Pathogen roid rage: Cholesterol utilization by Mycobacterium tuberculosis

References

• Ando M, Yoshimatsu T, Ko C, et al. (2003). Deletion of Mycobacterium tuberculosis sigma factor E results in delayed time to death with bacterial persistence in the lungs of aerosol-infected mice. Infect Immun 71:7170–2
   PubMed Web of Science ®Google Scholar
• Andor A, Jekkel A, Hopwood DA, et al. (2006). 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 72:6554–9
   Google Scholar
• Arruda S, Bomfim G, Knights R, et al. (1993). Cloning of an M. tuberculosis DNA fragment associated with entry and survival inside cells. Science 261:1454–7
   PubMed Web of Science ®Google Scholar
• Baes M, Huyghe S, Carmeliet P, et al. (2000). Inactivation of the peroxisomal multifunctional protein-2 in mice impedes the degradation of not only 2-methyl-branched fatty acids and bile acid intermediates but also of very long chain fatty acids. J Biol Chem 275:16329–36
   PubMed Web of Science ®Google Scholar
• Beste DJ, Noh K, Niedenfuhr S, et al. (2013). 13C-flux spectral analysis of host-pathogen metabolism reveals a mixed diet for intracellular Mycobacterium tuberculosis. Chem Biol 20:1012–21
   Google Scholar
• Bode HB, Zeggel B, Silakowski B, et al. (2003). Steroid biosynthesis in prokaryotes: identification of myxobacterial steroids and cloning of the first bacterial 2,3(S)-oxidosqualene cyclase from the myxobacterium Stigmatella aurantiaca. Mol Microbiol 47:471–81
   PubMed Web of Science ®Google Scholar
• Brzostek A, Dziadek B, Rumijowska-Galewicz A, et al. (2007). Cholesterol oxidase is required for virulence of Mycobacterium tuberculosis. FEMS Microbiol Lett 275:106–12
   PubMed Web of Science ®Google Scholar
• Brzostek A, Pawelczyk J, Rumijowska-Galewicz A, et al. (2009). Mycobacterium tuberculosis is able to accumulate and utilize cholesterol. J Bacteriol 191:6584–91
   PubMed Web of Science ®Google Scholar
• Brzostek A, Sliwinski T, Rumijowska-Galewicz A, et al. (2005). Identification and targeted disruption of the gene encoding the main 3-ketosteroid dehydrogenase in Mycobacterium smegmatis. Microbiology 151:2393–402
   Google Scholar
• Bushnell LD, Haas HF. (1941). The utilization of certain hydrocarbons by microorganisms. J Bacteriol 41:653–73
   PubMed Web of Science ®Google Scholar
• Camacho LR, Ensergueix D, Perez E, et al. (1999). Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34:257–67
   PubMed Web of Science ®Google Scholar
• Campbell JW, Cronan JE Jr. (2002). The enigmatic Escherichia coli fadE gene is yafH. J Bacteriol 184:3759–64
   Google Scholar
• Camus JC, Pryor MJ, Medigue C, Cole ST. (2002). Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology 148:2967–73
   PubMed Web of Science ®Google Scholar
• Capyk JK, Casabon I, Gruninger R, et al. (2011). Activity of 3-ketosteroid 9alpha-hydroxylase (KshAB) indicates cholesterol side chain and ring degradation occur simultaneously in Mycobacterium tuberculosis. J Biol Chem 286:40717–24
   Google Scholar
• Capyk JK, D'angelo I, Strynadka NC, Eltis LD. (2009a). Characterization of 3-ketosteroid 9-α-hydroxylase, a Rieske oxygenase in the cholesterol degradation pathway of Mycobacterium tuberculosis. J Biol Chem 284:9937–46
   PubMedGoogle Scholar
• Capyk JK, Kalscheuer R, Stewart GR, et al. (2009b). Mycobacterial cytochrome P450 125 (Cyp125) catalyzes the terminal hydroxylation of C27 steroids. J Biol Chem 284:35534–42
   PubMed Web of Science ®Google Scholar
• Carere J, Mckenna SE, Kimber MS, Seah SY. (2013). Characterization of an aldolase-dehydrogenase complex from the cholesterol degradation pathway of Mycobacterium tuberculosis. Biochemistry 52:3502–11
   Google Scholar
• Casabon I, Crowe AM, Liu J, Eltis LD. (2013a). FadD3 is an acyl-CoA synthetase that initiates catabolism of cholesterol rings C and D in actinobacteria. Mol Microbiol 87:269–83
   Google Scholar
• Casabon I, Swain K, Crowe AM, et al. (2014). Actinobacterial acyl-CoA synthetases involved in steroid side chain catabolism. J Bacteriol 196:579–87
   Google Scholar
