Unveiling the crucial intermediates in androgen production

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 52, 2015, Pages 15856-15861

  Mak, Piotr J ^a   Gregory, Michael C ^b   Denisov, Ilia G ^b   Sligar, Stephen G ^b,c,d   Kincaid, James R ^a  

^a Marquette University   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Cytochrome P450; Nanodiscs; Peroxo hemiacetal; Resonance Raman spectroscopy; Steroids

Indexed keywords

17 HYDROXYPREGNENOLONE; ANDROGEN; CARBON; CYTOCHROME P450; CYTOCHROME P450 17A1; FERROUS ION; MEMBRANE PROTEIN; NANODISC; OXYGEN; PRASTERONE; UNCLASSIFIED DRUG; CYP17A1 PROTEIN, HUMAN; PREGNENOLONE; STEROID 17ALPHA MONOOXYGENASE;

ABSORPTION SPECTROSCOPY; ANDROGEN SYNTHESIS; ARTICLE; CHEMICAL BOND; NUCLEOPHILICITY; PRIORITY JOURNAL; RAMAN SPECTROMETRY; BIOCATALYSIS; BIOSYNTHESIS; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; HUMAN; HYDROGEN BOND; HYDROXYLATION; METABOLISM; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; SPECTROPHOTOMETRY; TEMPERATURE;

17-ALPHA-HYDROXYPREGNENOLONE; ANDROGENS; BIOCATALYSIS; BIOSYNTHETIC PATHWAYS; DEHYDROEPIANDROSTERONE; HUMANS; HYDROGEN BONDING; HYDROXYLATION; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PREGNENOLONE; PROTEIN CONFORMATION; SPECTROPHOTOMETRY; STEROID 17-ALPHA-HYDROXYLASE; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 84952674074     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1519376113     Document Type: Article

References (46)

