At the crossroads of steroid hormone biosynthesis: The role, substrate specificity and evolutionary development of CYP17

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 1, 2011, Pages 200-209

  Gilep, Andrei A ^a   Sushko, Tatyana A ^a   Usanov, Sergey A ^a  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Belarus)

Author keywords

CYP17; Cytochrome P450; Steroid 17 alpha hydroxylase 17,20 lyase; Steroid hormone biosynthesis

Indexed keywords

CYTOCHROME P450 17; CYTOCHROME P450 INHIBITOR; GLUCOCORTICOID; MINERALOCORTICOID; PREGNENOLONE DERIVATIVE; PROGESTERONE DERIVATIVE; RECOMBINANT ENZYME; STEROID 17ALPHA MONOOXYGENASE; STEROID HORMONE;

AMINO ACID SEQUENCE; CATALYSIS; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENCE; STEROID HYDROXYLATION; STEROIDOGENESIS; XENOBIOTIC METABOLISM;

AMINO ACID SEQUENCE; ANIMALS; EVOLUTION, MOLECULAR; HORMONES; HUMANS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; STEROID 17-ALPHA-HYDROXYLASE; STEROIDS; SUBSTRATE SPECIFICITY;

CHORDATA;

EID: 78649450343     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.06.021     Document Type: Review

References (104)

1. W.L. Miller Structure of genes encoding steroidogenic enzymes J. Steroid Biochem. 27 1987 759 766
2. S. Dharia, A. Slane, M. Jian, M. Conner, A.J. Conley, and C.R. Jr Parker Colocalization of P450c17 and cytochrome b5 in androgen-synthesizing tissues of the human Biol. Reprod. 71 2004 83 88
3. A. Slominski, G. Ermak, and M. Mihm ACTH receptor, CYP11A1, CYP17 and CYP21A2 genes are expressed in skin J. Clin. Endocrinol. Metab. 81 1996 2746 2749
4. V. Pezzi, J.M. Mathis, W.E. Rainey, and B.R. Carr Profiling transcript levels for steroidogenic enzymes in fetal tissues J. Steroid Biochem. Mol. Biol. 87 2003 181 189
5. R. Voutilainen, and W.L. Miller Developmental expression of genes for the stereoidogenic enzymes P450scc (20, 22-desmolase), P450c17 (17 alpha-hydroxylase/17, 20-lyase), and P450c21 (21-hydroxylase) in the human fetus J. Clin. Endocrinol. Metab. 63 1986 1145 1150
6. C.J. Lin, J.W. Martens, and W.L. Miller NF-1C, Sp1, and Sp3 are essential for transcription of the human gene for P450c17 (steroid 17alpha-hydroxylase/ 17, 20 lyase) in human adrenal NCI-H295A cells Mol. Endocrinol. 15 2001 1277 1293
7. J.C. Huber, C. Schneeberger, and C.B. Tempfer Genetic modelling of the estrogen metabolism as a risk factor of hormone-dependent disorders Maturitas 42 2002 1 12 (Pubitemid 34521716)
8. I.L. Gilep, N.N. Ivanchikova, I.L. Rybina, and A.A. Gilep Interrelation of structural (C/T-34) polymorphism of human gene CYP17A1 with biochemical and bionergetics characteristics of the organism Vestn. FFR 4 2009 118 125
9. S. Monno, H. Ogawa, T. Date, M. Fujioka, W.L. Miller, and M. Kobayashi Mutation of histidine 373 to leucine in cytochrome P450c17 causes 17 alpha-hydroxylase deficiency J. Biol. Chem. 268 1993 25811 25817
10. C.E. Fardella, D.W. Hum, J. Homoki, and W.L. Miller Point mutation of Arg440 to His in cytochrome P450c17 causes severe 17 alpha-hydroxylase deficiency J. Clin. Endocrinol. Metab. 79 1994 160 164
11. D. Lin, J.A. Harikrishna, C.C. Moore, K.L. Jones, and W.L. Miller Missense mutation serine106-proline causes 17 alpha-hydroxylase deficiency J. Biol. Chem. 266 1991 15992 15998
