Metabolism of Mycobacterium tuberculosis

Systems Biology of Tuberculosis

Volumn , Issue , 2013, Pages 55-78

  Beste, Dany J V ^a   McFadden, Johnjoe ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84896998196     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-4966-9_4     Document Type: Chapter

References (80)

1. McKinney JD, Honerzu Bentrup K, Munoz-Elias EJ, Miczak ACB, Chan W-T, Senson D, Sacchettini JC, Jacobs-WR J, Russell DG (2000) Persistance of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406:735-738
2. Munoz-Elias EJ, McKinney JD (2005) Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med 11:638-644
3. Fritz C, Maass S, Kreft A, Bange FC (2002) Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue speci fi c. Infect Immun 70:286-291
4. Miner MD, Chang JC, Pandey AK, Sassetti CM, Sherman DR (2009) Role of cholesterol in Mycobacterium tuberculosis infection. Indian J Exp Biol 47:407-411
5. Movahedzadeh F, Smith DA, Norman RA, Dinadayala P, Murray-Rust J, Russell DG, Kendall SL, Rison SC, McAlister MS, Bancroft GJ et al (2004) The Mycobacterium tuberculosis ino1 gene is essential for growth and virulence. Mol Microbiol 51:1003-1014
6. Singh A, Crossman DK, Mai D, Guidry L, Voskuil MI, Renfrow MB, Steyn AJ (2009) Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog 5:e1000545
7. Glickman MS, Cox JS, Jacobs WR Jr (2000) A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol Cell 5:717-727
8. Keating LA, Wheeler PR, Mansoor H, Inwald JK, Dale J, Hewinson RG, Gordon SV (2005) The pyruvate requirement of some members of the Mycobacterium tuberculosis complex is due to an inactive pyruvate kinase: implications for in vivo growth. Mol Microbiol 56:163-174
9. 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 60:1109-1122
10. Gengenbacher M, Rao SP, Pethe K, Dick T (2010) Nutrient-starved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability. Microbiology 156:81-87
11. Baughn AD, Garforth SJ, Vilcheze C, Jacobs WR Jr (2009) An anaerobic-type alpha-ketoglutarate ferredoxin oxidoreductase completes the oxidative tricarboxylic acid cycle of Mycobacterium tuberculosis. PLoS Pathog 5:e1000662
12. Beste D, Hooper T, Stewart GS, Bonde B, Avignone-Rossa C, Bushell M, Wheeler PR, Klamt S, Kierzek AM, McFadden JJ (2007) GSMN-TB: a web-based genome scale network model of Mycobacterium tuberculosis metabolism. Genome Biol 8:R89
13. Beste DJ, Bonde B, Hawkins N, Ward JL, Beale MH, Noack S, Noh K, Kruger NJ, Ratcliffe RG, McFadden J (2011) 13 C metabolic fl ux analysis identi fi es an unusual route for pyruvate dissimilation in mycobacteria which requires isocitrate lyase and carbon dioxide fi xation. PLoS Pathog 7:e1002091
14. Tian J, Bryk R, Shi S, Erdjument-Bromage H, Tempst P, Nathan C (2005) Mycobacterium tuberculosis appears to lack alpha-ketoglutarate dehydrogenase and encodes pyruvate dehydrogenase in widely separated genes. Mol Microbiol 57:859-868
15. Tian J, Bryk R, Itoh M, Suematsu M, Nathan C (2005) Variant tricarboxylic acid cycle in Mycobacterium tuberculosis: identi fi cation of alpha-ketoglutarate decarboxylase. Proc Natl Acad Sci USA 102:10670-10675
16. de Carvalho LP, Zhao H, Dickinson CE, Arango NM, Lima CD, Fischer SM, Ouerfelli O, Nathan C, Rhee KY (2010) Activity-based metabolomic profiling of enzymatic function: identi fi cation of Rv1248c as a mycobacterial 2-hydroxy-3-oxoadipate synthase. Chem Biol 17:323-332
17. Wagner T, Bellinzoni M, Wehenkel A, O'Hare HM, Alzari PM (2011) Functional plasticity and allosteric regulation of alpha-ketoglutarate decarboxylase in central mycobacterial metabolism. Chem Biol 18:1011-1020
18. Watanabe S, Zimmermann M, Goodwin MB, Sauer U, Barry CE III, Boshoff HI (2011) Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS Pathog 7:e1002287
