Catalytically relevant electrostatic interactions of cytochrome P450c17 (CYP17A1) and cytochrome b5

Journal of Biological Chemistry

Volumn 289, Issue 49, 2014, Pages 33838-33849

  Peng, Hwei Ming ^a   Liu, Jiayan ^a   Forsberg, Sarah E ^a   Tran, Hong T ^b   Anderson, Sean M ^a   Auchus, Richard J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

CARBOXYLATE GROUPS; CYTOCHROME B; DATA SUPPORT; DRUG TARGETS; INTERACTION SITE;

CARBOXYLATION;

ARGININE; CYTOCHROME B5; CYTOCHROME P450; CYTOCHROME P450 17A1; GLUTAMIC ACID; LYSINE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; 1 (3 DIMETHYLAMINOPROPYL) 3 ETHYLCARBODIIMIDE; AMINO ACID; CROSS LINKING REAGENT; CYP17A1 PROTEIN, HUMAN; PROTEIN BINDING; STEROID 17ALPHA MONOOXYGENASE;

ARTICLE; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; ESCHERICHIA COLI; HUMAN; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR DOCKING; NONHUMAN; PLASMID; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; ULTRAVIOLET SPECTROSCOPY; WILD TYPE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ENZYME ACTIVE SITE; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; STATIC ELECTRICITY; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; AMINO ACIDS; CATALYTIC DOMAIN; CROSS-LINKING REAGENTS; CRYSTALLOGRAPHY, X-RAY; CYTOCHROMES B5; ESCHERICHIA COLI; ETHYLDIMETHYLAMINOPROPYL CARBODIIMIDE; GENE EXPRESSION; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; STATIC ELECTRICITY; STEROID 17-ALPHA-HYDROXYLASE; THERMODYNAMICS;

EID: 84917707291     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.608919     Document Type: Article

References (42)

