3-Ketosteroid 9α-hydroxylase is an essential factor in the pathogenesis of Mycobacterium tuberculosis

Molecular Microbiology

Volumn 75, Issue 1, 2010, Pages 107-121

  Hu, Yanmin ^a   Van Der Geize, Robert ^b   Besra, Gurdyal S ^c   Gurcha, Sudagar S ^c   Liu, Alexander ^d   Rohde, Manfred ^e   Singh, Mahavir ^f   Coates, Anthony ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^f LIONEX DIAGNOSTICS AND THERAPEUTICS GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3 KETOSTEROID 9 ALPHA HYDROXYLASE; ANDROSTENEDIONE; CHOLESTEROL; MEMBRANE LIPID; OXYGENASE; TREHALOSE; UNCLASSIFIED DRUG; 3 KETOSTEROID 9ALPHA HYDROXYLASE, MYCOBACTERIUM TUBERCULOSIS; 3-KETOSTEROID 9ALPHA-HYDROXYLASE, MYCOBACTERIUM TUBERCULOSIS; BACTERIAL PROTEIN; MIXED FUNCTION OXIDASE; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CONTROLLED STUDY; IN VITRO STUDY; LIPID ANALYSIS; LIPOGENESIS; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUBERCULOSIS; ANIMAL; BACTERIAL COUNT; BAGG ALBINO MOUSE; CELL CULTURE; ENZYMOLOGY; FEMALE; GENE DELETION; GENETICS; LUNG; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; SPLEEN; VIRULENCE;

MURINAE; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; BACTERIAL PROTEINS; CELLS, CULTURED; COLONY COUNT, MICROBIAL; FEMALE; GENE DELETION; LUNG; MACROPHAGES; METABOLIC NETWORKS AND PATHWAYS; MICE; MICE, INBRED BALB C; MICROBIAL VIABILITY; MIXED FUNCTION OXYGENASES; MYCOBACTERIUM TUBERCULOSIS; SPLEEN; TUBERCULOSIS; VIRULENCE; VIRULENCE FACTORS;

EID: 72949108894     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06957.x     Document Type: Article

References (40)

