Thermodynamics of Ligand Binding to P450 2B4 and P450eryF Studied by Isothermal Titration Calorimetry

REFERENCES

• Aldridge J. E., Gibbons J. A., Flaherty M. M., Kreider M. L., Romano J. A., Levin E. D. Heterogeneity of toxicant response: Sources of human variability. Toxicol. Sci. 2003; 76: 3–20
   PubMed Web of Science ®Google Scholar
• Amulphi C., Jin L., Tricerri M. A., Jonas A. Enthalpy-driven apolipoprotein A-I and lipid bilayer interaction indicating protein penetration upon lipid binding. Biochemistry 2004; 43: 12258–12264
   PubMed Web of Science ®Google Scholar
• Anderson T. G., Tan A., Ganz P., Seelig J. Calorimetric measurement of phospholipid interaction with methyl-beta-cyclodextrin. Biochemistry 2004; 43: 2251–2261
   PubMed Web of Science ®Google Scholar
• Atkins W. M. Implications of the allosteric kinetics of cytochrome P450s. Drug Discovery Today 2004; 9: 478–484
   PubMed Web of Science ®Google Scholar
• Atkins W. M., Wang R. W., Lu A. Y. H. Allosteric behavior in cytochrome p450-dependent in vitro drug-drug interactions: a prospective based on conformational dynamics. Chem. Res. Toxicol. 2000; 14: 338–347
   Web of Science ®Google Scholar
• Baas B. J., Denisov I. G., Sligar S. G. Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch. Biochem. Biophys. 2004; 430: 218–228
   PubMed Web of Science ®Google Scholar
• Bayburt T. H., Leitz A. J., Xie G., Oprian D. D., Sligar S. G. Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J. Biol. Chem. 2007, Mar 29, Epub.
   PubMed Web of Science ®Google Scholar
• Bayburt T. H., Sligar S. G. Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 6725–6730
   PubMed Web of Science ®Google Scholar
• Bridges A., Gruenke L., Chang Y. T., Vakser I. A., Loew G., Waskell L. Identification of the binding site on cytochrome P450 2B4 for cytochrome b5 and cytochrome P450 reductase. J. Biol. Chem. 1998; 273: 17036–17049
   PubMed Web of Science ®Google Scholar
• Campoy A. V., Freire E. ITC in the post-genomic era…? Priceless. Biophy. Chem. 2005; 115: 115–124
   PubMed Web of Science ®Google Scholar
• Campoy A. V., Freire E. Isothermal titration calorimetry to determine association constants for high-affinity ligands. Nature Protocols 2006; 1: 186–191
   PubMed Web of Science ®Google Scholar
• Cupp-Vickery J. R., Garcia C., Hofacre A., McGee-Estrada K. Ketoconazole-induced conformational changes in the active site of cytochrome P450eryF. J. Mol. Biol. 2001; 311: 101–110
   PubMed Web of Science ®Google Scholar
• Cupp-Vickery J., Anderson R., Hatziris Z. Crystal structures of ligand complexes of P450eryF exhibiting homotropic cooperativity. Proc. Natl. Acad. Sci. U.S.A. 2000; 97: 3050–3055
   PubMed Web of Science ®Google Scholar
• Davydov D. R., Botchkareva A. E., Davydova N. E., Halpert J. R. Resolution of two substrate-binding sites in an engineered cytochrome P450eryF bearing a fluorescent probe. Biophys. J. 2005; 89: 418–432
   PubMed Web of Science ®Google Scholar
• Davydov D. R., Botchkareva A. E., Kumar S., He Y. Q., Halpert J. R. An electrostatically driven conformational transition is involved in the mechanisms of substrate binding and cooperativity in cytochrome P450eryF. Biochemistry 2004; 43: 6475–6485
   PubMed Web of Science ®Google Scholar
• Davydov D. R., Fernando H., Baas B. J., Sligar S. G., Halpert J. R. Kinetics of dithionite-dependent reduction of cytochrome P450 3A4: heterogeneity of the enzyme caused by its oligomerization. Biochemistry 2005; 44: 13902–13913
   PubMed Web of Science ®Google Scholar
• Davydov D. R., Fernando H., Halpert J. R. Variable path length and counter-flow continuous variation methods for the study of the formation of high-affinity complexes by absorbance spectroscopy. An application to the studies of substrate binding in cytochrome P450. Biophys. Chem. 2006; 123: 95–101
