An enlarged, adaptable active site in CYP164 family P450 enzymes, the sole P450 in Mycobacterium leprae

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 1, 2012, Pages 391-402

  Agnew, Christopher R J ^a   Warrilow, Andrew G S ^b   Burton, Nicholas M ^a   Lamb, David C ^b   Kelly, Steven L ^b   Brady, R Leo ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLOTRIMAZOLE; CYTOCHROME P450; CYTOCHROME P450 164A1; CYTOCHROME P450 164A2; ECONAZOLE; FLUCONAZOLE; HISTIDINE; IRON; ITRACONAZOLE; KETOCONAZOLE; MICONAZOLE; PORPHYRIN IRON; PYRROLE; UNCLASSIFIED DRUG; VORICONAZOLE;

ARTICLE; BINDING SITE; DRUG PROTEIN BINDING; ENZYME STRUCTURE; LEPROSY; MYCOBACTERIUM LEPRAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANTIFUNGAL AGENTS; BACTERIAL PROTEINS; BINDING SITES; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; CYTOCHROME P-450 ENZYME SYSTEM; ECONAZOLE; HEME; HISTIDINE; HUMANS; IRON; KINETICS; LEPROSY; MODELS, MOLECULAR; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM SMEGMATIS; PORPHYRINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84455161890     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.05227-11     Document Type: Article

References (64)

