Cholesterol catabolism as a therapeutic target in Mycobacterium tuberculosis

Trends in Microbiology

Volumn 19, Issue 11, 2011, Pages 530-539

  Ouellet, Hugues ^a   Johnston, Jonathan B ^a   Montellano, Paul R Ortiz de ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLOTRIMAZOLE; CYTOCHROME P450; CYTOCHROME P450 51B1; ECONAZOLE; FINASTERIDE; KETOCONAZOLE; MICONAZOLE; STEROL 14ALPHA DEMETHYLASE; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CATABOLISM; CATALYSIS; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; DRUG STRUCTURE; DRUG TARGETING; HUMAN; LIPID DEGRADATION; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATION; PERSISTENT INFECTION; PHAGOCYTOSIS; PRIORITY JOURNAL; REGULON; REVIEW; STEROL METABOLISM; TUBERCULOSIS;

ANIMALS; ANTICHOLESTEREMIC AGENTS; BIOSYNTHETIC PATHWAYS; CHOLESTEROL; HOST-PATHOGEN INTERACTIONS; HUMANS; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS;

EID: 80755138435     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2011.07.009     Document Type: Review

References (72)

1. Cole S.T., et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393:537-544.
2. Lamb D.C., et al. Lanosterol biosynthesis in the prokaryote Methylococcus capsulatus: insight into the evolution of sterol biosynthesis. Mol. Biol. Evol. 2007, 24:1714-1721.
3. Pearson A., et al. Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:15352-15357.
4. Bellamine A., et al. Characterization and catalytic properties of the sterol 14alpha-demethylase from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:8937-8942.
5. Lamb D.C., et al. Sterol 14alpha-demethylase activity in Streptomyces coelicolor A3(2) is associated with an unusual member of the CYP51 gene family. Biochem. J. 2002, 364:555-562.
6. Clark-Curtiss J.E., Haydel S.E. Molecular genetics of Mycobacterium tuberculosis pathogenesis. Annu. Rev. Microbiol. 2003, 57:517-549.
7. Koul A., et al. Interplay between mycobacteria and host signalling pathways. Nat. Rev. Microbiol. 2004, 2:189-202.
8. Kim M.J., et al. Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol. Med. 2010, 2:258-274.
9. Schafer G., et al. The role of scavenger receptor B1 in infection with Mycobacterium tuberculosis in a murine model. PLoS ONE 2009, 4:e8448.
10. Martens G.W., et al. Hypercholesterolemia impairs immunity to tuberculosis. Infect. Immun. 2008, 76:3464-3472.
11. Gatfield J., Pieters J. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 2000, 288:1647-1650.
12. Peyron P., et al. Nonopsonic phagocytosis of Mycobacterium kansasii by human neutrophils depends on cholesterol and is mediated by CR3 associated with glycosylphosphatidylinositol-anchored proteins. J. Immunol. 2000, 165:5186-5191.
13. Munoz S., et al. Mycobacterium tuberculosis entry into mast cells through cholesterol-rich membrane microdomains. Scand. J. Immunol. 2009, 70:256-263.
14. Nguyen L., Pieters J. The Trojan horse: survival tactics of pathogenic mycobacteria in macrophages. Trends Cell Biol. 2005, 15:269-276.
15. Savvi S., et al. Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids. J. Bacteriol. 2008, 190:3886-3895.
16. Munoz-Elias E.J., McKinney J.D. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 2005, 11:638-644.
17. Bloch H., Segal W. Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J. Bacteriol. 1956, 72:132-141.
18. Pandey A.K., Sassetti C.M. Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:4376-4380.
19. Van der Geize R., et al. A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1947-1952.
20. Mohn W.W., et al. The actinobacterial mce4 locus encodes a steroid transporter. J. Biol. Chem. 2008, 283:35368-35374.
21. Av-Gay Y., Sobouti R. Cholesterol is accumulated by mycobacteria but its degradation is limited to non-pathogenic fast-growing mycobacteria. Can. J. Microbiol. 2000, 46:826-831.
22. Yang X., et al. Cholesterol metabolism increases the metabolic pool of propionate in Mycobacterium tuberculosis. Biochemistry 2009, 48:3819-3821.
23. Ouellet H., et al. Mycobacterium tuberculosis CYP125A1, a steroid C27 monooxygenase that detoxifies intracellularly generated cholest-4-en-3-one. Mol. Microbiol. 2010, 77:730-742.
