Biochemical and structural characterization of CYP124: A methyl-branched lipid ω-hydroxylase from Mycobacterium tuberculosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 49, 2009, Pages 20687-20692

  Johnston, Jonathan B ^a   Kells, Petrea M ^a   Podust, Larissa M ^a   Ortiz De Montellano, Paul R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

hydroxylation; Cytochrome P450; Phytanic acid; X ray structure

Indexed keywords

ALKANE 1 MONOOXYGENASE; CYTOCHROME P450; CYTOCHROME P450 124; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME BINDING; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME STRUCTURE; HYDROPHOBICITY; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

ALKANE 1-MONOOXYGENASE; BACTERIAL PROTEINS; BIOCATALYSIS; CATALYTIC DOMAIN; HYDROXYLATION; LIGANDS; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; PHYTANIC ACID; PROTEIN STRUCTURE, SECONDARY; SPECTROPHOTOMETRY, ULTRAVIOLET; SUBSTRATE SPECIFICITY;

MYCOBACTERIUM TUBERCULOSIS;

EID: 73949144656     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0907398106     Document Type: Article

References (60)

1. World Health Organization (2009) World Health Organization Facts Sheets on Tuberculosis.
2. Ouellet H, Johnston JB, Ortiz de Montellano PR, The Mycobacterium tuberculosis cytochrome P450 system. Arch Biochem Biophys, in press.
3. McLean KJ, MunroAW(2008) Structural biology and biochemistry of cytochrome P450 systems in Mycobacterium tuberculosis. Drug Metab Dispos 40:427-446.
4. Aguero F, et al. (2008) Genomic-scale prioritization of drug targets: The TDR Targets database. Nat Rev Drug Discov 7:900-907.
5. McLean KJ, Dunford AJ, Neeli R, Driscoll MD,MunroAW(2007) Structure, function and drug targeting in Mycobacterium tuberculosis cytochrome P450 systems. Arch Biochem Biophys 464:228-240.
6. Ouellet H, Lang J, Couture M, Ortiz de Montellano PR (2009) Reaction of Mycobacterium tuberculosis cytochrome P450 enzymes with nitric oxide. Biochemistry 48:863-872.
7. Ouellet H, Podust LM, Ortiz de Montellano PR (2008) Mycobacterium tuberculosis CYP130. Crystal structure, biophysical characterization, and interactions with antifungal azole drugs. J Biol Chem 283:5069-5080.
8. McLean KJ, et al. (2008) Characterization of active site structure in CYP121. A cytochrome P450 essential for viability of Mycobacterium tuberculosis H37Rv. J Biol Chem 283:33406-33416.
9. Seward HE, Roujeinikova A, McLean KJ, Munro AW, Leys D (2006) Crystal structure of the Mycobacterium tuberculosis P450 CYP121-fluconazole complex reveals new azole drug-P450 binding mode. J Biol Chem 281:39437-39443.
10. McLean KJ, et al. (2006) Biophysical characterization of the sterol demethylase P450 from Mycobacterium tuberculosis, its cognate ferredoxin, and their interactions. Biochemistry 45:8427-8443.
11. 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.
12. McLean KJ, et al. (2002) Expression, purification and spectroscopic characterization of the cytochrome P450 CYP121 from Mycobacterium tuberculosis. J Inorg Biochem 91:527-541.
13. Podust LM, Poulos TL, Waterman MR (2001) Crystal structure of cytochrome P450 14alpha-sterol demethylase (CYP51) from Mycobacterium tuberculosis in complex with azole inhibitors. Proc Natl Acad Sci USA 98:3068-3073.
14. Bellamine A, Mangla AT, Nes WD,Waterman MR (1999) Characterization and catalytic properties of the sterol 14-alpha-demethylase from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 96:8937-8942.
15. Belin P, et al. (2009) Identification and structural basis of the reaction catalyzed by CYP121, an essential cytochrome P450 in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 106:7426-7431.
16. Gondry M, et al. (2009) Cyclodipeptide synthases are a family of tRNA-dependent peptide bond-forming enzymes. Nat Chem Biol 5:414-420.
