Cytochrome P450 enzyme systems in fungi

Fungal Genetics and Biology

Volumn 23, Issue 1, 1998, Pages 1-17

  Van Den Brink, Hans M ^a,b   Van Gorcom, Robert F M ^a   Van Den Hondel, Cees A M J J ^a   Punt, Peter J ^a  

^a TNO   (Netherlands)

^b Gist Brocades NV   (Netherlands)

Author keywords

Bioconversion; Biotransformation; CPR; CYP; Cytochrome P450; Index descriptors

Indexed keywords

CYTOCHROME P450;

BIOTRANSFORMATION; FUNGAL GENETICS; FUNGUS; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE;

EID: 0031684276     PISSN: 10871845     EISSN: None     Source Type: Journal    
DOI: 10.1006/fgbi.1997.1021     Document Type: Review

References (146)

1. Ahmed, F., Williams, R. A. D., and Smith, K. E. 1995. Microbial transformation of steroids-IX Purification of progesterone hydroxylase cytochrome P450 from Phycomyces blakesleeanus. J. Steroid Biochem. Mol. Biol. 52(2): 203-208.
2. Attar, R. M., Grotewold, E., Taccioli, G. E., Aisenberg, G. D., Torres, H. N., and Judewicz, N. D. 1990. A cycloheximide inducible gene of Neurospora crassa belongs to the cytochrome P450 superfamily. Nucleic Acids Res. 17: 7535-7536.
3. Autrup, H. 1990. Carcinogen metabolism in cultured human tissue cells. Carcinogenesis 11: 707-712.
4. Baillie, G. S. 1993. The Characterization of Cytochromes P450 from Aspergillus fumigatus. Thesis No. DX 176224, University of Kent, Canterbury, UK.
5. Bezalel, L., Hadar, Y., and Cerniglia, C. E. 1996. Mineralization of polycyclic aromatic hydrocarbons by the white rot fungus Pleurotus ostreatus. Appl. Environ. Microbiol. 62: 292-295.
6. Bhatagnar, R. K., Ahmed, S., Kohli, K. K., Mukerji, K. G., and Venkitasubramanian, T. A. 1982. Induction of polysubstrate monooxygenase and aflatoxin production by phenobarbitone in Aspergillus parasiticus. Biochem. Biophys. Res. Commun. 104: 1287-1292.
7. Black, S. D., French, J. S., Williams, C. H. Jr., and Coon, M. J. 1979. Role of a hydrophobic polypeptide in the N-terminal region of NADPH-cytochrome P450 reductase in complex formation with P450LM. Biochem. Biophys. Res. Commun. 91: 1528-1535.
8. Black, S. D., and Coon, M. J. 1987. Cytochromes P450: Structure and function. Adv. Enzymol. 60: 35-87.
9. Bloch, K. 1983. Sterol structure and membrane function. CRC Crit. Rev. Biochem. 14: 47-92.
10. Boschloo, J. G., Paffen, A., Koot, T., Van den Tweel, W. J. J., Van Gorcom, R. F. M., Cordewener, J. H. G., and Bos, C. J. 1990. Genetic analysis of benzoate metabolism in Aspergillus niger. Appl. Microbiol. Biotechnol. 34: 225-228.
11. Breskvar, K., and Hudnik-Plevnik, T. 1977. Apossible role for cytochrome P450 in hydroxylation of progesterone by Rhizopus nigricans. Biochem. Biophys. Res. Commun. 74: 1192-1198.
12. Breskvar, K., Cresnar, B., Plaper, A., and Hudnik-Plevnik, T. 1991. Localization of the gene encoding steroid hydroxylase cytochrome P450 from Rhizopus nigricans inside a HindIII fragment of genomic DNA. Biochem. Biophys. Res. Commun. 178(3): 1078-1083.
13. Briza, P., Breitenbach, M., Ellinger, A., and Segall, J. 1990. Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev. 4: 1775-1789.
14. Brown, D. W., Yu, J. H., Kelkar, H. S., Fernandes, M., Nesbitt, T. C., Keller, N. P., Adams, T. H., and Leonard, T. J. 1996. Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 93: 1418-1422.
15. Bumpus, J. A., and Aust, S. D. 1987. Biodegradation of environmental pollutants by the white rot fungus Phanerochaete chrysosporium: Involvement of the lignin degrading system. BioEssays 6: 166-170.
16. Burgener-Kairuz, P., Zuber, J. P., Jaunin, P., Buchman, T. G., Bille, J., and Rossier, M. 1994. Rapid detection and identification of Candida albicans and Torulopsis (Candida) glabrata in clinical specimens by species specific nested PCR amplification of a cytochrome P450 lanosterol-α-demethylase (L1A1) gene fragment. J. Clin. Microbiol. 32: 1902-1907.
