. Cryptococcus neoformans melanin and virulence: mechanism of action. Infect Immun 1995; 63: 3131-3136.
66. Wang Y, Casadevall A. Growth of Cryptococcus neoformans in presence of L-Dopa decreases its susceptibility to Amphotericin B. Antimicrob Agents Chemoth 1994; 38: 2648-2650.
67. Kwon-Chung KJ, Hill WB, Bennett JE. New, special stain for histopathological diagnosis of cryptococcosis. J Clin Micro 1981; 13: 383-387.
68. Liu L. Wakamatsu K, Ito S, Williamson PR. Catecholamine oxidative products, but not melanin, are produced by Cryptococcus neoformans during neuropathogenesis in mice. Infect Immun 1999; 67: 108-112.
69. Nosanchuk JD, Valdon P, Feldmesser M, Casadevall A. Evidence of melanization of Cryptococcus neoformans infection, 1998 (98th American Society of Microbiology Annual Meeting. Atlanta, abstract F-38).
70. Nosanchuk JD, Valadon P, Feldmesser M, Casadevall A. Melanization of Cryptococcus neoformans in murine infection. Mol Cell Biol 1999; 19: 745-750.
71. Rosas AL, Nosanchuk JD, Casadevall A. Melanin-binding monoclonal antibodies for the study of melanogenesis of Cryptococcus neoformans in vivo, 1999 (99th American Society of Microbiology Annual Meeting, Chicago, abstract F-50).
72. Nosanchuk JD, Rosas AL, Casadevall A, The antibody response to fungal melanin in mice. J Immunol 1998: 160: 6026-6031.
73. Nosanchuk JD. Casadevall A. Glyphosate inhibits melanization of Cryptococcus neoformans and affects survival following systemic infection in mice, 1999 (99th American Society of Microbiology Annual Meeting, Chicago, abstract F-49).
74. Franzot SP, Mukherjee J, Cherniak R, Chen LC, Hamdan JS, Casadevall A. Microevolution of a standard strain of Cryptococcus neoformans resulting in differences in virulence and other phenotypes. Infect Immun 1998; 66: 89-97.
75. Geis PA, Wheeler MH, Szaniszlo PJ. Pentaketide metabolites of melanin synthesis in the dematiaceous fungus Wangiella dermatitidis. Arch Microbiol 1984; 137: 324-328.
76. Wheeler MH, Stipanovic RD. Melanin biosynthesis and the metabolism of flaviolin and 2-hydroxyjuglone in Wangiella dermatitidis. Arch Microbiol 1985: 142: 234-241.
77. Thaylor BE, Wheeler MH, Szaniszlo PJ. Evidence for pentaketide melanin biosynthesis in dematiaceous human pathogenic fungi. Mycologia 1987: 76: 268-273.
78. Jacobson ES, Hove E, Emery HS. Antioxidant function of melanin in black fungi. Infect Immun 1995; 63: 4944-4945.
79. Schnitzler N, Peltroche-Llacsahuanga H, Bestier N, Zundorf J, Lutticken R, Haase G. Effect of melanin and carotenoids of Exophiala (Wangiella) dermatitidis on phagocytosis, oxidative burst, and killing by human neutrophils. Infect Immun 1999; 67: 94-101.
80. Dixon DM, Polak A, Szaniszlo PJ. Pathogenicity and virulence of wild-type and melanin-deficient Wangiella dermatitidis. J Med Vet Mycol 1987; 25: 97-106.
81. Dixon DM, Polak A, Conner GW. Mel-mutants of Wangiella dermatitidis in mice: evaluation of multiple mouse and fungal strains. J Med Vet Mycol 1989; 27: 335-341.
82. Dixon DM, Migliozzi J, Cooper CR, Solis O, Breslin B, Szaniszlo PJ. Melanized and non-melanized multicellular form mutants of Wangiella dermatitidis in mice: mortality and histopathology studies. Mycoses 1992; 35: 17-21.
83. Feng B, Szaniszlo PJ. Cloning of the polyketide synthase gene of Wangiella dermatitidis, by a marker rescue approach, 199898th ASM Annual Meeting, Atlanta; abstract F-66.
84. Pirt SJ, Rowley BI. Melanin production in Aspergillus nidulans. Biochem J 1969; 114: 9-10.
85. Rowley BI, Pirt SJ. Melanin production by Aspergillus nidulans in batch and chemostat cultures. J Gen Micro 1972; 72: 553-563.
