Mycobacterium tuberculosis utilizes a unique heterotetrameric structure for dehydrogenation of the cholesterol side chain

Biochemistry

Volumn 52, Issue 17, 2013, Pages 2895-2904

  Thomas, Suzanne T ^a   Sampson, Nicole S ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL ULTRACENTRIFUGATION; BIOINFORMATIC ANALYSIS; CHOLESTEROL SIDE CHAINS; METABOLITE IDENTIFICATION; MOLECULAR MECHANISM; MYCOBACTERIUM TUBERCULOSIS; QUATERNARY STRUCTURE; STEADY-STATE KINETICS;

BACTERIA; BIOINFORMATICS; CENTRIFUGATION; DEHYDROGENATION; GENES; LIQUID CHROMATOGRAPHY; METABOLISM; PHYSIOLOGY; TUBES (COMPONENTS);

CHOLESTEROL;

ACYL COENZYME A DEHYDROGENASE; APOENZYME; CHOLESTEROL; CLORPRENALINE; GLUTAMIC ACID; INDANONE DERIVATIVE; MONOMER; OXIDOREDUCTASE; STEROID; TETRAMER;

ACTINOBACTERIA; ARTICLE; BINDING SITE; BIOINFORMATICS; CATALYSIS; CISTRON; CONTROLLED STUDY; DEHYDROGENATION; ENZYME ACTIVITY; ESCHERICHIA COLI; LIQUID CHROMATOGRAPHY; MOLECULAR RECOGNITION; MUTAGENESIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; STEADY STATE; STEROL METABOLISM; ULTRACENTRIFUGATION; ULTRAVIOLET RADIATION;

ACYL-COA DEHYDROGENASE; BIOPHYSICS; BIOPOLYMERS; CHOLESTEROL; CHROMATOGRAPHY, GEL; HYDROGENATION; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PLASMIDS; SPECTROPHOTOMETRY, ULTRAVIOLET;

ACTINOBACTERIA (CLASS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84877066765     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4002979     Document Type: Article

References (35)

