Human cytochrome P450 17A1 conformational selection: Modulation by ligand and cytochrome b5

Journal of Biological Chemistry

Volumn 289, Issue 20, 2014, Pages 14310-14320

  Estrada, D Fernando ^a   Skinner, Andria L ^a,b   Laurence, Jennifer S ^a   Scott, Emily E ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REACTION INTERMEDIATES; SUBSTRATES;

BIFUNCTIONAL ENZYMES; CONFORMATIONAL SELECTION; CONFORMATIONAL STATE; CRYSTALLOGRAPHIC STUDIES; CYTOCHROME P450 ENZYMES; DEHYDROEPIANDROSTERONE; STRUCTURAL CONFORMATIONS; SUBSTRATE RECOGNITION;

ENZYMES;

17 HYDROXYPREGNENOLONE; ANDROGEN; CYTOCHROME B5; CYTOCHROME P450 17; CYTOCHROME P450 17A1; ESTROGEN; LIGAND; PRASTERONE; PREGNENOLONE; PREGNENOLONE C17; STEROID 17ALPHA MONOOXYGENASE; UNCLASSIFIED DRUG; ABIRATERONE; ANDROSTANE DERIVATIVE; CYP17A1 PROTEIN, HUMAN; CYTOCHROME P450 INHIBITOR;

ARTICLE; CONFORMATIONAL TRANSITION; DRUG METABOLISM; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; HORMONE SYNTHESIS; HYDROXYLATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; STEROIDOGENESIS; TEMPERATURE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYME SPECIFICITY; HUMAN; METABOLISM; PROTEIN CONFORMATION;

ANDROSTENOLS; CYTOCHROME P-450 ENZYME INHIBITORS; CYTOCHROMES B5; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; STEROID 17-ALPHA-HYDROXYLASE; SUBSTRATE SPECIFICITY;

EID: 84901044257     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.560144     Document Type: Article

References (44)