1. Huggins C, Hodges CV (2002) Studies on prostatic cancer: I. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. 1941. J Urol 168(1):9-12.
2. Gomez L, Kovac JR, Lamb DJ (2015) CYP17A1 inhibitors in castration-resistant prostate cancer. Steroids 95:80-87.
3. Porubek D (2013) CYP17A1: A biochemistry, chemistry, and clinical review. Curr Top Med Chem 13(12):1364-1384.
4. Ortiz De Montellano PR, ed (2005) Cytochrome P450 Structure, Mechanism and Biochemistry (Kluwer/Plenum, New York), 3rd Ed.
5. Hrycay EG, Bandiera SM, eds (2015) Monooxygenase, Peroxidase and Peroxygenase Properties and Mechanisms of Cytochrome P450. Advances in Experimental Medicine and Biology (Springer, London), Vol 851.
6. 21 steroid side-chain cleavage system (17 α-hydroxylase-C17, 20 lyase). J Biol Chem 256(8):3871-3876.
7. Nakajin S, Shively JE, Yuan PM, Hall PF (1981) Microsomal cytochrome P-450 from neonatal pig testis: Two enzymatic activities (17 α-hydroxylase and c17, 20-lyase) associated with one protein. Biochemistry 20(14):4037-4042.
8. Gilep AA, Sushko TA, Usanov SA (2011) At the crossroads of steroid hormone biosynthesis: The role, substrate specificity and evolutionary development of CYP17. Biochim Biophys Acta 1814(1):200-209.
9. Akhtar M, Wright JN, Lee-Robichaud P (2011) A review ofmechanistic studies on aromatase (CYP19) and 17α-hydroxylase-17, 20-lyase (CYP17). J Steroid BiochemMol Biol 125(1-2):2-12.
10. Mathieu AP, Le Houx JG, Auchus RJ (2003) Molecular dynamics of substrate complexes with hamster cytochrome P450c17 (CYP17): Mechanistic approach to understanding substrate binding and activities. Biochim Biophys Acta 1619(3):291-300.
11. Auchus RJ (2001) The genetics, pathophysiology, and management of human deficiencies of P450c17. Endocrinol Metab Clin North Am 30(1):101-119, vii.
12. Rittle J, Green MT (2010) Cytochrome P450 compound I: Capture, characterization, and C-H bond activation kinetics. Science 330(6006):933-937.
13. Yosca TH, et al. (2013) Iron (IV) hydroxide pK (a) and the role of thiolate ligation in C-H bond activation by cytochrome P450. Science 342(6160):825-829.
14. Pallan PS, et al. (2015) Structural and kinetic basis of steroid 17α, 20-lyase activity in teleost fish cytochrome P450 17A1 and its absence in cytochrome P450 17A2. J Biol Chem 290(6):3248-3268.
15. De Vore NM, Scott EE (2012) Structures of cytochrome P450 17A1 with prostate cancer drugs abiraterone and TOK-001. Nature 482(7383):116-119.
16. Cupp-Vickery JR, Han O, Hutchinson CR, Poulos TL (1996) Substrate-assisted catalysis in cytochrome P450eryF. Nat Struct Biol 3(7):632-637.
17. Akhtar M, Corina D, Miller S, Shyadehi AZ, Wright JN (1994) Mechanism of the acylcarbon cleavage and related reactions catalyzed by multifunctional P-450s: Studies on cytochrome P-450 (17) alpha. Biochemistry 33(14):4410-4418.
18. Gregory MC, Denisov IG, Grinkova YV, Khatri Y, Sligar SG (2013) Kinetic solvent isotope effect in human P450 CYP17A1-mediated androgen formation: evidence for a reactive peroxoanion intermediate. J Am Chem Soc 135(44):16245-16247.
19. 2 into acetate during side-chain cleavage catalysed by cytochrome P-45017α (17α-hydroxylase-17, 20-lyase). J Chem Soc Perkin 1, (3):263-267.
20. 2]-[ferrite] center from irradiated oxyhemo- and oxymyoglobin. Biochim Biophys Acta 827(3):327-343.
21. Davydov R, Hoffman BM (2011) Active intermediates in heme monooxygenase reactions as revealed by cryoreduction/annealing, EPR/ENDOR studies. Arch Biochem Biophys 507(1):36-43.
22. Denisov IG, Grinkova YV, Sligar SG (2012) Cryoradiolysis and cryospectroscopy for studies of heme-oxygen intermediates in cytochromes p450. Methods Mol Biol 875:375-391.
23. Denisov IG, Mak PJ, Makris TM, Sligar SG, Kincaid JR (2008) Resonance Raman characterization of the peroxo and hydroperoxo intermediates in cytochrome P450. J Phys Chem A 112(50):13172-13179.
24. Denisov IG, Makris TM, Sligar SG (2001) Cryotrapped reaction intermediates of cytochrome p450 studied by radiolytic reduction with phosphorus-32. J Biol Chem 276(15):11648-11652.
25. Luthra A, Gregory M, Grinkova YV, Denisov IG, Sligar SG (2013) Nanodiscs in the studies of membrane-bound cytochrome P450 enzymes. Methods Mol Biol 987:115-127.
26. Grinkova YV, et al. (2008) The ferrous-oxy complex of human aromatase. Biochem Biophys Res Commun 372(2):379-382.
27. Gregory M, Mak PJ, Sligar SG, Kincaid JR (2013) Differential hydrogen bonding in human CYP17 dictates hydroxylation versus lyase chemistry. Angew Chem Int Ed Engl 52(20):5342-5345.
28. 2 in heme proteins. J Inorg Biochem 115:204-210.
29. 2 as vibrational probes of heme protein interactions. Coord Chem Rev 257(2):511-527.
30. Harris DL, Loew GH (1998) Theoretical investigation of the proton assisted pathway to formation of cytochrome P450 Compound I. J Am Chem Soc 120(35):8941-8948.
31. Ogliaro F, De Visser SP, Cohen S, Sharma PK, Shaik S (2002) Searching for the second oxidant in the catalytic cycle of cytochrome P450: A theoretical investigation of the iron (III) - hydroperoxo species and its epoxidation pathways. J Am Chem Soc 124(11):2806-2817.
32. Davydov R, et al. (2001) Hydroxylation of camphor by reduced oxy-cytochrome P450cam: Mechanistic implications of EPR and ENDOR studies of catalytic intermediates in native and mutant enzymes. J Am Chem Soc 123(7):1403-1415.
33. Davydov R, Macdonald IDG, Makris TM, Sligar SG, Hoffman BM (1999) EPR and ENDOR of catalytic intermediates in cryoreduced native and mutant oxy-cytochromes P450cam: Mutation-induced changes in the proton delivery system. J AmChem Soc 121(45):10654-10655.
34. Mak PJ, Thammawichai W, Wiedenhoeft D, Kincaid JR (2015) Resonance Raman spectroscopy reveals pH-dependent active site structural changes of lactoperoxidase compound 0 and its ferryl heme O-O bond cleavage products. J Am Chem Soc 137(1):349-361.
35. Nakamoto K (2009) Infrared and Raman Spectra of Inorganic and Coordination Compounds, Part A: Theory and Applications in Inorganic Chemistry (Wiley, Hoboken, NJ), 6th Ed.
36. Terner J, et al. (2006) Resonance Raman spectroscopy of oxoiron (IV) porphyrin π-cation radical and oxoiron (IV) hemes in peroxidase intermediates. J Inorg Biochem 100(4):480-501.
37. Spolitak T, Dawson JH, Ballou DP (2005) Reaction of ferric cytochrome P450cam with peracids: Kinetic characterization of intermediates on the reaction pathway. J Biol Chem 280(21):20300-20309.
38. Spolitak T, Funhoff EG, Ballou DP (2010) Spectroscopic studies of the oxidation of ferric CYP153A6 by peracids: Insights into P450 higher oxidation states. Arch Biochem Biophys 493(2):184-191.
39. Collins DP (2012) Spectroscopic characterization of reaction intermediates of the heme-thiolate proteins. PhD thesis (University of South Carolina, Columbia, SC).
40. Oloo WN, et al. (2014) Identification of a low-spin acylperoxoiron (III) intermediate in bio-inspired non-heme iron-catalyzed oxidations. Nat Commun 5:4046/1-4046/9.
41. Imai T, Globerman H, Gertner JM, Kagawa N, Waterman MR (1993) Expression and purification of functional human 17 α-hydroxylase/17, 20-lyase (P450c17) in Escherichia coli. Use of this system for study of a novel form of combined 17 α-hydroxylase/17, 20-lyase deficiency. J Biol Chem 268(26):19681-19689.
42. Barnes HJ, Arlotto MP, Waterman MR (1991) Expression and enzymatic activity of recombinant cytochrome P450 17 α-hydroxylase in Escherichia coli. Proc Natl Acad Sci USA 88(13):5597-5601.
43. Glasoe PK, Long FA (1960) Use of glass electrodes to measure acidities in deuterium oxide. J Phys Chem 64(1):188-190.
44. Denisov IG, Makris TM, Sligar SG (2002) Cryoradiolysis for the study of P450 reaction intermediates. Methods Enzymol 357:103-115.
45. Shriver DF, Dunn JBR (1974) Backscattering geometry for Raman-spectroscopy of colored materials. Appl Spectrosc 28(4):319-323.
46. Luthra A, Denisov IG, Sligar SG (2011) Temperature derivative spectroscopy to monitor the autoxidation decay of cytochromes P450. Anal Chem 83(13):5394-5399.