17. McLean KJ, et al. (2006) The preponderance of P450s in the Mycobacterium tuberculosis genome. Trends Microbiol 14:220-228.
18. Kelly SL, Kelly DE, Jackson CJ, Warrilow AGS, Lamb DC (2005) The diversity and importance of microbial cytochromes P450. Cytochrome P450. Structure, Mechanism, and Biochemistry, ed Ortiz de Montellano PR (Kluwer Academic/Plenum Publishers, New York), pp 585-617.
19. Holsclaw CM, et al. (2008) Structural characterization of a novel sulfated menaquinone produced by Sft3 from Mycobacterium tuberculosis. ACS Chem Biol 3:619-624.
20. Mougous JD, et al. (2006) A sulfated metabolite produced by sft3 negatively regulates the virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103:4258-4263.
21. Balding PR, et al. (2008) How do azoles inhibit cytochrome P450 enzymes? A density functional study. J Phys Chem 112:12911-12918.
22. Jefcoate CR (1978) Measurement of substrate and inhibitor binding to microsomal cytochrome P-450 by optical-difference spectroscopy. Methods Enzymol 52:258-279.
23. Xu F, Ng VY, Kroetz DL, Ortiz de Montellano PR (2006) CYP4 isoform specificity in the omega-hydroxylation of phytanic acid, a potential route to elimination of the causative agent of Refsum's disease. J Pharm Exp Ther 318:835-839.
24. DeBarber AE, Bleyle LA, Roullet J-BO, Koop DR (2004) Omega-hydroxylation of farnesol by mammalian cytochromes P450. Biochim Biophys Acta 1682:18-27.
25. Poulos TL, Johnson EF (2005) Structures of cytochrome P450 enzymes. Cytochrome P450. Structure, Mechanism, and Biochemistry, ed Ortiz de Montellano PR (Kluwer Academic/Plenum Publishers, New York), pp 87-114.
26. Dubnau E, Chan J, Mohan VP, Smith I (2005) Response of Mycobacterium tuberculosis to growth in the mouse lung. Infect Immun 73:3754-3757.
27. Rohdich F, Bacher A, Eisenreich W (2005) Isoprenoid biosynthetic pathways as anti-infective drug targets. Biochem Soc Trans 33:785-791.
28. Dhiman RK, et al. (2009) Menaquinone synthesis is critical for maintaining mycobacterial viability during exponential growth and recovery from non-replicating persistence. Mol Microbiol 72:85-97.
29. Schulbach MC, et al. (2001) Purification, enzymatic characterization, and inhibition of the Z-farnesyl diphosphate synthase from Mycobacterium tuberculosis. J Biol Chem 276:11624-11630.
30. Crick DC, et al. (2000) Polyprenyl phosphate biosynthesis in Mycobacterium tuberculosis and Mycobacterium smegmatis. J Bacteriol 182:5771-5778.
31. Brennan PJ (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83:91-97.
32. Gokhale RS, Saxena P, Chopra T, Mohanty D (2007) Versatile polyketide machinery for the biosynthesis of complex mycobacterial lipids. Nat Prod Rep 24:267-277.
33. Minnikin DE, Kremer L, Dover LG, Besra GS (2002) The methyl-branched fortifications of Mycobacterium tuberculosis. Chem Biol 9:545-553.
34. Kumar P, et al. (2007) PapA1 and PapA2 are acyltransferases essential for the biosynthesis of the Mycobacterium tuberculosis virulence factor Sulfolipid-1. Proc Natl Acad Sci USA 104:11221-11226.
35. Van der Geize R, et al. (2007) A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into survival in macrophages. Proc Natl Acad Sci USA 104:1947-1952.
36. Pandey AK, Sassetti CM (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105:4376-4380.
37. de Visser SP, Kumar D, Cohen S, Shacham R, Shaik S (2004) A predictive pattern of computed barriers for C-H hydroxylation by Compound I of cytochrome P450. J Am Chem Soc 126:8362-8363.
38. Korzekwa KR, Jones JP, Gillette JR (1990) Theoretical studies on cytochrome P-450 mediated hydroxylation: A predictive model for hydrogen atom abstractions. J Am Chem Soc 112:7042-7046.