17. Cerniglia, C. E. 1984. Microbial metabolism of polycyclic aromatic hydrocarbons. In Advances in Applied Microbiology (A. I. Laskin, Ed.), pp. 31-71. Academic Press, New York.
18. Cerniglia, C. E., Freeman, J. P., and Mitchum, R. K. 1982. Glucuronide and sulfate conjugation in the fungal metabolism of aromatic hydrocarbons. Appl. Environ. Microbiol. 43: 1070.
19. Cerniglia, C. E., Sutherland, J. B., and Crow, S. A. 1992. Fungal metabolism of aromatic hydrocarbons. In Microbial Degradation of Natural Products (G. Winkelmann, Ed.), pp. 194-217. Wiley-VCH, Weinheim.
20. Chen, C., Turi, T. G., Sanglard, D., and Loper, J. C. 1987. Isolation of the Candida tropicalis gene for P450 lanosterol demethylase and its expression in Saccharommyces cerevisiae. Biochem. Biophys. Res. Commun. 146: 1311-1317.
21. Ciuffetti, L. M., and VanEtten, H. D. 1996. Virulence of a pisatin demethylase deficient Nectria haematococca MPVI isolate is increased by transformation with a pisatin demethylase gene. Mol. Plant-Microb. Interact. 9: 787-792.
22. De Groot, P. W. J., Schaap, P. J., Van Griensven, L. J. L., and Visser, J. 1997. Isolation of developmentally regulated genes from the edible mushroom Agaricus bisporus. Microbiol. 143: in press.
23. Degtyarenko, K. N. 1995. Structural domains of P450-containing monooxygenase systems. Protein Eng. 8(8): 737-747.
24. Desjardins, A. E., Hohn, T. M., and McCormick, S. P. 1992. The effect of gene disruption of trichodiene synthase (Tox5) on the virulence of Gibberella pulicaris. Mol. Plant-Microb. Interact. 5: 214-222.
25. Dlugonski J., Bartnicka K., Zemelko I., Chojecka V., and Sedlaczek L. (1991). Determination of cytochrome P-450 in Cunninghamella elegans intact protoplasts and cell-free preparations capable of steroid hydroxylation. J. Basic. Microbiol. 31(5): 347-356.
26. Dutta, D., Ghosh, D. K., Mishra, A. K., and Samanta, T. B. 1983. Induction of a Benz"a〉Pyrene hydroxylase in Aspergillus ochraceus TS: Evidence for multiple forms of cytochrome P450. Biochem. Biophys. Res. Commun. 115(2): 692-699.
27. Fowler, T., Rey, M. W., Vähävahe, P., Power, S. D., and Berka, R. M. 1993. 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. 9(5): 989-998.
28. Fukuda, H., Fujii, T., Sukita, E., Tazaki, M., Nagahama, S., and Ogawa, T. 1994. Reconstitution of the isobutene forming reaction catalyzed by cytochrome P450 and P450 reductase from Rhodotorula minuta: Decarboxylation with the formation of isobutene. Biochem. Biophys. Res. Commun. 201: 516-522.
29. Garfinkel, D. 1958. Studies on pig liver microsomes. I. Enzyme and pigment composition of different microsomal fractions. Arch. Biochem. Biophys. 77: 493-509.
30. Geber, A., Hitchcock, C. A., Swartz, J. E., Pullen, F. S., Marsden, K. E., Kwon-Chung, K. J., and Bennet, J. E. 1995. Deletion of the Candida glabrata erg3 and erg11 genes: effect on cell viability, cell growth, sterol composition and antifungal susceptibility. Antomicrob. Agents Chemother. 39: 2708-2717.
31. Ghosh, D. K., Dutta, D., Samanta, T. B., and Mishra, A. K. 1983. Microsomal Benzo"a〉Pyrene hydroxylase in Aspergillus ochraceus TS: Assay and characterization of the enzyme system. Biochem. Biophys. Res. Commun. 113(2): 497-505.
32. Gibson, D. T., and Subramanian, V. 1984. Microbial Degradation of Organic Compounds (D. T. Gibson, Ed.), pp. 181-252. Dekker, New York.
33. Gonzalez, F. J. 1989. The molecular biology of cytochrome P450s. Pharmacol. Rev. 40: 243-288.
34. Gonzalez, F. J., Samore, M., McQuiddy P., and Kasper, C. B. 1982. Effects of 2-acetylaminofluorene and N-hydroxy-2-acetylaminofluorene on the cellular levels of epoxide hydratase, cytochrome P450b and NADPH-cytochrome c (P450) oxidoreductase messenger ribonucleic acids. J. Biol. Chem. 257: 11032-11036.