1. Ahmad Z, Pandey R, Sharma S, Khuller GK. 2008. Novel chemotherapy for tuberculosis: chemotherapeutic potential of econazole- and moxifloxacin-loaded PLG nanoparticles. Int. J. Antimicrob. Agents 31:142-146.
2. Ahmad Z, Sharma S, Khuller GK. 2005. In vitro and ex vivo antimycobacterial potential of azole drugs against Mycobacterium tuberculosis H37Rv. FEMS Microbiol. Lett. 251:19-22. (Pubitemid 41306223)
3. Ahmad Z, Sharma S, Khuller GK. 2006. The potential of azole antifungals against latent/persistent tuberculosis. FEMS Microbiol. Lett. 258:200-203.
4. Ahmad Z, et al. 2006. Antimycobacterial activity of econazole against multidrug-resistant strains of Mycobacterium tuberculosis. Int. J. Antimicrob. Agents 28:543-544. (Pubitemid 44779183)
5. Bellamine A, Mangla AT, Nes WD, Waterman MR. 1999. Characterization and catalytic properties of the sterol 14alpha-demethylase from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 96:8937-8942. (Pubitemid 29374686)
6. Byrne ST, Denkin SM, Gu P, Nuermberger E, Zhang Y. 2007. Activity of ketoconazole against Mycobacterium tuberculosis in vitro and in the mouse model. J. Med. Microbiol. 56:1047-1051. (Pubitemid 47262666)
7. Castagnolo D, et al. 2009. Synthesis and biological evaluation of new enantiomerically pure azole derivatives as inhibitors of Mycobacterium tuberculosis. Bioorg. Med. Chem. Lett. 19:2203-2205.
8. Chen VB, et al. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66:12-21.
9. Cole ST, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544. (Pubitemid 28319235)
10. Cole ST, et al. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007-1011. (Pubitemid 32204045)
11. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
12. Cuppvickery JR, Poulos TL. 1995. Structure of cytochrome P450eryf involved in erythromycin biosynthesis. Nat. Struct. Biol. 2:144-153. (Pubitemid 26040651)
13. Davydov DR, Botchkareva AE, Kumar S, He YQ, Halpert JR. 2004. An electrostatically driven conformational transition is involved in the mechanisms of substrate binding and cooperativity in cytochrome P450eryF. Biochemistry 43:6475-6485. (Pubitemid 38697547)
14. Deprez E, Gill E, Helms V, Wade RC, Hui Bon Hoa G. 2002. Specific and non-specific effects of potassium cations on substrate-protein interactions in cytochromes P450cam and P450lin. J. Inorg. Biochem. 91:597-606.
15. Di Primo C, Deprez E, Sligar SG, Hui Bon Hoa G. 1997. Origin of the photoacoustic signal in cytochrome P-450cam: role of the Arg186-Asp251-Lys178 bifurcated salt bridge. Biochemistry 36:112-118.
16. Driscoll MD, et al. 2010. Structural and biochemical characterization of Mycobacterium tuberculosis CYP142: evidence for multiple cholesterol 27-hydroxylase activities in a human pathogen. J. Biol. Chem. 285:38270-38282.
17. Ekroos M, Sjogren T. 2006. Structural basis for ligand promiscuity in cytochrome P450 3A4. Proc. Natl. Acad. Sci. U. S. A. 103:13682-13687. (Pubitemid 44413967)
18. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501.
19. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62:72-82.
20. Guardiola-Diaz HM, Foster LA, Mushrush D, Vaz AD. 2001. Azole-antifungal binding to a novel cytochrome P450 from Mycobacterium tuberculosis: implications for treatment of tuberculosis. Biochem. Pharmacol. 61:1463-1470. (Pubitemid 32476901)
21. Haines DC, Tomchick DR, Machius M, Peterson JA. 2001. Pivotal role of water in the mechanism of P450BM-3. Biochemistry 40:13456-13465. (Pubitemid 33130773)
22. Huang CY. 1982. Determination of binding stoichiometry by the continuous variation method: the Job plot. Methods Enzymol. 87:509-525.
23. Jackson CJ, Lamb DC, Kelly DE, Kelly SL. 2000. Bactericidal and inhibitory effects of azole antifungal compounds on Mycobacterium smegmatis. FEMS Microbiol. Lett. 192:159-162.
24. Jackson CJ, et al. 2003. Conservation and cloning of CYP51: a sterol 14 alpha-demethylase from Mycobacterium smegmatis. Biochem. Biophys. Res. Commun. 301:558-563. (Pubitemid 36279277)
25. Jefcoate CR. 1978. Measurement of substrate and inhibitor binding to microsomal cytochrome P-450 by optical-difference spectroscopy. Methods Enzymol. 52:258-279.
26. Ji BH, Chauffour A, Andries K, Jarlier V. 2006. Bactericidal activities of R207910 and other newer antimicrobial agents against Mycobacterium leprae in mice. Antimicrob. Agents Chemother. 50:1558-1560.
27. Jones G, Willett P, Glen RC, Leach AR, Taylor R. 1997. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267:727-748. (Pubitemid 27170693)
28. Kelly SL, Lamb DC, Jackson CJ, Warrilow AG, Kelly DE. 2003. The biodiversity of microbial cytochromes P450. Adv. Microb. Physiol. 47:131-186. (Pubitemid 37214150)
29. Lamb DC, Kelly DE, Baldwin BC, Kelly SL. 2000. Differential inhibition of human CYP3A4 and Candida albicans CYP51 with azole antifungal agents. Chem. Biol. Interact. 125:165-175. (Pubitemid 30145626)
30. Lamb DC, et al. 2002. The cytochrome P450 complement (CYPome) of Streptomyces coelicolor A3(2). J. Biol. Chem. 277:24000-24005. (Pubitemid 34951911)
31. Lange R, Bonfils C, Debey P. 1977. The low-spin/high-spin transition equilibrium of camphor-bound cytochrome P-450. Effects of medium and temperature on equilibrium data. Eur. J. Biochem. 79:623-628. (Pubitemid 8198826)
