Cytochrome b5: Novel roles in steroidogenesis

Molecular and Cellular Endocrinology

Volumn 371, Issue 1-2, 2013, Pages 87-99

  Storbeck, Karl Heinz ^a   Swart, Amanda C ^a   Goosen, Pierre ^a   Swart, Pieter ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

3 Hydroxysteroid dehydrogenase 5 4 isomerase; 3 HSD; CYP17A1; Cytochrome P450 17 hydroxylase 17,20 lyase; Steroidogenesis

Indexed keywords

17 HYDROXYPREGNENOLONE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANDROSTENEDIONE; CORTICOSTEROID; CYTOCHROME B5; CYTOCHROME P450 17; CYTOCHROME P450 17A1; CYTOCHROME P450 21A2; CYTOCHROME P450 REDUCTASE; PRASTERONE; SEX HORMONE; STEROID 21 MONOOXYGENASE; UNCLASSIFIED DRUG; CYP17A1 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE; STEROID; STEROID 17ALPHA MONOOXYGENASE;

ALLOSTERISM; ANDROGEN SYNTHESIS; BINDING AFFINITY; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME CONFORMATION; HORMONAL REGULATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SEQUENCE ANALYSIS; STEROIDOGENESIS; STRUCTURE ACTIVITY RELATION; BIOSYNTHESIS; METABOLISM; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE;

3-HYDROXYSTEROID DEHYDROGENASES; ANDROSTENEDIONE; CYTOCHROMES B5; HUMANS; NAD; NADPH-FERRIHEMOPROTEIN REDUCTASE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; STEROID 17-ALPHA-HYDROXYLASE; STEROIDS;

EID: 84876073004     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.11.020     Document Type: Review

References (146)

1. Abbott D., Bird I. Nonhuman primates as models for human adrenal androgen production: function and dysfunction. Rev. Endocr. Metab. Disorder 2009, 10:33-42.
2. Agarwal A.K., Auchus R.J. Minireview: cellular redox state regulates hydroxysteroid dehydrogenase activity and intracellular hormone potency. Endocrinology 2005, 146:2531-2538.
3. Akhtar M., Wright J.N., Lee-Robichaud P. A review of mechanistic studies on aromatase (CYP19) and 17α-hydroxylase-17,20-lyase (CYP17). J. Steroid Biochem. Mol. Biol. 2011, 125:2-12.
4. Arlt W., Martens J.W.M., Song M., Wang J.T., Auchus R.J., Miller W.L. Molecular evolution of adrenarche: structural and functional analysis of p450c17 from four primate species. Endocrinology 2002, 143:4665-4672.
5. Auchus R.J., Rainey W.E. Adrenarche-physiology, biochemistry and human disease. Clin. Endocrinol. (Oxf) 2004, 60:288-296.
6. Auchus R.J., Lee T.C., Miller W.L. Cytochrome b5 augments the 17,20-lyase activity of human P450c17 without direct electron transfer. J. Biol. Chem. 1998, 273:3158-3165.
7. Brock B.J., Waterman M.R. Biochemical differences between rat and human cytochrome P450c17 support the different steroidogenic needs of these two species. Biochemistry (N.Y.) 1999, 38:1598-1606.
8. Burger H.G. Androgen production in women. Fertil. Steril. 2002, 77:3-5.
9. Calabro M.A., Katz J.T., Holloway P.W. Self-association of cytochrome b5 in aqueous solution. Gel filtration and ultracentirfugational studies. J. Biol. Chem. 1976, 251:2113-2118.
10. Chapman J.C., Polanco J.R., Min S., Michael S.D. Mitochondrial 3 beta-hydroxysteroid dehydrogenase (HSD) is essential for the synthesis of progesterone by corpora lutea: an hypothesis. Reprod. Biol. Endocrinol. 2005, 3:11.
11. Chung B.C., Picado-Leonard J., Haniu M., Bienkowski M., Hall P.F., Shively J.E., Miller W.L. Cytochrome P450c17 (steroid 17 alpha-hydroxylase/17, 20 lyase): cloning of human adrenal and testis cDNAs indicates the same gene is expressed in both tissues. Proc. Natl. Acad. Sci. 1987, 84:407-411.
12. Clarke T.A., Im S.C., Bidwai A., Waskell L. The role of the length and sequence of the linker domain of cytochrome b5 in stimulating cytochrome P450 2B4 catalysis. J. Biol. Chem. 2004, 279:36809-36818.
13. Colombo S.F., Longhi R., Borgese N. The role of cytosolic proteins in the insertion of tail-anchored proteins into phospholipid bilayers. J. Cell. Sci. 2009, 122:2383-2392.