   PubMed Web of Science ®Google Scholar
• Davydov D. R., Hui Bon Hoa G., Peterson J. A. Dynamics of protein-bound water in the heme domain of P450BM3 studied by high-pressure spectroscopy: comparison with P450cam and P450 2B4. Biochemistry 1999; 38: 751–761
   PubMed Web of Science ®Google Scholar
• Davydov D., Kumar S., Halpert J. R. Allosteric mechanisms in P450eryF probed with 1‐pyrenebutanol, a novel fluorescent substrate. Biochem. Biophys. Res. Commun. 2002; 294: 806–812
   PubMed Web of Science ®Google Scholar
• Denisov I. G., Makris T. M., Sligar S. G., Schlichting I. Structure and chemistry of cytochrome P450. Chem. Rev. 2005; 105: 2253–2277
   PubMed Web of Science ®Google Scholar
• Denisov I. G., Grinkova Y. Y., Lazarides A. A., Sligar S. G. Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J. Am. Chem. Soc. 2004; 126: 1377–1387
   PubMedGoogle Scholar
• Ekroos M., Sjogren T. Structural basis for ligand promiscuity in cytochrome P450 3A4. Proc. Natl. Acad. Sci. U S A 2006; 103: 13682–13687
   PubMed Web of Science ®Google Scholar
• Fernando F., Halpert J. R., Davydov D. R. Resolution of multiple substrate binding sites in cytochrome P450 3A4: the stoichiometry of the enzyme-substrate complexes probed by FRET and Job's titration. Biochemistry 2006; 45: 4199–4209
   PubMed Web of Science ®Google Scholar
• French J. S., Guengerich F. P., Coon M. J. Interactions of cytochrome P-450, NADPH-cytochrome P-450 reductase, phospholipid, and substrate in the reconstituted liver microsomal enzyme system. J. Biol. Chem. 1980; 225: 4112–4119
   Google Scholar
• de Graaf C., Vermeulen N. P., Feenstra K. A. Cytochrome p450 in silico: An integrative modeling approach. J. Med. Chem. 2005; 48: 2725–2755
   PubMed Web of Science ®Google Scholar
• de Groot M. J. Designing better drugs: predicting cytochrome P450 metabolism. Drug. Discov. Today 2006; 11: 601–606
   PubMed Web of Science ®Google Scholar
• Guengerich F. P. Cytochrome P450s and other enzymes in drug metabolism and toxicity. AAPS J 2006; 8: E101–E111
   PubMed Web of Science ®Google Scholar
• Harlow G. R., Halpert J. R. Analysis of human cytochrome P450 3A4 cooperativity: construction and characterization of a site-directed mutant that displays hyperbolic steroid hydroxylation kinetics. Proc. Natl. Acad. Sci. USA. 1998; 95: 6636–6641
   PubMed Web of Science ®Google Scholar
• Hilser V. J., Garcia-Moreno E. B., Oas T. G., Kapp G., Whitten S. T. A statistical thermodynamic model of the protein ensemble. Chem. Rev. 2006; 106: 1545–1558
   PubMed Web of Science ®Google Scholar
• Huang Y. Y., Hara T., Sligar S., Coon M. J., Kimura T. Thermodynamic properties of oxidation-reduction reactions of bacterial, microsomal, and mitochondrial cytochromes P-450: an entropy-enthalpy compensation effect. Biochemistry 1986; 25: 1390–1394
   PubMed Web of Science ®Google Scholar
• Isin E. M., Guengerich F. P. Kinetics and thermodynamics of ligand binding by cytochrome P450 3A4. J. Biol. Chem. 2006; 281: 9127–9136
   PubMed Web of Science ®Google Scholar
• Johnson E. F., Stout C. D. Structural diversity of human xenobiotic-metabolizing cytochrome P450 monooxygenases. Biochem. Biophys. Res. Commun. 2005; 338: 331–336
   PubMed Web of Science ®Google Scholar
• Khan K. K., He Y. A., He Y. Q., Halpert J. R. Site-directed mutagenesis of cytochrome P450eryF: implications for substrate oxidation, cooperativity, and topology of the active site. Chem. Res. Toxicol. 2002; 15: 843–853
   PubMed Web of Science ®Google Scholar
• Khan K. K., Liu H., Halpert J. R. Homotropic versus heterotopic cooperativity of cytochrome P450eryF: a substrate oxidation and spectral titration study. Drug Metab. Dispos. 2003; 31: 356–359
   PubMed Web of Science ®Google Scholar