35. Griffiths, D. A., Best, D. J., and Jezequel, S. G. 1991. The screening of selected micro-organisms for use as models of mammalian drug metabolism. Appl. Microbiol. Biotechnol. 35: 373-381.
36. Griffiths, D. A., Brown, D. E., and Jezequel, S. G. 1993. Metabolism of xenobiotics by Beauveria bassiana. Xenobiotica 23: 1085-1100.
37. Guengerich, F. P., Gillam, E. M. J., Ohmori, S., Sandhu, P., Brian, W. R., Sari, M.-A., and Iwasaki, M. 1993. Expression of human cytrochrome P450 enzymes in yeast and bacteria and relevance to studies on catalytic activities. Toxicology 82: 21-37.
38. Haemmerli, S. D., Leisola, M. S., Sanglard, D., and Fiechter, A. 1986. Oxidation of benzo"a〉pyrene by extracellular ligninase of Phanerochaete chrysosporium: veratryl alcohol and stability of ligninase. J. Biol. Chem. 261: 6900-6903.
39. Hamid, A. B., and Smith, J. E. 1987. Degradation of aflatoxin by Aspergillus flavus. J. Gen. Microbiol. 133: 2023-2029.
40. Hargreaves, J. A., and Keon, J. P. R. 1996. Isolation of an Ustilago maydis erg11 gene and its expression in a mutant deficient in sterol 14 alpha-demethylase activity. FEMS Microbiol. Lett. 139: 203-207.
41. He, J., Ruan, Y., and Straney, D. C. 1996. Analysis of determinants of binding and transcriptional activation of the pisatin responsive DNA binding factor of Nectria haematococca. Mol. Plant-Microb. Interact. 9: 171-179.
42. Hohn, T. M., McCormick, S. P., and Desjardins, A. E. 1993. Evidence for a gene cluster involving trichothecene pathway biosynthesis genes in Fusarium sporotrichioides. Curr. Genet. 24(4): 291-295.
43. Hohn, T. M., Desjardins, A. E., and McCormick, S. P. 1995. The Tri4 gene of Fusarium sporotrichioides encodes a cytochrome P450 monooxygenase involved in trichothecene biosynthesis. Mol. Gen. Genet. 248: 95-102.
44. Holland, H. L. 1992. Bioconversions. In Biotechnology of Filamentous Fungi: Technology and Products (D. B. Finkelstein and C. Ball, Eds.), Chap. 7, pp. 157-187. Butterworth-Heineman, Stoneham.
45. Holland, H. L., Bergen, E. J., Chenchaiah, P. C., Khan, S. H., Munoz, B., Niniss, R. W., and Richards, D. 1987. Side chain hydroxylation of aromatic compounds by fungi. 1. Products and stereochemistry. Can. J. Chem. 65: 502-507.
46. Holland, H. L., Destefano, D., and Ozog, J. 1994. Side chain hydroxylation of aromatic hydrocarbons by fungi. Part 6. Biotransformation of olefins by Mortierella isbellina. Biocatalysis 10: 65-76.
47. Horecker, B. L. 1950. Triphosphorydine nucleotide-cytochrome c reductase in liver. J. Biol. Chem. 183: 593-605.
48. Kaergel, E., Menzel, R., Honeck, H., Vogel, F., Bohmer, A., and Schunck, W. H. 1996. Candida maltosa NADPH-cytochrome P450 reductase: Cloning of a full-length cDNA, heterologous expression in Saccharomyces cerevisiae and function of the N-terminal region for membrane anchoring and proliferation of the endoplasmic reticulum. Yeast 12: 333-348.
49. Kalb, V. F., Loper, J. C., Dey, C. R., Woods, C. W., and Sutter, T. R. 1986. Isolation of a cytochrome P450 structural gene from Saccharomyces cerevisiae. Gene 45: 237-245.
50. Kalb, V. F., Woods, C. W., Turi, T. G., Dey, C. R., Sutter, T. R., and Loper, J. C. 1987. Primary structure of the P450 lanosterol demethylase gene from Saccharomyces cerevisiae. DNA 6: 529-537.
51. Kapteyn, J. C., Pillmoor, J. B., and de Waard, M. A. 1992. Biochemical mechanisms involved in the selective fungitoxicity of two eburicol 14α-demethylation inhibitors, procloraz and an quinconazole: accumulation and metabolism studies. Pestic. Sci. 36: 85-93.
52. Kasper, C. B. 1971. Biochemical distinctions between the nuclear and microsomal membranes from rat hepatocytes. J. Biol. Chem. 246: 577-581.