86. Mayorga ME, Timberlake WE. Isolation and molecular characterization of the Aspergillus nidulans wA gene. Genetics 1990; 126: 73-79.
87. Mayorga ME, Timberlake WE. The developmentally regulated Aspergillus nidulans wA gene encodes a polypeptide homologous to polyketide and fatty acid synthases. Mol Gen Genet 1992; 235: 205-212.
88. O'Hara EB, Timberlake WE. Molecular characterization of the Aspergillus nidulans yA locus. Genetics 1989; 121: 249-254.
89. Aramayo R, Timberlake WE. Sequence and molecular structure of the Aspergillus nidulans yA (laccase I) gene. Nucl Acid Res 1990; 18: 3415.
90. Chang YC, Segal BH, Holland SM, Miller GF, Know-Chung KJ. Virulence of catalase-deficient Aspergillus nidulans in p47(phox)-/-mice. Implications for fungal pathogenicity and host defence in chronic granulomatous disease. J Clin Invest 1998; 101: 1843-1850.
91. Jahn B, Koch A, Schmidt A, Wanner G, Gehringer H, Bhakdi S, Brakhage AA. Isolation and characterization of a pigment-less-conidium mutant of Aspergillus fumigatus with altered conidial surface and reduced virulence. Infect Immun 1997; 65: 5110-5117.
92. Tsai HF, Chang YC, Washburn RG, Wheeler MH, KwonChung KJ. The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence. J Bact 1998: 180: 3031-3038.
93. Tsai HF, Washburn RG, Chang YC, Kwon-Chung KJ. Aspergillus fumigatus arp1 modulates conidial pigmentation and complement deposition. Mol Microbiol 1997; 26: 175-183.
94. Fridovitch I. Superoxide dismutases. An adaptation to a paramagnetic gas. J Biol Chem 1989; 264: 7761-7764.
95. Fridovitch I. Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol 1986; 58: 61-97.
96. Marklund SL. Human copper-containing superoxide dismutase of high molecular weight. Proc Natl Acad Sci USA 1982; 79: 7634-7638.
97. Zhu D. Scandalios JG. Expression of the maize MnSod (Sod3) gene in Mn SOD-deficient yeast rescues the mutant yeast under oxidative stress. Genetics 1992; 131: 803-809.
98. Tesfa-Selase F. Hay RJ. Superoxide dismutase of Cryptococcus neoformans: purification and characterization. J Med Vet Mycol 1995; 33: 253-259.
99. Crameri R, Faith A, Hemmann S, Jaussi R, Ismail C, Menz G, Blaser K. Humoral and cell-mediated autoimmunity in allergy to Aspergillus fumigatus. J Exp Med 1996; 184: 256-270.
100. Mayer C, Hemmann S, Faith A, Blaser K, Crameri R. Cloning, production, characterization and IgE cross-reactivity of different manganese superoxide dismutases in individuals sensitized to Aspergillus fumigatus. Intern Arch Aller Immunol 1997; 113: 213-215.
101. Hemmann S, Nikolaizik WH, Schoni MH, Blaser K, Crameri R. Differntial IgE recognition of recombinant Aspergillus fumigatus allergens by cystic fibrosis patients with allergic bronchopulmonary aspergillosis or Aspergillus allergy. Eur J Immunol 1998; 28: 1155-1160.
102. Brummer E, Stevens DA. Candidacidal mechanisms of peritoneal macrophages activated with lymphokines or gamma-interferon. J Med Microbiol 1989; 28: 173-181.
103. Desai G, Nassar F, Brummer E, Stevens DA. Killing of Histoplasma capsulatum by macrophage colony stimulating factor-treated human monocyte-derived macrophages: role for reactive oxygen intermediates. J Med Microbiol 1995; 43: 224-229.
104. Potoka DA. Takao S, Owaki T, Bulkley GB, Klein AS. Endothelial cells potentiate oxidant-mediated Kupffer cell phagocytic killing. Free Rad Biol Med 1998; 24: 1217-1227.
105. Misra HP, Fridovich I. The purification and properties of superoxide dismutase from Neurospora crassa. J Biol Chem 1972; 247: 3410-3414.
106. Lerch K, Schenk E. Primary structure of copper-zinc superoxide dismutase from Neurospora crassa. J Biol Chem 1985; 260: 9559-9566.
107. Gralla EB, Kosman DJ. Molecular genetics of superoxide dismutases in yeasts and related fungi. Adv Genet 1992; 30: 251-319.
108. Goscin SA, Fridovich I. The purification and properties of superoxide dismutase from Saccharomyces cerevisiae. Biochim Biophys Acta 1972; 289: 279-283.