1. World Health Organization (2011) Global Tuberculosis Control 2011.
2. Russell, D. G., Cardona, P. J., Kim, M. J., Allain, S., and Altare, F. (2009) Foamy macrophages and the progression of the human tuberculosis granuloma Nat. Immunol. 10, 943-948
3. Peyron, P., Vaubourgeix, J., Poquet, Y., Levillain, F., Botanch, C., Bardou, F., Daffe, M., Emile, J. F., Marchou, B., Cardona, P. J., de Chastellier, C., and Altare, F. (2008) Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence PLoS Pathog. 4, e1000204
4. Pandey, A. K. and Sassetti, C. M. (2008) Mycobacterial persistence requires the utilization of host cholesterol Proc. Natl. Acad. Sci. U.S.A. 105, 4376-4380
5. Mohn, W. W., van der Geize, R., Stewart, G. R., Okamoto, S., Liu, J., Dijkhuizen, L., and Eltis, L. D. (2008) The actinobacterial mce4 locus encodes a steroid transporter J. Biol. Chem. 283, 35368-35374
6. Nesbitt, N., Yang, X., Fontán, P., Kolesnikova, I., Smith, I., Sampson, N. S., and Dubnau, E. (2010) A thiolase of M. tuberculosis is required for virulence and for production of androstenedione and androstadienedione from cholesterol Infect. Immun. 78, 275-282
7. Chang, J. C., Miner, M. D., Pandey, A. K., Gill, W. P., Harik, N. S., Sassetti, C. M., and Sherman, D. R. (2009) igr Genes and Mycobacterium tuberculosis cholesterol metabolism J. Bacteriol. 191, 5232-5239
8. Chang, J. C., Harik, N. S., Liao, R. P., and Sherman, D. R. (2007) Identification of Mycobacterial genes that alter growth and pathology in macrophages and in mice J. Infect. Dis. 196, 788-795
9. Thomas, S. T., VanderVen, B. C., Sherman, D. R., Russell, D. G., and Sampson, N. S. (2011) Pathway profiling in Mycobacterium tuberculosis: Elucidation of cholesterol-derived catabolite and enzymes that catalyze its metabolism J. Biol. Chem. 286, 43668-43678
10. Zhang, J., Zhang, W., Zou, D., Chen, G., Wan, T., Zhang, M., and Cao, X. (2002) Cloning and functional characterization of ACAD-9, a novel member of human acyl-CoA dehydrogenase family Biochem. Biophys. Res. Commun. 297, 1033-1042
11. Souri, M., Aoyama, T., Hoganson, G., and Hashimoto, T. (1998) Very-long-chain acyl-CoA dehydrogenase subunit assembles to the dimer form on mitochondrial inner membrane FEBS Lett. 426, 187-190
12. Moore, S. (2012) 'Round-the-horn site-directed mutagenesis. Wikiomics.
13. Daugelat, S., Kowall, J., Mattow, J., Bumann, D., Winter, R., Hurwitz, R., and Kaufmann, S. H. (2003) The RD1 proteins of Mycobacterium tuberculosis: Expression in Mycobacterium smegmatis and biochemical characterization Microbes Infect. 5, 1082-1095
14. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes Nat. Protoc. 1, 2856-2860
15. Winkler, R. (2010) ESIprot: A universal tool for charge state determination and molecular weight calculation of proteins from electrospray ionization mass spectrometry data Rapid Commun. Mass Spectrom. 24, 285-294
16. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice Nucleic Acids Res. 22, 4673-4680
17. Stierand, K., Maass, P. C., and Rarey, M. (2006) Molecular complexes at a glance: Automated generation of two-dimensional complex diagrams Bioinformatics 22, 1710-1716
18. Capyk, J. K., Casabon, I., Gruninger, R., Strynadka, N. C., and Eltis, L. D. (2011) Activity of 3-ketosteroid 9α-hydroxylase (KshAB) indicates cholesterol side chain and ring degradation occur simultaneously in Mycobacterium tuberculosis J. Biol. Chem. 286, 40717-40724
19. Lehman, T. C. and Thorpe, C. (1990) Alternate electron acceptors for medium-chain acyl-CoA dehydrogenase: Use of ferricenium salts Biochemistry 29, 10594-10602
20. Ellis, K. J. and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes Methods Enzymol. 87, 405-426
21. Hwang, T. L. and Shaka, A. J. (1995) Water suppression that works: Excitation sculpting using arbitrary wave-forms and pulsed-field gradients J. Magn. Reson., Ser. A 112, 275-279
22. Djordjevic, S., Dong, Y., Paschke, R., Frerman, F. E., Strauss, A. W., and Kim, J. J. (1994) Identification of the catalytic base in long chain acyl-CoA dehydrogenase Biochemistry 33, 4258-4264
23. Sih, C. J., Tai, H. H., and Tsong, Y. Y. (1967) The mechanism of microbial conversion of cholesterol into 17-keto steroids J. Am. Chem. Soc. 89, 1957-1958
24. Sih, C. J., Tai, H. H., Tsong, Y. Y., Lee, S. S., and Coombe, R. G. (1968) Mechanisms of steroid oxidation by microorganisms. XIV. Pathway of cholesterol side-chain degradation Biochemistry 7, 808-818
25. Sih, C. J., Wang, K. C., and Tai, H. H. (1968) Mechanisms of steroid oxidation by microorganisms. XIII. C22 acid intermediates in degradation of cholesterol side chain Biochemistry 7, 796-807
26. Bode, K., Hooks, M. A., and Couee, I. I. (1999) Identification, separation, and characterization of acyl-coenzyme A dehydrogenases involved in mitochondrial β-oxidation in higher plants Plant Physiol. 119, 1305-1314
27. Komuniecki, R., Fekete, S., and Thissen-Parra, J. (1985) Purification and characterization of the 2-methyl branched-chain Acyl-CoA dehydrogenase, an enzyme involved in NADH-dependent enoyl-CoA reduction in anaerobic mitochondria of the nematode, Ascaris suum J. Biol. Chem. 260, 4770-4777
28. Kionka, C. and Kunau, W. H. (1985) Inducible β-oxidation pathway in Neurospora crassa J. Bacteriol. 161, 153-157
29. Kunau, W. H., Dommes, V., and Schulz, H. (1995) β-Oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: A century of continued progress Prog. Lipid Res. 34, 267-342
30. Campbell, J. W. and Cronan, J. E., Jr. (2002) The enigmatic Escherichia coli fadE gene is yafH J. Bacteriol. 184, 3759-3764
31. Shen, Y. Q., Lang, B. F., and Burger, G. (2009) Diversity and dispersal of a ubiquitous protein family: Acyl-CoA dehydrogenases Nucleic Acids Res. 37, 5619-5631
32. Swigonova, Z., Mohsen, A. W., and Vockley, J. (2009) Acyl-CoA dehydrogenases: Dynamic history of protein family evolution J. Mol. Evol. 69, 176-193
33. McAndrew, R. P., Wang, Y., Mohsen, A. W., He, M., Vockley, J., and Kim, J. J. (2008) Structural basis for substrate fatty acyl chain specificity: Crystal structure of human very-long-chain acyl-CoA dehydrogenase J. Biol. Chem. 283, 9435-9443
34. Hiltunen, J. K. and Qin, Y. (2000) β-Oxidation: Strategies for the metabolism of a wide variety of acyl-CoA esters Biochim. Biophys. Acta 1484, 117-128
35. Cole, S. T., Brosch, R., Parkhil, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., III, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence Nature 393, 537-544