• Koley A. P., Buters J. T., Robinson R. C., Markowitz A., Friedman F. K. Differential mechanisms of cytochrome P450 inhibition and activation by alpha-naphthoflavone. J. Biol. Chem. 1997; 272: 3149–3159
   PubMed Web of Science ®Google Scholar
• Korzekwa K. R., Krishnamachary N., Shou M., Ogai A., Parise R. A., Rettie A. E., Gonzalez F. J., Tracy T. S. Evaluation of atypical cytochrome P450 kinetics with two-substrate models: evidence that multiple substrates can simultaneously bind to cytochrome P450 active sites. Biochemistry 1998; 37: 4137–4147
   PubMed Web of Science ®Google Scholar
• Lawson R. J., Leys D., Sutcliffe M. J., Kemp C. A., Cheesman M. R., Smith S. J., Clarkson J., Smith W. E., Haq I., Perkins J. B., Munro A. W. Thermodynamic and biophysical characterization of cytochrome P450 BioI from Bacillus subtilis. Biochemistry 2004; 43: 12410–12426
   PubMed Web of Science ®Google Scholar
• Leavitt S., Freire E. Direct measurement of protein binding energetics by isothermal titration calorimetry. Curr. Opin. Struct. Biol. 2001; 11: 560–566
   PubMed Web of Science ®Google Scholar
• Lewis D. F. 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
   PubMed Web of Science ®Google Scholar
• Li H., Poulos T. L. Crystallization of cytochromes P450 and substrate-enzyme interactions. Curr. Top. Med. Chem. 2004; 4: 1789–1802
   PubMed Web of Science ®Google Scholar
• Lokesh G. L., Muralidhara B. K., Negi S. S., Natarajan A. Thermodynamics of phosphopeptide tethering to BRCT: The structural minima for inhibitor design. J. Am. Chem. So. 2007, In Press.
   PubMed Web of Science ®Google Scholar
• Lopez M. M., Makhatadze G. I. Isothermal titration calorimetry. Methods Mol. Biol. 2002; 173: 121–126
   PubMedGoogle Scholar
• Miller G. P., Guengerich F. P. Binding and oxidation of alkyl 4-nitrophenyl ethers by rabbit cytochrome P450 1A2: evidence for two binding sites. Biochemistry 2001; 40: 7262–7272
   PubMed Web of Science ®Google Scholar
• Muralidhara B. K., Chen M., Ma J., Wittung-Stafshede P. Effect of inorganic phosphate on FMN binding and loop flexibility in Desulfovibrio desulfuricans apo-flavodoxin. J. Mol. Biol. 2005; 349: 89–97
   Google Scholar
• Muralidhara B. K., Negi S. S., Halpert J. R. Dissecting the thermodynamics and cooperativity of ligand binding in cytochrome P450eryF. J. Am. Chem. Soc. 2007; 129: 2015–2024
   PubMed Web of Science ®Google Scholar
• Muralidhara B. K., Negi S., Chin C. C., Braun W., Halpert J. R. Conformational flexibility of mammalian cytochrome P450 2B4 in binding imidazole inhibitors with different ring chemistry and side chains. Solution thermodynamics and molecular modeling. J. Biol. Chem. 2006; 281: 8051–8061
   PubMed Web of Science ®Google Scholar
• Muralidhara B. K., Prakash V. Interaction of 3′-O-caffeoyl D-quinic acid with human serum albumin. Int. J Pept. Protein Res. 1995; 41: 1–8
   Google Scholar
• Muralidhara B. K., Wittung-Stafshede P. Can cofactor-binding sites in proteins be flexible? Desulfovibrio desulfuricans flavodoxin binds FMN dimer. Biochemistry 2003; 42: 13074–13080
   PubMed Web of Science ®Google Scholar
• Muralidhara B. K., Wittung-Stafshede P. Thermal unfolding of Apo and Holo Desulfovibrio desulfuricans flavodoxin: cofactor stabilizes folded and intermediate states. Biochemistry 2004; 43: 12855–12864
   PubMed Web of Science ®Google Scholar
• Muralidhara B. K., Wittung-Stafshede P. FMN binding and unfolding of Desulfovibrio desulfuricans flavodoxin: “hidden” intermediates at low denaturant concentrations. Biochem. Biophys. Acta 2005; 1747: 239–250
   PubMed Web of Science ®Google Scholar
• Nagano S., Cupp-Vickery J. R., Poulos T. L. Crystal structures of the ferrous dioxygen complex of wild-type cytochrome P450eryF and its mutants, A245S and A245T: investigation of the proton transfer system in P450eryF. J. Biol. Chem. 2005; 280: 22102–22107