14. Correia M.A., Mannering G. Reduced diphosphopyridine nucleotide synergism of the reduced triphosphopyridine nucleotide-dependent mixed-function oxidase system of hepatic microsomes. Mol. Pharmacol. 1973, 9:455-469.
15. Cristiano R.J., Giordano S.J., Steggles A.W. The isolation and characterization of the bovine cytochrome b5 gene, and a transcribed pseudogene. Genomics 1993, 17:348-354.
16. Dailey H.A., Strittmatter P. Structural and functional properties of the membrane binding segment of cytochrome b5. J. Biol. Chem. 1978, 253:8203-8209.
17. Davydov D.R. Microsomal monooxygenase as a multienzyme system: the role of P450-P450 interactions. Expert Opin. Drug Met. 2011, 7:1-16.
18. Fevold H.R., Lorence M.C., McCarthy J.L., Trant J.M., Kagimoto M., Waterman M.R., Mason J.I. Rat P45017α from testis: characterization of a full-length cDNA encoding a unique steroid hydroxylase capable of catalyzing both Δ4- and Δ5-steroid-17,20-lyase reactions. Mol. Endocrinol. 1989, 3:968-975.
19. Fleming P.J., Dailey H.A., Corcoran D., Strittmatter P. The primary structure of the nonpolar segment of bovine cytochrome b5. J. Biol. Chem. 1978, 253:5369-5372.
20. Fukushima H., Grinstead G.F., Gaylor J.L. Total enzymic synthesis of cholesterol from lanosterol. Cytochrome b5-dependence of 4-methyl sterol oxidase. J. Biol. Chem. 1981, 256:4822-4826.
21. Ganjam V.K., Campbell A.L., Murphy B.E. Changing patterns of circulating corticosteroids in rabbits following prolonged treatment with ACTH. Endocrinology 1972, 91:607-611.
22. Garfinkel D. A comparative study of electron transport in microsomes. Comput. Biochem. Physiol. 1963, 34:367-379.
23. Gell J.S., Carr B.R., Sasano H., Atkins B., Margraf L., Mason J.I., Rainey W.E. Adrenarche results from development of a 3β-hydroxysteroid dehydrogenase-deficient adrenal reticularis. J. Clin. Endocrinol. Metab. 1998, 83:3695-3701.
24. Geller D.H., Auchus R.J., Miller W.L. P450c17 mutations R347H and R358Q selectively disrupt 17,20-lyase activity by disrupting interactions with P450 oxidoreductase and cytochrome b5. Mol. Endocrinol. 1999, 13:167-175.
25. Georgiadis E., Matzoros C., Aliferis C., Batrinos M. Are adrenal and testicular androgen levels correlated?. Horm. Metab. Res. 1992, 24:488-491.
26. Giordano S.J., Steggles A.W. The human liver and reticulocyte cytochrome b5 mRNAs are products from a single gene. Biochem. Biophys. Res. Commun. 1991, 178:38-44.
27. Giordano S.J., Steggles A.W. Differential expression of the mRNAs for the soluble and membrane-bound forms of rabbit cytochrome b5. Biochim. Et Biophys. Acta (BBA)-Gene Struct. Express. 1993, 1172:95-100.
28. Giordano S.J., Yoo M., Ward D.C., Bhatt M., Overhauser J., Steggles A.W. The human cytochrome b5 gene and two of its pseudogenes are located on chromosomes 18q23, 14q31-32.1 and 20p11. 2, respectively. Hum. Genet. 1993, 92:615-618.
29. Giordano S.J., Kaftory A., Steggles A.W. A splicing mutation in the cytochrome b5 gene from a patient with congenital methemoglobinemia and pseudohermaphrodism. Hum. Genet. 1994, 93:568-570.
30. Goosen P., Storbeck K., Swart A.C., Conradie R., Swart P. Cytochrome b5 augments 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase activity. J. Steroid Biochem. Mol. Biol. 2011, 127:238-247.
31. Goosen P., Swart A.C., Storbeck K., Swart P. Allosteric interaction between 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase and cytochrome b5 influences cofactor binding. FASEB J. 2012.
32. Gruenke L.D., Konopka K., Cadieu M., Waskell L. The stoichiometry of the cytochrome P-450-catalyzed metabolism of methoxyflurane and benzphetamine in the presence and absence of cytochrome b5. J. Biol. Chem. 1995, 270:24707-24718.
33. Guryev O.L., Gilep A.A., Usanov S.A., Estabrook R.W. Interaction of apo-cytochrome b5 with cytochromes P4503A4 and P45017A: relevance of heme transfer reactions. Biochemistry (N.Y.) 2001, 40:5018-5031.