12. T. Imai, H. Globerman, J.M. Gertner, N. Kagawa, and M.R. Waterman Expression and purification of functional human 17 alpha-hydroxylase/17, 20-lyase (P450c17) in Escherichia coli. Use of this system for study of a novel form of combined 17 alpha-hydroxylase/17, 20-lyase deficiency J. Biol. Chem. 268 1993 19681 19689
13. R. Ahlgren, T. Yanase, E.R. Simpson, J.S. Winter, and M.R. Waterman Compound heterozygous mutations (Arg 239-stop, Pro 342-Thr) in the CYP17 (P45017 alpha) gene lead to ambiguous external genitalia in a male patient with partial combined 17 alpha-hydroxylase/17, 20-lyase deficiency J. Clin. Endocrinol. Metab. 74 1992 667 672
14. T. Yanase, M.R. Waterman, M. Zachmann, J.S. Winter, E.R. Simpson, and M. Kagimoto Molecular basis of apparent isolated 17, 20-lyase deficiency: compound heterozygous mutations in the C-terminal region (Arg(496)-Cys, Gln(461)-Stop) actually cause combined 17 alpha-hydroxylase/17, 20-lyase deficiency Biochim. Biophys. Acta 1139 1992 275 279
15. D.H. Geller, R.J. Auchus, B.B. Mendonca, and W.L. Miller The genetic and functional basis of isolated 17, 20-lyase deficiency Nat. Genet. 17 1997 201 205
16. D.H. Geller, R.J. Auchus, and W.L. Miller P450c17 mutations R347H and R358Q selectively disrupt 17, 20-lyase activity by disrupting interactions with P450 oxidoreductase and cytochrome b5 Mol. Endocrinol. 13 1999 167 175
17. R.J. Auchus, and W.L. Miller Molecular modeling of human P450c17 (17alpha-hydroxylase/17, 20-lyase): insights into reaction mechanisms and effects of mutations Mol. Endocrinol. 13 1999 1169 1182
18. A. Biason-Lauber, E. Leiberman, and M. Zachmann A single amino acid substitution in the putative redox partner-binding site of P450c17 as cause of isolated 17, 20-lyase deficiency J. Clin. Endocrinol. Metab. 82 1997 3807 3812
19. P. Swart, A.C. Swart, M.R. Waterman, R.W. Estabrook, and J.I. Mason Progesterone 16 alpha-hydroxylase activity is catalyzed by human cytochrome P450 17 alpha-hydroxylase J. Clin. Endocrinol. Metab. 77 1993 98 102
20. C. Beaudoin, B. Lavallee, Y. Tremblay, D.W. Hum, R. Breton, Y. de Launoit, and A. Belanger Modulation of 17alpha-hydroxylase/17, 20-lyase activity of guinea pig cytochrome P450c17 by site-directed mutagenesis DNA Cell Biol. 17 1998 707 715
21. M. Cloutier, A. Fleury, J. Courtemanche, L. Ducharme, J.I. Mason, and J.G. Lehoux Characterization of the adrenal cytochrome P450C17 in the hamster, a small animal model for the study of adrenal dehydroepiandrosterone biosynthesis DNA Cell Biol. 16 1997 357 368
22. W. Arlt, J.W. Martens, M. Song, J.T. Wang, R.J. Auchus, and W.L. Miller Molecular evolution of adrenarche: structural and functional analysis of P450c17 from four primate species Endocrinology 143 2002 4665 4672
23. G.B. Cutler Jr., M. Glenn, M. Bush, G.D. Hodgen, C.E. Graham, and D.L. Loriaux Adrenarche: a survey of rodents, domestic animals, and primates Endocrinology 103 1978 2112 2118
24. V.D. Castracane, G.B. Cutler Jr., and D.L. Loriaux Pubertal endocrinology of the baboon: adrenarche Am. J. Physiol. 241 1981 305 309
25. D.B. Gower 16-Unsaturated C 19 steroids. A review of their chemistry, biochemistry and possible physiological role J. Steroid Biochem. 3 1972 45 103
26. N. Ahmad, and D.B. Gower The biosynthesis of some androst-16-enes from C21 and C19 steroids in boar testicular and adrenal tissue Biochem. J. 108 1968 233 241
