Erratum: Concurrent cooperativity and substrate inhibition in the epoxidation of carbamazepine by cytochrome p450 3A4 active site mutants inspired by molecular dynamics simulations (Biochemistry (2015) 54:3 (711-721) DOI: 10.1021/bi5011656);Concurrent cooperativity and substrate inhibition in the epoxidation of carbamazepine by cytochrome P450 3A4 active site mutants inspired by molecular dynamics simulations

Biochemistry

Volumn 54, Issue 3, 2015, Pages 711-721

  Müller, Christian S ^a,b   Knehans, Tim ^c   Davydov, Dmitri R ^d,e   Bounds, Patricia L ^b,f   Von Mandach, Ursula ^a   Halpert, James R ^d,g   Caflisch, Amedeo ^c   Koppenol, Willem H ^b  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e INSTITUTE OF BIOMEDICAL CHEMISTRY   (Russian Federation)

^f FOUNDATION FOR RESEARCH ON INFORMATION TECHNOLOGIES IN SOCIETY IT IS   (Switzerland)

^g UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDES; METABOLISM; MOLECULES; PHYSIOLOGY;

BACTERIAL MEMBRANES; BINDING ORIENTATION; CONTROL CONSTRUCTS; CYTOCHROME P450-3A4; HOMOTROPIC COOPERATIVITY; MOLECULAR DYNAMICS SIMULATIONS; MULTIPLE SUBSTRATES; SUBSTRATE INHIBITION;

MOLECULAR DYNAMICS;

CARBAMAZEPINE; CYTOCHROME P450 3A4; HEME IRON PROTEIN; HEMOPROTEIN; METALLOPROTEIN; METYRAPONE; UNCLASSIFIED DRUG; CYTOCHROME P450 3A; EPOXIDE; HEME; MUTANT PROTEIN;

ARTICLE; BACTERIAL MEMBRANE; CONTROLLED STUDY; DISSOCIATION CONSTANT; DRUG METABOLISM; ENZYME PURIFICATION; EPOXIDATION; ESCHERICHIA COLI; HILL EQUATION; HUMAN; HYDROGEN BOND; MATHEMATICAL PARAMETERS; MICHAELIS MENTEN KINETICS; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TURNOVER TIME; WILD TYPE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ISOLATION AND PURIFICATION; METABOLISM; MUTATION;

BACTERIA (MICROORGANISMS);

CARBAMAZEPINE; CATALYTIC DOMAIN; CYTOCHROME P-450 CYP3A; EPOXY COMPOUNDS; HEME; HUMANS; MOLECULAR DYNAMICS SIMULATION; MUTANT PROTEINS; MUTATION; SUBSTRATE SPECIFICITY;

EID: 84922019585     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.6b00904     Document Type: Erratum

References (52)