53. Keller, N. P., and Hohn, T. M. 1997. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet. Biol. 21: 17-29.
54. Keller, N. P., Kantz, N. J., and Adams, T. H. 1994. Aspergillus nidulans verA is required for the production of the mycotoxin sterigmatocystin. Appl. Environ. Microbiol. 60: 1444-1450.
55. Keller, N. P., Segner, S., Bhatnagar, D., and Adams, T. H. 1995. stcS, a putative P-450 monooxygenase, is required for the conversion of versicolorin A to sterigmatocystin in Aspergillus nidulans. Appl. Environ. Microbiol. 61(10): 3628-3632.
56. Keyser, P., Kirk, T. K., and Zeikus, J. G. 1978. Enzyme system of Phanerochaete chrysosporium synthesized in the absence of lignin in response to nitrogen starvation. J. Bacteriol. 135: 790.
57. Kinoshita, H., Atomi, H., Ueda, M., and Tanaka, A. 1994. Characterization of the catalase of the n-alkane utilizing yeast Candida tropicalis functionally expressed in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 40: 682-686.
58. Kizawa, H., Tomura, D., Oda, M., Fukamizu, A., Hoshino, T., Gotoh, O., Yasui, T., and Shoun, H. 1991. Nucleotide sequence of the unique nitrate/nitrite-inducible cytochrome P-450 cDNA from Fusarium oxysporum. J. Biol. Chem. 266(16): 10632-10637.
59. Klingenberg, M. 1958. Pigments of rat liver microsomes. Arch. Biochem. Biophys. 75: 376-386.
60. Kudo, T., Tomura, D., Liu, D. L., Dai, X. Q., and Shoun, H. 1996. Two isozyme sof P450nor of Cylindrocarpon tonkinense: Molecular cloning of the cDNAs and genes, expression in the yeast, and the putative NAD(P)H binding site. Biochimie 78: 792-799.
61. Kurzban, G. P., and Strobel, H. W. 1986. Preparation and characterization of FAD dependent NADPH cytochrome P450 reductase. J. Biol. Chem. 261: 7824-7830.
62. Lai, M. H., and Kirsch, D. R. 1989. Nucleotide sequence of cytochrome P450 L1A1 (lanosterol 14 alpha-demethylase) from Candida albicans. Nucleic Acids Res. 17: 804.
63. Lambert, M., Kremer, S., Sterner, O., and Anke, H. 1994. Metabolism of pyrene by the basidiomycete Crinipellis stipitaria and identification of pyrene quinones and their hydroxylated precursors in strain JK375. Appl. Environ. Microbiol. 60(10): 3597-3601.
64. Lange, B., Kremer, S., Sterner, O., and Anke, H. 1994. Pyrene metabolism in Crinipellis stipitaria: identification of trans-4,5-dihydro-4,5-dihydroxypyrene and 1-pyrenesulfate in strain JK374. Appl. Environ. Microbiol. 60(10): 3602-3607.
65. Launen, L., Pinto, L., Wiebe, C., Kiehlmann, E., and Moore, M. 1995. The oxidation of pyrene and benzo〈a〉;pyrene by nonbasidiomycete soil fungi. Can. J. Microbiol. 41: 477-488.
66. Lesot, A., Hasenfratz, M.-P., Batard, Y., Durst, F., and Benveniste, I. 1995. Two messenger RNAs are encoding for NADPH-cytochrome P450 reductases in Helianthus tuberosus tuber tissues. Plant Physiol. Biochem. 33: 751-757.
67. Lottermoser, K., Schunck, W. H., and Asperger, O. 1996. Cytochrome P450 of the sophorose lipid-producing yeast Candida apicola: Heterogeneity and polymerase chain reaction mediated cloning of two genes. Yeast 12: 565-575.
68. Mahato, S. B., and Majumdar, I. 1993. Current trends in microbial steroid biotransformation. Phytochemistry 34: 883-898.
69. Maloney, A. P., and VanEtten, H. D. 1994. A gene from the fungal plant pathogen Nectria haematococca that encodes the phytoalexin-detoxifying enzyme pisatin demethylase, defines a new cytochrome P450 family. Mol. Gen. Genet. 243: 506-514.
70. Masaphy, S., Levanon, D., Henis, Y., Venkateswarlu, K., and Kelly, S. L. 1995. Microsomal and cytosolic cytochrome P450-mediated benzo〈a〉pyrene hydroxylation in Pleurotus pulmonarius. Biotechnol. Lett. 17(9): 969-974.
71. Masaphy, S., Levanon, D., Henis, Y., Venkateswarlu, K., and Kelly, S. L. 1996. Evidence for cytochrome P450 and P450-mediated benzo〈a〉pyrene hydroxylation in the white rot fungus Phanerochaete chrysosporium. FEMS Microbiol. Lett. 135: 51-55.