34. Hanlon M.R., Begum R.R., Newbold R.J., Whitford D., Wallace B.A. In vitro membrane-inserted conformation of the cytochrome b(5) tail. Biochem. J. 2000, 352:117-124.
35. Hegesh E., Hegesh J., Kaftory A. Congenital methemoglobinemia with a deficiency of cytochrome b5. New Engl. J. Med. 1986, 314:757-761.
36. Hildebrandt A., Estabrook R.W. Evidence for the participation of cytochrome b5 in hepatic microsomal mixed-function oxidation reactions. Arch. Biochem. Biophys. 1971, 143:66-79.
37. Hlavica P., Lewis D.F.V. Allosteric phenomena in cytochrome P450-catalyzed monooxygenations. Eur. J. Biochem. 2001, 268:4817-4832.
38. Holloway P.W., Buchheit C. Topography of the membrane-binding domain of cytochrome b5 in lipids by Fourier-transform infrared spectroscopy. Biochemistry (N.Y.) 1990, 29:9631-9637.
39. Holloway P.W., Mantsch H.H. Structure of cytochrome b5 in solution by Fourier-transform infrared spectroscopy. Biochemistry (N.Y.) 1989, 28:931-935.
40. Hultquist D.E., Passon P.G. Catalysis of methaemoglobin reduction by erythrocyte cytochrome b5 and cytochrome b5 reductase. Nature 1971, 229:252-254.
41. Idkowiak J., Randell T., Dhir V., Patel P., Shackleton C.H.L., Taylor N.F., Krone N., Arlt W. A missense mutation in the human cytochrome b5 Gene causes 46, XY disorder of sex development due to true isolated 17,20lyase deficiency. J. Clin. Endocrinol. Metab. 2012, 97:E465-E475.
42. Im S., Waskell L. The interaction of microsomal cytochrome P450 2B4 with its redox partners, cytochrome P450 reductase and cytochrome b5. Arch. Biochem. Biophys. 2011, 507:144-153.
43. Imai Y., Sato R. The roles of cytochrome in a reconstituted N-demethylase system containing cytochrome P-450. Biochem. Biophys. Res. Commun. 1977, 75:420-426.
44. Ishii-Ohba H., Matsumura R., Inano H., Tamaoki B. Contribution of cytochrome b5 to androgen synthesis in rat testicular microsomes. J. Biochem. 1984, 95:335-343.
45. Ito A. Cytochrome b5-like hemoprotein of outer mitochondrial membrane; OM cytochrome b. I. Purification of OM cytochrome b from rat liver mitochondria and comparison of its molecular properties with those of cytochrome b5. J. Biochem. 1980, 87:63-71.
46. Katagiri M., Suhara K., Shiroo M., Fujimura Y. Role of cytochrome b5 in the cytochrome P-450-mediated C21-steroid 17,20-lyase reaction. Biochem. Biophys. Res. Commun. 1982, 108:379-384.
47. Katagiri M., Kagawa N., Waterman M.R. The role of cytochrome b5 in the biosynthesis of androgens by human P450c17. Arch. Biochem. Biophys. 1995, 317:343-347.
48. Kawano T., Kozutsumi Y., Kawasaki T., Suzuki A. Biosynthesis of N-glycolylneuraminic acid-containing glycoconjugates. Purification and characterization of the key enzyme of the cytidine monophospho-N-acetylneuraminic acid hydroxylation system. J. Biol. Chem. 1994, 269:9024-9029.
49. Keilin D., Hartree E.F. Effect of low temperature on the absorption spectra of haemoproteins; with observations on the absorption spectrum of oxygen. Nature 1949, 164:254-259.
50. Keyes S.R., Cinti D.L. Biochemical properties of cytochrome b5-dependent microsomal fatty acid elongation and identification of products. J. Biol. Chem. 1980, 255:11357-11364.
51. Kok R.C., Timmerman M.A., Wolffenbuttel K.P., Drop S.L.S., de Jong F.H. Isolated 17,20-lyase deficiency due to the cytochrome b5 mutation W27X. J. Clin. Endocrinol. Metab. 2010, 95:994-999.
52. Kominami S., Noriyuki O., Reiko M., Huang D.Y., Shigeki T. The role of cytochrome b5 in adrenal microsomal steroidogenesis. J. Steroid Biochem. Mol. Biol. 1992, 42:57-64.
53. Kumar S., Davydov D.R., Halpert J.R. Role of cytochrome b5 in modulating peroxide-supported CYP3A4 activity: evidence for a conformational transition and cytochrome P450 heterogeneity. Drug Metab. Dispos. 2005, 33:1131-1136.