27. S. Nakajin, M. Takahashi, M. Shinoda, and P.F. Hall Cytochrome b5 promotes the synthesis of delta 16-C19 steroids by homogeneous cytochrome P-450 C21 side-chain cleavage from pig testis Biochem. Biophys. Res. Commun. 132 1985 708 713
28. P. Soucy, L. Lacoste, and V. Luu-The Assessment of porcine and human 16-ene-synthase, a third activity of P450c17, in the formation of an androstenol precursor. Role of recombinant cytochrome b5 and P450 reductase Eur. J. Biochem. 270 2003 1349 1355
29. P. Lee-Robichaud, J.N. Wright, M.E. Akhtar, and M. Akhtar Modulation of the activity of human 17 alpha-hydroxylase-17, 20-lyase (CYP17) by cytochrome b5: endocrinological and mechanistic implications Biochem. J. 308 Pt 3 1995 901 908
30. A.C. Swart, N.W. Kolar, N. Lombard, J.I. Mason, and P. Swart Baboon cytochrome P450 17alpha-hydroxylase/17, 20-lyase (CYP17) Eur. J. Biochem. 269 2002 5608 5616
31. M.S. Shet, C.W. Fisher, Y. Tremblay, A. Belanger, A.J. Conley, J.I. Mason, and R.W. Estabrook Comparison of the 17 alpha-hydroxylase/C17, 20-lyase activities of porcine, guinea pig and bovine P450c17 using purified recombinant fusion proteins containing P450c17 linked to NADPH-P450 reductase Drug Metab. Rev. 39 2-3 2007 289 307
32. K. Suhara, Y. Fujimura, M. Shiroo, and M. Katagiri Multiple catalytic properties of the purified and reconstituted cytochrome P-450 (P-450sccII) system of pig testis microsomes J. Biol. Chem. 259 1984 8729 8736
33. M.K. Gupta, O.L. Guryev, and R.J. Auchus 5alpha-reduced C21 steroids are substrates for human cytochrome P450c17 Arch. Biochem. Biophys. 418 2003 151 160
34. O. Guryev, R.A. Carvalho, S. Usanov, A. Gilep, and R.W. Estabrook A pathway for the metabolism of vitamin D3: unique hydroxylated metabolites formed during catalysis with cytochrome P450scc (CYP11A1) Proc. Natl. Acad. Sci. USA 100 2003 14754 14759
35. T.A. Pechurskaya, A.A. Gilep, T.S. Cherkesova, M.P. Duarte, J. Rueff, M. Kranendonk, R.W. Estabrook, and S.A. Usanov CYP17 substrate specificity 16th International Symposium on Microsomes and Drug Oxidation, Budapest, Hungary, September 3-7 2006 178
36. V. Papadopoulos, Y. Liu, and Z.X. Yao Cytochrome P450 17alpha hydroxylase/17, 20 lyase (CYP17) function in cholesterol biosynthesis: identification of squalene monooxygenase (epoxidase) activity associated with CYP17 in Leydig cells Mol. Endocrinol. 19 2005 1918 1931
37. N. Mast, R. Norcross, U. Andersson, M. Shou, K. Nakayama, I. Bjorkhem, and I.A. Pikuleva Broad substrate specificity of human cytochrome P450 46A1 which initiates cholesterol degradation in the brain Biochemistry 42 2003 14284 14292
38. B.O. Lund, and J. Lund Novel involvement of a mitochondrial steroid hydroxylase (P450c11) in xenobiotic metabolism J. Biol. Chem. 270 1995 20895 20897
39. T. Niwa, R. Sato, Y. Yabusaki, F. Ishibashi, and M. Katagiri Contribution of human hepatic cytochrome P450s and steroidogenic CYP17 to the N-demethylation of aminopyrine Xenobiotica 29 1999 187 193
40. E. Baston, and F.R. Leroux Inhibitors of steroidal cytochrome P450 enzymes as targets for drug development Recent Pat. Anticancer Drug Discov. 2 2007 31 58
41. V.C. Njar, and A.M. Brodie Inhibitors of 17alpha-hydroxylase/17, 20-lyase (CYP17): potential agents for the treatment of prostate cancer Curr. Pharm. Des. 5 1999 163 180