19. Kitano H (2007) Towards a theory of biological robustness. Mol Syst Biol 3:137
20. Hoskisson PA, Hobbs G (2005) Continuous culture-making a comeback? Microbiology 151:3153-3159
21. Boer VM, de Winde JH, Pronk JT, Piper MD (2003) The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. J Biol Chem 278:3265-3274
22. Boer VM, Tai SL, Vuralhan Z, Arifin Y, Walsh MC, Piper MD, de Winde JH, Pronk JT, Daran JM (2007) Transcriptional responses of Saccharomyces cerevisiae to preferred and nonpreferred nitrogen sources in glucose-limited chemostat cultures. FEMS Yeast Res 7:604-620
23. Hayes A, Zhang N, Wu J, Butler PR, Hauser NC, Hoheisel JD, Lim FL, Sharrocks AD, Oliver SG (2002) Hybridization array technology coupled with chemostat culture: tools to interrogate gene expression in Saccharomyces cerevisiae. Methods 26:281-290
24. James BW, Williams A, Marsh PD (2000) The physiology and pathogenicity of Mycobacterium tuberculosis grown under controlled conditions in a de fi ned medium. J Appl Microbiol 88:669-677
25. Bacon J, James BW, Wernisch L, Williams A, Morley KA, Hatch GJ, Mangan JA, Hinds J, Stoker NG, Butcher PD et al (2004) The in fl uence of reduced oxygen availability on pathogenicity and gene expression in Mycobacterium tuberculosis. Tuberculosis (Edinb) 84:205-217
26. Bacon J, Dover LG, Hatch KA, Zhang Y, Gomes JM, Kendall S, Wernisch L, Stoker NG, Butcher PD, Besra GS et al (2007) Lipid composition and transcriptional response of Mycobacterium tuberculosis grown under iron-limitation in continuous culture: identi fi cation of a novel wax ester. Microbiology 153:1435-1444
27. Jenkins C, Bacon J, Allnutt J, Hatch KA, Bose A, O'Sullivan DM, Arnold C, Gillespie SH, McHugh TD (2009) Enhanced heterogeneity of rpoB in Mycobacterium tuberculosis found at low pH. J Antimicrob Chemother 63:1118-1120
28. Daran-Lapujade P, Daran JM, Kotter P, Petit T, Piper MD, Pronk JT (2003) Comparative genotyping of the Saccharomyces cerevisiae laboratory strains S288C and CEN.PK113-7D using oligonucleotide microarrays. FEMS Yeast Res 4:259-269
29. Beste DJ, Peters J, Hooper T, Avignone-Rossa C, Bushell ME, McFadden J (2005) Compiling a molecular inventory for Mycobacterium bovis BCG at two growth rates: evidence for growth rate-mediated regulation of ribosome biosynthesis and lipid metabolism. J Bacteriol 187:1677-1684
30. Beste DJ, Espasa M, Bonde B, Kierzek AM, Stewart GR, McFadden J (2009) The genetic requirements for fast and slow growth in mycobacteria. PLoS One 4:e5349
31. Beste DJ, Laing E, Bonde B, Avignone-Rossa C, Bushell ME, McFadden JJ (2007) Transcriptomic analysis identi fi es growth rate modulation as a component of the adaptation of mycobacteria to survival inside the macrophage. J Bacteriol 189:3969-3976
32. Bumann D (2009) System-level analysis of Salmonella metabolism during infection. Curr Opin Microbiol 12:559-567
33. Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson BO (2009) Reconstruction of biochemical networks in microorganisms. Nat Rev Microbiol 7:129-143
34. Durot M, Bourguignon PY, Schachter V (2009) Genome-scale models of bacterial metabolism: reconstruction and applications. FEMS Microbiol Rev 33:164-190
35. Bettenbrock K, Fischer S, Kremling A, Jahreis K, Sauter T, Gilles ED (2006) A quantitative approach to catabolite repression in Escherichia coli. J Biol Chem 281:2578-2584
36. AbuOun M, Suthers PF, Jones GI, Carter BR, Saunders MP, Maranas CD, Woodward MJ, Anjum MF (2009) Genome scale reconstruction of a Salmonella metabolic model: comparison of similarity and differences with a commensal Escherichia coli strain. J Biol Chem 284:29480-29488
