Long-range effects of a peripheral mutation on the enzymatic activity of cytochrome P450 1A2

Journal of Chemical Information and Modeling

Volumn 51, Issue 6, 2011, Pages 1336-1346

  Zhang, Tao ^a   Liu, Limin Angela ^b   Lewis, David F V ^c   Wei, Dong Qing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; MOLECULAR DYNAMICS; REACTION KINETICS;

CHANNEL ANALYSIS; ENZYMATIC ACTIVITIES; HUMAN CYTOCHROME; LONG RANGE EFFECTS; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN ENGINEERING; PROTEIN FLEXIBILITY; STRUCTURAL MODELING;

BIOCHEMICAL ENGINEERING;

CYTOCHROME P450 1A2; MUTANT PROTEIN;

ARTICLE; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOVEMENT (PHYSIOLOGY); MUTATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN SECONDARY STRUCTURE;

CATALYTIC DOMAIN; CYTOCHROME P-450 CYP1A2; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOVEMENT; MUTANT PROTEINS; MUTATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN STRUCTURE, SECONDARY;

EID: 79959714612     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci200112b     Document Type: Article

References (73)

1. Nebert, D.; Russell, D. Clinical importance of the cytochromes P450 J.-Lancet. 2002, 360, 1155-1162 (Pubitemid 35246494)
2. Lindberg, R. L. P.; Negishi, M. Alteration of mouse cytochrome P450coh substrate specificity by mutation of a single amino-acid residue Nature 1989, 339, 632-634
3. Guengerich, F. Cytochromes P450, drugs, and diseases Mol. Interventions 2003, 3, 194-204
4. Ortiz de Montellano, P.; Voss, J. Substrate oxidation by cytochrome P450 enzymes. In Cytochrome P450: structure, mechanism, and biochemistry, 3 rd ed.; Ortiz de Montellano, P., Ed.; Kluwer Academic/Plenum Publishers: New York, NY, 2005; pp 183-245.
5. Lamb, D.; Waterman, M.; Kelly, S.; Guengerich, F. Cytochromes P450 and drug discovery Curr. Opin. Biotechnol. 2007, 18, 504-512
6. Brown, C.; Reisfeld, B.; Mayeno, A. Cytochromes P450: a structure-based summary of biotransformations using representative substrates Drug Metab. Rev. 2008, 40, 1-100 (Pubitemid 351220646)
7. Isin, E.; Guengerich, F. Substrate binding to cytochromes P450 Anal. Bioanal. Chem. 2008, 392, 1019-1030
8. Lewis, D. F. V.; Ito, Y. Cytochrome P450 structure and Function: An Evolutionary Perspective In Cytochromes P450: role in the metabolism and toxicity of drugs and other xenobiotics, 1 st ed.; Ioannides, C., Ed.; Royal Society of Chemistry: Cambridge, UK, 2008; pp 4-39.
9. Hlavica, P. Control by substrate of the cytochrome P450-dependent redox machinery: Mechanistic insights Curr. Drug Metab. 2007, 8, 594-611 (Pubitemid 47209097)
10. Davydov, D.; Halpert, J. Allosteric P450 mechanisms: multiple binding sites, multiple conformers or both? Expert Opin. Drug Metab. Toxicol. 2008, 4, 1523-1535
11. Zhou, S.; Liu, J.; Chowbay, B. Polymorphism of human cytochrome P450 enzymes and its clinical impact Drug Metab. Rev. 2009, 41, 89-295
12. Wang, J.; Zhang, C.; Chou, K.; Wei, D. Structure of cytochrome P450s and personalized drug Curr. Med. Chem. 2009, 16, 232-244
13. Hodgson, J. ADMET-turning chemicals into drugs Nat. Biotechnol. 2001, 19, 722-726
14. Lewis, D. F. V. Human cytochromes P450 associated with the phase 1 metabolism of drugs and other xenobiotics: a compilation of substrates and inhibitors of the CYP1, CYP2 and CYP3 families Curr. Med. Chem. 2003, 10, 1955-1972 (Pubitemid 37139057)
15. Ding, X.; Kaminsky, L. Human extrahepatic cytochromes P450: function in xenobiotic metabolism and tissue-selective chemical toxicity in the respiratory and gastrointestinal tracts Annu. Rev. Pharmacol. Toxicol. 2003, 43, 149-173 (Pubitemid 37372638)
