Crystallization of cytochromes P450 and substrate-enzyme interactions

Current Topics in Medicinal Chemistry

Volumn 4, Issue 16, 2004, Pages 1789-1802

  Li, Huiying ^a   Poulos, Thomas L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crystal structure; Crystallization; Cytochrome P450; Substrate enzyme interaction

Indexed keywords

4 PHENYLIMIDAZOLE; ANTIBIOTIC AGENT; CRYOPROTECTIVE AGENT; CYTOCHROME P450; CYTOCHROME P450 INHIBITOR; DETERGENT; DICLOFENAC; IMIDAZOLE; LIGAND; MICROSOME ENZYME;

AMINO TERMINAL SEQUENCE; CONCENTRATION RESPONSE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ASSAY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME ENGINEERING; ENZYME RELEASE; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN; LIGAND BINDING; NONHUMAN; PH; PROTEIN DATABASE; PROTEIN EXPRESSION; REVIEW; SOLUBILITY; STRUCTURE ACTIVITY RELATION;

BINDING SITES; CRYSTALLIZATION; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN ENGINEERING; SUBSTRATE SPECIFICITY;

EID: 10644234762     PISSN: 15680266     EISSN: None     Source Type: Journal    
DOI: 10.2174/1568026043387205     Document Type: Review

References (64)