1. Besra, G.S. (1998) Preparation of Cell-Wall Fractions from Mycobacteria. Totowa : Humana press.
2. Besra, G.S., McNeil, M.R. Brennan, P.J. (1992) Characterization of the specific antigenicity of Mycobacterium fortuitum. Biochemistry 31 : 6504 6509.
3. Capyk, J.K., D'Angelo, I., Strynadka, N.C. Eltis, L.D. (2009) Characterization of 3-Ketosteroid 9{alpha}-hydroxylase, a Rieske oxygenase in the cholesterol degradation pathway of Mycobacterium tuberculosis. J Biol Chem 284 : 9937 9946.
4. Chang, J.C., Miner, M.D., Pandey, A.K., Gill, W.P., Harik, N.S., Sassetti, C.M. Sherman, D.R. (2009) igr genes and Mycobacterium tuberculosis cholesterol metabolism. J Bacteriol 191 : 5232 5239.
5. Chesne-Seck, M.L., Barilone, N., Boudou, F., Gonzalo Asensio, J., Kolattukudy, P.E., Martin, C., et al. (2008) A point mutation in the two-component regulator PhoP-PhoR accounts for the absence of polyketide-derived acyltrehaloses but not that of phthiocerol dimycocerosates in Mycobacterium tuberculosis H37Ra. J Bacteriol 190 : 1329 1334.
6. Corbett, E.L., Watt, C.J., Walker, N., Maher, D., Williams, B.G., Raviglione, M.C. Dye, C. (2003) The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163 : 1009 1021.
7. Dainese, E., Rodrigue, S., Delogu, G., Provvedi, R., Laflamme, L., Brzezinski, R., et al. (2006) Posttranslational regulation of Mycobacterium tuberculosis extracytoplasmic-function sigma factor sigma L and roles in virulence and in global regulation of gene expression. Infect Immun 74 : 2457 2461.
8. Dubey, V.S., Sirakova, T.D. Kolattukudy, P.E. (2002) Disruption of msl3 abolishes the synthesis of mycolipanoic and mycolipenic acids required for polyacyltrehalose synthesis in Mycobacterium tuberculosis H37Rv and causes cell aggregation. Mol Microbiol 45 : 1451 1459.
9. Fujiwara, N. (1997) Distribution of antigenic glycolipids among Mycobacterium tuberculosis strains and their contribution to virulence]. Kekkaku 72 : 193 205.
10. van der Geize, R., Hessels, G.I. Dijkhuizen, L. (2002a) Molecular and functional characterization of the kstD2 gene of Rhodococcus erythropolis SQ1 encoding a second 3-ketosteroid Delta(1)-dehydrogenase isoenzyme. Microbiology (Reading, England) 148 : 3285 3292. (Pubitemid 35243728)
11. van der Geize, R., Hessels, G.I., van Gerwen, R., van der Meijden, P. Dijkhuizen, L. (2002b) Molecular and functional characterization of kshA and kshB, encoding two components of 3-ketosteroid 9alpha-hydroxylase, a class IA monooxygenase. Rhodococcus erythropolis strain SQ1. Mol Microbiol 45 : 1007 1018.
12. van der Geize, R., Yam, K., Heuser, T., Wilbrink, M.H., Hara, H., Anderton, M.C., et al. (2007) A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc Natl Acad Sci USA 104 : 1947 1952.
13. van der Geize, R., de Jong, W., Hessels, G.I., Grommen, A.W., Jacobs, A.A. Dijkhuizen, L. (2008) A novel method to generate unmarked gene deletions in the intracellular pathogen Rhodococcus equi using 5-fluorocytosine conditional lethality. Nucleic Acids Res 36 : e151.
14. Hernandez-Pando, R., De La Luz Streber, M., Orozco, H., Arriaga, K., Pavon, L., Al-Nakhli, S.A. Rook, G.A. (1998) The effects of androstenediol and dehydroepiandrosterone on the course and cytokine profile of tuberculosis in BALB/c mice. Immunology 95 : 234 241.
15. Hu, Y., Butcher, P.D., Mangan, J.A., Rajandream, M.A. Coates, A.R. (1999) Regulation of hmp gene transcription in Mycobacterium tuberculosis: effects of oxygen limitation and nitrosative and oxidative stress. J Bacteriol 181 : 3486 3493.
16. Hu, Y., Movahedzadeh, F., Stoker, N.G. Coates, A.R. (2006) Deletion of the Mycobacterium tuberculosis alpha-crystallin-like hspX gene causes increased bacterial growth in vivo. Infect Immun 74 : 861 868.
17. Jain, M., Petzold, C.J., Schelle, M.W., Leavell, M.D., Mougous, J.D., Bertozzi, C.R., Leary, J.A. Cox, J.S. (2007) Lipidomics reveals control of Mycobacterium tuberculosis virulence lipids via metabolic coupling. Proc Natl Acad Sci USA 104 : 5133 5138.
18. Kaul, D., Anand, P.K. Verma, I. (2004) Cholesterol-sensor initiates M. tuberculosis entry into human macrophages. Mol Cell Biochem 258 : 219 222.
19. Kendall, S.L., Withers, M., Soffair, C.N., Moreland, N.J., Gurcha, S., Sidders, B., et al. (2007) A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis. Mol Microb 65 : 684 699.
20. Kondo, E. Kanai, K. (1976) Accumulation of cholesterol esters in macrophages incubated with mycobacteria in vitro. Jpn J Med Sci Biol 29 : 123 137.
21. Lee, M.H., Pascopella, L., Jacobs, W.R., Jr. Hatfull, G.F. (1991) Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guerin. Proc Natl Acad Sci USA 88 : 3111 3115.
22. Loria, R.M. (2009) Beta-androstenes and resistance to viral and bacterial infections. Neuroimmunomodulation 16 : 88 95.
23. Minnikin, D.E., Kremer, L., Dover, L.G. Besra, G.S. (2002) The methyl-branched fortifications of Mycobacterium tuberculosis. Chem Biol 9 : 545 553.
24. Mohn, W.W., van der Geize, R., Stewart, G.R., Okamoto, S., Liu, J., Dijkhuizen, L. Eltis, L.D. (2008) The actinobacterial mce4 locus encodes a steroid transporter. J Biol Chem 283 : 35368 35374.
25. Orme, I.M. (1988) A mouse model of the recrudescence of latent tuberculosis in the elderly. Am Rev Respir Dis 137 : 716 718.
26. Ortalo-Magne, A., Dupont, M.A., Lemassu, A., Andersen, A.B., Gounon, P. Daffe, M. (1995) Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology (Reading, England) 141 : 1609 1620.
27. Ortalo-Magne, A., Lemassu, A., Laneelle, M.A., Bardou, F., Silve, G., Gounon, P., Marchal, G. Daffe, M. (1996) Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species. J Bacteriol 178 : 456 461.
28. Pandey, A.K. Sassetti, C.M. (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105 : 4376 4380.
29. Parish, T. Stoker, N.G. (1998) Electroporation of Mycobacteria. Totowa : Humana press.
30. Parish, T. Stoker, N.G. (2000) Use of a flexible cassette method to generate a double unmarked Mycobacterium tuberculosis tlyA plcABC mutant by gene replacement. Microbiology (Reading, England) 146 : 1969 1975.
31. Petrusma, M., Dijkhuizen, L. van der Geize, R. (2009) Rhodococcus rhodochrous DSM 43269 3-ketosteroid 9alpha-hydroxylase, a two-component iron-sulfur-containing monooxygenase with subtle steroid substrate specificity. Appl Environ Microbiol 75 : 5300 5307.
32. Raymond, J.B., Mahapatra, S., Crick, D.C. Pavelka, M.S., Jr (2005) Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J Biol Chem 280 : 326 333.
33. Rengarajan, J., Bloom, B.R. Rubin, E.J. (2005) Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci USA 102 : 8327 8332.
34. Rousseau, C., Turner, O.C., Rush, E., Bordat, Y., Sirakova, T.D., Kolattukudy, P.E., et al. (2003) Sulfolipid deficiency does not affect the virulence of Mycobacterium tuberculosis H37Rv in mice and guinea pigs. Infect Immun 71 : 4684 4690.
35. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory.
36. Sassetti, C.M. Rubin, E.J. (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100 : 12989 12994.
37. Smith, D.A., Parish, T., Stoker, N.G. Bancroft, G.J. (2001) Characterization of auxotrophic mutants of Mycobacterium tuberculosis and their potential as vaccine candidates. Infect Immun 69 : 1142 1150.
38. Sudre, P., ten Dam, G. Kochi, A 1992) Tuberculosis: a global overview of the situation today. Bull World Health Organ 70 : 149 159.
39. Yam, K.C., D'Angelo, I., Kalscheuer, R., Zhu, H., Wang, J.X., Snieckus, V., et al. (2009) Studies of a ring-cleaving dioxygenase illuminate the role of cholesterol metabolism in the pathogenesis of Mycobacterium tuberculosis. PLoS Pathog 5 : e1000344.
40. Yang, X., Dubnau, E., Smith, I. Sampson, N.S. (2007) Rv1106c from Mycobacterium tuberculosis is a 3beta-hydroxysteroid dehydrogenase. Biochemistry 46 : 9058 9067.