72. Meijer, A. H., Lopes-Cardoso, M. I., Voskuilen, J. Th., De Waal, A., Verpoorte, R., and Hoge, J. H. C. 1993. Isolation and characterization of a cDNA clone from Catharanthus roseus encoding NADPH: cytochrome P450 reductase, an enzyme essential for reactions catalyzed by cytochrome P450 monooxygenases in plants. Plant J. 4 (1): 47-60.
73. Miao, V. P., Covert, S. F., and VanEtten, H. D. 1991. A fungal gene for antibiotic resistance on a dispensable ("B") chromosome. Science 254: 1773-1776.
74. Miles, J. S. 1992. Structurally and functionally conserved regions of cytochrome P450 reductase as targets for PCR amplification by the polymerase chain reaction. Cloning and nucleotide sequencing of the Schizosaccharomyces pombe cDNA. Biochem. J. 287: 195-200.
75. Morace, G., Sanguinetti, M., Posteraro, B., Lo Cascio, G., and Fadda, G. 1997. Identification of various medically important Candida species in clinical specimens by PCR-restriction enzyme analysis. J. Clin. Microbiol. 35: 667-672.
76. Mukhopadhyay, C. K., and Chatterjee, I. B. 1994. NADPH intitiated cytochrome P450-mediated free metal ion independent oxidative damage of microsomal proteins. J. Biol. Chem. 269(18): 13390-13397.
77. dNIR) acts as nitric oxide reductase employing NADH as the direct electron donor. J. Biol. Chem. 268: 8350-8355.
78. Nakahara, K., and Shoun, H. 1996. N-terminal processing and amino-acid sequence of two isoforms of nitric oxide reductase cytochrome P450nor from Fusarium oxysporum. J. Biochem. 120: 1082-1087.
79. Nakayama, N., Takemae, A., and Shoun, H. 1996. Cytochrome P450foxy, a catalytically self-sufficient fatty acid hydroxylase of the fungus Fusarium oxysporum. J. Biochem. 119: 435-440.
80. Narhi, L. O., and Fulco, A. J. 1986. Characterization of a catalytically self sufficient 119.000 Dalton P-450 monooxygenase induced by barbiturates in Bacillus megaterium. J. Biol. Chem. 261: 7160-7169.
81. Nebert, D. W., and Gonzalez, F. J. 1987. P-450 genes: Structure, evolution and regulation. Annu. Rev. Biochem. 56: 943-993.
82. Nelson, D. R., Kamataki, T., Waxman, D. J., Guengerich, F. P., Estabrook, R. W., Feyereisen, R., Gonzalez, F. J., Coon, M. J., Gunsalus, I. C., Gotoh, O., Okuda, K., and Nebert, D. W. 1993. The P450 superfamily: Update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol. 12(1): 1-51.
83. Nelson, D. R., Koymans, L., Kamataki, T., Stegeman, J. J., Feyereisen, R., Waxman, D. J., Waterman, M. R., Gotoh, O., Coon, M. J., Estabrook, R. W., Gunsalus, I. C., and Nebert, D. W. 1996. P450 superfamily: Update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics. 6: 1-42.
84. Ohkuma, M., Masuda, Y., Park, S. M., Ohtomo, R., Ohta, A., and Takagi, M. 1995. Evidence that the expression of the gene for NADPH-cytochrome P450 reductase is n-alkane inducible in Candida maltosa. Biosci. Biotech. Biochem. 59(7): 1328-1330.
85. Omura, T., and Sato, R. 1961. A new cytochrome in liver microsomes. J. Biol. Chem. 237: 1375-1376.
86. Paszcynski, A., Huynh, V.-B., and Crawford, R. 1986. Comparison of ligninase-I and peroxidase-M2 from the white rot fungus Phanerochaete chrysosporium. Arch. Biochem. Biophys. 244: 750-765.
87. Pelkonen, O., and Nebert, D. W. 1982. Metabolism of polycyclic aromatic hydrocarbons: Etiologic role in carcinogenesis. Pharmacol. Rev. 34: 189-222.
88. Peterson, D. H., and Murray, H. C. 1952. Microbial oxygenation of steroids at carbon 11. J. Am. Chem. Soc. 74: 1871-1872.
89. Picataggio, S., Rohrer, T., Deanda, K., Lanning, D., Reynolds, R., Mielenz, J., and Eirich, L. D. 1992. Metabolic engineering of Candida tropicalis for the production of long-chain dicarboxylic acids. Bio/ Technology 10: 894-898.
90. Pompon, D., Perret, A., Bellamine, A., Laine, R., Gautier, J.-C., and Urban, P. 1995. Genetically engineered yeast cells and their applications. Toxicol. Lett. 82-83: 815-822.
