Structural and kinetic basis of steroid 17α,20-lyase activity in Teleost fish cytochrome P450 17A1 and its absence in cytochrome P450 17A2

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3248-3268

  Pallan, Pradeep S ^a   Nagy, Leslie D ^a   Lei, Li ^a   Gonzalez, Eric ^a   Kramlinger, Valerie M ^a   Azumaya, Caleigh M ^a   Wawrzak, Zdzislaw ^b   Waterman, Michael R ^a   Guengerich, F Peter ^a   Egli, Martin ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; ENZYMES; HYDROXYLATION;

ACTIVE SITE; CYTOCHROME B; CYTOCHROME P450; GLUCOCORTICOIDS; LYASE ACTIVITY; PREGNENOLONE; TELEOST FISH; X RAY CRYSTAL STRUCTURES;

FISH;

CYTOCHROME P450 17; CYTOCHROME P450 17A1; CYTOCHROME P450 17A2; STEROID 17ALPHA MONOOXYGENASE; UNCLASSIFIED DRUG; ABIRATERONE; ANDROSTANE DERIVATIVE; PROGESTERONE; PROTEIN BINDING; ZEBRAFISH PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CATALYST; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME STRUCTURE; HYDROXYLATION; NONHUMAN; PROTEIN EXPRESSION; STEADY STATE; TELEOST; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; KINETICS; METABOLISM; MOLECULAR DOCKING; MOLECULAR GENETICS;

DANIO RERIO; MAMMALIA; TELEOSTEI;

AMINO ACID SEQUENCE; ANDROSTENES; ANIMALS; CATALYTIC DOMAIN; KINETICS; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; PROGESTERONE; PROTEIN BINDING; STEROID 17-ALPHA-HYDROXYLASE; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84922311088     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.627265     Document Type: Article

References (77)