16. Wang, B.; Zhou, S. F. Synthetic and natural compounds that interact with human cytochrome P450 1A2 and implications in drug development Curr. Med. Chem. 2009, 16, 4066-4218
17. Sansen, S.; Yano, J.; Reynald, R.; Schoch, G.; Griffin, K.; Stout, C.; Johnson, E. Adaptations for the oxidation of polycyclic aromatic hydrocarbons exhibited by the structure of human P450 1A2 J. Biol. Chem. 2007, 282, 14348-14355 (Pubitemid 47100434)
18. Cojocaru, V.; Winn, P.; Wade, R. The ins and outs of cytochrome P450s Biochim. Biophys. Acta 2007, 1770, 390-401 (Pubitemid 46136742)
19. Yaffe, E.; Fishelovitch, D.; Wolfson, H. J.; Halperin, D.; Nussinov, R. MolAxis: Efficient and accurate identification of channels in macromolecules Proteins: Struct., Funct., Bioinf. 2008, 73, 72-86
20. Li, W.; Liu, H.; Luo, X.; Zhu, W.; Tang, Y.; Halpert, J. R.; Jiang, H. Possible pathway(s) of metyrapone egress from the active site of cytochrome P450 3A4: a molecular dynamics simulation Drug Metab. Dispos. 2007, 35, 689-96 (Pubitemid 46513274)
21. Li, W.; Liu, H.; Scott, E. E.; Grater, F.; Halpert, J. R.; Luo, X.; Shen, J.; Jiang, H. Possible pathway(s) of testosterone egress from the active site of cytochrome P450 2B1: a steered molecular dynamics simulation Drug Metab. Dispos. 2005, 33, 910-9 (Pubitemid 41002771)
22. Behera, R.; Mazumdar, S. Roles of two surface residues near the access channel in the substrate recognition by cytochrome P450cam Biophys. Chem. 2008, 135, 1-6
23. Bechtel, S.; Belkina, N.; Bernhardt, R. The effect of amino-acid substitutions I112P, D147E and K152N in CYP11B2 on the catalytic activities of the enzyme Eur. J. Biochem. 2002, 269, 1118-1127 (Pubitemid 34175370)
24. Scott, E.; He, Y.; Halpert, J. Substrate Routes to the Buried Active Site May Vary among Cytochromes P450: Mutagenesis of the F- G Region in P450 2B1 Chem. Res. Toxicol. 2002, 15, 1407-1413 (Pubitemid 35364902)
25. Fishelovitch, D.; Shaik, S.; Wolfson, H.; Nussinov, R. How Does the Reductase Help To Regulate the Catalytic Cycle of Cytochrome P450 3A4 Using the Conserved Water Channel? J. Phys. Chem. B 2010, 114, 5964-5970
26. Rydberg, P.; Rod, T.; Olsen, L.; Ryde, U. Dynamics of water molecules in the active-site cavity of human cytochromes P450 J. Phys. Chem. B 2007, 111, 5445-5457 (Pubitemid 46854538)
27. Winn, P.; Lüdemann, S.; Gauges, R.; Lounnas, V.; Wade, R. Comparison of the dynamics of substrate access channels in three cytochrome P450s reveals different opening mechanisms and a novel functional role for a buried arginine Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 5361-5366 (Pubitemid 34411553)
28. Fishelovitch, D.; Shaik, S.; Wolfson, H.; Nussinov, R. Theoretical Characterization of Substrate Access/Exit Channels in the Human Cytochrome P450 3A4 Enzyme: Involvement of Phenylalanine Residues in the Gating Mechanism J. Phys. Chem. B 2009, 113, 13018-13025
29. Wen, Z.; Baudry, J.; Berenbaum, M.; Schuler, M. Ile115Leu mutation in the SRS1 region of an insect cytochrome P450 (CYP6B1) compromises substrate turnover via changes in a predicted product release channel Protein Eng., Des. Sel. 2005, 18, 191-199 (Pubitemid 40695124)
30. Yun, C.; Miller, G.; Guengerich, F. Rate-Determining Steps in Phenacetin Oxidations by Human Cytochrome P450 1A2 and Selected Mutants Biochemistry 2000, 39, 11319-11329
31. Hadjokas, N.; Dai, R.; Friedman, F.; Spence, M.; Cusack, B.; Vestal, R.; Ma, Y. Arginine to lysine 108 substitution in recombinant CYP1A2 abolishes methoxyresorufin metabolism in lymphoblastoid cells Br. J. Pharmacol. 2002, 136, 347-352 (Pubitemid 34620514)