• Casabon I, Zhu SH, Otani H, et al. (2013b). Regulation of the KstR2 regulon of Mycobacterium tuberculosis by a cholesterol catabolite. Mol Microbiol 89:1201–12
   Google Scholar
• Caspi R, Altman T, Dale JM, et al. (2010). The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 38:D473–9
   PubMed Web of Science ®Google Scholar
• Chang JC, Harik NS, Liao RP, Sherman DR. (2007). Identification of Mycobacterial genes that alter growth and pathology in macrophages and in mice. J Infect Dis 196:788–95
   PubMed Web of Science ®Google Scholar
• Chang JC, Miner MD, Pandey AK, et al. (2009). igr Genes and Mycobacterium tuberculosis cholesterol metabolism. J Bacteriol 191:5232–9
   PubMed Web of Science ®Google Scholar
• Cole ST, Brosch R, Parkhill J, et al. (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–44
   PubMed Web of Science ®Google Scholar
• Cox JS, Chen B, Mcneil M, Jacobs WR Jr. (1999). Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402:79–83
   PubMed Web of Science ®Google Scholar
• De Carvalho LP, Fischer SM, Marrero J, et al. (2010). Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem Biol 17:1122–31
   PubMed Web of Science ®Google Scholar
• De La Paz Santangelo M, Klepp L, Nunez-Garcia J, et al. (2009). Mce3R, a TetR-type transcriptional repressor, controls the expression of a regulon involved in lipid metabolism in Mycobacterium tuberculosis. Microbiology 155:2245–55
   Google Scholar
• Donova MV. (2007). Transformation of steroids by actinobacteria: a review. Prikl Biokhim Mikrobiol 43:5–18
   Google Scholar
• Dresen C, Lin LY, D'angelo I, et al. (2010). A flavin-dependent monooxygenase from Mycobacterium tuberculosis involved in cholesterol catabolism. J Biol Chem 285:22264–75
   Google Scholar
• Driscoll MD, Mclean KJ, Cheesman MR, et al. (2011). Expression and characterization of Mycobacterium tuberculosis CYP144: common themes and lessons learned in the M. tuberculosis P450 enzyme family. Biochim Biophys Acta 1814:76–87
   PubMed Web of Science ®Google Scholar
• Drzyzga O, Fernandez De Las Heras L, Morales V, et al. (2011). Cholesterol degradation by Gordonia cholesterolivorans. Appl Environ Microbiol 77:4802–10
   Google Scholar
• Dubnau E, Chan J, Mohan VP, Smith I. (2005). Responses of Mycobacterium tuberculosis to growth in the mouse lung. Infect Immun 73:3754–7
   PubMed Web of Science ®Google Scholar
• Dubnau E, Fontán P, Manganelli R, et al. (2002). Mycobacterium tuberculosis genes induced during infection of human macrophages. Infect Immun 70:2787–95
   PubMed Web of Science ®Google Scholar
• Dye C, Scheele S, Dolin P, et al. (1999). Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 282:677–86
   PubMed Web of Science ®Google Scholar
• Fleischmann RD, Alland D, Eisen JA, et al. (2002). Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J Bacteriol 184:5479–90
   PubMed Web of Science ®Google Scholar
• Fontán P, Aris V, Ghanny S, et al. (2008a). Global transcriptional profile of Mycobacterium tuberculosis during THP-1 human macrophage infection. Infect Immun 76:717–25
   PubMed Web of Science ®Google Scholar
• Fontán PA, Aris V, Alvarez ME, et al. (2008b). Mycobacterium tuberculosis sigma factor E regulon modulates the host inflammatory response. J Infect Dis 198:877–85
   Google Scholar
• Fukui T, Shiomi N, Doi Y. (1998). Expression and characterization of (R)-specific enoyl coenzyme A hydratase involved in polyhydroxyalkanoate biosynthesis by Aeromonas caviae. J Bacteriol 180:667–73
   PubMed Web of Science ®Google Scholar
• Galagan JE, Minch K, Peterson M, et al. (2013). The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 499:178–83
   PubMed Web of Science ®Google Scholar
• Gao J, Sampson NS. (2014). A GMC oxidoreductase homologue is required for acetylation of glycopeptidolipid in Mycobacterium smegmatis. Biochemistry 53:611–13
   Google Scholar
• García JL, Uhía I, García E, Galán B. (2011). Bacterial degradation of cholesterol and other contaminant sterols. In: Koukkou A-I, ed. Microbial bioremediation of non-metals: current research. Norfolk, UK: Caister Academic Press, 23–43