24. Chang J.C., et al. Identification of mycobacterial genes that alter growth and pathology in macrophages and in mice. J. Infect. Dis. 2007, 196:788-795.
25. Chang J.C., et al. igr genes and Mycobacterium tuberculosis cholesterol metabolism. J. Bacteriol. 2009, 191:5232-5239.
26. Kendall S.L., et al. A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis. Mol. Microbiol. 2007, 65:684-699.
27. Nesbitt N.M., et al. A thiolase of Mycobacterium tuberculosis is required for virulence and production of androstenedione and androstadienedione from cholesterol. Infect. Immun. 2010, 78:275-282.
28. Kendall S.L., et al. Cholesterol utilization in mycobacteria is controlled by two TetR-type transcriptional regulators: kstR and kstR2. Microbiology 2010, 156:1362-1371.
29. Schnappinger D., et al. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 2003, 198:693-704.
30. Sassetti C.M., Rubin E.J. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:12989-12994.
31. Rengarajan J., et al. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8327-8332.
32. Rosloniec K.Z., et al. Cytochrome P450 125 (CYP125) catalyses C26-hydroxylation to initiate sterol side-chain degradation in Rhodococcus jostii RHA1. Mol. Microbiol. 2009, 74:1031-1043.
33. Wilbrink M.H., et al. FadD19 of Rhodococcus rhodochrous DSM43269, a steroid-coenzyme A ligase essential for degradation of C-24 branched sterol side chains. Appl. Environ. Microbiol. 2011, 77:4455-4464.
34. Yang X., et al. Rv1106c from Mycobacterium tuberculosis is a 3beta-hydroxysteroid dehydrogenase. Biochemistry 2007, 46:9058-9067.
35. Brzostek A., et al. Cholesterol oxidase is required for virulence of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 2007, 275:106-112.
36. Yang X., et al. Cholesterol is not an essential source of nutrition for Mycobacterium tuberculosis during infection. J. Bacteriol. 2011, 193:1473-1476.
37. Tabas I., et al. Acyl coenzyme A:cholesterol acyl transferase in macrophages utilizes a cellular pool of cholesterol oxidase-accessible cholesterol as substrate. J. Biol. Chem. 1988, 263:1266-1272.
38. Uhia I., et al. Initial step in the catabolism of cholesterol by Mycobacterium smegmatis mc(2)155. Environ. Microbiol. 2011, 4:943-959.
39. Itagaki E., et al. Spectral properties of 3-ketosteroid-delta 1-dehydrogenase from Nocardia corallina. Biochim. Biophys. Acta 1990, 1040:281-286.
40. Itagaki E., et al. Purification and characterization of 3-ketosteroid-delta 1-dehydrogenase from Nocardia corallina. Biochim. Biophys. Acta 1990, 1038:60-67.
41. Knol J., et al. 3-Keto-5alpha-steroid Delta(1)-dehydrogenase from Rhodococcus erythropolis SQ1 and its orthologue in Mycobacterium tuberculosis H37Rv are highly specific enzymes that function in cholesterol catabolism. Biochem. J. 2008, 410:339-346.
42. Brzostek A., et al. Mycobacterium tuberculosis is able to accumulate and utilize cholesterol. J. Bacteriol. 2009, 191:6584-6591.
43. van der Geize R., et al. Molecular and functional characterization of the kstD2 gene of Rhodococcus erythropolis SQ1 encoding a second 3-ketosteroid Delta(1)-dehydrogenase isoenzyme. Microbiology 2002, 148:3285-3292.
44. van der Geize R., et al. Unmarked gene deletion mutagenesis of kstD, encoding 3-ketosteroid Delta1-dehydrogenase, in Rhodococcus erythropolis SQ1 using sacB as counter-selectable marker. FEMS Microbiol. Lett. 2001, 205:197-202.
45. Capyk J.K., et al. Characterization of 3-ketosteroid 9-alpha-hydroxylase, a Rieske oxygenase in the cholesterol degradation pathway of Mycobacterium tuberculosis. J. Biol. Chem. 2009, 284:9937-9946.
46. Hu Y., et al. 3-Ketosteroid 9alpha-hydroxylase is an essential factor in the pathogenesis of Mycobacterium tuberculosis. Mol. Microbiol. 2010, 75:107-121.
47. van der Geize R., et al. Characterization of a second Rhodococcus erythropolis SQ1 3-ketosteroid 9alpha-hydroxylase activity comprising a terminal oxygenase homologue, KshA2, active with oxygenase-reductase component KshB. Appl. Environ. Microbiol. 2008, 74:7197-7203.
48. Andor A., et al. Generation of useful insertionally blocked sterol degradation pathway mutants of fast-growing mycobacteria and cloning, characterization, and expression of the terminal oxygenase of the 3-ketosteroid 9alpha-hydroxylase in Mycobacterium smegmatis mc(2)155. Appl. Environ. Microbiol. 2006, 72:6554-6559.