91. Porter, T. D. 1991. An unusual yet strongly conserved flavoprotein reductase in bacteria and mammals. Trends Biochem. Sci. 16: 154-158.
92. Porter, T. D., and Kasper, C. D. 1986. NADPH-cytochrome P450 oxidoreductase: Flavin mononucleotide and flavin adenine dinucleotide domains evolved from different flavoproteins. Biochemistry 29: 1682-1687.
93. Reimman, C., and VanEtten, H. D. 1994. Cloning and characterization of the PD A6-1 gene encoding a fungal cytochrome P450 which detoxifies the phytoalexin pisatin from garden pea. Gene 146: 221-226.
94. Ross, A. D., Varghese, G., Oporto, B., Carmichael, F. J., and Israel, Y. 1995. Effects of propylthiouracil treatment on NADPH-cytochrome P450 reductase levels, oxygen consumption and hydroxyl radical formation in liver microsomes from rats fed ethanol or acetone chronically. Biochem. Pharmacol. 49(7): 979-989.
95. Rozman, D., and Komel, R. 1992. Transformation of Cochliobolus lunatus with pUT720 changes the steroid hydroxylating ability of the fungus. Curr. Genet. 22: 123-127.
96. Ruan, Y., and Straney, D. C. 1996. Identification of elements in the PDA1 promoter of Nectria haematococca necessary for a high level of transcription in vitro. Mol. Gen. Genet. 250: 29-38.
97. BM-3, a single peptide cytochrome P-450:NADPH-P-450 reductase from Bacillus megaterium. J. Biol. Chem. 264: 10987-10995.
98. Sakaki, T., Shibata, M., Yabusaki, Y., Murakami, H., and Ohkawa, H. 1990. Expression of bovine cytochrome P450c21 and its fused enzyme with yeast NADPH-cytochrome P450 reductase in Saccharomyces cerevisiae. DNA Cell Biol. 9: 603-614.
99. Sakaki, T., Akiyoshi-Shibata, M., Yabusaki, Y., Manabe, K., Murakami, H., and Ohkawa, H. 1991. Progesterone metabolism in recombinant yeast simultaneously expressing bovine cytochromes P450c17 (CYP17A1) and P450c21 (CYP21B1) and yeast NADPH-P450 oxidoreductase. Pharmacogenetics. 1: 86-93.
100. Sanglard, D., Chen, C., and Loper, J. C. 1987. Isolation of the alkane inducible cytochrome P450 (P450alk) gene from the yeast Candida tropicalis. Biochem. Biophys. Res. Commun. 144: 251-257.
101. Sanglard, D., and Loper, J. C. 1989. Characterization of the alkane inducible cytochrome P450 (P450alk) gene from the yeast Candida tropicalis. Gene 76: 121-136.
102. Sanglard, D., and Fiechter, A. 1989. Heterogenity within the alkane inducible cytochrome P450 gene family of Candida tropicalis. FEBS Lett. 256(1,2): 128-134.
103. Sariaslani, F. S. 1989. Microbial enzymes for oxidation of organic molecules. Crit. Rev. Biotech. 9(3): 171-257.
104. Schäfer, W., Straney D., Ciuffetti, L., Vanetten, H. D., and Yoder, O. C. 1989. One enzym makes a fungal pathogen, but not a saprophyte, virulent on a new host plant. Science 246: 247-249.
105. Scala, F., Matthews, D., Costa, M., and Vanetten, H. D. 1988. Immunochemical relatedness of fungal NADPH-cytochrome P450 reductases and their ability to reconstitute pisatin demethylase activity. Exp. Mycol. 12: 377-385.
106. Scheller, U., Zimmer, T., Kärgel, E., and Schunck, W. H. 1996. Characterization of the n-alkane and fatty acid hydroxylating cytochrome P450 forms 52A3 and 52A4. Arch. Biochem. Biophys. 328: 245-254.
107. Schunck, W.-H., Vogel, F., Gross, B., Kaergel, E., Mauersberger, S., Koepke, K., Gengnagel, C., and Mueller, H. G. 1991. Comparison of two cytochrome P450s from Candida maltosa: Primary structure, substrate specificities, and effects of their expression in Saccharomyces cerevisiae on the proliferation of the endoplasmic reticulum. Eur. J. Cell. Biol. 55: 336-345.
108. Seghezzi, W., Sanglard, D., and Fiechter, A. 1991. Characterization of a second alkane inducible cytochrome P450-encoding gen, Cyp52A2, from Candida tropicalis. Gene 106: 51-60.
109. Seghezzi, W., Meili, C., Ruffiner, R., Künzi, R., Sanglard, D., and Fiechter, A. 1992. Identification and characterization of additional members of the cytochrome P450 multigene family cyp52 of Candida tropicalis. DNA Cell Biol. 11(10): 767-780.