   Google Scholar
• Ghai R, Mcmahon KD, Rodriguez-Valera F. (2012). Breaking a paradigm: cosmopolitan and abundant freshwater actinobacteria are low GC. Environ Microbiol Rep 4:29–35
   Google Scholar
• Gioffre A, Infante E, Aguilar D, et al. (2005). Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. Microbes Infect 7:325–34
   PubMed Web of Science ®Google Scholar
• Griffin JE, Gawronski JD, Dejesus MA, et al. (2011). High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7:e1002251
   PubMed Web of Science ®Google Scholar
• Han R. (2009). Is hypercholesterolemia a friend or a foe of tuberculosis? Infect Immun 77:3514–15
   Google Scholar
• Hogg JA. (1992). Steroids, the steroid community, and Upjohn in perspective: a profile of innovation. Steroids 57:593–616
   PubMed Web of Science ®Google Scholar
• Holert J, Jagmann N, Philipp B. (2013a). The essential function of genes for a hydratase and an aldehyde dehydrogenase for growth of Pseudomonas sp. strain Chol1 with the steroid compound cholate indicates an aldolytic reaction step for deacetylation of the side chain. J Bacteriol 195:3371–80
   Google Scholar
• Holert J, Kulic Z, Yucel O, et al. (2013b). Degradation of the acyl side chain of the steroid compound cholate in Pseudomonas sp. strain Chol1 proceeds via an aldehyde intermediate. J Bacteriol 195:585–95
   Google Scholar
• Horinouchi M, Hayashi T, Koshino H, Kudo T. (2006). ORF18-disrupted mutant of Comamonas testosteroni TA441 accumulates significant amounts of 9,17-dioxo-1,2,3,4,10,19-hexanorandrostan-5-oic acid and its derivatives after incubation with steroids. J Steroid Biochem Mol Biol 101:78–84
   Google Scholar
• Horinouchi M, Hayashi T, Koshino H, et al. (2005). Identification of 9,17-dioxo-1,2,3,4,10,19-hexanorandrostan-5-oic acid, 4-hydroxy-2-oxohexanoic acid, and 2-hydroxyhexa-2,4-dienoic acid and related enzymes involved in testosterone degradation in Comamonas testosteroni TA441. Appl Environ Microbiol 71:5275–81
   Google Scholar
• Horinouchi M, Hayashi T, Kudo T. (2012). Steroid degradation in Comamonas testosteroni. J Steroid Biochem Mol Biol 129:4–14
   Google Scholar
• Horinouchi M, Hayashi T, Yamamoto T, Kudo T. (2003). A new bacterial steroid degradation gene cluster in Comamonas testosteroni TA441 which consists of aromatic-compound degradation genes for seco-steroids and 3-ketosteroid dehydrogenase genes. Appl Environ Microbiol 69:4421–30
   Google Scholar
• Horinouchi M, Kurita T, Yamamoto T, et al. (2004). Steroid degradation gene cluster of Comamonas testosteroni consisting of 18 putative genes from meta-cleavage enzyme gene tesB to regulator gene tesR. Biochem Biophys Res Commun 324:597–604
   Google Scholar
• Horinouchi M, Yamamoto T, Taguchi K, et al. (2001). Meta-cleavage enzyme gene tesB is necessary for testosterone degradation in Comamonas testosteroni TA441. Microbiology 147:3367–75
   Google Scholar
• Horinouchi S, Ishizuka H, Beppu T. (1991). Cloning, nucleotide sequence, and transcriptional analysis of the NAD(P)-dependent cholesterol dehydrogenase gene from a Nocardia sp. and its hyperexpression in Streptomyces spp. Appl Environ Microbiol 57:1386–93
   PubMed Web of Science ®Google Scholar
• Hu Y, Van Der Geize R, Besra GS, et al. (2010). 3-Ketosteroid 9alpha-hydroxylase is an essential factor in the pathogenesis of Mycobacterium tuberculosis. Mol Microbiol 75:107–21
   PubMed Web of Science ®Google Scholar
• Ishizaki T, Hirayama N, Shinkawa H, et al. (1989). Nucleotide sequence of the gene for cholesterol oxidase from a Streptomyces sp. J Bacteriol 171:596–601
   PubMed Web of Science ®Google Scholar
• Ivashina TV, Nikolayeva VM, Dovbnya DV, Donova MV. (2012). Cholesterol oxidase ChoD is not a critical enzyme accounting for oxidation of sterols to 3-keto-4-ene steroids in fast-growing Mycobacterium sp. VKM Ac-1815D. J Steroid Biochem Mol Biol 129:47–53
   Google Scholar
• Jain M, Petzold CJ, Schelle MW, et al. (2007). Lipidomics reveals control of Mycobacterium tuberculosis virulence lipids via metabolic coupling. Proc Natl Acad Sci USA 104:5133–8