39. Olsen L, Rydberg P, Rod TH, Ryde U (2006) Prediction of activation energies for hydrogen abstraction by cytochrome P450. J Med Chem 49:6489-6499.
40. Feenstra KA, Starikov EB, Urlacher VB, Commandeur JNM, Vermeulen NPE (2007) Combining substrate dynamics, binding statistics, and energy barriers to rationalize regioselective hydroxylation of octane and lauric acid by CYP102A1 and mutants. Prot Sci 16:420-431.
41. Ortiz de Montellano PR, ed. (2005) Cytochrome P450. Structure, Mechanism, and Biochemistry (Kluwer Academic/Plenum Publishers, New York), 3rd Ed.
42. CaJacob CA, Chan WK, Shephard E, Ortiz de Montellano PR (1988) The catalytic site of rat hepatic lauric acid omega-hydroxylase. Protein versus prosthetic heme alkylation in the omega-hydroxylation of acetylenic fatty acids. J Biol Chem 263:18640-18649.
43. Alterman MA, Hanzlik RP (2002) Hydroxylation of fatty acids by microsomal and reconstituted cytochrome P450 2B1. FEBS Lett 512:319-322.
44. He X, Cryle MJ, De Voss JJ, Ortiz de Montellano PR (2005) Calibration of the channel that determines the omega-hydroxylation regiospecificity of cytochrome P4504A1. J Biol Chem 280:22697-22706.
45. Bambal RB, Hanzlik RP (1996) Active site structure and substrate specificity of cytochrome P450 4A1: Steric control of ligand approach perpendicular to heme plane. Biochem Biophys Res Commun 219:445-449.
46. Fisher MB, Zheng Y-M, Rettie AE (1998) Positional specificity of rabbit CYP4B1 for omega-hydroxylation of short-medium chain fatty acids and hydrocarbons. Biochem Biophys Res Commun 248:352-355.
47. Cook BR, Reinert TJ, Suslick KS (1986) Shape selective alkane hydroxylation by metalloporphyrin. J Am Chem Soc 108:7281-7286.
48. White RE, McCarthy M-B, Egeberg KD, Sligar SG (1984) Regioselectivity in the cytochromes P-450: Control by protein constraints and by chemical reactivities. Arch Biochem Biophys 228:493-502.
49. Bambal RB, Hanzlik RP (1996) Effects of steric bulk and conformational rigidity on fatty acid omega hydroxylation by a cytochrome P450 4A1 fusion protein. Arch Biochem Biophys 334:59-66.
50. Oliver CF, et al. (1997) A single mutation in cytochrome P450 BM3 changes substrate orientation in a catalytic intermediate and the regiospecificity of hydroxylation. Biochemistry 36:1567-1572.
51. Adas F, et al. (1999) Requirement for omega and (omega-1)-hydroxylations of fatty acids by human cytochromes P450 2E1 and 4A11. J Lipid Res 40:1990-1997.
52. Hoch U, Falck JR, Ortiz de Montellano PR (2000) Molecular basis for the omega-regiospecificity of the CYP4A2 and CYP4A3 fatty acid hydroxylases. J Biol Chem 275:26952-26958.
53. Rock DA, Perkins BNS, Wahlstrom J, Jones JP (2003) A method for determining two substrates binding in the same active site of cytochrome P450BM3: An explanation of high energy product formation. Arch Biochem Biophys 416:9-16.
54. Hoch U, Zhang Z, Kroetz DL, Ortiz de Montellano PR (2000) Structural determination of the substrate specificities and regioselectivities of the rat and human fatty acid omega-hydroxylases. Arch Biochem Biophys 373(1):63-71.
55. Coon MJ (2005) Omega oxygenases: nonheme-iron enzymes and P450 cytochromes. Biochem Biophys Res Commun 338:378-385.
56. Omura T, Sata R (1965) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239:2370-2378.
57. Jiang Y, Ortiz de Montellano PR (2009) Cooperative effects on radical recombination in CYP3A4-catalyzed oxidation of the radical clock beta-thujone. ChemBioChem 10:650-653.
58. Leslie AGW (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 ESF-EAMCB Newslett. Protein Crystallogr 26.
59. Otwinowski Z, Minor W (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
60. Holton J, Alber T (2004) Automated protein crystal structure determination using ELVES. Proc Natl Acad Sci USA 101:1537-1542.