The Mycobacterium tuberculosis cytochromes P450: Physiology, biochemistry & molecular intervention

Future Medicinal Chemistry

Volumn 2, Issue 8, 2010, Pages 1339-1353

  McLean, Kirsty J ^a   Belcher, James ^a   Driscoll, Max D ^a   Fernandez, Christine C ^a   Le Van, Duyet ^a   Bui, Soi ^a   Golovanova, Marina ^a   Munro, Andrew W ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 121; CYTOCHROME P450 124; CYTOCHROME P450 125; CYTOCHROME P450 128; CYTOCHROME P450 130; CYTOCHROME P450 132; CYTOCHROME P450 139; CYTOCHROME P450 141; CYTOCHROME P450 142; CYTOCHROME P450 51B1; PYRROLE DERIVATIVE; STEROL 14ALPHA DEMETHYLASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIAL VIABILITY; BACTERIAL VIRULENCE; CHOLESTEROL METABOLISM; DIMERIZATION; DRUG TARGETING; LIGAND BINDING; MULTIDRUG RESISTANCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW;

ANIMALS; ANTITUBERCULAR AGENTS; AZOLES; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 77956052304     PISSN: 17568919     EISSN: None     Source Type: Journal    
DOI: 10.4155/fmc.10.216     Document Type: Review

References (92)

1. Ormerod LP. Multidrug-resistant tuberculosis (MDR-TB): epidemiology, prevention and treatment. Br. Med. Bull. 14(73-74), 17-24 (2005).
2. Shenoi S, Friedland G. Extensively drug-resistant tuberculosis: a new face to an old pathogen. Annu. Rev. Med. 60, 307-320 (2009).
3. Cole ST, Brosch R, Parkhill J et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685), 537-544 (1998).
4. Zhang L, Kang, S, Keller, TH et al. PA-824 kills nonreplicating Mycobacterium tuberculosis by intracellular NO release. Science 322(5906), 1392-1395 (2008).
5. Diacon AH, Pym A, Grobusch M et al. The diarylquinoline TMC207 for multidrug-resistant tuberculosis. New Engl. J. Med. 360(23), 2397-2405 (2009).
6. Makarov V, Manina G, Mikusova K et al. Benzothiazinones kill Mycobacterium tuberculosis by blocking arabinan synthesis. Science 324(5928), 801-804 (2009).
7. Guerin ME, Kaur D, Somashekar BS et al. New insights into the early steps of phosphatidylinositol mannoside biosynthesis in mycobacteria: PimB́ is an essential enzyme of Mycobacterium smegmatis. J. Biol. Chem. 284(38), 25687-25696 (2009).
8. Wehenkel A, Bellinzono M, Graňa M et al. Mycobacterial Ser/Thr protein kinases and phosphatases: physiological roles and therapeutic potential. Biochim. Biophys. Acta 1784(1), 193-202 (2008).
9. McLean KJ, Scrutton NS, Munro AW. Kinetic, spectroscopic and thermodynamic characterizaton of the Mycobacterium tuberculosis adrenodoxin reductase homolog FprA. Biochem. J. 372(2), 317-327 (2003).
10. McLean KJ, Clift D, Lewis DG et al. The preponderance of P450s in the Mycobacterium tuberculosis genome. Trends Microbiol. 14(5), 220-228 (2006).
11. Perera R, Sono, M, Sigman JR et al. Neutral thiol as a proximal ligand to ferrous heme iron: implications for heme proteins that lose cysteine thiolate ligation on reduction. Proc. Natl Acad. Sci. USA 100(7), 3641-3646 (2003).
12. Munro AW, Girvan HM, McLean KJ. Variations on a (t)heme - novel mechanisms, redox partners and catalytic functions in the cytochrome P450 superfamily. Nat. Prod. Rep. 24(3), 585-609 (2007).