   PubMed Web of Science ®Google Scholar
• Johnston JB, Ouellet H, Ortiz De Montellano PR. (2010). Functional redundancy of steroid C26-monooxygenase activity in Mycobacterium tuberculosis revealed by biochemical and genetic analyses. J Biol Chem 285:36352–60
   Google Scholar
• Kameda K, Nunn WD. (1981). Purification and characterization of acyl coenzyme A synthetase from Escherichia coli. J Biol Chem 256:5702–7
   Google Scholar
• Kang Y, Zarzycki-Siek J, Walton CB, et al. (2010). Multiple FadD acyl-CoA synthetases contribute to differential fatty acid degradation and virulence in Pseudomonas aeruginosa. PLoS One 5:e13557
   PubMed Web of Science ®Google Scholar
• Kaufmann G, Thole H, Kraft R, Atrat P. (1992). Steroid-1-dehydrogenase of Rhodococcus erythropolis: purification and N-terminal amino acid sequence. J Steroid Biochem Mol Biol 43:297–301
   Google Scholar
• Kendall SL, Burgess P, Balhana R, et al. (2010). Cholesterol utilization in mycobacteria is controlled by two TetR-type transcriptional regulators: KstR and KstR2. Microbiology 156:1362–71
   Google Scholar
• Kendall SL, Withers M, Soffair CN, et al. (2007). A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis. Mol Microbiol 65:684–99
   PubMed Web of Science ®Google Scholar
• Khare G, Gupta V, Gupta RK, et al. (2009). Dissecting the role of critical residues and substrate preference of a Fatty Acyl-CoA Synthetase (FadD13) of Mycobacterium tuberculosis. PLoS One 4:e8387
   Google Scholar
• Kim MJ, Wainwright HC, Locketz M, et al. (2010). Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol Med 2:258–74
   PubMed Web of Science ®Google Scholar
• Kishi K, Watazu Y, Katayama Y, Okabe H. (2000). The characteristics and applications of recombinant cholesterol dehydrogenase. Biosci Biotechnol Biochem 64:1352–8
   PubMed Web of Science ®Google Scholar
• Klink M, Brzezinska M, Szulc I, et al. (2013). Cholesterol oxidase is indispensable in the pathogenesis of Mycobacterium tuberculosis. PLoS One 8:e73333
   Google Scholar
• Knol J, Bodewits K, Hessels GI, et al. (2008). 3-Keto-5α-steroid Δ(1)-dehydrogenase from Rhodococcus erythropolis SQ1 and its orthologue in Mycobacterium tuberculosis H37Rv are highly specific enzymes that function in cholesterol catabolism. Biochem J 410:339–46
   Google Scholar
• Kobayashi H, Rittmann BE. (1982). Microbial removal of hazardous organic compounds. Environ Sci Technol 16:170A–83A
   Web of Science ®Google Scholar
• Koski KM, Haapalainen AM, Hiltunen JK, Glumoff T. (2005). Crystal structure of 2-enoyl-CoA hydratase 2 from human peroxisomal multifunctional enzyme type 2. J Mol Biol 345:1157–69
   Google Scholar
• Lack NA, Yam KC, Lowe ED, et al. (2010). Characterization of a carbon-carbon hydrolase from Mycobacterium tuberculosis involved in cholesterol metabolism. J Biol Chem 285:434–43
   PubMed Web of Science ®Google Scholar
• Lamarca BB, Zhu W, Arceneaux JE, et al. (2004). Participation of fad and mbt genes in synthesis of mycobactin in Mycobacterium smegmatis. J Bacteriol 186:374–82
   PubMed Web of Science ®Google Scholar
• Lamichhane G, Zignol M, Blades NJ, et al. (2003). A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 100:7213–8
   PubMed Web of Science ®Google Scholar
• Lechat P, Hummel L, Rousseau S, Moszer I. (2008). GenoList: an integrated environment for comparative analysis of microbial genomes. Nucleic Acids Res 36:D469–74
   Google Scholar
• Lew JM, Kapopoulou A, Jones LM, Cole ST. (2011). TubercuList – 10 years after. Tuberculosis (Edinb) 91:1–7
   PubMed Web of Science ®Google Scholar
• Lin G, Li D, De Carvalho LP, et al. (2009). Inhibitors selective for mycobacterial versus human proteasomes. Nature 461:621–6
   PubMed Web of Science ®Google Scholar
• Machang'u RS, Prescott JF. (1991). Purification and properties of cholesterol oxidase and choline phosphohydrolase from Rhodococcus equi. Can J Vet Res 55:332–40
   Google Scholar
• Malaviya A, Gomes J. (2008). Androstenedione production by biotransformation of phytosterols. Bioresour Technol 99:6725–37