110. Sengstag, C., Eugster, H.-P., and Würgler, F. E. 1994. High promutagen activating capacity of yeast microsomes containing human cytochrome P450 1A and human NADPH-cytochrome P450 reductase. Carcinogenesis 15(5): 837-843.
111. Shen, A. L., Porter, T. D., Wilson, T. E., and Kasper, C. B. 1989. Structural analysis of the FMN binding domain of NADPH-cytochrome P450 oxidoreductase by site directed mutagenesis. J. Biol. Chem. 264: 7584-7589.
112. Shephard, E. A., Plamer, C. N., Segall, H. J., and Phillips, I. R. 1992. Quantification of cytochrome P450 reductase gene expression in human tissue. Arch. Biochem. Biophys. 294: 168-172.
113. Shibata, M., Sakaki, T., Yabusaki, Y., Murakami, H., and Ohkawa, H. 1990. Genetically engineered P450 monooxygenase: Construction of bovine P450c17/Yeast reductase fused enzymes. DNA Cell Biol. 9(1): 27-36.
114. Shoun, H., and Tanimoto, T. 1991. Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P450 in the respiratory nitrite reduction. J. Biol. Chem. 266(17): 11078-11082.
115. Skaggs, B. A., Alexander, J. F., Pierson, C. A., Scweitzer, K. S., Chun, K. T., Koegel, C., Barbuch, R., and Bard, M. 1996. Cloning and characterization of the Saccharomyces cerevisiae C-22 sterol desaturase gene, encoding a second cytochrome P450 involved in ergosterol biosynthesis. Gene 169: 105-109.
116. Smith, K. E., Ahmed, F., and Antoniou, T. 1993. Microbial transformations of steroids. Biochem. Soc. Trans. 21: 1077-1080.
117. Smith, K. E., Ahmed, F., Williams, R. A. D., and Kelly, S. L. 1994. Microbial transformation of steroids-VIII. Transformation of progesterone by whole cells and microsomes of Aspergillus fumigatus. J. Steroid Biochem. Mol. Biol. 49(1): 93-100.
118. Stewart, P., Whitwam, R. E., Kersten, P. J., Cullen, D., and Tien, M. 1996. Efficient expression of a Phanerochaete chrysosporium manganese peroxidase gene in Aspergillus oryzae. Appl. Environ. Microbiol. 62: 860-864.
119. Straney, D. C., and VanEtten, H. D. 1994. Characterization of the PDA1 promoter of Nectria haematococca and identification of a region that binds a pisatin-responsive DNA binding factor. Mol. Plant.-Microb. Interact. 7: 256-266.
120. Sutherland, J. B. 1992. Detoxification of polycyclic aromatic hydrocarbons by fungi. J. Indian Microbiol. 9: 53-62.
121. Sutter, T. R., Sanglard, D., and Loper, J. C. 1990. Isolation and characterization of the alkane-inducible NADPH-cytochrome P450 oxidoreductase gene from Candida tropicalis. J. Biol. Chem. 265(27): 16428-16436.
122. Takagi, M., Ohkuma, M., Kobayashi, N., Watanabe, M., and Yano, K. 1989. Purification of cytochrome P450alk from n-alkane grown cells of Candida maltosa, and cloning and nucleotide sequencing of the encoding gene. Agric. Biol. Chem. 53: 2217-2226.
123. 5. Gene 125: 49-55.
124. Urban, P., Cullin, C., and Pompon, D. 1990. Maximizing the expression of mammalian cytochrome P450 monooxygenase activities in yeast cells. Biochemie 72: 463-472.
125. Urban, P., Mignotte, C., Kazmaier, M., Delorme, F., and Pompon, D. 1997. Cloning, yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450 CYP73A5. J. Biol. Chem. 272: 19176-19186.
126. Vanden Bossche, H. 1988. Mode of action of pyridine, pyrimidine and azole antifungals. In Sterol Biosynthesis Inhibitors: Pharmaceutical and Agrochemical Aspects (D. Berg and M. Plempel, Eds.), pp. 79-119. Horwood, Chichester, UK.
127. Vanden Bossche, H. 1990. Importance and role of sterols in fungal membranes. In Biochemistry of Cell Walls and Membranes in Fungi (P. J. Kuhn, A. P. J. Trinci, M. J. Jung, M. W. Goosey, and L. G. Copping, Eds.), pp. 135-158. Springer-Verlag, Berlin.
128. Van den Brink, J. M. 1997. Cytochrome P450 Reductase of Aspergillus niger: A Molecular Biological Study. Thesis, Leiden State Univ., The Netherlands.