109. Krems B, Charizanis C, Entian KD. Mutants of Saccharomyces cerevisiae sensitive to oxidative and osmotic stress. Curr Gen 1995; 27: 427-434.
110. Longo VD, Gralla EB, Valentine JS. Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 1996; 271: 12275-12280.
111. Gamonet F, Lauquin GJ. The Saccharomyces cerevisiae LYS7 gene is involved in oxidative stress protection. Eur J Biochem 1998; 251: 716-723.
112. Holdom MD, Hay RJ, Hamilton AJ. Purification, N-terminal amino acid sequence and partial characterization of a Cu,Zn superoxide dismutase from the pathogenic fungus Aspergillus fumigatus. Free Rad Res 1995; 22: 519-531.
113. Callahan HL, Crouch RK, James ER. Dirofilaria immitis superoxide dismutase: purification and characterization. Mol Biochem Parasit 1991; 49: 245-251.
114. Schinina ME, Bossa F, Lania A, Capo CR, Carlini P, Calabrese L. The primary structure of turtle Cu,Zn superoxide dismutase. Structural and functional irrelevance of an insert conferring proteolytic susceptibility. Eur J Biochem 1993; 211: 843-849.
115. Hamilton AJ, Holdom MD, Hay RJ. Specific recognition of purified Cu,Zn superoxide dismutase from Aspergillus fumigatus by immune human sera. J Clin Microbiol 1995; 33: 495-496.
116. Hamilton AJ, Holdom MD, Jeavons L. Expression of the Cu,Zn superoxide dismutase of Aspergillus fumigatus as determined by immunochemistry and immunoelectron microscopy. FEMS Immunol Med Microbiol 1996; 14: 95-102.
117. Holdom MD, Hay RJ, Hamilton AJ. The Cu,Zn superoxide dismutases of Aspergillus flavus, Aspergillus niger, Aspergillus nidulans, and Aspergillus terreus: purification and biochemical comparison with the Aspergillus fumigatus Cu,Zn superoxide dismutase. Infect Immun 1996; 64: 3326-3332.
118. Hamilton AJ, Holdom MD. Biochemical comparison of the Cu,Zn superoxide dismutases of Cryptococcus neoformans var. neoformans and Cryptococcus neoformans var. gattii. Infect Immun 1997; 65: 488-494.
119. Franzot SP, Salkin IF, Casadevall A. Cryptococcus neoformans var. grubii: separate varietal status for Cryptococcus neoformans serotype A isolate. J Clin Micro 1999; 37: 838-840.
120. 2-dependent methionine auxotrophy in Cu,Zn superoxide dismutase-deficient mutants of Saccharomyces cerevisiae. J Bact 1990; 172: 1840-1845.
121. Liu XF, Elashvili I, Gralla EB, Valentine JS, Lapinskas P, Culotta VC. Yeast lacking superoxide dismutase. Isolation of genetic suppressors. J Biol Chem 1992; 267: 18298-18302.
122. Tamai KT, Gralla EB, Ellerby LM, Valentine JS, Thiele DJ. Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. Proc Natl Acad Sci USA 1993; 90: 8013-8017.
123. Fortuniak A, Jakubowski W, Bilinski T, Bartosz G. Lack of evidence of oxidative damage in antioxidant-deficient strains of Saccharomyces cerevisiae. Biochem Mol Biol Intern 1996; 38: 1271-1276.
124. Ungpakorn R, Holdom MD, Hamilton AJ, Hay RJ. Purification and partial characterization of the Cu,Zn superoxide dismutase from the dermatophyte Trichophyton mentagrophytes var. interdigitale. Clin Exp Derm 1996: 21: 190-196.
125. Ogihara, NL, Parge HE, Hart PJ, Weiss MS et al. NCBI submission, accession no. 1633493.
126. Schonbaum G, Chance B. Catalase. Enzymes 1976; 13: 363-409.
127. Veenhuis M, Mateblowski M, Kunau WH, Harder W. Proliferation of microbodies in Saccharomyces cerevisiae. Yeast 1987; 3: 77-84.
128. Levitz SM, Diamond RD. Mechanisms of resistance of Aspergillus fumigatus conidia to killing by neutrophils in vitro. J Infect Dis 1985; 152: 33-42.
129. McEwan JG, Sugar AM, Brummer E, Restrepo A, Stevens DA. Toxic effects of oxidative metabolism on the yeast form of Paracoccidioides brasiliensis. J Med Microbiol 1984; 18: 423-428.