   PubMed Web of Science ®Google Scholar
• Mcguire AM, Weiner B, Park ST, et al. (2012). Comparative analysis of Mycobacterium and related Actinomycetes yields insight into the evolution of Mycobacterium tuberculosis pathogenesis. BMC Genomics 13:120
   PubMed Web of Science ®Google Scholar
• Mclean KJ, Lafite P, Levy C, et al. (2009). The structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection. J Biol Chem 284:35524–33
   PubMed Web of Science ®Google Scholar
• Mitra D, Saha B, Das D, et al. (2005). Correlating sequential homology of Mce1A, Mce2A, Mce3A and Mce4A with their possible functions in mammalian cell entry of Mycobacterium tuberculosis performing homology modeling. Tuberculosis (Edinb) 85:337–45
   PubMed Web of Science ®Google Scholar
• Mohn WW, Van Der Geize R, Stewart GR, et al. (2008). The actinobacterial mce4 locus encodes a steroid transporter. J Biol Chem 283:35368–74
   PubMed Web of Science ®Google Scholar
• Mohn WW, Wilbrink MH, Casabon I, et al. (2012). Gene cluster encoding cholate catabolism in Rhodococcus spp. J Bacteriol 194:6712–9
   Google Scholar
• Munoz-Elias EJ, Upton AM, Cherian J, Mckinney JD. (2006). Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol Microbiol 60:1109–22
   PubMed Web of Science ®Google Scholar
• Nesbitt NM, Yang X, Fontán P, et al. (2010). A thiolase of Mycobacterium tuberculosis is required for virulence and production of androstenedione and androstadienedione from cholesterol. Infect Immun 78:275–82
   PubMed Web of Science ®Google Scholar
• Ouellet H, Guan S, Johnston JB, et al. (2010). Mycobacterium tuberculosis CYP125A1, a steroid C27 monooxygenase that detoxifies intracellularly generated cholest-4-en-3-one. Mol Microbiol 77:730–42
   Google Scholar
• Pandey AK, Sassetti CM. (2008). Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105:4376–80
   PubMed Web of Science ®Google Scholar
• Pang L, Tian X, Pan W, Xie J. (2013). Structure and function of mycobacterium glycopeptidolipids from comparative genomics perspective. J Cell Biochem 114:1705–13
   PubMed Web of Science ®Google Scholar
• Park SJ, Lee SY. (2003). Identification and characterization of a new enoyl coenzyme A hydratase involved in biosynthesis of medium-chain-length polyhydroxyalkanoates in recombinant Escherichia coli. J Bacteriol 185:5391–7
   PubMed Web of Science ®Google Scholar
• Peterson DH, Murray HC. (1952). Microbiological oxygenation of steroids at carbon-11. J Am Chem Soc 74:1871–2
   Web of Science ®Google Scholar
• Pethe K, Sequeira PC, Agarwalla S, et al. (2010). A chemical genetic screen in Mycobacterium tuberculosis identifies carbon-source-dependent growth inhibitors devoid of in vivo efficacy. Nat Commun 1:57
   PubMed Web of Science ®Google Scholar
• 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 75:5300–7
   Google Scholar
• Petrusma M, Hessels G, Dijkhuizen L, Van Der Geize R. (2011). Multiplicity of 3-ketosteroid-9alpha-hydroxylase enzymes in Rhodococcus rhodochrous DSM43269 for specific degradation of different classes of steroids. J Bacteriol 193:3931–40
   Google Scholar
• Peyron P, Vaubourgeix J, Poquet Y, et al. (2008). Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4:e1000204
   PubMed Web of Science ®Google Scholar
• Qin YM, Haapalainen AM, Conry D, et al. (1997). Recombinant 2-enoyl-CoA hydratase derived from rat peroxisomal multifunctional enzyme 2: role of the hydratase reaction in bile acid synthesis. Biochem J 328:377–82
   Google Scholar
• Raman S, Song T, Puyang X, et al. (2001). The alternative sigma factor SigH regulates major components of oxidative and heat stress responses in Mycobacterium tuberculosis. J Bacteriol 183:6119–25
   PubMed Web of Science ®Google Scholar
• Ramos JL, Martinez-Bueno M, Molina-Henares AJ, et al. (2005). The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69:326–56
   PubMed Web of Science ®Google Scholar
• Reed MB, Domenech P, Manca C, et al. (2004). A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431:84–7
   PubMed Web of Science ®Google Scholar