1. Nelson, D. R. Mining databases for cytochrome P450 genes. Methods Enzymol. 2002, 357, 3-15.
2. Mansuy, D.; Renaud, J.-P. Heme-thiolate proteins different from cytochrome P450 catalyzing monooxygenations. in Cytochrome P450 Structure, Mechanism, and Biochemistry Ortiz de Montellano, P. R., ed Plenum Press: New York and London, 1995; pp. 537-574.
3. Andersen, J. F.; Hutchinson, C. R. Characterization of Saccharopolyspora erythraea cytochrome P-450 genes and enzymes, including 6-deoxyerythronolide B hydroxylase. J. Bacter. 1992, 174, 725-735.
4. Guengerich, F. P. Human cytochrome P450 enzymes. in Cytochrome P-450 Structure, Mechanism and Biochemistry Ortiz de Montellano, P. R., ed Plenum Press: New York and London, 1995; pp. 473-535.
5. Hawkes, D. B.; Adams, G. W.; Burlingame, A. L.; Ortiz de Montellano, P. R.; De Voss, J. J. Cytochrome P450(cin) (CYP176A), isolation, expression, and characterization. J. Biol. Chem. 2002, 277, 27725-27732.
6. Jackson, C. J.; Lamb, D. C.; Marczylo, T. H.; Warrilow, A. G. S.; Manning, N. J.; Lowe, D. J.; Kelly, D. E.; Kelly, S. L. A novel sterol 14alpha-demethylase/ferredoxin fusion protein (MCCYP51FX) from Methylococcus capsulatus represents a new class of the cytochrome P450 superfamily. J. Biol. Chem. 2002, 277, 46959-46965.
7. Roberts, G. A.; Celik, A.; Hunter, D. J.; Ost, T. W.; White, J. H.; Chapman, S. K.; Turner, N. J.; Flitsch, S. L. A self-sufficient cytochrome p450 with a primary structural organization that includes a flavin domain and a [2Fe-2S] redox center. J. Biol. Chem. 2003, 278, 48914-48920.
8. Hecker, M.; Ullrich, V. On the mechanism of prostacyclin and thromboxane A2 biosynthesis. J. Biol. Chem. 1989, 264, 141-150.
9. Shiro, Y.; Fujii, M.; Iizuka, T.; Adachi, S.; Tsukamoto, K.; Nakahara, K.; Shoun, H. Spectroscopic and kinetic studies on reaction of cytochrome P450nor with nitric oxide. Implication for its nitric oxide reduction mechanism. J. Biol. Chem. 1995, 270, 1617-1623.
10. McPherson, A. Crystallization of Biological Macromolecules. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York, 1999.
11. Poulos, T. L.; Perez, M.; Wagner, G. C. Preliminary crystallographic data on cytochrome P-450CAM. J. Biol. Chem. 1982, 257, 10427-10429.
12. Poulos, T. L. Approaches to crystallizing P450s. Methods Enzymol. 1996, 272, 359-368.
13. Nickerson, D.; Wong, L.-L.; Rao, A. An improved procedure for the preparation of X-ray diffraction-quality crystals of cytochrome P450cam. Acta Cryst. 1997, D54, 470-472.
14. Yano, J. K.; Koo, L. S.; Schuller, D. J.; Li, H.; Ortiz de Montellano, P. R.; Poulos, T. L. Crystal structure of a thermophilic cytochrome P450 from the archaeon Sulfolobus solfataricus. J. Biol. Chem. 2000, 275, 31086-31092.
15. Scott, E. E.; He, Y. A.; Wester, M. R.; White, M. A.; Chin, C. C.; Halpert, J. R.; Johnson, E. F.; Stout, C. D. An open conformation of mammalian cytochrome P450 2B4 at 1.6-A resolution. Proc. Natl. Acad. Sci. USA 2003, 100, 13196-13201.
16. Podust, L. M.; Poulos, T. L.; Waterman, M. R. Crystal structure of cytochrome P450 14alpha-sterol demethylase (CYP51) from Mycobacterium tuberculosis in complex with azole inhibitors. Proc. Natl. Acad. Sci. USA 2001, 98, 3068-3073.
17. Boddupalli, S. S.; Hasemann, C. A.; Ravichandran, K. G.; Lu, J. Y.; Goldsmith, E. J.; Deisenhofer, J.; Peterson, J. A. Crystallization and preliminary x-ray diffraction analysis of P450terp and the hemoprotein domain of P450BM-3, enzymes belonging to two distinct classes of the cytochrome P450 superfamily. Proc. Natl. Acad. Sci. USA 1992, 89, 5567-5571.
18. Li, H.; Poulos, T. L. The structure of the cytochrome P450BM-3 haem domain complexed with the fatty acid substrate, palmitoleic acid. Nature Struc. Biol. 1997, 4, 140-146.
19. Stura, E. A.; Wilson, I. A. Analytical and production seeding techniques. Methods 1990, 1, 38-49.
20. Cupp-Vickery, J. R.; Li, H.; Poulos, T. L. Preliminary crystallographic analysis of an enzyme involved in erythromycin biosynthesis: cytochrome P450eryF. Proteins 1994, 20, 197-201.
21. Shimizu, H.; Park, S.-Y.; Shiro, Y.; Adachi, S. X-ray structure of nitric oxide reductase (cytochrome P450nor) at atomic resolution. Acta Cryst. 2002, D58, 81-89.