13. Guengerich FP. Cytochrome P450 and chemical toxicology. Chem. Res. Toxicol. 21(1), 70-83 (2008).
14. Omura T. Mitochondrial P450s. Chem. Biol. Interact. 163(1-2), 86-93 (2006).
15. McLean KJ, Sabri M, Marshall KR et al. Biodiversity of cytochrome P450 redox systems. Biochem. Soc. Trans. 33(4), 796-801 (2005).
16. McLean KJ, Munro AW. Structural biology and biochemistry of cytochrome P450 systems in Mycobacterium tuberculosis. Drug Metab. Rev. 40(3), 427-446 (2008).
17. McLean KJ, Munro AW, Girvan HM Cytochrome P450/redox partner fusion enzymes: biotechnological and toxicological prospects. Expert Opin. Drug Metab. Toxicol. 3(6), 847-863 (2007).
18. Poulos TL. The past and present of P450cam structural biology. Biochem. Biophys. Res. Commun. 312(1), 35-39 (2003).
19. Cupp-Vickery JR, Poulos TL. Structure of cytochrome P450eryF: substrate, inhibitors, and model compounds bound in the active site. Steroids 62(1), 112-116 (1997).
20. Ogura H, Nishida CR, Hoch UR et al. EpoK, a cytochrome P450 involved in biosynthesis of the anticancer agents epothilones A and B. Substrate-mediated rescue of a P450 enzyme. Biochemistry 43(46), 14712-14721 (2004).
21. Holsclaw CM, Sogi KM, Gilmore SA et al. Structural characterization of a novel sulfated menaquinone produced by stf3 from Mycobacterium tuberculosis. ACS Chem. Biol. 3(10), 619-624 (2008).
22. Nelson DR. Cytochrome P450 and the individuality of species. Arch. Biochem. Biophys. 369(1), 1-10 (1999).
23. Recchi C, Sclavu B, Rauzier J et al. Mycobacterium tuberculosis Rv1395 is a class III regulator of the AraC family involved in cytochrome P450 regulation. J. Biol. Chem. 278(36), 33763-33773 (2003).
24. Akins RA. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43(4), 285-318 (2005).
25. Sable CA, Strohmaier KM, Chodakewitz JA. Advances in antifungal therapy. Annu. Rev. Med. 59, 361-379 (2008).
26. Bellamine A, Mangla AT, Nes WD et al. Characterization and catalytic properties of the sterol 14 a-demethylase from Mycobacterium tuberculosis, Proc. Natl Acad. Sci. USA 96(16), 8937-8942 (1999).
27. Podust LM, Poulos TL, Waterman MR. Crystal structure of cytochrome P450 14a-demethylase (CYP51) from Mycobacterium tuberculosis in complex with azole inhibitors, Proc. Natl Acad. Sci. USA 98(6), 3068-3073 (2001).
28. Aoyama Y, Horiuchi T, Gotoh O et al. CYP51-like gene of Mycobacterium tuberculosis actually encodes a P450 similar to eukaryotic CYP51. J. Biochem. 124(4), 694-696 (1998).
29. McLean KJ, Warman AJ, Seward HE et al. Biophysical characterization of the sterol demethylase from Mycobacterium tuberculosis, its cognate ferredoxin, and their interactions. Biochemistry 45(27), 8427-8443 (2006).
30. Sassetti CM, Boyd DH, Rubin EJ. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48(1), 77-84 (2003).
31. Sassetti CM, Rubin EJ. Genetic requirements for mycobacterial survival during infection. Proc. Natl Acad. Sci. USA 100(22), 12989-12994 (2003).
32. Podust LM, von Kries JP, Eddine AN. Small-molecule scaffolds for CYP51 inhibitors identified by high-throughput screening and defined by x-ray crystallography. Antimicrob. Agents Chemother. 51(11), 3915-3923 (2007).