• Reichman LB, Tanne JH. (2002). Timebomb: the global epidemic of multi-drug-resistant tuberculosis. New York: McGraw-Hill
   Google Scholar
• Reiser SE, Mitsky TA, Gruys KJ. (2000). Characterization and cloning of an (R)-specific trans-2,3-enoylacyl-CoA hydratase from Rhodospirillum rubrum and use of this enzyme for PHA production in Escherichia coli. Appl Microbiol Biotechnol 53:209–18
   Google Scholar
• Rengarajan J, Bloom BR, Rubin EJ. (2005). Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci USA 102:8327–32
   PubMed Web of Science ®Google Scholar
• Robertson HE. (1933). The persistence of tuberculous infections. Am J Pathol 9:711–18.1
   Google Scholar
• Rodriguez GM, Voskuil MI, Gold B, et al. (2002). ideR, An essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 70:3371–81
   PubMed Web of Science ®Google Scholar
• Rohde KH, Veiga DF, Caldwell S, et al. (2012). Linking the transcriptional profiles and the physiological states of Mycobacterium tuberculosis during an extended intracellular infection. PLoS Pathog 8:e1002769
   PubMed Web of Science ®Google Scholar
• Rosloniec KZ, Wilbrink MH, Capyk JK, et al. (2009). Cytochrome P450 125 (CYP125) catalyses C26-hydroxylation to initiate sterol side-chain degradation in Rhodococcus jostii RHA1. Mol Microbiol 74:1031–43
   Google Scholar
• Rousseau C, Winter N, Pivert E, et al. (2004). Production of phthiocerol dimycocerosates protects Mycobacterium tuberculosis from the cidal activity of reactive nitrogen intermediates produced by macrophages and modulates the early immune response to infection. Cell Microbiol 6:277–87
   PubMed Web of Science ®Google Scholar
• Russell DG, Cardona PJ, Kim MJ, et al. (2009). Foamy macrophages and the progression of the human tuberculosis granuloma. Nature Immunol 10:943–8
   PubMed Web of Science ®Google Scholar
• Santangelo MP, Blanco FC, Bianco MV, et al. (2008). Study of the role of Mce3R on the transcription of mce genes of Mycobacterium tuberculosis. BMC Microbiol 8:38
   PubMed Web of Science ®Google Scholar
• Santangelo MP, Goldstein J, Alito A, et al. (2002). Negative transcriptional regulation of the mce3 operon in Mycobacterium tuberculosis. Microbiology 148:2997–3006
   Google Scholar
• Santer M, Ajl SJ, Turner RA. (1952). Steroid metabolism by a species of Pseudomonas. I. J Biol Chem 198:397–404
   Google Scholar
• Sassetti CM, Rubin EJ. (2003). Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100:12989–94
   PubMed Web of Science ®Google Scholar
• Savvi S, Warner DF, Kana BD, et al. (2008). Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids. J Bacteriol 190:3886–95
   PubMed Web of Science ®Google Scholar
• Scanga CA, Mohan VP, Joseph H, et al. (1999). Reactivation of latent tuberculosis: variations on the Cornell murine model. Infect Immun 67:4531–8
   PubMed Web of Science ®Google Scholar
• Schafer G, Guler R, Murray G, et al. (2009). The role of scavenger receptor B1 in infection with Mycobacterium tuberculosis in a murine model. PLoS One 4:e8448
   PubMed Web of Science ®Google Scholar
• Schnappinger D, Ehrt S, Voskuil MI, et al. (2003). Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198:693–704
   PubMed Web of Science ®Google Scholar
• Schnoes AM, Brown SD, Dodevski I, Babbitt PC. (2009). Annotation error in public databases: misannotation of molecular function in enzyme superfamilies. PLoS Comput Biol 5:e1000605
   PubMed Web of Science ®Google Scholar
• Schorey JS, Sweet L. (2008). The mycobacterial glycopeptidolipids: structure, function, and their role in pathogenesis. Glycobiology 18:832–41
   PubMed Web of Science ®Google Scholar
• Senaratne RH, Sidders B, Sequeira P, et al. (2008). Mycobacterium tuberculosis strains disrupted in mce3 and mce4 operons are attenuated in mice. J Med Microbiol 57:164–70
   PubMed Web of Science ®Google Scholar
• Sih CJ. (1962). Mechanisms of steroid oxidation by microorganisms. Biochim Biophys Acta 62:541–7
   Google Scholar
• Sih CJ, Tai HH, Tsong YY. (1967). The mechanism of microbial conversion of cholesterol into 17-keto steroids. J Am Chem Soc 89:1957–8