54. Kun E. Properties of a chromoprotein containing extract of the particulate fraction of rat liver. Proc. Soc. Exp. Bioi. Med. 1951, 77:441-445.
55. Labrie C., Simard J., Zhao H.U.I.F.E.N., Belanger A., Pelletier G., Labrie F. Stimulation of androgen-dependent gene expression by the adrenal precursors dehydroepiandrosterone and androstenedione in the rat ventral prostate. Endocrinology 1989, 124:2745-2754.
56. Lederer F., Ghrir R., Guiard B., Cortrail S., Ito A. Two homologous cytochromes b5 in a single cell. Eur. J. Biochem. 1983, 132:95-102.
57. Lee Y.N., Chen L.K., Ma H.C., Yang H.H., Li H.P., Lo S.Y. Thermal aggregation of SARS-CoV membrane protein. J. Virol. Methods 2005, 129:152-161.
58. Lee-Robichaud P., Akhtar M.E., Akhtar M. Control of androgen biosynthesis in the human through the interaction of Arg347 and Arg358 of CYP17 with cytochrome b5. Biochem. J. 1998, 332(Pt 2):293-296.
59. Lee-Robichaud P., Akhtar M.E., Akhtar M. Lysine mutagenesis identifies cationic charges of human CYP17 that interact with cytochrome b5 to promote male sex-hormone biosynthesis. Biochem. J. 1999, 342:309-312.
60. Lee-Robichaud P., Akhtar M.E., Wright J.N., Sheikh Q.I., Akhtar M. The cationic charges on Arg347, Arg358 and Arg449 of human cytochrome P450c17 (CYP17) are essential for the enzyme's cytochrome b5-dependent acyl-carbon cleavage activities. J. Steroid Biochem. Mol. Biol. 2004, 92:119-130.
61. Lesné S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-b protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
62. Levine J., Wolfe L.G., Schiebinger R.J., Loriaux D.L., Cutler G.B. Rapid regression of fetal adrenal zone and absence of adrenal reticular zone in the marmoset. Endocrinology 1982, 111:1797-1802.
63. Li X.R., Giordano S.J., Yoo M., Steggles A.W. The isolation and characterization of the human cytochrome b5 gene. Biochem. Biophys. Res. Commun. 1995, 209:894-900.
64. Lin D., Black S., Nagahama Y., Miller W. Steroid 17 alpha-hydroxylase and 17,20-lyase activities of P450c17: contributions of serine106 and P450 reductase. Endocrinology 1993, 132:2498-2506.
65. Locuson C.W., Wienkers L.C., Jones J.P., Tracy T.S. CYP2C9 protein interactions with cytochrome b5: effects on the coupling of catalysis. Drug Metab. Dispos. 2007, 35:1174-1181.
66. Lombard N., Swart A.C., van der Merwe M.J., Swart P. Sheep adrenal cytochrome b5: active as a monomer or a tetramer in vivo?. Endocr. Res. 2002, 28:485-492.
67. Lorence M.C., Trant J.M., Clark B.J., Khyatt B., Mason J.I., Estabrook R.W., Waterman M.R. Construction and expression of human/bovine P45017. Alpha. chimeric proteins: evidence for distinct tertiary structures in the same P450 from two different species. Biochemistry (N.Y.) 1990, 29:9819-9824.
68. Luu-The V., Masakazu T., de Launoit Y., Dumont M., Lachance Y., Labrie F. Evidence for distinct dehydrogenase and isomerase sites within a single 3β-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase protein. Biochemistry (N.Y.) 1991, 36:8861-8865.
69. Mapes S., Tarantal A.F., Parker C.R., Moran F.M., Bahr J.M., Pyter L., Conley A.J. Adrenocortical cytochrome b5 expression during fetal development of the rhesus macaque. Endocrinology 2002, 143:1451-1458.
70. Mason J.I., Estabrook R.W., Purvis J.L. Testicular cytochrome P-450 and iron-sulfur protein as related to steroid metabolism. Ann. N.Y. Acad. Sci. 1973, 212:406-419.
71. McLaughlin L.A., Ronseaux S., Finn R.D., Henderson C.J., Roland Wolf C. Deletion of microsomal cytochrome b5 Profoundly affects hepatic and extrahepatic drug metabolism. Mol. Pharmacol. 2010, 78:269-278.