1. 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
2. Attard, G., Reid, A. H., Yap, T. A., Raynaud, F., Dowsett, M., Settatree, S., Barrett, M., Parker, C., Martins, V., Folkerd, E., Clark, J., Cooper, C. S., Kaye, S. B., Dearnaley, D., Lee, G., and de Bono, J. S. (2008) Phase I clinical trial of a selective inhibitor of CYP17, abiraterone acetate, confirms that castration-resistant prostate cancer commonly remains hormone driven. J. Clin. Oncol. 26, 4563-4571
3. Mostaghel, E. A., and Nelson, P. S. (2008) Intracrine androgen metabolism in prostate cancer progression: mechanisms of castration resistance and therapeutic implications. Best Pract. Res. Clin. Endocrinol. Metab. 22, 243-258
4. Miller, W. L., Auchus, R. J., and Geller, D. H. (1997) The regulation of 17,20 lyase activity. Steroids 62, 133-142
5. 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
6. Naffin-Olivos, J. L., and Auchus, R. J. (2006) Human cytochrome b5 requires residues E48 and E49 to stimulate the 17,20-lyase activity of cytochrome P450c17. Biochemistry 45, 755-762
7. Peng, H. M., and Auchus, R. J. (2013) The action of cytochrome b5 on CYP2E1 and CYP2C19 activities requires anionic residues D58 and D65. Biochemistry 52, 210-220
8. 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
9. Lee-Robichaud, P., Kaderbhai, M. A., Kaderbhai, N., Wright, J. N., and Akhtar, M. (1997) Interaction of human CYP17 (P-450(17α), 17α-hydroxylase-17,20-lyase) with cytochrome b5: importance of the orientation of the hydrophobic domain of cytochrome b5. Biochem. J. 321, 857-863
10. 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
11. Lee-Robichaud, P., Akhtar, M. E., Wright, J. N., Sheikh, Q. I., and Akhtar, M. (2004) 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. 92, 119-130
12. Geller, D. H., Auchus, R. J., Mendonça, B. B., and Miller, W. L. (1997) The genetic and functional basis of isolated 17,20-lyase deficiency. Nat. Genet. 17, 201-205
13. Hershkovitz, E., Parvari, R., Wudy, S. A., Hartmann, M. F., Gomes, L. G., Loewental, N., and Miller, W. L. (2008) Homozygous mutation G539R in the gene for P450 oxidoreductase in a family previously diagnosed as having 17,20-lyase deficiency. J. Clin. Endocrinol. Metab. 93, 3584-3588
14. Kok, R. C., Timmerman, M. A., Wolffenbuttel, K. P., Drop, S. L., and de Jong, F. H. (2010) Isolated 17,20-lyase deficiency due to the cytochrome b5 mutation W27X. J. Clin. Endocrinol. Metab. 95, 994-999
15. Idkowiak, J., Randell, T., Dhir, V., Patel, P., Shackleton, C. H., Taylor, N. F., Krone, N., and Arlt, W. (2012) A missense mutation in the human cytochrome b5 gene causes 46,XY disorder of sex development due to true isolated 17,20 lyase deficiency. J. Clin. Endocrinol. Metab. 97, E465-E475
16. Peng, H. M., and Auchus, R. J. (2014) Two surfaces of cytochrome b5 with major and minor contributions to CYP3A4-catalyzed steroid and nifedipine oxygenation chemistries. Arch. Biochem. Biophys. 541, 53-60
17. Yoshimoto, F. K., Zhou, Y., Peng, H. M., Stidd, D., Yoshimoto, J. A., Sharma, K. K., Matthew, S., and Auchus, R. J. (2012) Minor activities and transition state properties of the human steroid hydroxylases cytochromes P450c17 and P450c21, from reactions observed with deuteriumlabeled substrates. Biochemistry 51, 7064-7077
18. Sandee, D., and Miller, W. L. (2011) High-yield expression of a catalytically active membrane-bound protein: human P450 oxidoreductase. Endocrinology 152, 2904-2908
19. Mulrooney, S. B., and Waskell, L. (2000) High-level expression in Escherichia coli and purification of the membrane-bound form of cytochrome b5. Protein Expr. Purif. 19, 173-178
20. Sherbet, D. P., Tiosano, D., Kwist, K. M., Hochberg, Z., and Auchus, R. J. (2003) CYP17 mutation E305G causes isolated 17,20-lyase deficiency by selectively altering substrate binding. J. Biol. Chem. 278, 48563-48569
21. Götze, M., Pettelkau, J., Schaks, S., Bosse, K., Ihling, C. H., Krauth, F., Fritzsche, R., Kühn, U., and Sinz, A. (2012) StavroX-a software for analyzing crosslinked products in protein interaction studies. J. Am. Soc. Mass Spectrom. 23, 76-87
22. Li, W., O'Neill, H. A., and Wysocki, V. H. (2012) SQID-XLink: implementation of an intensity-incorporated algorithm for cross-linked peptide identification. Bioinformatics 28, 2548-2550