32. Zhou, H.; Josephy, P.; Kim, D.; Guengerich, F. Functional characterization of four allelic variants of human cytochrome P450 1A2 Arch. Biochem. Biophys. 2004, 422, 23-30 (Pubitemid 38064307)
33. Saito, Y.; Hanioka, N.; Maekawa, K.; Isobe, T.; Tsuneto, Y.; Nakamura, R.; Soyama, A.; Ozawa, S.; Tanaka-Kagawa, T.; Jinno, H. Functional analysis of three CYP1A2 variants found in a Japanese population Drug Metab. Dispos. 2005, 33, 1905
34. Murayama, N.; Soyama, A.; Saito, Y.; Nakajima, Y.; Komamura, K.; Ueno, K.; Kamakura, S.; Kitakaze, M.; Kimura, H.; Goto, Y. Six novel nonsynonymous CYP1A2 gene polymorphisms: catalytic activities of the naturally occurring variant enzymes J. Pharmacol. Exp. Ther. 2004, 308, 300-306 (Pubitemid 38090731)
35. Laskowski, R.; Gerick, F.; Thornton, J. The structural basis of allosteric regulation in proteins FEBS Lett. 2009, 583, 1692-1698
36. Goodey, N.; Benkovic, S. Allosteric regulation and catalysis emerge via a common route Nat. Chem. Biol. 2008, 4, 474-482 (Pubitemid 352019763)
37. Tsai, C.; del Sol, A.; Nussinov, R. Allostery: absence of a change in shape does not imply that allostery is not at play J. Mol. Biol. 2008, 378, 1-11
38. del Sol, A.; Tsai, C.; Ma, B.; Nussinov, R. The origin of allosteric functional modulation: multiple pre-existing pathways Structure 2009, 17, 1042-1050
39. Cui, Q.; Karplus, M. Allostery and cooperativity revisited Protein Sci. 2008, 17, 1295-1307
40. Gunasekaran, K.; Hagler, A.; Gierasch, L. Sequence and structural analysis of cellular retinoic acid-binding proteins reveals a network of conserved hydrophobic interactions Proteins: Struct., Funct., Bioinf. 2004, 54, 179-194 (Pubitemid 38084059)
41. Kuriyan, J.; Eisenberg, D. The origin of protein interactions and allostery in colocalization Nature 2007, 450, 983-990 (Pubitemid 350273628)
42. Ackers, G.; Smith, F. Effects of site-specific amino acid modification on protein interactions and biological function Annu. Rev. Biochem. 1985, 54, 597-629 (Pubitemid 15073659)
43. Tousignant, A.; Pelletier, J. Protein motions promote catalysis Chem. Biol. 2004, 11, 1037-1042 (Pubitemid 39138755)
44. Pettersen, E.; Goddard, T.; Huang, C.; Couch, G.; Greenblatt, D.; Meng, E.; Ferrin, T. UCSF Chimera-a visualization system for exploratory research and analysis J. Comput. Chem. 2004, 25, 1605-1612
45. Bahar, I.; Chennubhotla, C.; Tobi, D. Intrinsic dynamics of enzymes in the unbound state and relation to allosteric regulation Curr. Opin. Struct. Biol. 2007, 17, 633-640 (Pubitemid 350180409)
46. Case, D.; Darden, T.; Cheatham, III, T.; Simmerling, C.; Wang, J.; Duke, R.; Luo, R.; Merz, K.; Wang, B.; Pearlman, D. AMBER 8; University of California: San Francisco: 2004.
47. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 1983, 22, 2577-2637
48. Hayward, S.; de Groot, B. Normal modes and essential dynamics Methods Mol. Biol. 2008, 443, 89-106
49. Mongan, J. Interactive essential dynamics J. Comput.-Aided Mol. Des. 2004, 18, 433-436 (Pubitemid 40069139)
50. Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics J. Mol. Graphics 1996, 14, 33-38 (Pubitemid 26152973)
51. Ahmad, S.; Gromiha, M.; Fawareh, H.; Sarai, A. ASAView: database and tool for solvent accessibility representation in proteins BMC Bioinf. 2004, 5, 51-55
52. Connolly, M. Solvent-accessible surfaces of proteins and nucleic acids Science 1983, 221, 709-713
53. Hubbard, S.; Thornton, J. NACCESS computer program, Department of Biochemistry and Molecular Biology, University College London: 1993.