1. Shimada, T., Yamazaki, H., Mimura, M., Inui, Y., and Guengerich, F. P. (1994) Interindividual variants in human liver cytochrome-P-450 enzymes involved in the oxidation of drugs, carcinogens and toxic chemicals: studies with liver-microsomes of 30 Japanese and 30 Caucasians J. Pharmacol. Exp. Ther. 270, 414-423
2. Guengerich, F. P. (1999) Cytochrome P-450 3A4: Regulation and role in drug metabolism Annu. Rev. Pharmacol. Toxicol. 39, 1-17
3. Pearce, R. E., Vakkalagadda, G. R., and Leeder, J. S. (2002) Pathways of carbamazepine bioactivation in vitro I. Characterization of human cytochromes P450 responsible for the formation of 2- and 3-hydroxylated metabolites Drug Metab. Dispos. 30, 1170-1179
4. Kerr, B. M., Thummel, K. E., Wurden, C. J., Klein, S. M., Kroetz, D. L., Gonzalez, F. J., and Levy, R. (1994) Human liver carbamazepine metabolism: Role of CYP3A4 and CYP2C8 in 10,11-epoxide formation Biochem. Pharmacol. (Amsterdam, Neth.) 47, 1969-1979
5. Nakamura, H., Nakasa, H., Ishii, I., Ariyoshi, N., Igarashi, T., Ohmori, S., and Kitada, M. (2002) Effects of endogenous steroids on CYP3A4-mediated drug metabolism by human liver microsomes Drug Metab. Dispos. 30, 534-540
6. Nakamura, H., Torimoto, N., Ishii, I., Ariyoshi, N., Nakasa, H., Ohmori, S., and Kitada, M. (2003) CYP3A4 and CYP3A7-mediated carbamazepine 10,11-epoxidation are activated by differential endogenous steroids Drug Metab. Dispos. 31, 432-438
7. Egnell, A.-C., Houston, B., and Boyer, S. (2003) In vivo CYP3A4 heteroactivation is a possible mechanism for the drug interaction between felbamate and carbamazepine J. Pharmacol. Exp. Ther. 305, 1251-1262
8. Egnell, A.-C., Houston, J. B., and Boyer, C. S. (2005) Predictive models of CYP3A4 heteroactivation: In vitro-in vivo scaling and pharmacophore modeling J. Pharmacol. Exp. Ther. 312, 926-937
9. Maekawa, K., Yoshimura, T., Saito, Y., Fujimura, Y., Aohara, F., Emoto, C., Iwasaki, K., Hanioka, N., Narimatsu, S., Niwa, T., and Sawada, J. (2009) Functional characterization of CYP3A4.16: Catalytic activities toward midazolam and carbamazepine Xenobiotica 39, 140-147
10. Torimoto, N., Ishii, I., Hata, M., Nakamura, H., Imada, H., Ariyoshi, N., Ohmori, S., Igarashi, T., and Kitada, M. (2003) Direct interaction between substrates and endogenous steroids in the active site may change the activity of cytochrome P450 3A4 Biochemistry 42, 15068-15077
11. Ueng, Y.-F., Kuwabara, T., Chun, Y.-J., and Guengerich, F. P. (1997) Cooperativity in oxidations catalyzed by cytochrome P450 3A4 Biochemistry 36, 370-381
12. Korzekwa, K. R., Krishnamachary, N., Shou, M., Ogai, A., Parise, R. A., Rettie, A. E., Gonzalez, F. J., and Tracy, T. S. (1998) Evaluation of atypical cytochrome P450 kinetics with two-substrate models: Evidence that multiple substrates can simultaneously bind to cytochrome P450 active sites Biochemistry 37, 4137-4147
13. Houston, J. B. and Kenworthy, K. E. (2000) In vitro - in vivo scaling of CYP kinetic data not consistent with the classical Michaelis-Menten model Drug Metab. Dispos. 28, 246-254
14. Yacobi, A., Zlotnick, S., Colaizzi, J. L., Moros, D., Masson, E., Abolfathi, Z., LeBel, M., Mehta, R., Golander, Y., and Levitt, B. (1999) A multiple-dose safety and bioequivalence study of a narrow therapeutic index drug: A case for carbamazepine Clin. Pharmacol. Ther. (N.Y., NY, U.S.) 65, 389-394
15. Bistolas, N., Wollenberger, U., Jung, C., and Scheller, F. W. (2005) Cytochrome p450 biosensors-a review Biosens. Bioelectron. 20, 2408-2423
16. Dodhia, V. R., Sassone, C., Fantuzzi, A., Nardo, G. D., Sadeghi, S. J., and Gilardi, G. (2008) Modulating the coupling efficiency of human cytochrome P450 CYP3A4 at electrode surfaces through protein engineering Electrochem. Commun. 10, 1744-1747
17. Krishnan, S., Wasalathanthri, D., Zhao, L., Schenkman, J. B., and Rusling, J. F. (2011) Efficient bioelectronic actuation of the natural catalytic pathway of human metabolic cytochrome P450s J. Am. Chem. Soc. 133, 1459-1465
18. Williams, P. A., Cosme, J., Vinković, D. M., Ward, A., Angove, H. C., Day, P. J., Vonrhein, C., Tickle, I. J., and Jhoti, H. (2004) Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone Science 305, 683-686
19. Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: The biomolecular simulation program J. Comput. Chem. 30, 1545-1614
20. MacKerell, A. D., Feig, M., and Brooks, C. L. (2003) Improved treatment of the protein backbone in empirical force fields J. Am. Chem. Soc. 126, 698-699
21. Foloppe, N., Sagemark, J., Nordstrand, K., Berndt, K. D., and Nilsson, L. (2001) Structure, dynamics and electrostatics of the active site of glutaredoxin 3 from Escherichia coli: Comparison with functionally related proteins J. Mol. Biol. 310, 449-470
22. Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., and Mackerell, A. D. (2010) CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields J. Comput. Chem. 31, 671-690
23. Vanommeslaeghe, K. and MacKerell, A. D. (2012) Automation of the CHARMM general force field (CGenFF) I: Bond perception and atom typing J. Chem. Inf. Model. 52, 3144-3154