1. rd Ed., Kluwer Academic/Plenum Publishers, New York
2. Miller, W. L., and Auchus, R. J. (2011) The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr. Rev. 32, 81-151
3. rd Ed., pp. 377-530, Kluwer Academic/Plenum Press, New York
4. th Ed., Springer-Verlag, in press
5. DeVore, N. M., and Scott, E. E. (2012) Structures of cytochrome P450 17A1 with prostate cancer drugs abiraterone and TOK-001. Nature 482, 116-119
6. Kaku, T., Hitaka, T., Ojida, A., Matsunaga, N., Adachi, M., Tanaka, T., Hara, T., Yamaoka, M., Kusaka, M., Okuda, T., Asahi, S., Furuya, S., and Tasaka, A. (2011) Discovery of orteronel (TAK-700), a naphthylmethylimidazole derivative, as a highly selective 17,20-lyase inhibitor with potential utility in the treatment of prostate cancer. Bioorg. Med. Chem. 19, 6383-6399
7. Yamaoka, M., Hara, T., Hitaka, T., Kaku, T., Takeuchi, T., Takahashi, J., Asahi, S., Miki, H., Tasaka, A., and Kusaka, M. (2012) Orteronel (TAK-700), a novel non-steroidal 17,20-lyase inhibitor: effects on steroid synthesis in human and monkey adrenal cells and serum steroid levels in cynomolgus monkeys. J. Steroid Biochem. Mol. Biol. 129, 115-128
8. Petrunak, E. M., DeVore, N. M., Porubsky, P. R., and Scott, E. E. (2014) Structures of human steroidogenic cytochrome P450 17A1 with substrates. J. Biol. Chem. 289, 32952-32964
9. Akhtar, M., Corina, D., Miller, S., Shyadehi, A. Z., and Wright, J. N. (1994) Mechanism of the acyl-carbon cleavage and related reactions catalyzed by multifunctional P-450s: studies on cytochrome P45017α. Biochemistry 33, 4410-4418
10. Gregory, M. C., Denisov, I. G., Grinkova, Y. V., Khatri, Y., and Sligar, S. G. (2013) Kinetic solvent isotope effect in human P450 CYP17A1-mediated androgen formation: evidence for a reactive peroxoanion intermediate. J. Am. Chem. Soc. 135, 16245-16247
11. Gregory, M., Mak, P. J., Sligar, S. G., and Kincaid, J. R. (2013) Differential hydrogen bonding in human CYP17 dictates hydroxylation versus lyase chemistry. Angew. Chem. Int. Ed. Engl. 52, 5342-5345
12. Katagiri, M., Suhara, K., Shiroo, M., and Fujimura, Y. (1982) Role of cytochrome b5 in the cytochrome P-450-mediated C21-steroid 17,20-lyase reaction. Biochem. Biophys. Res. Commun. 108, 379-384
13. Katagiri, M., Kagawa, N., and Waterman, M. R. (1995) The role of cytochrome b5 in the biosynthesis of androgens by human P450c17. Arch. Biochem. Biophys. 317, 343-347
14. Zhang, L. H., Rodriguez, H., Ohno, S., and Miller, W. L. (1995) Serine phosphorylation of human P450c17 increases 17,20-lyase activity: implications for adrenarche and the polycystic ovary syndrome. Proc. Natl. Acad. Sci. U.S.A. 92, 10619-10623
15. Tee, M. K., Dong, Q., and Miller, W. L. (2008) Pathways leading to phosphorylation of P450c17 and to the posttranslational regulation of androgen biosynthesis. Endocrinology 149, 2667-2677
16. Tee, M. K., and Miller, W. L. (2013) Phosphorylation of human cytochrome P450c17 by p38α selectively increases 17,20-lyase activity and androgen biosynthesis. J. Biol. Chem. 288, 23903-23913
17. Auchus, R. J., Lee, T. C., and Miller, W. L. (1998) Cytochrome b5 augments the 17,20-lyase activity of human P450c17 without direct electron transfer. J. Biol. Chem. 273, 3158-3165
18. Estrada, D. F., Laurence, J. S., and Scott, E. E. (2013) Substrate-modulated cytochrome P450 17A1 and cytochrome b5 interactions revealed by NMR. J. Biol. Chem. 288, 17008-17018
19. 17α, lyase. Biochemistry 37, 2800-2806
20. Soucy, P., and Luu-The, V. (2000) 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. 267, 3243-3247
21. Higuchi, A., Kominami, S., and Takemori, S. (1991) Kinetic control of steroidogenesis by steroid concentration in guinea pig adrenal microsomes. Biochim. Biophys. Acta 1084, 240-246
22. Ku?hn-Velten, W. N., Bunse, T., and Fo?rster, M. E. (1991) Enzyme kinetic and inhibition analyses of cytochrome P450XVII, a protein with a bifunctional catalytic site: quantification of effective substrate concentrations at the active site and their significance for intrinsic control of the hydroxylase/ lyase reaction sequence. J. Biol. Chem. 266, 6291-6301
23. Swinney, D. C., and Mak, A. Y. (1994) Androgen formation by cytochrome P450 CYP17. Solvent isotope effect and pL studies suggest a role for protons in the regulation of oxene versus peroxide chemistry. Biochemistry 33, 2185-2190
24. 17α, lyase-mediating pathway of androgen synthesis in bovine adrenocortical cultured cells. Biochim. Biophys. Acta 1134, 143-148
25. Yamazaki, T., Marumoto, T., Kominami, S., Ishimura, K., Yamamoto, A., and Takemori, S. (1992) Kinetic studies on androstenedione production in ovarian microsomes from immature rats. Biochim. Biophys. Acta 1125, 335-340