130. Meloni-Bruneri LH, Campa A, Abdalla DS, Calich VL, Lenzi HL, Burger E. Neutrophil oxidative metabolism and killing of Paracoccidioides brasiliensis after air pouch infection of susceptible and resistant mice. J Leuk Biol 1996; 59: 526-533.
131. Brummer E, Sugar AM, Stevens DA. Immunological activation of polymorphonuclear neutrophils for fungal killing: studies with murine cells and Blastomyces dermatitidis in vitro. J Leuk Biol 1984; 36: 505-520.
132. Morrison CJ, Isenberg RA, Stevens DA. Enhanced oxidative mechanisms in immunologically activated versus elicited polymorphonuclear neutrophils: correlations with fungicidal activity. J Med Microbiol 1988; 25: 115-121.
133. Morrison CJ, Brummer E, Stevens DA. In vivo activation of peripheral blood polymorphonuclear neutrophils by gamma interferon results in enhanced fungal killing. Infect Immun 1989; 57: 2953-2958.
134. Brummer E, Stevens DA. Antifungal mechanisms of activated murine bronchoalveolar or peritoneal macrophages for Histoplasma capsulatum. Clin Exp Immunol 1995: 102: 65-70.
135. Diamond RD, Clark RA. Haudenschild CC. Damage to Candida albicans hyphae and pseudohyphae by the myeloperoxidase system and oxidative products of neutrophil metabolism in vitro. J Clin Invest 1980; 66: 908-917.
136. Potoka DA, Takao S, Owaki T, Bulkley GB. Klein AS. Endothelial cells potentiate oxidant-mediated Kupffer cell phagocytic killing. Free Rad Biol Med 1998; 24: 1217-1227.
137. Miller RA, Britigan BE. Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 1997: 10: 1-18.
138. Sokol-Anderson ML, Brajtburg J, Medoff G. Amphotericin B-induced oxidative damage and killing of Candida albicans. J Infect Dis 1986; 154: 76-83.
139. Navarro RE, Stringer MA, Hansberg W, Timberlake WE, Aguirre J. cat A, a new Aspergillus nidulans gene encoding a developmentally regulated catalase. Curr Gen 1996; 29: 352-359.
140. Kawasaki L, Wysong D, Diamond R, Aguirre J, Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. J Bact 1997: 179: 3284-3292.
141. Kikuchi-Toree K, Hayashi S, Nakamoto H, Nakamura S. Properties of Aspergillus niger catalase. J Biochem 1982; 92: 1449-1456.
142. Gruft H, Ruck R, Traynor J. Properties of a unique catalase isolated from Aspergillus niger. Can J Biochem 1978; 56: 916-919.
143. Fowler T, Rey MW, Vaha-Vahe P, Power SD, Berka RM. The catR gene encoding a catalase from Aspergillus niger: primary structure and elevated expression through increased gene copy number and use of a strong promoter. Mol Microbiol 1993; 9: 989-998.
144. Lardinois OM, Rouxhet PG. Characterization of hydrogen peroxide and superoxide degrading pathways of Aspergillus niger catalase: a steady state analysis. Free Rad Res 1994; 20: 29-50.
145. Lardinois OM, Mestdagh MM, Rouxhet PG. Reversible inhibition and irreversible inactivation of catalase in presence of hydrogen peroxide. Biochim Biophy Acta 1996; 1295: 222-238.
146. Tran Van Ky P, Biguet J, Vaucelle T. Etude d'une fraction antigenique d' Aspergillus fumigatus support d'une activité catalasique. Consequence sur le diagnostic immunologique de l'aspergillose. Rev Immunol 1968; 32: 37-52.
147. Schonheyder H, Andersen P, Petersen JC. Rapid immunoelectrophoretic assay for detection of serum antibodies to Aspergillus fumigatus catalase in patients with pulmonary aspergillosis. Eur J Clin Microbiol 1985; 4: 299-303.
148. Schonheyder H, Jensen T, Lassoe IH, Hoiby N, Kock C. Serum antibodies to Aspergillus fumigatus catalase in patients with cystic fibrosis. Eur J Clin Microbiol Infect Dis 1988; 7: 40-44.
149. Schonheyder H. Storgaard L, Andersen P. Variation of a 470000 daltons antigen complex and catalase antigen in clinical isolates of Aspergillus fumigatus. Sabouraudia 1985; 23: 339-349.