72. Miller W.L. The syndrome of 17,20lyase deficiency. J. Clin. Endocrinol. Metab. 2012, 97:59-67.
73. Miller W.L., Auchus R.J. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr. Rev. 2011, 32:81-151.
74. Miller W.L., Auchus R.J., Geller D.H. The regulation of 17, 20 lyase activity. Steroids 1997, 62:133-142.
75. Morgan E.T., Coon M.J. Effects of cytochrome b5 on cytochrome P-450-catalyzed reactions. Studies with manganese-substituted cytochrome b5. Drug Metab. Dispos. 1984, 12:358-364.
76. Mulrooney S.B., Meinhardt D.R., Waskell L. The α-helical membrane spanning domain of cytochrome b5 interacts with cytochrome P450 via nonspecific interactions. Biochim. Et Biophys. Acta (BBA)-Gener. Subject 2004, 1674:319-326.
77. Naffin-Olivos J.L., Auchus R.J. Human cytochrome b5 requires residues E48 and E49 to stimulate the 17,20-lyase activity of cytochrome P450c17. Biochemistry 2006, 45:755-762.
78. Nakajin S., Shively J., Yuan P.M., Hall P.F. Microsomal cytochrome P-450 from neonatal pig testis: two enzymic activities (17. alpha.-hydroxalase and C17, 20 associated with one protein. Biochemistry (N.Y.) 1981, 20:4037-4042.
79. Nakajin S., Shinoda M., Haniu M., Shively J., Hall P. C21 steroid side chain cleavage enzyme from porcine adrenal microsomes. Purification and characterization of the 17 alpha-hydroxylase/C17,20-lyase cytochrome P-450. J. Biol. Chem. 1984, 259:3971-3976.
80. Nakamura Y., Xing Y., Hui X.G., Kurotaki Y., Ono K., Cohen T., Sasano H., Rainey W.E. Human adrenal cells that express both 3β-hydroxysteroid dehydrogenase type 2 (HSD3B2) and cytochrome b5 (CYB5A) contribute to adrenal androstenedione production. J. Steroid Biochem. Mol. Biol. 2011, 123:122-126.
81. Nash W.E., Mercer R.W., Blanco G., Strickler R.C., Mason J.I., Thomas J.L. Over-expression of human type I (placental) 3β-hydroxy-5-ene-steroid dehydrogenase/isomerase in insect cells infected with recombinant baculovirus. J. Steroid Biochem. Mol. Biol. 1994, 50:235-240.
82. Nguyen A.D., Mapes S.M., Corbin C.J., Conley A.J. Morphological adrenarche in rhesus macaques: development of the zona reticularis is concurrent with fetal zone regression in the early neonatal period. J. Endocrinol. 2008, 199:367-378.
83. Nguyen A.D., Corbin C.J., Pattison J.C., Bird I.M., Conley A.J. The developmental increase in adrenocortical 17,20-lyase activity (biochemical adrenarche) is driven primarily by increasing cytochrome b5 in neonatal rhesus macaques. Endocrinology 2009, 150:1748-1756.
84. Nguyen K.T., Soong R., lm S.C., Waskell L., Ramamoorthy A., Chen Z. Probing the spontaneous membrane insertion of a tail-anchored membrane protein by sum frequency generation spectroscopy. J. Am. Chem. Soc. 2010, 132:15112-15115.
85. Nguyen P.T.T., Lee R.S.F., Conley A.J., Sneyd J., Soboleva T.K. Variation in 3β-hydroxysteroid dehydrogenase activity and in pregnenolone supply rate can paradoxically alter androstenedione synthesis. J. Steroid Biochem. Mol. Biol. 2011, 128:12-20.
86. Oddie C.J., Blaine E.H., Bradshaw S.D., Coghlan J.P., Denton D.A., Nelson J.F., Scoggins B.A. Blood corticosteroids in Australian marsupial and placental mammals and one monotreme. J. Endocrinol. 1976, 69:341-348.
87. Odell W.D., Parker L.N. Control of adrenal androgen production. Endocr. Res. 1984, 10:617-630.
88. Okayasu T., Nagao M., Ishibashi T., Imai Y. Purification and partial characterization of linoleoyl-CoA desaturase from rat liver microsomes. Arch. Biochem. Biophys. 1981, 206:21-28.
89. Omura T. Structural diversity of cytochrome P450 enzyme system. J. Biochem. 2010, 147:297-306.
90. Onoda M., Hall P.F. Cytochrome b5 stimulates purified testicular microsomal cytochrome P-450 (C21 side-chain cleavage). Biochem. Biophys. Res. Commun. 1982, 108:454-460.
91. Oshino N., Yoshio I. A function of cytochrome b5 in fatty acid desaturation by rat liver microsomes. J. Biochem. 1971, 69:155-167.
92. Ouali R., Langlois D., Saez J., Begeot M. Opposite effects of angiotensin-II and corticotropin on bovine adrenocortical cell steroidogenic responsiveness. Mol. Cell. Endocrinol. 1991, 81:43-52.