26. 17α,lyase dependent androstenedione formation from progesterone. Biochemistry 34, 10939-10945
27. Brock, B. J., and Waterman, M. R. (1999) Biochemical differences between rat and human cytochrome P450c17 support the different steroidogenic needs of these two species. Biochemistry 38, 1598-1606
28. Zhou, L. Y., Wang, D. S., Kobayashi, T., Yano, A., Paul-Prasanth, B., Suzuki, A., Sakai, F., and Nagahama, Y. (2007) A novel type of P450c17 lacking the lyase activity is responsible for C21-steroid biosynthesis in the fish ovary and head kidney. Endocrinology 148, 4282-4291
29. Hanna, I. H., Teiber, J. F., Kokones, K. L., and Hollenberg, P. F. (1998) Role of the alanine at position 363 of cytochrome P450 2B2 in influencing the NADPH- and hydroperoxide-supported activities. Arch. Biochem. Biophys. 350, 324-332
30. Guengerich, F. P. (2005) Reduction of cytochrome b5 by NADPH-cytochrome P450 reductase. Arch. Biochem. Biophys. 440, 204-211
31. Shimada, T., Misono, K. S., and Guengerich, F. P. (1986) Human liver microsomal cytochrome P-450 mephenytoin 4-hydroxylase, a prototype of genetic polymorphism in oxidative drug metabolism. Purification and characterization of two similar forms involved in the reaction. J. Biol. Chem. 261, 909-921
32. Richardson, T. H., Jung, F., Griffin, K. J., Wester, M., Raucy, J. L., Kemper, B., Bornheim, L. M., Hassett, C., Omiecinski, C. J., and Johnson, E. F. (1995) A universal approach to the expression of human and rabbit cytochrome P450s of the 2C subfamily in Escherichia coli. Arch. Biochem. Biophys. 323, 87-96
33. Nishihara, K., Kanemori, M., Kitagawa, M., Yanagi, H., and Yura, T. (1998) Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli. Appl. Environ. Microbiol. 64, 1694-1699
34. Sandhu, P., Baba, T., and Guengerich, F. P. (1993) Expression of modified cytochrome P450 2C10 (2C9) in Escherichia coli, purification, and reconstitution of catalytic activity. Arch. Biochem. Biophys. 306, 443-450
35. Omura, T., and Sato, R. (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J. Biol. Chem. 239, 2370-2378
36. Zhao, B., Lei, L., Kagawa, N., Sundaramoorthy, M., Banerjee, S., Nagy, L. D., Guengerich, F. P., and Waterman, M. R. (2012) Three-dimensional structure of steroid 21-hydroxylase (cytochrome P450 21A2) with two substrates reveals locations of disease-associated variants. J. Biol. Chem. 287, 10613-10622
37. Strittmatter, P., Fleming, P., Connors, M., and Corcoran, D. (1978) Purification of cytochrome b5. Methods Enzymol. 52, 97-101
38. Olsen, J. V., Ong, S. E., and Mann, M. (2004) Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 3, 608-614
39. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
40. Winter, G. (2010) xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186-190
41. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
42. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
43. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
44. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
45. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
46. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
47. th Ed., pp. 1905-1964, CRC Press-Taylor & Francis, Boca Raton, FL
48. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global Kinetic Explorer: a new computer program for dynamic simulation and fitting of kinetic data. Anal. Biochem. 387, 20-29
49. Hara, T., Kouno, J., Kaku, T., Takeuchi, T., Kusaka, M., Tasaka, A., and Yamaoka, M. (2013) Effect of a novel 17,20-lyase inhibitor, orteronel (TAK-700), on androgen synthesis in male rats. J. Steroid Biochem. Mol. Biol. 134, 80-91
50. Fersht, A. (1999) Structure and Mechanism in Protein Science, pp. 158-168, W. H. Freeman & Co., New York
51. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., So?ding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539
52. Dong, A., Xu, X., Edwards, A. M., Midwest Center for Structural Genomics, Structural Genomics Consortium, Chang, C., Chruszcz, M., Cuff, M., Cymborowski, M., Di Leo, R., Egorova, O., Evdokimova, E., Filippova, E., Gu, J., Guthrie, J., Ignatchenko, A., Joachimiak, A., Klostermann, N., Kim, Y., Korniyenko, Y., Minor, W., Que, Q., Savchenko, A., Skarina, T., Tan, K., Yakunin, A., Yee, A., Yim, V., Zhang, R., Zheng, H., Akutsu, M., Arrowsmith, C., Avvakumov, G. V., Bochkarev, A., Dahlgren, L. G., Dhe-Paganon, S., Dimov, S., Dombrovski, L., Finerty, P., Jr., Flodin, S., Flores, A., Gra?slund, S., Hammerstro?m, M., Herman, M. D., Hong, B. S., Hui, R., Johansson, I., Liu, Y., Nilsson, M., Nedyalkova, L., Nordlund, P., Nyman, T., Min, J., Ouyang, H., Park, H. W., Qi, C., Rabeh, W., Shen, L., Shen, Y., Sukumard, D., Tempel, W., Tong, Y., Tresagues, L., Vedadi, M., Walker, J. R., Weigelt, J., Welin, M., Wu, H., Xiao, T., Zeng, H., and Zhu, H. (2007) In situ proteolysis for protein crystallization and structure determination. Nat. Methods 4, 1019-1021