24. Vanommeslaeghe, K., Raman, E. P., and MacKerell, A. D. (2012) Automation of the charmm general force field (CGenFF) II: Assignment of bonded parameters and partial atomic charges J. Chem. Inf. Model. 52, 3155-3168
25. van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. C. (2005) GROMACS: Fast, flexible, and free J. Comput. Chem. 26, 1701-1718
26. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
27. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems J. Chem. Phys. 98, 10089-10092
28. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18, 1463-1472
29. Bussi, G., Donadio, D., and Parrinello, M. (2007) Canonical sampling through velocity rescaling J. Chem. Phys. 126, 14101-14107
30. Parrinello, M. and Rahman, A. (1981) Polymorphic transitions in single crystals: A new molecular dynamics method J. Appl. Phys. 52, 7182-7190
31. Nosé, S. and Klein, M. L. (1983) Constant pressure molecular dynamics for molecular systems Mol. Phys. 50, 1055-1076
32. (2014) The PyMOL Molecular Graphics System, version 1.5.0.4; Schrödinger, LLC: Camberley, U.K. http://www.pymol.org/
33. Seeber, M., Cecchini, M., Rao, F., Settanni, G., and Caflisch, A. (2007) Wordom: A program for efficient analysis of molecular dynamics simulations Bioinformatics 23, 2625-2627
34. Vitalis, A. and Caflisch, A. (2012) Efficient construction of mesostate networks from molecular dynamics trajectories J. Chem. Theory Comput. 8, 1108-1120
35. Vitalis, A. and Pappu, R. V. (2009) Methods for Monte Carlo simulations of biomacromolecules Annu. Rep. Comput. Chem. 5, 49-76
36. Harlow, G. R. and Halpert, J. R. (1997) Alanine-scanning mutagenesis of a putative substrate recognition site in human cytochrome P450 3A4: role of residues 210 and 211 in flavonoid activation and substrate specificity J. Biol. Chem. 272, 5396-5402
37. Omura, T. and Sato, R. (1964) Carbon monoxide-binding pigment of liver microsomes: II. Solubilization, purification, and properties J. Biol. Chem. 239, 2379-&
38. Tsalkova, T. N., Davydova, N. Y., Halpert, J. R., and Davydov, D. R. (2007) Mechanism of interactions of alpha-naphthoflavone with cytochrome P450 3A4 explored with an engineered enzyme bearing a fluorescent probe Biochemistry 46, 106-119
39. Davydov, D. R., Sineva, E. V., Sistla, S., Davydova, N. Y., Frank, D. J., Sligar, S. G., and Halpert, J. R. (2010) Electron transfer in the complex of membrane-bound human cytochrome P450 3A4 with the flavin domain of P450BM-3: The effect of oligomerization of the heme protein and intermittent modulation of the spin equilibrium Biochim. Biophys. Acta, Bioenerg. 1797, 378-390
40. Fernando, H., Davydov, D. R., Chin, C. C., and Halpert, J. R. (2007) Role of subunit interactions in p450 oligomers in the loss of homotropic cooperativity in the cytochrome P450 3A4 mutant L211F/D214E/F304W Arch. Biochem. Biophys. 460, 129-140
41. French, J. S. and Coon, M. J. (1979) Properties of NADPH-cytochrome P-450 reductase purified from rabbit liver microsomes Arch. Biochem. Biophys. 195, 565-577
42. Davydov, D. R., Deprez, E., Hui Bon Hoa, G., Knyushko, T. V., Kuznetsova, G. P., Koen, Y. M., and Archakov, A. I. (1995) High-pressure-induced transitions in microsomal cytochrome P450 2B4 in solution: Evidence for conformational inhomogeneity in the oligomers Arch. Biochem. Biophys. 320, 330-344
43. Khan, K. K., He, Y. Q., Domanski, T. L., and Halpert, J. R. (2002) Midazolam oxidation by cytochrome P450 3A4 and active-site mutants: An evaluation of multiple binding sites and of the metabolic pathway that leads to enzyme inactivation Mol. Pharmacol. 61, 495-506
44. He, Y. A., He, Y. Q., Szklarz, G. D., and Halpert, J. R. (1997) Identification of three key residues in substrate recognition site 5 of human cytochrome P450 3A4 by cassette and site-directed mutagenesis Biochemistry 36, 8831-8839
45. 5 in modulating peroxide-supported CY3A4 activity: Evidence for a conformational transition and cytochrome P450 heterogeneity Drug Metab. Dispos. 33, 1131-1136
46. Sevrioukova, I. F. and Poulos, T. L. (2013) Understanding the mechanism of cytochrome P450 3A4: Recent advances and remaining problems Dalton Trans. 42, 3116-3126
47. Ekroos, M. and Sjögren, T. (2006) Structural basis for ligand promiscuity in cytochrome P450 3A4 Proc. Natl. Acad. Sci. U.S.A. 103, 13682-13687
48. Sevrioukova, I. F. and Poulos, T. L. (2010) Structure and mechanism of the complex between cytochrome P4503A4 and ritonavir Proc. Natl. Acad. Sci. U.S.A. 107, 18422-18427
49. Park, H., Lee, S., and Suh, J. (2005) Structural and dynamical basis of broad substrate specificity, catalytic mechanism, and inhibition of cytochrome P450 3A4 J. Am. Chem. Soc. 127, 13634-13642
50. Sevrioukova, I. F. and Poulos, T. L. (2013) Dissecting cytochrome P450 3A4-ligand interactions using ritonavir analogues Biochemistry 52, 4474-4481
51. Baas, B. J., Denisov, I. G., and Sligar, S. G. (2004) Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment Arch. Biochem. Biophys. 430, 218-228
52. Sineva, E. V., Rumfeldt, J. A. O., Halpert, J. R., and Davydov, D. R. (2013) A large-scale allosteric transition in cytochrome P450 3A4 revealed by luminescence resonance energy transfer (LRET) PLoS One 8, e83898