93. Ozols J. Structure of cytochrome b5 and its topology in the microsomal membrane. Biochim. Et Biophys. Acta (BBA)-Protein Struct. Mol. Enzymol. 1989, 997:121-130.
94. Paltauf F., Prough R.A., Masters B.S.S., Johnston J.M. Evidence for the participation of cytochrome b5 in plasmalogen biosynthesis. J. Biol. Chem. 1974, 249:2661-2662.
95. Pandey A.V., Miller W.L. Regulation of 17,20lyase activity by cytochrome b5 and by serine phosphorylation of P450c17. J. Biol. Chem. 2005, 280:13265-13271.
96. Pappenheimer A.M., Williams C.M. The effects of diphtheria toxin on the Cecropia silkworm. J. Gen. Physiol. 1952, 35:727-740.
97. Pattison J.C., Abbott D.H., Saltzman W., Nguyen A.D., Henderson G., Jing H., Pryce C.R., Allen A.J., Conley A.J., Bird I.M. Male marmoset monkeys express an adrenal fetal zone at birth, but not a zona reticularis in adulthood. Endocrinology 2005, 146:365-374.
98. Pattison J.C., Saltzman W., Abbott D.H., Hogan B.K., Nguyen A.D., Husen B., Einspanier A., Conley A.J., Bird I.M. Gender and gonadal status differences in zona reticularis expression in marmoset monkey adrenals: Cytochrome b5 localization with respect to cytochrome P450 17,20-lyase activity. Mol. Cell. Endocrinol. 2007, 265-266:93-101.
99. Perkins L.M., Payne A.H. Quantification of P450scc, P45017α, and iron sulfur protein reductase in Leydig cells and adrenals of inbred strains of mice. Endocrinology 1988, 123:2675-2682.
100. Piltonen T., Koivunen R., Morin-Papunen L., Ruokonen A., Huhtaniemi I., Tapanainen J. Ovarian and adrenal steroid production: regulatory role of LH/HCG. Human Reprod. 2002, 17:620-624.
101. Porter T.D. The roles of cytochrome b5 in cytochrome P450 reactions. J. Biochem. Mol. Toxicol. 2002, 16:311-316.
102. Praporski S., Ng S.M., Nguyen A.D., Corbin C.J., Mechler A., Zheng J., Conley A.J., Martin L.L. Organization of cytochrome P450 enzymes involved in sex steroid synthesis. J. Biol. Chem. 2009, 284:33224-33232.
103. Qian W., Sun Y.L., Wang Y.H., Zhuang J.H., Xie Y., Huang Z.X. The influence of mutation at Glu44 and Glu56 of cytochrome b5 on the protein's stabilization and interaction between cytochrome c and cytochrome b5. Biochemistry (N.Y.) 1998, 37:14137-14150.
104. Rainey W.E., Nakamura Y. Regulation of the adrenal androgen biosynthesis. J. Steroid Biochem. Mol. Biol. 2008, 108:281-286.
105. Rainey W.E., Carr B.R., Sasano H., Suzuki T., Mason J.I. Dissecting human adrenal androgen production. Trend Endocrinol. Metab. 2002, 13:234-239.
106. Rege J., Rainey W.E. The steroid metabolome of adrenarche. J. Endocrinol. 2012, 214:133-143.
107. Renthal R. Helix insertion into bilayers and the evolution of membrane proteins. Cell. Mol. Life Sci. 2010, 67:1077-1088.
108. Sagné C., Isambert M.F., Henry J.P., Gasnier B. SDS-resistant aggregation of membrane proteins: application to the purification of the vesicular monoamine transporter. Biochem. J. 1996, 316:825-831.
109. Sakai Y., Yanase T., Takayanagi R., Nakao R., Nishi Y., Haji M., Nawata H. High expression of cytochrome b5 in adrenocortical adenomas from patients with Cushing's syndrome associated with high secretion of adrenal androgens. J. Clin. Endocrinol. Metab. 1993, 76:1286-1290.
110. Sakai Y., Yanase T., Hara T., Takayanagi R., Haji M., Nawata H. In-vitro evidence for the regulation of 17,20-lyase activity by cytochrome b5 in adrenocortical adenomas from patients with Cushing's syndrome. Clin. Endocrinol. (Oxf) 1994, 40:205-209.
111. Sanborn R.C., Williams C.M. The cytochrome system in the cecropia silkworm, with special reference to the properties of a new component. J. Gen. Physiol. 1950, 33:579-588.