42. S.E. Barrie, B.P. Haynes, G.A. Potter, F.C. Chan, P.M. Goddard, M. Dowsett, and M. Jarman Biochemistry and pharmacokinetics of potent non-steroidal cytochrome P450(17alpha) inhibitors J. Steroid Biochem. Mol. Biol. 60 1997 347 351
43. G.A. Potter, S.E. Barrie, M. Jarman, and M.G. Rowlands Novel steroidal inhibitors of human cytochrome P45017 alpha (17 alpha-hydroxylase-C17, 20-lyase): potential agents for the treatment of prostatic cancer J. Med. Chem. 38 1995 2463 2471
44. T.D. Porter, and C.B. Kasper NADPH-cytochrome P-450 oxidoreductase: flavin mononucleotide and flavin adenine dinucleotide domains evolved from different flavoproteins Biochemistry 25 1986 1682 1687
45. T.D. Porter An unusual yet strongly conserved flavoprotein reductase in bacteria and mammals Trends Biochem. Sci. 16 1991 154 158
46. T.D. Porter, and C.B. Kasper Coding nucleotide sequence of rat NADPH-cytochrome P-450 oxidoreductase cDNA and identification of flavin-binding domains Proc. Natl. Acad. Sci. USA 82 1985 973 977
47. I. Schuster, and R. Bernhardt Inhibition of cytochromes p450: existing and new promising therapeutic targets Drug Metab. Rev. 39 2-3 2007 481 499
48. T. Hakki, and R. Bernhardt CYP 17- and CYP11B-dependent steroid hydroxylases as drug development targets Pharmacol. Therap. 111 2006 27 52
49. R. Narayanasami, J.D. Otvos, C.B. Kasper, A. Shen, J. Rajagopalan, T.J. McCabe, J.R. Okita, D.J. Hanahan, and B.S. Masters 31P NMR spectroscopic studies on purified, native and cloned, expressed forms of NADPH-cytochrome P450 reductase Biochemistry 31 1992 4210 4218
50. T. Sugiyama, Y. Nisimoto, H.S. Mason, and T.M. Loehr Flavins of NADPH-cytochrome P-450 reductase: evidence for structural alteration of flavins in their one-electron-reduced semiquinone states from resonance Raman spectroscopy Biochemistry 24 1985 3012 3019
51. L. Aigrain, D. Pompon, S. Morera, and G. Truan Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase EMBO Rep. 10 2009 742 747
52. M. Wang, D.L. Roberts, R. Paschke, T.M. Shea, B.S. Masters, and J.J. Kim Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes Proc. Natl. Acad. Sci. USA 94 1997 8411 8416
53. P.A. Hubbard, A.L. Shen, R. Paschke, C.B. Kasper, and J.J. Kim NADPH-cytochrome P450 oxidoreductase. Structural basis for hydride and electron transfer J. Biol. Chem. 276 2001 29163 29170
54. D. Hamdane, C. Xia, S.C. Im, H. Zhang, J.J. Kim, and L. Waskell Structure and function of an NADPH-cytochrome P450 oxidoreductase in an open conformation capable of reducing cytochrome P450 J. Biol. Chem. 284 2009 11374 11384
55. J.L. Vermilion, and M.J. Coon Identification of the high and low potential flavins of liver microsomal NADPH-cytochrome P-450 reductase J. Biol. Chem. 253 1978 8812 8819
56. T. Iyanagi, R. Makino, and F.K. Anan Studies on the microsomal mixed-function oxidase system: mechanism of action of hepatic NADPH-cytochrome P-450 reductase Biochemistry 20 1981 1722 1730
57. A.Y. Lu, K.W. Junk, and M.J. Coon Resolution of the cytochrome P-450-containing omega-hydroxylation system of liver microsomes into three components J. Biol. Chem. 244 1969 3714 3721
58. A.A. Gilep, O.L. Guryev, S.A. Usanov, and R.W. Estabrook An enzymatically active chimeric protein containing the hydrophilic form of NADPH-cytochrome P450 reductase fused to the membrane-binding domain of cytochrome b5 Biochem. Biophys. Res. Commun. 284 2001 937 941