1. Ortiz de Montellano, P. R. (2005) Cytochrome P450: Structure, Mechanism, and Biochemistry (de Montellano, O., ed) 3rd Ed., pp. 377-530, Kluwer Academic/Plenum Publishers, New York
2. Guengerich, F. P. (2009) Cataloging the repertoire of nature's blowtorch, P450. Chem. Biol. 16, 1215-1216
3. Villali, J., and Kern, D. (2010) Choreographing an enzyme's dance. Curr. Opin. Chem. Biol. 14, 636-643
4. Williams, P. A., Cosme, J., Sridhar, V., Johnson, E. F., and McRee, D. E. (2000) Mammalian microsomal cytochrome P450 monooxygenase: structural adaptations for membrane binding and functional diversity. Mol. Cell 5, 121-131 (Pubitemid 30105441)
5. Johnson, E. F., Connick, J. P., Reed, J. R., Backes, W. L., Desai, M. C., Xu, L., Estrada, D. F., Laurence, J. S., and Scott, E. E. (2014) Correlating structure and function of drug-metabolizing enzymes: progress and ongoing challenges. Drug Metab. Dispos. 42, 9-22
6. Johnson, E. F., and Stout, C. D. (2013) Structural diversity of eukaryotic membrane cytochrome P450s. J. Biol. Chem. 288, 17082-17090
7. Wilderman, P. R., Gay, S. C., Jang, H. H., Zhang, Q., Stout, C. D., and Halpert, J. R. (2012) Investigation by site-directed mutagenesis of the role of cytochrome P450 2B4 non-active-site residues in protein-ligand interactions based on crystal structures of the ligand-bound enzyme. FEBS J. 279, 1607-1620
8. Zhang, Z. G., Liu, Y., Guengerich, F. P., Matse, J. H., Chen, J., and Wu, Z. L. (2009) Identification of amino acid residues involved in 4-chloroindole 3-hydroxylation by cytochrome P450 2A6 using screening of random libraries. J. Biotechnol. 139, 12-18
9. Kim, D., and Guengerich, F. P. (2004) Selection of human cytochrome P450 1A2 mutants with enhanced catalytic activity for heterocyclic amine N-hydroxylation. Biochemistry 43, 981-988 (Pubitemid 38141496)
10. Kim, D., and Guengerich, F. P. (2004) Enhancement of 7-methoxyresorufin O-demethylation activity of human cytochrome P450 1A2 by molecular breeding. Arch. Biochem. Biophys. 432, 102-108 (Pubitemid 39425033)
11. 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
12. Rittle, J., and Green, M. T. (2010) Cytochrome P450 compound I: capture, characterization, and C-H bond activation kinetics. Science 330, 933-937
13. Luthra, A., Denisov, I. G., and Sligar, S. G. (2011) Spectroscopic features of cytochrome P450 reaction intermediates. Arch. Biochem. Biophys. 507, 26-35
14. Tripathi, S., Li, H., and Poulos, T. L. (2013) Structural basis for effector control and redox partner recognition in cytochrome P450. Science 340, 1227-1230
15. Hiruma, Y., Hass, M. A., Kikui, Y., Liu, W. M.,O lmez, B., Skinner, S. P., Blok, A., Kloosterman, A., Koteishi, H., Löhr, F., Schwalbe, H., Nojiri, M., and Ubbink, M. (2013) The structure of the cytochrome P450cam-putidaredoxin complex determined by paramagnetic NMR spectroscopy and crystallography. J. Mol. Biol. 425, 4353-4365
16. Haider, S. M., Patel, J. S., Poojari, C. S., and Neidle, S. (2010) Molecular modeling on inhibitor complexes and active-site dynamics of cytochrome P450 C17, a target for prostate cancer therapy. J. Mol. Biol. 400, 1078-1098
17. Yang, Y., Wong, S. E., and Lightstone, F. C. (2014) Understanding a substrate's product regioselectivity in a family of enzymes: a case study of acetaminophen binding in cytochrome P450s. PloS One 9, e87058
18. Shi, R., Li, J., Cao, X., Zhu, X., and Lu, X. (2011) Exploration of the binding of proton pump inhibitors to human P450 2C9 based on docking and molecular dynamics simulation. J. Mol. Model. 17, 1941-1951
19. Lampe, J. N., Brandman, R., Sivaramakrishnan, S., and de Montellano, P. R. (2010) Two-dimensional NMR and all-atom molecular dynamics of cytochrome P450 CYP119 reveal hidden conformational substates. J. Biol. Chem. 285, 9594-9603
20. Lampe, J. N., Floor, S. N., Gross, J. D., Nishida, C. R., Jiang, Y., Trnka, M. J., and Ortiz de Montellano, P. R. (2008) Ligand-induced conformational heterogeneity of cytochrome P450 CYP119 identified by 2D NMR spectroscopy with the unnatural amino acid 13C-p-methoxyphenylalanine. J. Am. Chem. Soc. 130, 16168-16169