32. Lepesheva GI, Virus C, Waterman MR. 2003. Conservation in the CYP51 family. Role of the B= helix/BC loop and helices F and G in enzymatic function. Biochemistry 42:9091-9101. (Pubitemid 36935417)
33. Leslie AGW, Powell HR. 2007. Processing diffraction data with MOSFLM, p 41-51. In Read RJ, Sussman JL (ed), NATO Science Series II: Mathematics, Physics and Chemistry vol 245. Springer, New York, NY.
34. Leys D, et al. 2003. Atomic structure of Mycobacterium tuberculosis CYP121 to 1.06 A reveals novel features of cytochrome P450. J. Biol. Chem. 278:5141-5147. (Pubitemid 36801025)
35. Lutz JD, et al. 2009. Expression and functional characterization of cytochrome P450 26A1, a retinoic acid hydroxylase. Biochem. Pharmacol. 77:258-268.
36. Manjunatha UH, et al. 2006. Mycobacterium leprae is naturally resistant to PA-824. Antimicrob. Agents Chemother. 50:3350-3354. (Pubitemid 44527509)
37. McCoy AJ, et al. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40:658-674. (Pubitemid 47080256)
38. McGaughey GB, Gagne M, Rappe AK. 1998. Pi-stacking interactions. Alive and well in proteins. J. Biol. Chem. 273:15458-15463. (Pubitemid 28298153)
39. McLean KJ, et al. 2009. The structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection. J. Biol. Chem. 284:35524-35533.
40. McLean KJ, et al. 2002. Azole antifungals are potent inhibitors of cytochrome P450 mono-oxygenases and bacterial growth in mycobacteria and streptomycetes. Microbiology 148:2937-2949. (Pubitemid 35243693)
41. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255. (Pubitemid 27235885)
42. Nelson DR. 2009. The cytochrome p450 homepage. Hum. Genomics 4:59-65.
43. Omura T, Sato R. 1964. The carbon monoxide-binding pigment of liver microsomes. II. Solubilization, purification, and properties. J. Biol. Chem. 239:2379-2385.
44. Omura T, Sato R. 1964. The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J. Biol. Chem. 239:2370-2378.
45. Ortiz de Montellano PR. 2004. Cytochrome P-450: structure, mechanism, and biochemistry, 3rd ed. Kluwer Academics/Plenum, New York, NY.
46. Ouellet H, Johnston JB, Ortiz de Montellano PR. 2010. The Mycobacterium tuberculosis cytochrome P450 system. Arch. Biochem. Biophys. 493:82-95.
47. Ouellet H, Podust LM, de Montellano PR. 2008. Mycobacterium tuberculosis CYP130: crystal structure, biophysical characterization, and interactions with antifungal azole drugs. J. Biol. Chem. 283:5069-5080.
48. Parker JE, et al. 2008. Differential azole antifungal efficacies contrasted using a Saccharomyces cerevisiae strain humanized for sterol 14 alpha-demethylase at the homologous locus. Antimicrob. Agents Chemother. 52:3597-3603.
49. Pearson JT, et al. 2006. Surface plasmon resonance analysis of antifungal azoles binding to CYP3A4 with kinetic resolution of multiple binding orientations. Biochemistry 45:6341-6353. (Pubitemid 43787801)
50. Perrakis A, Harkiolaki M, Wilson KS, Lamzin VS. 2001. ARP/wARP and molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 57:1445-1450. (Pubitemid 36117195)
51. Phillips JC, et al. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802. (Pubitemid 43078511)
52. Pikuleva IA, Mast N, Charvet C, Stout CD. 2010. Structural basis of drug binding to CYP46A1, an enzyme that controls cholesterol turnover in the brain. J. Biol. Chem. 285:31783-31795.
53. Podust LM, Poulos TL, Waterman MR. 2001. Crystal structure of cytochrome P450 14 alpha-sterol demethylase (CYP51) from Mycobacterium tuberculosis in complex with azole inhibitors. Proc. Natl. Acad. Sci. U. S. A. 98:3068-3073. (Pubitemid 32220800)
54. Podust LM, et al. 2004. Estriol bound and ligand-free structures of sterol 14 alpha-demethylase. Structure 12:1937-1945. (Pubitemid 39469391)
55. Poulos TL, Finzel BC, Howard AJ. 1987. High-resolution crystal structure of cytochrome P450cam. J. Mol. Biol. 195:687-700.
56. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815. (Pubitemid 24007801)
57. Savino C, Montemiglio LC, Gianni S, Vallone B. 2010. Azole drugs trap cytochrome P450 EryK in alternative conformational states. Biochemistry 49:9199-9206.
58. Reference deleted.
59. Scollard DM, et al. 2006. The continuing challenges of leprosy. Clin. Microbiol. Rev. 19:338-381.
60. Sheldrick GM. 2010. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66:479-485.
61. Sligar SG. 1976. Coupling of spin, substrate, and redox equilibria in cytochrome P450. Biochemistry 15:5399-5406.
62. Warrilow AG, et al. 2009. Identification, characterization, and azole-binding properties of Mycobacterium smegmatis CYP164A2, a homolog of ML2088, the sole cytochrome P450 gene of Mycobacterium leprae. Antimicrob. Agents Chemother. 53:1157-1164.
63. Yun CH, Ahn T, Guengerich FP. 1998. Conformational change and activation of cytochrome P450 2B1 induced by salt and phospholipid. Arch. Biochem. Biophys. 356:229-238. (Pubitemid 28387727)
64. Yun CH, Song M, Ahn T, Kim H. 1996. Conformational change of cytochrome P450 1A2 induced by sodium chloride. J. Biol. Chem. 271:31312-31316. (Pubitemid 26408580)