   Google Scholar
• Sih CJ, Tai HH, Tsong YY, et al. (1968a). Mechanisms of steroid oxidation by microorganisms. XIV. Pathway of cholesterol side-chain degradation. Biochemistry 7:808–18
   PubMed Web of Science ®Google Scholar
• Sih CJ, Wang KC, Tai HH. (1968b). Mechanisms of steroid oxidation by microorganisms. 13. C22 acid intermediates in the degradation of the cholesterol side chain. Biochemistry 7:796–807
   PubMedGoogle Scholar
• Simeone R, Leger M, Constant P, et al. (2010). Delineation of the roles of FadD22, FadD26 and FadD29 in the biosynthesis of phthiocerol dimycocerosates and related compounds in Mycobacterium tuberculosis. FEBS J 277:2715–25
   PubMed Web of Science ®Google Scholar
• Söhngen NL. (1913). Benzin Petroleum Paraffinöl und Paraffin als Kohlenstoff- und energiequelle für Mikroben. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt 37:595–609
   Google Scholar
• Stadtman TC, Cherkes A, Anfinsen CB. (1954). Studies on the microbiological degradation of cholesterol. J Biol Chem 206:511–23
   PubMed Web of Science ®Google Scholar
• Stern JR, Del Campillo A. (1956). Enzymes of fatty acid metabolism. II. Properties of crystalline crotonase. J Biol Chem 218:985–1002
   Google Scholar
• Stover CK, Warrener P, Vandevanter DR, et al. (2000). A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis. Nature 405:962–6
   PubMed Web of Science ®Google Scholar
• Strijewski A. (1982). The steroid-9 alpha-hydroxylation system from Nocardia species. Eur J Biochem 128:125–35
   Google Scholar
• Tak JD. (1942). On bacteria decomposing cholesterol. Antonie Van Leeuwenhoek 8:32–40
   Google Scholar
• Talalay P, Dobson MM, Tapley DF. (1952). Oxidative degradation of testosterone by adaptive enzymes. Nature 170:620–1
   PubMed Web of Science ®Google Scholar
• Taylor RC. (2011). Mycobacterial fatty acid metabolism: identification of novel drug targets and chemotherapeutics. Ph.D, University of Birmingham
   Google Scholar
• Taylor RC, Brown AK, Singh A, et al. (2010). Characterization of a beta-hydroxybutyryl-CoA dehydrogenase from Mycobacterium tuberculosis. Microbiology 156:1975–82
   Google Scholar
• Thomas ST, Sampson NS. (2013). Mycobacterium tuberculosis utilizes a unique heterotetrameric structure for dehydrogenation of the cholesterol side chain. Biochemistry 52:2895–904
   PubMed Web of Science ®Google Scholar
• Thomas ST, Vanderven BC, Sherman DR, et al. (2011). Pathway profiling in Mycobacterium tuberculosis: elucidation of cholesterol-derived catabolite and enzymes that catalyze its metabolism. J Biol Chem 286:43668–78
   PubMed Web of Science ®Google Scholar
• Timm J, Post FA, Bekker LG, et al. (2003). Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proc Natl Acad Sci U S A 100:14321–6
   PubMed Web of Science ®Google Scholar
• Trivedi OA, Arora P, Sridharan V, et al. (2004). Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 428:441–5
   PubMed Web of Science ®Google Scholar
• Tsuge T, Fukui T, Matsusaki H, et al. (2000). Molecular cloning of two (R)-specific enoyl-CoA hydratase genes from Pseudomonas aeruginosa and their use for polyhydroxyalkanoate synthesis. FEMS Microbiol Lett 184:193–8
   PubMed Web of Science ®Google Scholar
• Turfitt GE. (1947). Microbiological agencies in the degradation of steroids; steroid utilization by the microflora of soils. J Bacteriol 54:557–62
   Web of Science ®Google Scholar
• Uchida Y, Casali N, White A, et al. (2007). Accelerated immunopathological response of mice infected with Mycobacterium tuberculosis disrupted in the mce1 operon negative transcriptional regulator. Cell Microbiol 9:1275–83
   PubMed Web of Science ®Google Scholar
• Udwadia ZF, Amale RA, Ajbani KK, Rodrigues C. (2012). Totally drug-resistant tuberculosis in India. Clin Infect Dis 54:579–81
   PubMed Web of Science ®Google Scholar
• Uhía I, Galán B, Kendall SL, et al. (2012). Cholesterol metabolism in Mycobacterium smegmatis. Environ Microbiol Rep 4:168–82
   Google Scholar