21. Roberts, A. G., Díaz, M. D., Lampe, J. N., Shireman, L. M., Grinstead, J. S., Dabrowski, M. J., Pearson, J. T., Bowman, M. K., Atkins, W. M., and Campbell, A. P. (2006) NMR studies of ligand binding to P450(eryF) provides insight into the mechanism of cooperativity. Biochemistry 45, 1673-1684 (Pubitemid 43222111)
22. Jovanovic, T., and McDermott, A. E. (2005) Observation of ligand binding to cytochrome P450 BM-3 by means of solid-state NMR spectroscopy. J. Am. Chem. Soc. 127, 13816-13821 (Pubitemid 41437031)
23. Asciutto, E. K., Young, M. J., Madura, J., Pochapsky, S. S., and Pochapsky, T. C. (2012) Solution structural ensembles of substrate-free cytochrome P450(cam). Biochemistry 51, 3383-3393
24. de Bono, J. S., Logothetis, C. J., Molina, A., Fizazi, K., North, S., Chu, L., Chi, K. N., Jones, R. J., Goodman, O. B., Jr., Saad, F., Staffurth, J. N., Mainwaring, P., Harland, S., Flaig, T. W., Hutson, T. E., Cheng, T., Patterson, H., Hainsworth, J. D., Ryan, C. J., Sternberg, C. N., Ellard, S. L., Fléchon, A., Saleh, M., Scholz, M., Efstathiou, E., Zivi, A., Bianchini, D., Loriot, Y., Chieffo, N., Kheoh, T., Haqq, C. M., Scher, H. I., and COU-AA-301 Investigators (2011) Abiraterone and increased survival in metastatic prostate cancer. New Engl. J. Med. 364, 1995-2005
25. Siegel, R., Ma, J., Zou, Z., and Jemal, A. (2014) Cancer statistics, 2014. CA Cancer J. Clin. 64, 9-29
26. Akhtar, M. K., Kelly, S. L., and Kaderbhai, M. A. (2005) Cytochrome b5 modulation of 17{alpha} hydroxylase and 17-20 lyase (CYP17) activities in steroidogenesis. J. Endocrinol. 187, 267-274 (Pubitemid 41685186)
27. 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 (Pubitemid 29016484)
28. 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
29. Lee-Robichaud, P., Wright, J. N., Akhtar, M. E., and Akhtar, M. (1995) Modulation of the activity of human 17α-hydroxylase-17,20-lyase (CYP17) by cytochrome b5: endocrinological and mechanistic implications. Biochem. J. 308, 901-908
30. Ciaccio, N. A., Moreno, M. L., Bauer, R. L., and Laurence, J. S. (2008) High-yield expression in E. coli and refolding of the bZIP domain of activating transcription factor 5. Protein Expr. Purif. 62, 235-243
31. Lian, L.-Y., and Middleton, D. A. (2001) Labelling approaches for protein structural studies by solution-state and solid-state NMR. Progr. NMR Spectrosc. 39, 171-190 (Pubitemid 32997728)
32. 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
33. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
34. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352
35. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696 (Pubitemid 40695845)
36. Hildebrandt, P., Heibel, G., Anzenbacher, P., Lange, R., Krüger, V., and Stier, A. (1994) Conformational analysis of mitochondrial and microsomal cytochrome P-450 by resonance Raman spectroscopy. Biochemistry 33, 12920-12929 (Pubitemid 24352883)
37. Lange, R., Pantaloni, A., and Saldana, J. L. (1992) The cholesterol-sidechain- cleaving cytochrome P450 spin-state equilibrium. 2. Conformational analysis. Eur. J. Biochem. 207, 75-79
38. Davydov, D. R., Halpert, J. R., Renaud, J. P., and Hui Bon Hoa, G. (2003) Conformational heterogeneity of cytochrome P450 3A4 revealed by high pressure spectroscopy. Biochem. Biophys. Res. Commun. 312, 121-130 (Pubitemid 37443936)
39. Pochapsky, T. C., Kazanis, S., and Dang, M. (2010) Conformational plasticity and structure/function relationships in cytochromes P450. Antioxid. Redox Signal. 13, 1273-1296
40. Ahuja, S., Jahr, N., Im, S. C., Vivekanandan, S., Popovych, N., Le Clair, S. V., Huang, R., Soong, R., Xu, J., Yamamoto, K., Nanga, R. P., Bridges, A., Waskell, L., and Ramamoorthy, A. (2013) A model of the membranebound cytochrome b5 -cytochrome P450 complex from NMR and mutagenesis data. J. Biol. Chem. 288, 22080-22095
41. 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 (Pubitemid 28109723)
42. Khatri, Y., Gregory, M. C., Grinkova, Y. V., Denisov, I. G., and Sligar, S. G. (2014) Active site proton delivery and the lyase activity of human CYP17A1. Biochem. Biophys. Res. Commun. 443, 179-184
43. Perret, A., and Pompon, D. (1998) Electron shuttle between membranebound cytochrome P450 3A4 and b5 rules uncoupling mechanisms. Biochemistry 37, 11412-11424 (Pubitemid 28388182)
44. Schenkman, J. B., and Jansson, I. (2003) The many roles of cytochrome b5. Pharmacol. Ther. 97, 139-152