49. Dresen C., et al. A flavin-dependent monooxygenase from Mycobacterium tuberculosis involved in cholesterol catabolism. J. Biol. Chem. 2010, 285:22264-22275.
50. Lack N., et al. Structure of HsaD, a steroid-degrading hydrolase, from Mycobacterium tuberculosis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2008, 64:2-7.
51. Lack N.A., et al. Characterization of a carbon-carbon hydrolase from Mycobacterium tuberculosis involved in cholesterol metabolism. J. Biol. Chem. 2010, 285:434-443.
52. Kunau W.H., et al. Beta-oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog. Lipid Res. 1995, 34:267-342.
53. Johnston J.B., et al. Structural control of cytochrome P450-catalyzed omega-hydroxylation. Arch. Biochem. Biophys. 2011, 507:86-94.
54. Johnston J.B., et al. Functional redundancy of steroid C26-monooxygenase activity in Mycobacterium tuberculosis revealed by biochemical and genetic analyses. J. Biol. Chem. 2010, 285:36352-36360.
55. McLean K.J., et al. The structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection. J. Biol. Chem. 2009, 284:35524-35533.
56. Capyk J.K., et al. Mycobacterial cytochrome p450 125 (cyp125) catalyzes the terminal hydroxylation of c27 steroids. J. Biol. Chem. 2009, 284:35534-35542.
57. Yam K.C., et al. Studies of a ring-cleaving dioxygenase illuminate the role of cholesterol metabolism in the pathogenesis of Mycobacterium tuberculosis. PLoS Pathog. 2009, 5:e1000344.
58. Xu X., London E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 2000, 39:843-849.
59. Beattie M.E., et al. Sterol structure determines miscibility versus melting transitions in lipid vesicles. Biophys. J. 2005, 89:1760-1768.
60. Ahmad Z., et al. The potential of azole antifungals against latent/persistent tuberculosis. FEMS Microbiol. Lett. 2006, 258:200-203.
61. Ahmad Z., et al. Antimycobacterial activity of econazole against multidrug-resistant strains of Mycobacterium tuberculosis. Int. J. Antimicrob. Agents 2006, 28:543-544.
62. Driscoll M.D., et al. Expression and characterization of Mycobacterium tuberculosis CYP144: common themes and lessons learned in the Mycobacterium tuberculosis P450 enzyme family. Biochim. Biophys. Acta 2011, 1814:76-87.
63. Driscoll M.D., et al. Structural and biochemical characterization of Mycobacterium tuberculosis CYP142: evidence for multiple cholesterol 27-hydroxylase activities in a human pathogen. J. Biol. Chem. 2010, 285:38270-38282.
64. Johnston J.B., et al. Biochemical and structural characterization of CYP124: a methyl-branched lipid omega-hydroxylase from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:20687-20692.
65. McLean K.J., et al. Expression, purification and spectroscopic characterization of the cytochrome P450 CYP121 from Mycobacterium tuberculosis. J. Inorg. Biochem. 2002, 91:527-541.
66. McLean K.J., et al. Azole antifungals are potent inhibitors of cytochrome P450 mono-oxygenases and bacterial growth in mycobacteria and streptomycetes. Microbiology 2002, 148:2937-2949.
67. Ouellet H., et al. Mycobacterium tuberculosis CYP130: crystal structure, biophysical characterization, and interactions with antifungal azole drugs. J. Biol. Chem. 2008, 283:5069-5080.
68. Ouellet H., et al. Reverse type I inhibitor of Mycobacterium tuberculosis CYP125A1. Bioorg. Med. Chem. Lett. 2011, 21:332-337.
69. Thomas S.T., et al. Inhibition of the Mycobacterium tuberculosis 3beta-hydroxysteroid dehydrogenase by azasteroids. Bioorg. Med. Chem. Lett. 2011, 21:2216-2219.
70. Frye S.V., et al. 6-Azasteroids: potent dual inhibitors of human type 1 and 2 steroid 5 alpha-reductase. J. Med. Chem. 1993, 36:4313-4315.
71. Frye S.V., et al. 6-Azasteroids: structure-activity relationships for inhibition of type 1 and 2 human 5 alpha-reductase and human adrenal 3 beta-hydroxy-delta 5-steroid dehydrogenase/3-keto-delta 5-steroid isomerase. J. Med. Chem. 1994, 37:2352-2360.
72. McLean K.J., et al. Characterization of active site structure in CYP121. A cytochrome P450 essential for viability of Mycobacterium tuberculosis H37Rv. J. Biol. Chem. 2008, 283:33406-33416.