59. T.A. Bonina, A.A. Gilep, R.W. Estabrook, and S.A. Usanov Engineering of proteolytically stable NADPH-cytochrome P450 reductase Biochem. Mosc. 70 2005 357 365
60. A. Bridges, L. Gruenke, Y.T. Chang, I.A. Vakser, G. Loew, and L. Waskell Identification of the binding site on cytochrome P450 2B4 for cytochrome b5 and cytochrome P450 reductase J. Biol. Chem. 273 1998 17036 17049 (Pubitemid 28311737)
61. A.L. Shen, K.A. O'Leary, and C.B. Kasper Association of multiple developmental defects and embryonic lethality with loss of microsomal NADPH-cytochrome P450 oxidoreductase J. Biol. Chem. 277 2002 6536 6541
62. D.M. Otto, C.J. Henderson, D. Carrie, M. Davey, T.E. Gundersen, R. Blomhoff, R.H. Adams, C. Tickle, and C.R. Wolf Identification of novel roles of the cytochrome p450 system in early embryogenesis: effects on vasculogenesis and retinoic Acid homeostasis Mol. Cell. Biol. 23 2003 6103 6116
63. J. Gu, Y. Weng, Q.Y. Zhang, H. Cui, M. Behr, L. Wu, W. Yang, L. Zhang, and X. Ding Liver-specific deletion of the NADPH-cytochrome P450 reductase gene: impact on plasma cholesterol homeostasis and the function and regulation of microsomal cytochrome P450 and heme oxygenase J. Biol. Chem. 278 2003 25895 25901
64. B.B. Dunning, and X. Machne Membrane capacitance measurements during acetylcholine action Neuropharmacology 15 1976 73 75
65. C.E. Fluck, and W.L. Miller P450 oxidoreductase deficiency: a new form of congenital adrenal hyperplasia Curr. Opin. Pediatr. 18 2006 435 441
66. A.V. Pandey, C.E. Fluck, N. Huang, T. Tajima, K. Fujieda, and W.L. Miller P450 oxidoreductase deficiency: a new disorder of steroidogenesis affecting all microsomal P450 enzymes Endocr. Res. 30 2004 881 888
67. A.V. Pandey, P. Kempna, G. Hofer, P.E. Mullis, and C.E. Fluck Modulation of human CYP19A1 activity by mutant NADPH P450 oxidoreductase Mol. Endocrinol. 21 2007 2579 2595
68. M. Janner, A.V. Pandey, P.E. Mullis, and C.E. Fluck Clinical and biochemical description of a novel CYP21A2 gene mutation 962-963insA using a new 3D model for the P450c21 protein Eur. J. Endocrinol. 155 2006 143 151
69. M. Sakaguchi, K. Mihara, and R. Sato Signal recognition particle is required for co-translational insertion of cytochrome P-450 into microsomal membranes Proc. Natl. Acad. Sci. USA 81 1984 3361 3364
70. E.P. Neve, and M. Ingelman-Sundberg A soluble NH(2)-terminally truncated catalytically active form of rat cytochrome P450 2E1 targeted to liver mitochondria(1) FEBS Lett. 460 1999 309 314
71. H.K. Anandatheerthavarada, S. Addya, J. Mullick, and N.G. Avadhani Interaction of adrenodoxin with P4501A1 and its truncated form P450MT2 through different domains: differential modulation of enzyme activities Biochemistry 37 1998 1150 1160
72. S.J. Pernecky, and M.J. Coon N-terminal modifications that alter P450 membrane targeting and function Meth. Enzymol. 272 1996 25 34
73. E.M. Gillam, T. Baba, B.R. Kim, S. Ohmori, and F.P. Guengerich Expression of modified human cytochrome P450 3A4 in Escherichia coli and purification and reconstitution of the enzyme Arch. Biochem. Biophys. 305 1993 123 131 (Pubitemid 23242002)