• Uhía I, Galán B, Medrano FJ, García JL. (2011a). Characterization of the KstR-dependent promoter of the gene for the first step of the cholesterol degradative pathway in Mycobacterium smegmatis. Microbiology 157:2670–80
   PubMed Web of Science ®Google Scholar
• Uhía I, Galán B, Morales V, García JL. (2011b). Initial step in the catabolism of cholesterol by Mycobacterium smegmatis mc2155. Environ Microbiol 13:943–59
   Google Scholar
• Van Der Geize R, Dijkhuizen L. (2004). Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr Opin Microbiol 7:255–61
   PubMed Web of Science ®Google Scholar
• Van Der Geize R, Grommen AW, Hessels GI, et al. (2011). The steroid catabolic pathway of the intracellular pathogen Rhodococcus equi is important for pathogenesis and a target for vaccine development. PLoS Pathog 7:e1002181
   Google Scholar
• Van Der Geize R, Hessels GI, Van Gerwen R, et al. (2002). Molecular and functional characterization of kshA and kshB, encoding two components of 3-ketosteroid 9alpha-hydroxylase, a class IA monooxygenase, in Rhodococcus erythropolis strain SQ1. Mol Microbiol 45:1007–18
   Google Scholar
• Van Der Geize R, Yam K, Heuser T, 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 U S A 104:1947–52
   PubMed Web of Science ®Google Scholar
• Venkatesan R, Wierenga RK. (2013). Structure of mycobacterial beta-oxidation trifunctional enzyme reveals its altered assembly and putative substrate channeling pathway. ACS Chem Biol 8:1063–73
   Google Scholar
• Villemagne B, Crauste C, Flipo M, et al. (2012). Tuberculosis: The drug development pipeline at a glance. Eur J Med Chem 51:1–16
   PubMed Web of Science ®Google Scholar
• Waksman SA. (1953). Streptomycin: background, isolation, properties, and utilization. Science 118:259–66
   PubMed Web of Science ®Google Scholar
• Wanders RJ, Komen J, Ferdinandusse S. (2011). Phytanic acid metabolism in health and disease. Biochim Biophys Acta 1811:498–507
   PubMed Web of Science ®Google Scholar
• Wang SF, Kawahara FS, Talalay P. (1963). The mechanism of the delta5-3-ketosteroid isomerase reaction: absorption and fluorescence spectra of enzyme-steroid complexes. J Biol Chem 238:576–85
   Google Scholar
• Wheeler PR, Brosch R, Coldham NG, et al. (2008). Functional analysis of a clonal deletion in an epidemic strain of Mycobacterium bovis reveals a role in lipid metabolism. Microbiology 154:3731–42
   Google Scholar
• WHO. 2013. Global Tuberculosis Report 2013 [Online]. The World Health Organization. Available from: http://apps.who.int/iris/bitstream/10665/91355/1/9789241564656_eng.pdf?ua=1 [last accessed 26 Feb 2014]
   Google Scholar
• Wilbrink MH, Petrusma M, Dijkhuizen L, Van Der Geize R. (2011). FadD19 of Rhodococcus rhodochrous DSM43269, a steroid-coenzyme A ligase essential for degradation of C-24 branched sterol side chains. Appl Environ Microbiol 77:4455–64
   PubMed Web of Science ®Google Scholar
• Williams KJ, Boshoff HI, Krishnan N, et al. (2011). The Mycobacterium tuberculosis beta-oxidation genes echA5 and fadB3 are dispensable for growth in vitro and in vivo. Tuberculosis (Edinb) 91:549–55
   PubMed Web of Science ®Google Scholar
• Wipperman MF, Yang M, Thomas ST, Sampson NS. (2013). Shrinking the FadE proteome of Mycobacterium tuberculosis: insights into cholesterol metabolism through identification of an α2β2 heterotetrameric acyl coenzyme A dehydrogenase family. J Bacteriol 195:4331–41
   PubMed Web of Science ®Google Scholar
• Yam KC, D'angelo I, Kalscheuer R, 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
   PubMed Web of Science ®Google Scholar
• Yang X, Dubnau E, Smith I, Sampson NS. (2007). Rv1106c from Mycobacterium tuberculosis is a 3-β-hydroxysteroid dehydrogenase. Biochemistry 46:9058–67
   Google Scholar
• Yang X, Gao J, Smith I, et al. (2011). Cholesterol is not an essential source of nutrition for Mycobacterium tuberculosis during infection. J Bacteriol 193:1473–6
   Google Scholar
• Yang X, Nesbitt NM, Dubnau E, et al. (2009). Cholesterol metabolism increases the metabolic pool of propionate in Mycobacterium tuberculosis. Biochemistry 48:3819–21
   PubMed Web of Science ®Google Scholar