23. Tovchigrechko, A., and Vakser, I. A. (2006) GRAMM-X public web server for protein-protein docking. Nucleic Acids Res. 34, W310-W314
24. de Vries, S. J., van Dijk, M., and Bonvin, A. M. (2010) TheHADDOCKweb server for data-driven biomolecular docking. Nat. Protoc. 5, 883-897
25. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK: a protein- protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125, 1731-1737
26. de Vries, S. J., van Dijk, A. D., Krzeminski, M., van Dijk, M., Thureau, A., Hsu, V., Wassenaar, T., and Bonvin, A. M. (2007) HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 69, 726-733
27. 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
28. Dehouck, Y., Kwasigroch, J. M., Rooman, M., and Gilis, D. (2013) BeAt- MuSiC: Prediction of changes in protein-protein binding affinity on mutations. Nucleic Acids Res. 41, W333-W339
29. Hlavica, P., Schulze, J., and Lewis, D. F. (2003) Functional interaction of cytochrome P450 with its redox partners: a critical assessment and update of the topology of predicted contact regions. J. Inorg. Biochem. 96, 279-297
30. Lewis, D. F., and Lee-Robichaud, P. (1998) Molecular modelling of steroidogenic cytochromes P450 from families CYP11, CYP17, CYP19 and CYP21 based on the CYP102 crystal structure. J. Steroid Biochem. Mol. Biol. 66, 217-233
31. Auchus, R. J., and Miller, W. L. (1999) Molecular modeling of human P450c17 (17α-hydroxylase/17,20-lyase): insights into reaction mechanisms and effects of mutations. Mol. Endocrinol. 13, 1169-1182
32. Zhao, C., Gao, Q., Roberts, A. G., Shaffer, S. A., Doneanu, C. E., Xue, S., Goodlett, D. R., Nelson, S. D., and Atkins, W. M. (2012) Cross-linking mass spectrometry and mutagenesis confirm the functional importance of surface interactions between CYP3A4 and holo/apo cytochrome b5. Biochemistry 51, 9488-9500
33. Im, S. C., and Waskell, L. (2011) The interaction of microsomal cytochrome P450 2B4 with its redox partners, cytochrome P450 reductase and cytochrome b5. Arch. Biochem. Biophys. 507, 144-153
34. Pandey, M. K., Vivekanandan, S., Ahuja, S., Huang, R., Im, S. C., Waskell, L., and Ramamoorthy, A. (2013) Cytochrome-P450-cytochrome-b5 interaction in a membrane environment changes 15Nchemical shift anisotropy tensors. J. Phys. Chem. B 117, 13851-13860
35. Gao, Q., Doneanu, C. E., Shaffer, S. A., Adman, E. T., Goodlett, D. R., and Nelson, S. D. (2006) Identification of the interactions between cytochrome P450 2E1 and cytochrome b5 by mass spectrometry and site-directed mutagenesis. J. Biol. Chem. 281, 20404-20417
36. Handratta, V. D., Vasaitis, T. S., Njar, V. C., Gediya, L. K., Kataria, R., Chopra, P., Newman, D., Jr., Farquhar, R., Guo, Z., Qiu, Y., and Brodie, A. M. (2005) Novel C-17-heteroaryl steroidal CYP17 inhibitors/antiandrogens: synthesis, in vitro biological activity, pharmacokinetics, and antitumor activity in the LAPC4 human prostate cancer xenograft model. J. Med. Chem. 48, 2972-2984
37. Schweizer, M. T., and Antonarakis, E. S. (2012) Abiraterone and other novel androgen-directed strategies for the treatment of prostate cancer: a new era of hormonal therapies is born. Ther. Adv. Urol. 4, 167-178
38. Auchus, R. J., Buschur, E. O., Chang, A. Y., Hammer, G. D., Ramm, C., Madrigal, D., Wang, G., Gonzalez, M., Xu, X. S., Smit, J. W., Jiao, J., and Yu, M. K. (2014) Abiraterone acetate to lower androgens in women with classic 21-hydroxylase deficiency. J. Clin. Endocrinol. Metab. 99, 2763-2770
39. Attard, G., Reid, A. H., Auchus, R. J., Hughes, B. A., Cassidy, A. M., Thompson, E., Oommen, N. B., Folkerd, E., Dowsett, M., Arlt, W., and de Bono, J. S. (2012) Clinical and biochemical consequences of CYP17A1 inhibition with abiraterone given with and without exogenous glucocorticoids in castrate men with advanced prostate cancer. J. Clin. Endocrinol. Metab. 97, 507-516
40. Auchus, M. L., and Auchus, R. J. (2012) Human steroid biosynthesis for the oncologist. J. Investig. Med. 60, 495-503
41. Kater, C. E., and Biglieri, E. G. (1994) Disorders of steroid 17α-hydroxylase deficiency. Endocrinol. Metab. Clin. North Am. 23, 341-357
42. Friberg, A., Vigil, D., Zhao, B., Daniels, R. N., Burke, J. P., Garcia-Barrantes, P. M., Camper, D., Chauder, B. A., Lee, T., Olejniczak, E. T., and Fesik, S. W. (2013) Discovery of potent myeloid cell leukemia 1 (Mcl-1) inhibitors using fragment-based methods and structure-based design. J. Med. Chem. 56, 15-30