54. Liang, J.; Edelsbrunner, H.; Woodward, C. Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design Protein Sci. 1998, 7, 1884-1897 (Pubitemid 28432430)
55. Petrek, M.; Otyepka, M.; Banás, P.; Kosinová, P.; Koca, J.; Damborsky, J. CAVER: a new tool to explore routes from protein clefts, pockets and cavities BMC Bioinf. 2006, 7, 316-324
56. DeLano, W. The case for open-source software in drug discovery Drug Discovery Today 2005, 10, 213-217
57. Morris, G.; Goodsell, D.; Halliday, R.; Huey, R.; Hart, W.; Belew, R.; Olson, A. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 1998, 19, 1639-1662 (Pubitemid 128590223)
58. Totrov, M.; Abagyan, R. Flexible ligand docking to multiple receptor conformations: a practical alternative Curr. Opin. Struct. Biol. 2008, 18, 178-184
59. Lin, J.; Perryman, A.; Schames, J.; McCammon, J. Computational drug design accommodating receptor flexibility: the relaxed complex scheme J. Am. Chem. Soc. 2002, 124, 5632-5633 (Pubitemid 34533490)
60. Achary, M.; Nagarajaram, H. Effects of disease causing mutations on the essential motions in proteins J. Biomol. Struct. Dyn. 2009, 26, 609-624
61. Daily, M.; Gray, J. Local motions in a benchmark of allosteric proteins Proteins: Struct., Funct., Bioinf. 2007, 67, 385-399 (Pubitemid 46449415)
62. Eyal, E.; Yang, L.; Bahar, I. Anisotropic network model: systematic evaluation and a new web interface Bioinformatics 2006, 22, 2619-2627 (Pubitemid 44642600)
63. Lee, Y.; Wilson, R.; Rupniewski, I.; Goodin, D. P450cam Visits an Open Conformation in the Absence of Substrate Biochemistry 2010, 49, 3412-3419
64. Zhou, S.; Yang, L.; Zhou, Z.; Liu, Y.; Chan, E. Insights into the substrate specificity, inhibitors, regulation, and polymorphisms and the clinical impact of human cytochrome P450 1A2 AAPS J. 2009, 11, 481-494
65. Puchkaev, A. V.; Koo, L. S.; Ortiz de Montellano, P. R. Aromatic stacking as a determinant of the thermal stability of CYP119 from Sulfolobus solfataricus Arch. Biochem. Biophys. 2003, 409, 52-58 (Pubitemid 36042901)
66. Headen, T. F.; Howard, C. A.; Skipper, N. T.; Wilkinson, M. A.; Bowron, D. T.; Soper, A. K. Structure of π- π Interactions in Aromatic Liquids J. Am. Chem. Soc. 2010, 132, 5735-5742
67. Sano, E.; Li, W.; Yuki, H.; Liu, X.; Furihata, T.; Kobayashi, K.; Chiba, K.; Neya, S.; Hoshino, T. Mechanism of the decrease in catalytic activity of human cytochrome P450 2C9 polymorphic variants investigated by computational analysis J. Comput. Chem. 2010, 31, 2746-2758
68. Bauer, E.; Guo, Z.; Ueng, Y.; Bell, L.; Zeldin, D.; Guengerich, F. Oxidation of benzo [a] pyrene by recombinant human cytochrome P450 enzymes Chem. Res. Toxicol. 1995, 8, 136-142
69. Süel, G.; Lockless, S.; Wall, M.; Ranganathan, R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins Nat. Struct. Mol. Biol. 2002, 10, 59-69 (Pubitemid 36034178)
70. Daily, M. D.; Upadhyaya, T. J.; Gray, J. J. Contact rearrangements form coupled networks from local motions in allosteric proteins Proteins: Struct., Funct., Bioinf. 2008, 71, 455-466 (Pubitemid 351358624)
71. Konc, J.; Janezic, D. ProBiS algorithm for detection of structurally similar protein binding sites by local structural alignment Bioinformatics 2010, 26, 1160-1168
72. Konc, J.; Janezic, D. ProBiS: a web server for detection of structurally similar protein binding sites Nucleic Acids Res. 2010, 38, W436-W440
73. Bradley, M. J.; Chivers, P. T.; Baker, N. A. Molecular dynamics simulation of the Escherichia coli NikR protein: equilibrium conformational fluctuations reveal interdomain allosteric communication pathways J. Mol. Biol. 2008, 378, 1155-1173