22. von Wachenfeldt, C.; Johnson, E. F. Structure of eukaryotic cytochrome P450 enzymes. in Cytochrome P-450 Structure, Mechanism and Biochemistry Ortiz de Montellano, P. R., ed Plenum Press: New York and London, 1995; pp. 183-223.
23. Garavito, R. M.; Picot, D. The art of crystallizing membrane proteins. Methods 1990, 1, 57-69.
24. Pernecky, S. J.; Coon, M. J. N-terminal modifications that alter P450 mambrane targeting and function. Methods Enzymol. 1996, 272, 25-34.
25. Cosme, J.; Johnson, E. F. Engineering microsomal cytochrome P450 2C5 to be a soluble,monomeric enzyme. J. Biol. Chem. 2000, 275, 2545-2553.
26. Williams, P. A.; Cosme, J.; Sridhar, V.; Johnson, E. F.; McRee, D. E. Mammalian microsomal cytochrome P450 monooxygenase: structural adaptations for membrane binding and functional diversity. Mol. Cell 2000, 5, 121-131.
27. Williams, P. A.; Cosme, J.; Ward, A.; Angove, H. C.; Matak Vinkovic, D.; Jhoti, H. Crystal structure of human cytochrome P450 2C9 with bound warfarin. Nature 2003, 424, 464-468.
28. Scott, E. E.; Spatzenegger, M.; Halpert, J. R. A truncation of 2B subfamily cytochromes P450 yields increased expression levels, increased solubility, and decreased aggregation while retaining function. Arch. Biochem. Biophys. 2001, 395, 57-68.
29. Wester, M. R.; Stout, C. D.; Johnson, E. F. Purification and crystallization of N-terminally truncated forms of microsomal cytochrome P450 2C5. Methods Enzymol. 2002, 357, 73-79.
30. Pechkova, E.; Nicolini, C. Protein nucleation and crystallization by homologous protein thin film template. J. Cellular Biochem. 2002, 85, 243-251.
31. Park, S.; Yamane, K.; Adachi, S.; Shiro, Y.; Weiss, K.; Maves, S.; Sligar, S. Thermophilic cytochrome P450(CYP119) from Sulfolobus Solfataricus: high resolution structure and functional properties. J. Inorg. Biochem. 2002, 91, 491-501.
32. Yano, J. K.; Blasco, F.; Li, H.; Schmid, R. D.; Henke, A.; Poulos, T. L. Preliminary characterization and crystal structure of a thermostable cytochrome P450 from Thermus thermophilus. J . Biol. Chem. 2003, 278, 608-616.
33. Zerbe, K.; Pylypenko, O.; Vitali, F.; Zhang, W.; Rouset, S.; Heck, M.; Vrijbloed, J. W.; Bischoff, D.; Bister, B.; Sussmuth, R. D.; Pelzer, S.; Wohlleben, W.; Robinson, J. A.; Schlichting, I. Crystal structure of OxyB, a cytochrome P450 implicated in an oxidative phenol coupling reaction during vancomycin biosynthesis. J. Biol. Chem. 2002, 277, 47476-47485.
34. Pylypenko, O.; Vitali, F.; Zerbe, K.; Robinson, J. A.; Schlichting, I. Crystal structure of OxyC, a cytochrome P450 implicated in an oxidative C-C coupling reaction during vancomycin biosynthesis. J. Biol. Chem. 2003, 278, 46727-46733.
35. Leys, D.; Mowat, C. G.; Mclean, K. J.; Richmond, A.; Chapman, S. K.; Walkinshaw, M. D.; Munro, A. W. Atomic structure of Mycobacterium tuberculosis CYP121 to 1.06A reveals novel features of cytochrome P450. J. Biol. Chem. 2003, 278, 5141-5147.
36. Lee, D.-S.; Yamada, A.; Sugimoto, H.; Matsunaga, I.; Ogura, H.; Ichihara, K.; Adachi, S.; Park, S.-Y.; Shiro, Y. Substrate recognition and molecular mechanism of fatty acid hydroxylation by cytochrome P450 from Bacillus subtilis: crystallographic, spectroscopic and mutational studies. J. Biol. Chem. 2003, 278, 9761-9767.
37. Podust, L. M.; Kim, Y.; Arase, M.; Neely, B. A.; Beck, B. J.; Bach, H.; Sherman, D. H.; Lamb, D. C.; Kelly, S. L.; Waterman, M. R. The 1.92-A structure of Streptomyces coelicolor A3(2) CYP154C1. A new monooxygenase that functionalizes macrolide ring systems. J. Biol. Chem. 2003, 278, 12214-12221.
38. Nagano, S.; Li, H.; Shimizu, H.; Nishida, C.; Ogura, H.; Ortiz de Montellano, P. R.; Poulos, T. L. Crystal structures of epothilone D-bound, epothilone B-bound, and substrate-free forms of cytochrome P450epoK. J. Biol. Chem. 2003, 278, 44886-44893.
39. de la Fortalle, E.; Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 1997, 226, 472-494.
40. Terwilliger, T. C.; Berendzen, J. Automated MAD and MIR structure solution. Acta Cryst. 1999, D55, 849-861.
41. Li, H.; Yano, J. K.; Poulos, T. L. Molecular replacement in P450 crystal structure determinations. Methods Enzymol 2002, 357, 79-93.
42. Navaza, J. AMoRe: an automatic package for molecular replacement. Acta Cryst. 1994, A50, 157-163.
43. Vagin, A.; Teplyakov, A. MOLREP: an automated program for molecular replacement. J. Appl. Cryst. 1997, 30, 1022-1025.