129. Van den Brink, J. M., Van Zeijl, C. M. J., Brons, J. F., Van den Hondel, C. A. M. J. J., and Van Gorcom, R. F. M. 1995. Cloning and characterization of the NADPH-cytochrome P450 oxidoreductase gene from the filamentous fungus Aspergillus niger. DNA Cell Biol. 14(8): 719-729.
130. Van den Brink, J. M., Van den Hondel, C. A. M. J. J., and Van Gorcom, R. F. M. 1996a. Optimization of the benzoate inducible benzoate p-hydroxylase cytochrome P450 enzyme system in Aspergillus niger. Appl. Microbiol. Biotechnol. 46: 360-364.
131. Van den Brink, J. M., Van Nistelrooy, J. G. M., De Waard, M. A., Van den Hondel, C. A. M. J. J., and Van Gorcom, R. F. M. 1996b. Increased resistance to 14α-demethylase inhibitors (DMIs) in Aspergillus niger by coexpression of the Penicillium italicum eburicol 14α-demethylase (cyp51) and the Aspergillus niger cytochrome P450 reductase (cprA) genes. J. Biotechnol. 49: 13-18.
132. Van Dyk, M. S., Kock, J. L. F., and Botha, A. 1994. Hydroxy long-chain acids in fungi. World J. Microbiol. Biotechnol. 10: 495-504.
133. VanEtten, H. D., Matthews, D. E., and Matthews, P. S. 1989. Phytoalexin detoxification: Importance for pathogenicity and practical implications. Annu. Rev. Phytopathol. 27: 143-164.
134. Van Gorcom, R. F. M., Boschloo, J. G., Kuijvenhoven, A., Lange, J., Van Vark, A. J., Bos, C. J., Van Balken, J. A. M., Pouwels, P. H., and Van den Hondel, C. A. M. J. J. 1990. Isolation and molecular characterisation of the benzoate-para-hydroxylase gene (bphA) of Aspergillus niger. A member of a new gene family of the cytochrome P450 superfamily. Mol. Gen. Genet. 223: 192-197.
135. Van Nistelrooy, J. G. M., Van den Brink, J. M., Van Kan, J. A. L., Van Gorcom, R. F. M., and De Waard, M. A. 1996. Isolation and molecular characterization of the gene encoding eburicol 14α-demethylase from Penicillium italicum. Mol. Gen. Genet. 250(6): 725-733.
136. 5 in yeast and characterization of mutants of the membrane anchor domain. J. Biol. Chem. 267: 12583-12591.
137. Vermillion, J. L., and Coon, M. J. 1974. Highly purified detergent-solubilized NADPH-cytochrome P450 reductase from phenobarbital-induced rat liver microsomes. Biochem. Biophys. Res. Commun. 60: 1315-1322.
138. Vermillion, J. L., Ballou, D. P., Massey, V., and Coon, M. J. 1981. Separate roles for FMN and FAD in catalysis by liver microsomal NADPH-cytochrome P450 reductase. J. Biol. Chem. 256: 266-277.
139. Vitas, M., Rozman, D., Komel, R., and Kelly, S. L. 1995. P450-mediated progesterone hydroxylation in Cochliobolus lunatus. J. Biotechnol. 42: 145-150.
140. Weltring, K. M., Turgeon, B. G., Yoder, O. C., and VanEtten, H. D. 1988. Isolation of a phytoalexin-detoxification gene from the plant pathogenic fungus Nectria haematococca by detecting its expression in Aspergillus nidulans. Gene 68: 335-344.
141. White, R. E., and Coon, M. J. 1980. Oxygen activation by cytochrome P-450. Annu. Rev. Biochem. 49: 315-356.
142. Wiseman, A. 1993. Genetically engineered mammalian cytochrome P450 from yeast-potential applications. Trends Biotechnol. 11: 131-136.
143. Wunder, T., Kremer, S., Sterner, O., and Anke, H. 1994. Metabolism of the polycyclic aromatic hydrocarbon pyrene by Aspergillus niger SK 9317. Appl. Microbiol. Biotechnol. 42: 636-641.
144. Yabusaki, Y. 1995. Artificial P450/reductase fusion enzymes: What can we learn from their structures? Biochemie 77: 594-603.
145. Yabusaki, Y., Murakami, H., and Ohkawa, H. 1988. Primary structure of Saccharomyces cerevisiae NADPH-cytochrome P450 reductase deduced from nucleotide sequence of its cloned gene. J. Biochem. 103: 1004-1010.
146. Yu, J., Chang, P. K., Cary, J. W., Wright, M., Bhatnagar, D., Cleveland, T. E., Payne, G. A., and Linz, J. E. 1995. Comparative mapping of aflatoxin pathway gene clusters in Aspergillus parasiticus and Aspergillus flavus. Appl. Environ. Microbiol. 61: 2365-2371.