112. Sannes L.J., Hultquist D.E. Effects of hemolysate concentration, ionic strength and cytochrome b5 concentration on the rate of methemoglobin reduction in hemolysates of human erythrocytes. Biochim. Et Biophys. Acta (BBA)-Gener. Subject 1978, 544:547-554.
113. Schenkman J.B., Jansson I. Interactions between cytochrome P450 and cytochrome b5. Drug Metab. Rev. 1999, 31:351-364.
114. Schenkman J.B., Jansson I. The many roles of cytochrome b5. Pharmacol. Ther. 2003, 97:139-152.
115. Schenkman J.B., Jansson I., Davis G., Tamburini P.P., Lu Z., Zhang Z., Rusling J.F. Protein-protein interactions in the P450 monooxygenase system. Molecular and Appplied Aspects of Oxidative Drug Metabolizing Enzymes 1999, 21-31. Plenum Publishers, New York. E. Arinç, J.B. Schenkman, E. Hodgson (Eds.).
116. Shinzawa K., Kominami S., Takemori S. Studies on cytochrome P-450 (P-450 17 alpha, lyase) from guinea pig adrenal microsomes. Dual function of a single enzyme and effect of cytochrome b5. Biochim. Biophys. Acta 1985, 833:151-160.
117. Soucy P., Luu-The V. Conversion of pregnenolone to DHEA by human 17α-hydroxylase/17,20-lyase (P450c17): evidence that DHEA is produced from the released intermediate, 17α-hydroxypregnenolone. Eur. J. Biochem. 2000, 267:3243-3247.
118. Soucy P., Lacoste L., Luu-The V. 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./FEBS 2003, 270:1349-1355.
119. Storbeck K.H., Swart A.C., Slabbert J.T., Swart P. The identification of two CYP17 alleles in the South African Angora goat. Drug Metab. Rev. 2007, 39:467-480.
120. Storbeck K.H., Kolar N.W., Stander M., Swart A.C., Prevoo D., Swart P. The development of an ultra performance liquid chromatography-coupled atmospheric pressure chemical ionization mass spectrometry assay for seven adrenal steroids. Anal. Biochem. 2008, 372:11-20.
121. Storbeck K.H., Swart P., Africander D., Conradie R., Louw R., Swart A.C. 16α-Hydroxyprogesterone: origin; biosynthesis and receptor interaction. Mol. Cell. Endocrinol. 2010, 1-2:92-101.
122. Storbeck K., Swart A.C., Lombard N., Adriaanse C.V., Swart P. Cytochrome b5 forms homomeric complexes in living cells. J. Steroid Biochem. Mol. Biol. 2012, 132:311-321.
123. Strittmatter C.F., Ball E.G. A Hemochromogen Component of Liver Microsomes. Proc. Natl. Acad. Sci. USA 1952, 38:19-25.
124. Strittmatter P., Hackett C.S., Korza G., Ozols J. Characterization of the covalent cross-links of the active sites of amidinated cytochrome b5 and NADH: cytochrome b5 reductase. J. Biol. Chem. 1990, 265:21709-21713.
125. Sugiyama T., Nobuo M., Yamano T. NADH-and NADPH-dependent reconstituted p-nitroanisole O-demethylation system containing cytochrome P-450 with high affinity for cytochrome b5. J. Biochem. 1980, 87:1457-1467.
126. Swart P., Swart A.C., Waterman M.R., Estabrook R.W., Mason J.I. Progesterone 16 alpha-hydroxylase activity is catalyzed by human cytochrome P450 17 alpha-hydroxylase. J. Clin. Endocrinol. Metab. 1993, 77:98-102.
127. Swart P., Engelbrecht Y., Bellstedt D.U., de Villiers C.A., Dreesbeimdieke C. The effect of cytochrome b5 on progesterone metabolism in the ovine adrenal. Endocr. Res. 1995, 21:297-306.
128. Swart P., Lombard N., Swart A.C., van der Merwe T., Murry B.A., Nicol M., Ian Mason J. Ovine steroid 17α-hydroxylase cytochrome P450: characteristics of the hydroxylase and lyase activities of the adrenal cortex enzyme. Arch. Biochem. Biophys. 2003, 409:145-152.
129. Swart A.C., Storbeck K.H., Swart P. A single amino acid residue, Ala 105, confers 16α-hydroxylase activity to human cytochrome P450 17α-hydroxylase/17,20 lyase. J. Steroid Biochem. Mol. Biol. 2010, 119:112-120.
130. Tardif S., Ziegler T. Features of female reproductive senescence in tamarins (Saguinus spp.), a New World primate. J. Reprod. Fertil. 1992, 94:411-421.