74. E.M. Gillam, Z. Guo, and F.P. Guengerich Expression of modified human cytochrome P450 2E1 in Escherichia coli, purification, and spectral and catalytic properties Arch. Biochem. Biophys. 312 1994 59 66
75. S.J. Pernecky, J.R. Larson, R.M. Philpot, and M.J. Coon Expression of truncated forms of liver microsomal P450 cytochromes 2B4 and 2E1 in Escherichia coli: influence of NH2-terminal region on localization in cytosol and membranes Proc. Natl. Acad. Sci. USA 90 1993 2651 2655
76. C. von Wachenfeldt, T.H. Richardson, J. Cosme, and E.F. Johnson Microsomal P450 2C3 is expressed as a soluble dimer in Escherichia coli following modification of its N-terminus Arch. Biochem. Biophys. 339 1997 107 114
77. J. Cosme, and E.F. Johnson Engineering microsomal cytochrome P450 2C5 to be a soluble, monomeric enzyme. Mutations that alter aggregation, phospholipid dependence of catalysis, and membrane binding J. Biol. Chem. 275 2000 2545 2553
78. Y. Sagara, H.J. Barnes, and M.R. Waterman Expression in Escherichia coli of functional cytochrome P450c17 lacking its hydrophobic amino-terminal signal anchor Arch. Biochem. Biophys. 304 1993 272 278
79. C. De Lemos-Chiarandini, A.B. Frey, D.D. Sabatini, and G. Kreibich Determination of the membrane topology of the phenobarbital-inducible rat liver cytochrome P-450 isoenzyme PB-4 using site-specific antibodies J. Cell Biol. 104 1987 209 219
80. S. Graham-Lorence, B. Amarneh, R.E. White, J.A. Peterson, and E.R. Simpson A three-dimensional model of aromatase cytochrome P450 Protein Sci. 4 1995 1065 1080
81. J.A. Peterson, and S.E. Graham A close family resemblance: the importance of structure in understanding cytochromes P450 Structure 6 1998 1079 1085
82. T.A. Pechurskaya, O.P. Lukashevich, A.A. Gilep, and S.A. Usanov Engineering, expression, and purification of "soluble" human cytochrome P45017alpha and its functional characterization Biochem. Mosc. 73 2008 806 811
83. M. Lehnerer, J. Schulze, R. Bernhardt, and P. Hlavica Some properties of mitochondrial adrenodoxin associated with its nonconventional electron donor function toward rabbit liver microsomal cytochrome P450 2B4 Biochem. Biophys. Res. Commun. 254 1999 83 87
84. M.S. Dong, H. Yamazaki, Z. Guo, and F.P. Guengerich Recombinant human cytochrome P450 1A2 and an N-terminal-truncated form: construction, purification, aggregation properties, and interactions with flavodoxin, ferredoxin, and NADPH-cytochrome P450 reductase Arch. Biochem. Biophys. 327 1996 11 19
85. T.A. Pechurskaya, I.N. Harnastai, I.P. Grabovec, A.A. Gilep, and S.A. Usanov Adrenodoxin supports reactions catalyzed by microsomal steroidogenic cytochrome P450s Biochem. Biophys. Res. Commun. 353 2007 598 604
86. R.W. Estabrook, M.R. Franklin, B. Cohen, A. Shigamatzu, and A.G. Hildebrandt Biochemical and genetic factors influencing drug metabolism. Influence of hepatic microsomal mixed function oxidation reactions on cellular metabolic control Metabolism 20 1971 187 199
87. W.L. Backes, C.J. Batie, and G.F. Cawley Interactions among P450 enzymes when combined in reconstituted systems: formation of a 2B4-1A2 complex with a high affinity for NADPH-cytochrome P450 reductase Biochemistry 37 1998 12852 12859
88. R.W. Kelley, D. Cheng, and W.L. Backes Heteromeric complex formation between CYP2E1 and CYP1A2: evidence for the involvement of electrostatic interactions Biochemistry 45 2006 15807 15816