44. Read, R. Pushing the boundary of molecular replacement with maximum likelihood. Acta Cryst. 2001, D57, 1373-1382.
45. Podust, L. M.; Stojan, J.; Poulos, T. L.; Waterman, M. R. Substrate recognition sites in 14alpha-sterol demethylase from comparative analysis of amino acid sequences and X-ray structure of Mycobacterium tuberculosis CYP51. J. Inorg. Biochem. 2001, 87, 227-235.
46. Wester, M. R.; Johnson, E. F.; Marques-Soares, C.; Dijols, S.; Dansette, P. M.; Mansuy, D.; Stout, C. D. Structure of mammalian cytochrome P450 2C5 complexed with diclofenac at 2.1 A resolution: evidence for an induced fit model of substrate binding. Biochemistry 2003, 42, 9335-9345.
47. Wester, M. R.; Johnson, E. F.; Marques-Soares, C.; Dansette, P. M.; Mansuy, D.; Stout, C. D. Structure of a substrate complex of mammalian cytochrome P450 2C5 at 2.3 A resolution: evidence for multiple substrate binding modes. Biochemistry 2003, 42, 6370-6379.
48. Poulos, T. L.; Finzel, B. C.; Howard, A. J. High-resolution crystal structure of cytochrome P450cam. J. Mol. Biol. 1987, 195, 687-700.
49. Gerber, N. C.; Sligar, S. G. A role for Asp-251 in cytochronle P-450cam oxygen activation. J. Biol. Chem. 1994, 269, 4260-4266.
50. Yeom, H.; Sligar, S. G.; Li, H.; Poulos, T. L.; Fulco, A. J. The role of Thr268 in oxygen activation of cytochrome P450BM-3. Biochemistry 1995, 34, 14733-14740.
51. Cupp-Vickery, J. R.; Poulos, T. L. Structure of cytochrome P450eryF involved in erythromycin biosynthesis. Nature Struc. Biol. 1995, 2, 144-153.
52. Poulos, T. L.; Finzel, B. C.; Howard, A. J. Crystal structure of substrate-free Pseudomonas putida cytochrome P-450. Biochemistry 1986, 25, 5314-5322.
53. Haines, D. C.; Tomchick, D. R.; Machius, M.; Peterson, J. A. Pivotal role of water in the mechanism of P450BM-3. Biochemistry 2001, 40, 13456-13465.
54. Kraulis, P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 1994, 24, 946-950.
55. Merritt, E. A.; Bacon, D. J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 1997, 277, 505-524.
56. Poulos, T. L. The crystal structure of cytochrome P-450cam. in Cytochrome P-450 Structure, Mechanism and Biochemistry Ortiz de Montellano, P. R., ed Plenum Press: New York and London, 1986; pp. 505-523.
57. Schlichting, I.; Berendzen, J.; Chu, K.; Stock, A. M.; Maves, S. A.; Benson, D. E.; Sweet, R. M.; Ringe, D.; Pestsko, G. A.; Sligar, S. G. The catalytic pathway of cytochrome P450cam at atomic resolution. Science 2000, 287, 1615-1622.
58. Ravichandran, K. G.; Boddupalli, S. S.; Hasermann,. C. A.; Peterson, J. A.; Deisenhofer, J. Crystal structure of hemoprotein domain of P450BM-3, a prototype for microsomal P450's. Sciences 1993, 261, 731-736.
59. Hasemann, C. A.; Ravichandran, K. G.; Peterson, J. A.; Deisenhofer, J. Crystal structure and refinement of cytochrome P450terp at 2.3 A resolution. J. Mol. Biol. 1994, 236, 1169-1185.
60. Park, S.-Y.; Shimizu, H.; Adachi, S.-I.; Shiro, Y.; Lizuka, T.; Nakagawa, A.; Tanaka, I.; Shoun, H.; Hori, H. Crystallization, preliminary diffraction and electron paramagnetic resonance studies of a single crystal of cytochrome P450nor. FEBS Lett. 1997, 412, 346-350.
61. Park, S. Y.; Shimizu, H.; Adachi, S.; Nakagawa, A.; Tanaka, I.; Nakahara, K.; Shoun, H.; Obayashi, E.; Nakamura, H.; Iizuka, T.; Shiro, Y. Crystal structure of nitric oxide reductase from denitrifying fungus Fusarium oxysporum. Nature Struc. Biol. 1997, 4, 827-832.
62. Park, S. Y.; Yamane, K.; Adachi, S.; Shiro, Y.; Weiss, K. E.; Sligar, S. G. Crystallization and preliminary X-ray diffraction analysis of a cytochrome P450 (CYP119) from sulfolobus solfataricus. Acta Cryst. 2000, 56, 1173-1175.
63. Mowat, C. G.; Leys, D.; McLean, K. J.; Rivers, S. L.; Richmond, A.; Munro, A. W.; Ortiz Lombardia, M.; Alzari, P. M.; Reid, G. A.; Chapman, S. K.; Walkinshaw, M. D. Crystallization and preliminary crystallographic analysis of a novel cytochrome P450 from Mycobacterium tuberculosis. Acta Cryst. 2002, D58, 704-705.
64. Lee, D. S.; Yamada, A.; Matsunaga, I.; Ichihara, K.; Adachi, S.; Park, S. Y.; Shiro, Y. Crystallization and preliminary X-ray diffraction analysis of fatty-acid hydroxylase cytochrome P450BSbeta from Bacillus subtilis. Acta Cryst. 2002, D58, 687-689.