33. Chen CK, Doyle PS, Yermalitskaya LV et al. Trypanosoma cruzi CYP51 inhibitor derived from a Mycobacterium tuberculosis screen hit. PLoS Negl. Trop. Dis. 3(2), e372 (2009).
34. McLean KJ, Lafite P, Levy C et al. The structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection. J. Biol. Chem. 284(51), 35524-35533 (2009).
35. Capyk JK, Kalscheuer R, Stewart GR et al. Mycobacterial cytochrome P450 CYP125 catalyzes the terminal hydroxylation of C27 steroids. J. Biol. Chem. 284(51), 35534-35542 (2009).
36. Van der Geize R, Yam K, Heuser T et al. A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc. Natl Acad. Sci. USA 104(6), 1947-1952 (2007).
37. Kendall SL, Rison SC, Movahedzadeh F et al. What do microarrays really tell us about M. tuberculosis. Trends Microbiol. 12(12), 537-544 (2004).
38. Pandey AK, Sassetti CM. Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl Acad. Sci. USA 105(11), 4376-4380 (2008).
39. Deniz O, Gumus S, Yaman H et al. Serum total cholesterol, HDL-C and LDL-C concentrations significantly correlate with the radiological extent of disease and the degree of smear positivity in patients with pulmonary tuberculosis. Clin. Biochem. 40(3-4), 162-166 (2007).
40. Garton NJ, Waddell SJ, Sherratt AL et al. Cytological and transcript analyses reval fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med. 5(4), e75 (2008).
41. Kaul D, Anand PK, Verma I. Cholesterol sensor initiates M. tuberculosis entry into human macrophage. Mol. Cell. Biochem. 258(1-2), 219-222 (2004).
42. Peyron P, Vaubourgeix J, Poquet Y et al. Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog. 4(11), e1000204 (2008).
43. Tauchi-Sato K, Ozeki S, Houjou T et al. The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J. Biol. Chem. 277(46), 44507-44512 (2002).
44. Gatfield J, Pieters J. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288(5741), 1647-1650 (2000).
45. Yam KC, D'Angelo I, Kalscheuer R et al. Studies of a ring-cleaving dioxygenase illuminate the role of cholesterol metabolism in the pathogenesis of Mycobacterium tuberculosis. PLoS Pathog. 5(3), e1000344 (2009).
46. Nesbitt NM, Yang X, Fontán P et al. A thiolase of Mycobacterium tuberculosis is required for virulence and production of androstenedione and androstadienedione from cholesterol. Infect. Immun. 78(1), 275-282 (2010).
47. Kaul D Coronin. 1A epigenomics govern mycobacterial persistence in tuberculosis. FEMS Microbiol. Lett. 278(1), 10-14 (2007).
48. Yang X, Nesbitt NM, Dubnau E et al. Cholesterol metabolism increases the metabolic pool of propionate in Mycobacterium tuberculosis Biochemistry 48(18), 3819-3821 (2009).
49. Reed MB, Domenech P, Manca C et al. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431(7004), 84-87 (2004).
50. Astarie-Dequeker C, Le Guyader K, Malaga W et al. Phthiocerol dimycoserates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog. 5(2), e1000289 (2009).
51. Joshi SM, Pandey AK, Capite N et al. Characterization of mycobacterial virulence genes through genetic interaction mapping. Proc. Natl Acad. Sci. USA 103(31), 11760-11765 (2006).
52. Mohn WW, van der Geize R, Stewart GR et al. The actinobacterial mce4 locus encodes a steroid transporter. J. Biol. Chem. 283(51), 35368-35374 (2008).
53. Lack NA, Yam KC, Lowe ED et al. Characterization of a carbon-carbon hydrolase from Mycobacterium tuberculosis involved in cholesterol metabolism. J. Biol. Chem. 285(1), 434-443 (2010).
54. Hu Y, van der Geize R, Besra GS et al. 3-ketosteroid 9a-hydroxylase is an essential factor in the pathogenesis of Mycobacterium tuberculosis. Mol. Microbiol. 75(1), 107-121 (2010).