89. G.F. Cawley, C.J. Batie, and W.L. Backes Substrate-dependent competition of different P450 isozymes for limiting NADPH-cytochrome P450 reductase Biochemistry 34 1995 1244 1247
90. E. Hazai, and D. Kupfer Interactions between CYP2C9 and CYP2C19 in reconstituted binary systems influence their catalytic activity: possible rationale for the inability of CYP2C19 to catalyze methoxychlor demethylation in human liver microsomes Drug Metab. Dispos. 33 2005 157 164
91. M. Subramanian, M. Low, C.W. Locuson, and T.S. Tracy CYP2D6-CYP2C9 protein-protein interactions and isoform-selective effects on substrate binding and catalysis Drug Metab. Dispos. 37 2009 1682 1689
92. R.W. Kelley, J.R. Reed, and W.L. Backes Effects of ionic strength on the functional interactions between CYP2B4 and CYP1A2 Biochemistry 44 2005 2632 2641
93. Y. Tan, C.J. Patten, T. Smith, and C.S. Yang Competitive interactions between cytochromes P450 2A6 and 2E1 for NADPH-cytochrome P450 oxidoreductase in the microsomal membranes produced by a baculovirus expression system Arch. Biochem. Biophys. 342 1997 82 91
94. W.L. Backes, and R.W. Kelley Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes Pharmacol. Ther. 98 2003 221 233
95. S. Praporski, S.M. Ng, A.D. Nguyen, C.J. Corbin, A. Mechler, J. Zheng, A.J. Conley, and L.L. Martin Organization of cytochrome P450 enzymes involved in sex steroid synthesis: protein-protein interactions in lipid membranes J. Biol. Chem. 284 2009 33224 33232
96. M. Subramanian, H. Tam, H. Zheng, and T.S. Tracy CYP2C9-CYP3A4 protein-protein interactions: role of the hydrophobic N-terminus Drug Metab. Dispos. 38 6 2010 1003 1009
97. M.K. Akhtar, S.L. Kelly, and M.A. Kaderbhai Cytochrome b(5) modulation of 17{alpha} hydroxylase and 17-20 lyase (CYP17) activities in steroidogenesis J. Endocrinol. 187 2005 267 274
98. A.A. Gilep, R.W. Estabrook, and S.A. Usanov Molecular cloning and heterologous expression in E. coli of cytochrome P45017alpha. Comparison of structural and functional properties of substrate-specific cytochromes P450 from different species Biochem. Mosc. 68 2003 86 98
99. A.A. Gilep, R.W. Estabrook, and S.A. Usanov Chimerogenesis in estimation of specificity and pathway directions for cytochrome p45017alpha catalyzed reactions Biochem. Mosc. 69 2004 364 375
100. R.J. Auchus, T.C. Lee, and W.L. Miller Cytochrome b5 augments the 17, 20-lyase activity of human P450c17 without direct electron transfer J. Biol. Chem. 273 1998 3158 3165
101. O.L. Guryev, A.A. Gilep, S.A. Usanov, and R.W. Estabrook Interaction of apo-cytochrome b5 with cytochromes P4503A4 and P45017A: relevance of heme transfer reactions Biochemistry 40 2001 5018 5031
102. T. Ogishima, J.Y. Kinoshita, F. Mitani, M. Suematsu, and A. Ito Identification of outer mitochondrial membrane cytochrome b5 as a modulator for androgen synthesis in Leydig cells J. Biol. Chem. 278 2003 21204 21211
103. L. Min, N.V. Strushkevich, I.N. Harnastai, H. Iwamoto, A.A. Gilep, H. Takemori, S.A. Usanov, Y. Nonaka, H. Hori, G.P. Vinson, and M. Okamoto Molecular identification of adrenal inner zone antigen as a heme-binding protein FEBS J. 272 2005 5832 5843
104. J.L. Naffin-Olivos, and R.J. Auchus Human cytochrome b5 requires residues E48 and E49 to stimulate the 17, 20-lyase activity of cytochrome P450c17 Biochemistry 45 2006 755 762