131. Thomas J.L., Berko E.A., Faustino A., Myers R.P., Strickler R.C. Human placental 3 beta-hydroxy-5-ene-steroid dehydrogenase and steroid 5-4-ene-isomerase: purification from microsomes, substrate kinetics, and inhibition by product steroids. J. Steroid Biochem. 1988, 31:785-793.
132. Thomas J.L., Myers R.P., Strickler R.C. Human placental 3 beta-hydroxy-5-ene-steroid dehydrogenase and steroid 5-4-ene-isomerase: purification from mitochondria and kinetic profiles, biophysical characterization of the purified mitochondrial and microsomal enzymes. J. Steroid Biochem. 1989, 33:209-217.
133. Thomas J.L., Frieden C., Nash W.E., Strickler R.C. An NADH-induced conformational change that mediates the sequential 3-hydroxysteroid dehydrogenase/isomerase activities is supported by affinity labeling and the time-dependent activation of isomerase. J. Biol. Chem. 1995, 270:21003-21008.
134. Thomas J.L., Duax W.L., Addlagatta A., Brandt S., Fuller R.R., Norris W. Structure/function relationships responsible for coenzyme specificity and the isomerase activity of human type 1 3β-hydroxysteroid dehydrogenase/isomerase. J. Biol. Chem. 2003, 278:35483-35490.
135. Tremblay Y., Fleury A., Beaudoin C., Vallée M., Bélanger A. Molecular cloning and expression of guinea pig cytochrome P450c17 cDNA (steroid 17α-hydroxylase/17, 20 lyase): tissue distribution, regulation, and substrate specificity of the expressed enzyme. DNA Cell Biol. 1994, 13:1199-1212.
136. Vergeres G., Waskell L. Expression of cytochrome b5 in yeast and characterization of mutants of the membrane-anchoring domain. J. Biol. Chem. 1992, 267:12583-12591.
137. Vergeres G., Waskell L. Cytochrome b5, its functions, structure and membrane topology. Biochimie 1995, 77:604-620.
138. Wang W., Yang L., Suwa T., Casson P.R., Hornsby P.J. Differentially expressed genes in zona reticularis cells of the human adrenal cortex. Mol. Cell. Endocrinol. 2001, 173:127-134.
139. Yamada M., Ohta Y., Bachmanova G.I., Nishimoto Y., Archakov A.I., Kawato S. Dynamic interactions of rabbit liver cytochromes P450IA2 and P450IIB4 with cytochrome b5 and NADPH-cytochrome P450 reductase in proteoliposomes. Biochemistry (N.Y.) 1995, 34:10113-10119.
140. Yamazaki H., Johnson W.W., Ueng Y.F., Shimada T., Guengerich F.P. Lack of electron transfer from cytochrome b5 in stimulation of catalytic activities of cytochrome P450 3A4. Characterization of a reconstituted cytochrome P450 3A4/NADPH-cytochrome P450 reductase system and studies with apo-cytochrome b5. J. Biol. Chem. 1996, 271:27438-27444.
141. Yamazaki H., Shimada T., Martin M.V., Guengerich F.P. Stimulation of cytochrome P450 reactions by apo-cytochrome b5: evidence against transfer of heme from cytochrome P450 3A4 to apo-cytochrome b5 or heme oxygenase. J. Biol. Chem. 2001, 276:30885-30891.
142. Yamazaki H., Nakamura M., Komatsu T., Ohyama K., Hatanaka N., Asahi S., Shimada N., Guengerich F.P., Shimada T., Nakajima M. Roles of NADPH-P450 reductase and apo-and holo-cytochrome b5 on xenobiotic oxidations catalyzed by 12 recombinant human cytochrome P450s expressed in membranes of Escherichia coli. Protein Expr. Purif. 2002, 24:329-337.
143. Yanagibashi K., Hall P. Role of electron transport in the regulation of the lyase activity of C21 side-chain cleavage P-450 from porcine adrenal and testicular microsomes. J. Biol. Chem. 1986, 261:8429-8433.
144. Yanase T., Sasano H., Yubisui T., Sakai Y., Takayanagi R., Nawata H. Immunohistochemical study of cytochrome b5 in human adrenal gland and in adrenocortical adenomas from patients with Cushing's syndrome. Endocr. J. 1998, 45:89-95.
145. Yoshikawa H. The oxidation-reduction potential of cytochrome b', a hemochromogen-like component of cytochrome in liver. J. Biochem. 1951, 38:1-5.
146. Zuber M.X., Simpson E.R., Waterman M.R. Expression of bovine 17 alpha-hydroxylase cytochrome P-450 cDNA in nonsteroidogenic (COS 1) cells. Science (New York, NY) 1986, 234:1258-1261.