   PubMed Web of Science ®Google Scholar
• Nelson D. R., Koymans L., Kamataki T., Stegeman J. J., Feyereisen R., Waxman D. J., Waterman M. R., Gotoh O., Coon M. J., Estabrook R. W., Gunsalus I. C., Nebert D. W. P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics 1996; 6: 1–42
   PubMedGoogle Scholar
• Ohtaka H., Velazquez-Compoy A., Xie D., Freire E. Overcoming drug resistance in HIV-1 chemotherapy: the binding thermodynamics of Amprenavir and TMC-126 to wild-type and drug-resistant mutants of the HIV-1 protease. Protein Sci. 2002; 11: 1908–1916
   PubMed Web of Science ®Google Scholar
• Peterson J. A., Graham S. E. A close family resemblance: the importance of structure in understanding cytochromes P450. Structure 1998; 6: 1079–1085
   PubMed Web of Science ®Google Scholar
• Poulos T. L., Finzel B. C., Gunsalus I. C., Wagner G. C., Kraut J. The 2.6-A crystal structure of Pseudomonas putida cytochrome P-450. J. Biol. Chem. 1985; 260: 16122–16130
   PubMed Web of Science ®Google Scholar
• Poulos T. L., Johnson E. F. Cytochrome P450: Structure, Mechanism, and Biochemistry 3rd, P. R. Ortiz de Montellano. Kluwer Academic / Plenum Publishers, NY 2005; 87–114
   Google Scholar
• Roberts A. G., Campbell A. P., Atkins W. M. The thermodynamic landscape of testosterone binding to cytochrome P450 3A4: ligand binding and spin state equilibria. Biochemistry 2005; 44: 1353–1366
   PubMed Web of Science ®Google Scholar
• Roberts A. G., Diaz M. D., Lampe J. N., Shireman L. M., Grinstead J. S., Dabrowski M. J., Pearson J. T., Bowman M. K., Atkins W. M., Campbell A. P. NMR studies of ligand binding to P450(eryF) provides insight into the mechanism of cooperativity. Biochemistry 2006; 45: 1673–1684
   PubMed Web of Science ®Google Scholar
• Rowland P., Blaney F. E., Smyth M. G., Jones J. J., Leydon V. R., Oxbrow A. K., Lewis C. J., Tennant M. G., Modi S., Eggleston D. S., Chenery R. J., Bridges A. M. Crystal structure of human cytochrome P450 2D6. J. Biol.Chem. 2006; 281: 7614–7622
   PubMed Web of Science ®Google Scholar
• Sakaguchi M., Omura T. Topology and biogenesis of microsomal cytochrome P450s. Medicinal Implications in Cytochrome P-450 Catalyzed Biotransformations, K. Ruckpaul, H. Rein. Akademie Verlag, Berlin 1993; 59–73
   Google Scholar
• Sansen S., Yano J. K., Reynald R. L., Schoch G. A., Griffin K. J., Stout C. d., Johnson E. F. Adaptations for the oxidation of polycyclic aromatic hydrocarbons exhibited by the structure of human P450 1A2. J. Bio. Chem 2007; 282: 14348–14355
   PubMed Web of Science ®Google Scholar
• Schoch G. A., Yano J. K., Wester M. R., Griffin K. J., Stout C. D., Johnson E. F. Structure of human microsomal cytochrome P450 2C8. Evidence for a peripheral fatty acid binding site. J. Biol. Chem. 2004; 279: 9497–9503
   PubMed Web of Science ®Google Scholar
• Schrag M. L., Wienkers L. C. Topological alteration of the CYP3A4 active site by the divalent cation Mg(2+). Drug Metab. Dispos. 2000; 28: 1198–1201
   PubMed Web of Science ®Google Scholar
• Scott E. E., White M. A., He Y. A., Johnson E. F., Stout D., Halpert J. R. Structure of mammalian cytochrome P450 2B4 complexed with 4-(4-chlorophenyl)imidazole at 1.9-A resolution: insight into the range of P450 conformations and the coordination of redox partner binding. J. Biol. Chem. 2004; 279: 27294–27301
   PubMed Web of Science ®Google Scholar
• Scott E. E., He Y. A., Wester M. R., White M. A., Chin C. C., Halpert J. R., Johnson E. F., Stout D. An open conformation of mammalian cytochrome P450 2B4 at 1.6-A resolution. Proc. Natl. Acad. Sci. U.S.A. 2003; 100: 13196–13201
   PubMed Web of Science ®Google Scholar