55. Chang JC, Harik NS, Liao RP et al. Identification of mycobacterial genes that alter growth and pathology in macrophages and in mice. J. Infect. Dis. 196(5), 788-795 (2007).
56. Chang JC, Miner MD, Pandey AK et al. Igr genes and Mycobacterium tuberculosis cholesterol metabolism. J. Bacteriol. 191(16), 5232-5239 (2009).
57. Schnappinger D, Ehrt S, Voskuil MI et al. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198(5), 693-704 (2003).
58. Wolf AJ, Linas B, Trevejo-Nuňez GJ et al. Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J. Immunol. 179(4), 2509-2519 (2007).
59. Tailleux L, Waddell SJ, Pelizzola M et al. Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS One 3(1), e1403 (2008).
60. Karakousis PC, Yoshimatsu T, Lamichhane G et al. Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J. Exp. Med. 200(5), 647-657 (2004).
61. Betts JC, Lukey PT, Robb LC et al. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43(3), 717-731 (2002).
62. Beste DC, Laing E, Bonde B et al. Transcriptomic analysis identifies growth rate modulation as a component of the adaptation of mycobacteria to survival inside the macrophage. J. Bacteriol. 189(11), 3969-3976 (2007).
63. Rostoniec KZ, Wilbrink MH, Capyk JK et al. Cytochrome P450 125 (CYP125) catalyzes C26-hydroxylation to initiate sterol side-chain degradation in Rhodococcus jostii RHA1. Mol. Microbiol. 74(5), 1031-1043 (2009).
64. Molina-Torres CA, Castro-Garza J, Ocampo-Cadiani J et al. Effect of serial subculturing on the genetic composition and cytotoxic activity of Mycobacterium tuberculosis. J. Med. Microbiol. 59(4), 384-391 (2010).
65. Domenech P, Reed MB. Rapid and spontaneous loss of phthiocerol dimycoserate (PDIM) from Mycobacterium tuberculosis grown in vitro: implications for virulence studies. Microbiology 155(11), 3532-3543 (2009).
66. McLean KJ, Cheesman MR, Rivers SL et al. Expression, purification and spectroscopic characterization of the cytochrome P450 CYP121 from Mycobacterium tuberculosis. J. Inorg. Biochem. 91(4), 527-541 (2002).
67. Denisov IG, Makris TM, Sligar SG et al. Structure and chemistry of cytochrome P450. Chem. Rev. 105(6), 2253-2277 (2005).
68. Gondry M, Sauguet L, Belin P et al. Cyclodipeptide synthases are a family of tRNA-dependent peptide bond-forming enzymes. Nat. Chem. Biol. 5(6), 414-420 (2009).
69. Belin P, Le Du MH, Fielding A et al. Identification and structural basis of the reaction catalyzed by CYP121, an essential cytochrome P450 in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 106(18), 7426-7431 (2009).
70. McLean KJ, Carroll P, Lewis DG et al. Characterization of active site structure in CYP121. A cytochrome P450 essential for viability of Mycobacterium tuberculosis H37Rv. J. Biol. Chem. 283(48), 33406-33416 (2008).
71. Lamichhane G, Zignol M, Blades NJ et al. A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 100(12), 7213-7218 (2003).
72. Tsolaki AG, Hirsh AE, DeRiemer K et al. Functional and evolutionary genetics of Mycobacterium tuberculosis: insights from genomic deletions in 100 strains. Proc. Natl Acad. Sci. USA 101(14), 4865-4870 (2004).
73. Gao Q, Kripke KE, Saldanha AJ et al. Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 151(1), 5-14 (2005).
74. Seward HE, Roujeinikova A, McLean KJ et al. Crystal structure of the Mycobacterium tuberculosis P450 CYP121-fluconazole complex reveals new azole drug-P450 binding mode. J. Biol. Chem. 281(51), 39437-39443 (2006).