150. Hearn VM, Wilson EV, Mackenzie DW. Analysis of Aspergillus fumigatus catalases possessing antigenic activity. J Med Micobiol 1992; 36: 61-67.
151. Lopez-Medrano R, Ovejero MC, Calera JA, Puente P, Leal F. An immunodominant 90-kilodalton Aspergillus fumigatus antigen is the subunit of a catalase. Infect Immun 1995; 63: 4774-4780.
152. Calera JA, Paris S, Monod M, Hamilton AJ, Debeaupuis JP, Diaquin M, Lopez-Medrano R, Leal F, Latge JP. Cloning and disruption of the antigenic catalase gene of Aspergillus fumigatus. Infect Immun 1997; 65: 4718-4724.
153. Kamasawa N, Ohtsuka I, Kamada Y, Ueda M, Tanaka A, Osumi M. Immunoelectron microscopic observation of the behaviors of peroxisomal enzymes inducibly sythesized in an n-alkane-utilizable yeast cell, Candida tropicalis. Cell Struct Funct 1996: 21: 117-122.
154. Rachubinski RA, Fujiki Y, Lazarow PB. Isolation of cDNA clones coding for peroxisomal proteins of Candida tropicalis: identification and sequence of a clone for catalase. Biochim Biophy Acta 1987; 909: 35-43.
155. Ueda M, Okada H, Hishida T, Teranishi Y, Tanaka A. Isolation of several cDNAs encoding yeast peroxisomal enzymes. FEBS Lett 1987; 220: 31 - 35.
156. Okada H, Ueda M, Sugaya T, Atomi H, Mozaffar S, Hishida T, et al. Catalase gene of the yeast Candida tropicalis. Sequence analysis and comparison with peroxisomal and cytosolic catalases from other sources. Eur J Bioechem 1987; 170: 105-110.
157. Murray WW, Rachubinski RA. Nucleotide sequence of peroxisomal catalase from the yeast Candida tropicalis pK233: identification of an upstream Bam HI site polymorphism. Nucl Acid Res 1989; 17: 3600.
158. Yamada T, Tanaka A, Horikawa S, Numa S, Fukai S. Cellfree translation and regulation of Candida tropicalis catalase messenger RNA. Eur J Biochem 1982; 129: 251-255.
159. Fujiki Y, Rachubinski RA, Zentella-Dehesa A, Lazarow PB, Induction, identification, and cell-free translation of mRNAs coding for peroxisomal proteins in Candida tropicalis. J Biol Chem 1986; 261: 15787-15793.
160. Kinoshita H, Atomi H, Ueda M, Tanaka A. Characterization of the catalase of the n-alkane-utilizing yeast Candida tropicalis functionally expressed in Saccharomyces cerevisiae. App Microbiol Biotech 1994; 40: 682-686.
161. Tosado-Acevedo R, Toranzos GA, Alsina A. Extraction and purification of a catalase from Candida albicans. Puer Rico Heal Sci J 1992; 11: 77-80.
162. Romandini P, Bonotto C, Bertoloni G, Beltramini M, Salvato B Superoxide dismutase, catalase and cell dimorphism in Candida albicans cells exposed to methanol and different temperatures. Comp Biochem Physiol Pharm Toxicol Endocrinol 1994; 108: 53-57.
163. Wysong DR, Christin L, Sugar AM, Robbins PW, Diamond RD. Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect Immun 1998: 66: 1953-1961.
164. Howard DH. Comparative sensitivity of Histoplasma capsulatum conidiospores and blastospores to oxidative antifungal systems. Infect Immun 1981; 32: 381-387.
165. Howard DH. Studies on the catalase of Histoplasma capsulatum. Infect Immun 1983; 39: 1161-1166.
166. Johnson CH, York JL, McEwen JE. Differentially expressed catalase genes in Histoplasma capsudatum, 1998 (98th ASM Annual Meeting, Atlanta, abstract F-65).
167. Zancope-Oliveira RM, Myers LW, Reiss E, Lott TJ. Isolation and characterisation of the M antigen of Histoplasma capsulatum, 199797th ASM Annual Meeting New Orleans, abstract F-35.
168. Hamilton AJ, Bartholomew MA, Figueroa J, Fenelon LE, Hay RJ. Evidence that the M antigen of Histoplasma capsulatum var. capsulatum is a catalase which exhibits cross-reactivity with other dimorphic fungi. J Med Vet Mycol 1990; 28: 479-485.
169. Jeavons L, Hamilton AJ, Vanittanakom N, Ungpakorn R, Evans EG, Sirisanthana T, Hay RJ. Identification and purification of specific Penicillium marneffei antigens and their recognition by human immune sera. J Clin Microbiol 1998; 36: 949-954.