• Shou M., Grogan J., Mancewicz J. A., Krausz K. W., Gonzalez F. J., Gelboin H. V., Korzekwa K. R. Activation of CYP3A4: evidence for the simultaneous binding of two substrates in a cytochrome P450 active site. Biochemistry 1994; 33: 6450–6455
   PubMed Web of Science ®Google Scholar
• Sigurskjold B. W. Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem. 2000; 277: 260–266
   PubMed Web of Science ®Google Scholar
• Sikka R., Magauran B., Ulrich A., Shannon M. Bench to bedside: Pharmacogenomics, adverse drug interactions, and the cytochrome P450 system. Acad. Emerg. Med. 2005; 12: 1227–1235
   PubMed Web of Science ®Google Scholar
• Smith B. D., Sanders J. L., Porubsky P. R., Lushington G. H., Stout C. D., Scott E. E. Structure of the human lung cytochrome P450 2A13. J. Biol. Chem. 2007; 282: 17306–17313
   PubMed Web of Science ®Google Scholar
• Turnbull W. B., Daranas A. H. On the value of c: can low affinity systems be studied by isothermal titration calorimetry?. J. Am. Chem. Soc. 2003; 125: 14859–14866
   PubMed Web of Science ®Google Scholar
• Ueng Y. F., Kuwabara T., Chun Y. J., Guengerich F. P. Cooperativity in oxidations catalyzed by cytochrome P450 3A4. Biochemistry 1997; 36: 370–381
   PubMed Web of Science ®Google Scholar
• Vaz A. D. N., Pernecky S. J., Raner G. M., Coon M. J. Peroxo-iron and oxenoid-iron species as alternative oxygenating agents in cytochrome P450-catalyzed reactions: switching by threonine-302 to alanine mutagenesis of cytochrome P450 2B4. Proc. Natl. Acad. Sci. U.S.A. 1996; 93: 4644–4648
   PubMed Web of Science ®Google Scholar
• Weber P. C., Salemme F. R. Applications of calorimetric methods to drug discovery and the study of protein interactions. Curr. Opin. Struct. Biol. 2003; 13: 115–121
   PubMed Web of Science ®Google Scholar
• Wester M. R., Yano J. K., Schoch G. A., Yang C., Griffin K. J., Stout C. D., Johnson E. F. The structure of human cytochrome P450 2C9 complexed with flurbiprofen at 2.0-A resolution. J. Biol. Chem. 2004; 279: 35630–35637
   PubMed Web of Science ®Google Scholar
• Williams P. A., Cosme J., Angove H. C., Vinkovic D. M., Jhoti H. Crystal structure of human cytochrome P450 2C9 with bound warfarin. Nature 2003; 424: 464–468
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Williams P. A., Cosme J., Vinkovic D. M., Ward A., Angove H. C., Day P. J., Vonrhein C., Tickle I. J., Jhoti H. Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science 2004; 305: 683–686
   PubMed Web of Science ®Google Scholar
• Wiseman T., Williston S., Brandts J. F., Lin L.-N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 1989; 179: 131–137
   PubMed Web of Science ®Google Scholar
• Wrighton S. A., Stevens J. C. The human hepatic cytochromes P450 involved in drug metabolism. CRC Crit. Rev. Toxicol. 1992; 22: 1–21
   Google Scholar
• Yano J. K., Hsu M. H., Griffin K. J., Stout C. D., Johnson E. F. Structures of human microsomal cytochrome P450 2A6 complexed with coumarin and methoxsalen. Nat. Struct. Mol. Biol. 2005; 12: 822–823
   PubMed Web of Science ®Google Scholar
• Yano J. K., Wester M. R., Schoch G. A., Griffin K. J., Stout C. D., Johnson E. F. The structure of human microsomal cytochrome P450 3A4 determined by X-ray crystallography to 2.05-A resolution. J. Biol. Chem. 2004; 279: 38091–38094
   PubMed Web of Science ®Google Scholar
• Zhao Y., White M. A., Muralidhara B. K., Sun L., Halpert J. R., Stout C. D. Structure of microsomal cytochrome P450 2B4 complexed with the antifungal drug bifonazole: insight into P450 conformational plasticity and membrane interaction. J. Biol. Chem. 2006; 281: 5973–5981
   PubMed Web of Science ®Google Scholar
• Zhao Y., Sun L., Muralidhara B. K., Kumar S., White M. A., Stout C. D., Halpert J. R. Structural and thermodynamic consequences of 1-(4-cholorophenyl)imidazole binding to cytochrome P450 2B4. Biochemistry 2007, in press.
   Web of Science ®Google Scholar