53. Wernimont, A., and Edwards, A. (2009) In situ proteolysis to generate crystals for structure determination: an update. PLoS One 4, e5094
54. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comp. Chem. 25, 1605-1612
55. Wang, Y., and Ge, W. (2004) Cloning of zebrafish ovarian P450c17 (CYP17, 17-hydroxylase/17,20-lyase) and characterization of its expression in gonadal and extra-gonadal tissues. Gen. Comp. Endocrinol. 135, 241-249
56. Chen, C. F., Wen, H. S., Wang, Z. P., He, F., Zhang, J. R., Chen, X. Y., Jin, G. X., Shi, B., Shi, D., Yang, Y. P., Li, J. F., Qi, B. X., and Li, N. (2010) Cloning and expression of P450c17-I (17α-hydroxylase/17,20-lyase) in brain and ovary during gonad development in Cynoglossus semilaevis. Fish Physiol. Biochem. 36, 1001-1012
57. 17α (17α-hydroxylase-17,20-lyase). J. Chem. Soc. Perkin Trans. 1, 263-267
58. 17α; 17α-hydroxylase-17,20-lyase). Biochemistry 34, 14104-14113
59. 5. J. Biol. Chem. 289, 14310-14320
60. 5 steroidogenic pathway. J. Clin. Endocrinol. Metab. 88, 3762-3766
61. Bell-Parikh, L. C., and Guengerich, F. P. (1999) Kinetics of cytochrome P450 2E1-catalyzed oxidation of ethanol to acetic acid via acetaldehyde. J. Biol. Chem. 274, 23833-23840
62. Chowdhury, G., Calcutt, M. W., and Guengerich, F. P. (2010) Oxidation of N-nitrosoalkylamines by human cytochrome P450 2A6: sequential oxidation to aldehydes and carboxylic acids and analysis of reaction steps. J. Biol. Chem. 285, 8031-8044
63. Chowdhury, G., Calcutt, M. W., Nagy, L. D., and Guengerich, F. P. (2012) Oxidation of methyl and ethyl nitrosamines by cytochrome P450 2E1 and 2B1. Biochemistry 51, 9995-10007
64. Guengerich, F. P., Sohl, C. D., and Chowdhury, G. (2011) Multi-step oxidations catalyzed by cytochrome P450 enzymes: Processive vs. distributive kinetics and the issue of carbonyl oxidation in chemical mechanisms. Arch. Biochem. Biophys. 507, 126-134
65. Hanson, K. L., VandenBrink, B. M., Babu, K. N., Allen, K. E., Nelson, W. L., and Kunze, K. L. (2010) Sequential metabolism of secondary alkyl amines to metabolic-intermediate complexes: opposing roles for the secondary hydroxylamine and primary amine metabolites of desipramine, (S)-fluoxetine, and N-desmethyl diltiazem. Drug Metab. Dispos. 38, 963-972
66. Isin, E. M., and Guengerich, F. P. (2007) Complex reactions catalyzed by cytochrome P450 enzymes. Biochim. Biophys. Acta 1770, 314-329
67. Johnson, K. A. (2003) in Kinetic Analysis of Macromolecules: A Practical Approach (Johnson, K. A., ed) pp. 1-18, Oxford University Press, Oxford, UK
68. Northrop, D. B. (1982) Deuterium and tritium kinetic isotope effects on initial rates. Methods Enzymol. 87, 607-625
69. Walsh, C. (1979) Enzymatic Reaction Mechanisms, pp. 33-35, W. H. Freeman, & Co., San Francisco, CA
70. Yamaoka, M., Hara, T., Araki, H., Kaku, T., Hitaka, T., Tasaka, A., and Kusaka, M. (2013) Effect of an investigational CYP17A1 inhibitor, orteronel (TAK-700), on estrogen- and corticoid-synthesis pathways in hypophysectomized female rats and on the serum estradiol levels in female cynomolgus monkeys. J. Steroid Biochem. Mol. Biol. 138, 298-306
71. Miller, W. L., Geller, D. H., and Auchus, R. J. (1998) The molecular basis of isolated 17,20 lyase deficiency. Endocr. Res. 24, 817-825
72. Geller, D. H., Auchus, R. J., and Miller, W. L. (1999) P450c17 mutations R347H and R358Q selectively disrupt 17,20-lyase activity by disrupting interactions with P450 oxidoreductase and cytochrome b5. Mol. Endocrinol. 13, 167-175
73. Peng, H. M., Liu, J., Forsberg, S. E., Tran, H. T., Anderson, S. M., and Auchus, R. J. (2014) Catalytically relevant electrostatic interactions of cytochrome P450c17 (CYP17A1) and cytochrome b5. J. Biol. Chem. 289, 33838-33849
74. Zhu, J., and DeLuca, H. F. (2012) Vitamin D 25-hydroxylase-Four decades of searching, are we there yet? Arch. Biochem. Biophys. 523, 30-36
75. Shimshoni, J. A., Roberts, A. G., Scian, M., Topletz, A. R., Blankert, S. A., Halpert, J. R., Nelson, W. L., and Isoherranen, N. (2012) Stereoselective formation and metabolism of 4-hydroxyretinoic acid enantiomers by cytochrome P450 enzymes. J. Biol. Chem. 287, 42223-42232
76. He, X., Cryle, M. J., De Voss, J. J., and de Montellano, P. R. (2005) Calibration of the channel that determines the ω-hydroxylation regiospecificity of cytochrome P450 4A1: Catalytic oxidation of 12-halododecanoic acids. J. Biol. Chem. 280, 22697-22705
77. nd Ed., pp. 419-442, Kluwer Academic/Plenum Press, New York