170. Morrison CJ, Stevens DA. Mechanisms of fungal pathogenicity: correlation of virulence in vivo, susceptibility to killing by polymorphonuclear neutrophils in vitro, and neutrophil superoxide anion induction among Blastomyces dermatitidis isolates. Infect Immun 1991; 59: 2744-2749.
171. Galgiani JN. Differences in oxidant release by human polymorphonuclear leukocytes produced by stimulation with different phases of Coccidioides immitis. J Infect Dis 1995; 172: 199-203.
172. Andre L, Hemming A, Alder L. Osmoregulation in Saccharomyces cerevisiae. Studies on the osmotic induction of glycerol production and glycerol-3-phosphate dehydrogenase. FEBS Lett 1991; 286: 13-17.
173. Chaturvedi V, Flynn T, Niehaus WG, Wong B. Stress tolerance and pathogenic potential of a mannitol mutant of Cryptococcus neoformans. Microbiology 1996; 142: 937-943.
174. Niehaus WG, Dilts RP. Purification and characterisation of mannitol dehydrogenase from Aspergillus parasiticus. J Bact 1982; 151: 243-250.
175. Witteveen CF, Visser J. Polyol pools in Aspergillus niger. FEMS Micro Lett 1995; 134: 57-62.
176. Wong B, Brauer KL, Tsai RR, Jayasimhulu K. Increased amounts of the Aspergillus metabolite D-mannitol in tissue and serum of rats with experimental aspergillosis. J Infect Dis 1989; 160: 95-103.
177. Wong B, Perfect JR, Beggs S, Wright KA. Production of the hexitol D-mannitol by Cryptococcus neoformans in vitro and in rabbits with experimental meningitis. Infect Immun 1990; 58: 1664-1670.
178. Megson GM, Stevens DA, Hamilton JR, Denning DW. Dmannitol in cerebrospinal fluid of patients with AIDS and cryptococcal meningitis. J Clin Microbiol 1996; 34: 218-221.
179. Niehaus WG, Flynn T. Regulation of mannitol biosynthesis and degradation by Cryptococcus neoformans. J Bact 1994; 176: 651-655.
180. Chaturvedi V, Wong B, Newman SL. Oxidatixe killing of Cryptococcus neoformans by human neutrophils. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. J Immunol 1996; 156: 3836-3840.
181. Buchanan KL, Murphy JW. What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 1998; 4: 71-83.
182. Perfect JR, Rude TH, Wong B, Flynn T, Chaturvedi V, Niehaus W. Identification of a Cryptococcus neoformans gene that directs expression of the cryptic Saccharomyces cerevisiae mannitol dehydrogenase gene. J Bact 1996; 178: 5257-5262.
183. Saha AK, Dowling JN, LaMarco KL, Das S, Remaley AT, Olomu N, et al. Properties of an acid phospatase from Legionella micdadei which blocks superoxide anion production by human neutrophils. Arch Biochem Biophys 1985; 243: 150-160.
184. Baca OG, Roman MJ, Glew RH, Christner RF. Buhler JE, Aragon AS. Acid phosphatase activity in Coxiella burnetii: a possible virulence factor. Infect Immun 1993; 61: 4232-4239.
185. Reilly JJ, Baron SG, Nano FE, Kuhlenschmidt MS. Characterization and sequence of a respiratory burst inhibiting acid phosphatase from Francisella tularensis. J Biol Chem 1996; 271: 10973-10983.
186. Chen LC, Pirofski LA, Casadevall A. Extracellular proteins of Cryptococcus neoformans and host antibody response. Infect Immun 1997; 65: 2599-2605.
187. Youngchim S, Vanittanakom N, Hamilton AJ. Analysis of the enzymatic activity of mycelial and yeast phases of Penicillium marneffei. Med Mycol 1999; 37: 445-456.
188. Callahan HL, Crouch RK, James ER. Helminth anti-oxidant enzymes: a protective mechanism against host oxidants. Parasit Today 1988; 4: 218-225.
189. Fraaije MW, Roubroeks HP, Hagen WR, Van Berkel WJ. Purification and characterization of an intracellular catalase-peroxidase from Penicillium simplicissimum. Eur J Biochem 1996; 235: 192-198.
190. Geis PA. Szaniszlo P. Carotenoid pigments of the dermatiaceous fungus Wangiella dermatitidis. Mycologia 1984; 76: 268-273.