75. Ouellet H, Podust LM, Ortiz de Montellano PR. Mycobacterium tuberculosis CYP130: crystal structure, biophysical characterization, and interactions with antifungal azole drugs. J. Biol. Chem. 283(8), 5069-5080 (2008).
76. Podust LM, Ouellet H, von Kries JP et al. Interaction of Mycobacterium tuberculosis CYP130 with heterocyclic arylamines. J. Biol. Chem. 284(37), 25211-25219 (2009).
77. Kim D, Guengerich FP. Cytochrome P450 activation of arylamines and heterocyclic amines. Annu. Rev. Pharmacol. Toxicol. 45, 27-49 (2005).
78. Johnston JB, Kells PM, Podust LM et al. Biochemical and structural characterization of CYP124: a methyl-branched lipid omega-hydroxylase from Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 106(49), 20687-20692 (2009).
79. Check E. After decades of drought, new drug possibilities flood TB pipeline. Nat. Med. 13(3), 266 (2007).
80. Guy ES, Mallampalli A. Managing TB in the 21st century: existing and novel drug therapies. Ther. Adv. Resp. Dis. 2(6), 401-408 (2008).
81. McLean KJ, Marshall KR, Richmond A et al. Azole antifungals are potent inhibitors of cytochrome P450 mono-oxygenases and bacterial growth in mycobacteria and streptomycetes. Microbiology 148(10), 2937-2949 (2002).
82. Ahmad Z, Sharma S, Khuller GK. The potential of azole antifungals against latent/persistent tuberculosis. FEMS Microbiol. Lett. 258(2), 200-203 (2006).
83. Ahmad Z, Sharma S, Khuller GK et al. Antimycobacterial activity of econazole against multidrug-resistant strains of Mycobacterium tuberculosis. Int. J. Antimicrob. Agents 28(6), 543-544 (2006).
84. Ahmad Z, Sharma S, Khuller GK. Azole antifungals as novel chemotherapeutic agents against murine tuberculosis. FEMS Microbiol. Lett. 261(2), 181-186 (2006).
85. Ahmad Z, Sharma S, Khuller GK. In vitro and ex vivo antimycobacterial potential of azole drugs against Mycobacterium tuberculosis H37Rv. FEMS Microbiol. Lett. 251(1), 19-22 (2005).
86. Castagnolo D, Radi M, Dessì F et al. Synthesis and biological evaluation of new enantiomerically pure azole derivatives as inhibitors of Mycobacterium tuberculosis. Bioorg. Med. Chem. Lett. 19(8), 2203-2204 (2009).
87. Pandey J, Tiwari VK, Verma SS et al. Synthesis and anti-tubercular screening of imidazole derivatives. Eur. J. Med. Chem. 44(8), 3350-3355 (2009).
88. Milano A, Pasca M, Provvedi R et al. Azole resistance in Mycobacterium tuberculosis is mediated by the MmpS5-MmpL5 efflux system. Tuberculosis 89(1), 84-90 (2009).
89. Girmenia C. New generation azole antifungals in clinical investigation. Exp. Opin. Investig. Drugs 18(9), 1279-1295 (2009).
90. Sacchettini JC, Rubin EJ, Freundlich JS. Drugs versus bugs: in pursuit of the persistent predator Mycobacterium tuberculosis. Nat. Rev. Microbiol. 6(1), 41-52 (2008).
91. Leys D, Mowat CG, McLean KJ et al. Atomic structure of Mycobacterium tuberculosis CYP121 to 1.06 Å reveals novel features of cytochrome P450. J. Biol. Chem. 278(7), 5141-5147 (2003).
92. Podust LM, Yermalitskaya LV, Lepesheva GI et al. Estriol bound and ligand-free structures of sterol 14a-demethylase. Structure 12(11), 1937-1945 (2004).