37. Duarte NC, Becker SA, Jamshidi N, Thiele I, Mo ML, Vo TD, Srivas R, Palsson BO (2007) Global reconstruction of the human metabolic network based on genomic and bibliomic data. Proc Natl Acad Sci USA 104:1777-1782
38. Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, Palsson BO (2007) A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol Syst Biol 3:121
39. Mo ML, Jamshidi N, Palsson BO (2007) A genome-scale, constraint-based approach to systems biology of human metabolism. Mol Biosyst 3:598-603
40. Oberhardt MA, Puchalka J, Fryer KE, Martins dos Santos VA, Papin JA (2008) Genome-scale metabolic network analysis of the opportunistic pathogen Pseudomonas aeruginosa PAO1. J Bacteriol 190:2790-2803
41. Thiele I, Jamshidi N, Fleming RM, Palsson BO (2009) Genome-scale reconstruction of Escherichia coli's transcriptional and translational machinery: a knowledge base, its mathematical formulation, and its functional characterization. PLoS Comput Biol 5:e1000312
42. Kim HU, Kim TY, Lee SY (2008) Metabolic fl ux analysis and metabolic engineering of microorganisms. Mol Biosyst 4:113-120
43. Wiechert W (2001) 13C metabolic fl ux analysis. Metab Eng 3:195-206
44. Boyle NR, Morgan JA (2009) Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst Biol 3:4
45. Raman K, Chandra N (2009) Flux balance analysis of biological systems: applications and challenges. Brief Bioinform 10:435-449
46. Varma A, Palsson BO (1994) Stoichiometric fl ux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110. Appl Environ Microbiol 60:3724-3731
47. Antoniewicz MR, Kraynie DF, Laffend LA, Gonzalez-Lergier J, Kelleher JK, Stephanopoulos G (2007) Metabolic fl ux analysis in a nonstationary system: fed-batch fermentation of a high yielding strain of E. coli producing 1, 3-propanediol. Metab Eng 9:277-292
48. Kayser A, Weber J, Hecht V, Rinas U (2005) Metabolic fl ux analysis of Escherichia coli in glucose-limited continuous culture. I. Growth-rate-dependent metabolic efficiency at steady state. Microbiology 151:693-706
49. Peng L, Arauzo-Bravo MJ, Shimizu K (2004) Metabolic fl ux analysis for a ppc mutant Escherichia coli based on 13C-labelling experiments together with enzyme activity assays and intracellular metabolite measurements. FEMS Microbiol Lett 235:17-23
50. Raman K, Rajagopalan P, Chandra N (2005) Flux balance analysis of mycolic acid pathway: targets for anti-tubercular drugs. PLoS Comput Biol 1:e46
51. Schuetz R, Kuepfer L, Sauer U (2007) Systematic evaluation of objective functions for predicting intracellular fl uxes in Escherichia coli. Mol Syst Biol 3:119
52. Jamshidi N, Palsson BO (2007) Investigating the metabolic capabilities of Mycobacterium tuberculosis H37Rv using the in silico strain iNJ661 and proposing alternative drug targets. BMC Syst Biol 1:26
53. Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth de fi ned by high density mutagenesis. Mol Microbiol 48:77-84
54. Feist AM, Palsson BO (2008) The growing scope of applications of genome-scale metabolic reconstructions using Escherichia coli. Nat Biotechnol 26:659-667
55. Sassetti CM, Rubin EJ (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100:12989-12994
56. Sohaskey CD, Wayne LG (2003) Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 185:7247-7256
57. Bordbar A, Lewis NE, Schellenberger J, Palsson BO, Jamshidi N (2010) Insight into human alveolar macrophage and M. tuberculosis interactions via metabolic reconstructions. Mol Syst Biol 6:422
58. Weber I, Fritz C, Ruttkowski S, Kreft A, Bange FC (2000) Anaerobic nitrate reductase (narGHJI) activity of Mycobacterium bovis BCG in vitro and its contribution to virulence in immunode fi cient mice. Mol Microbiol 35:1017-1025
59. Oberhardt MA, Palsson BO, Papin JA (2009) Applications of genome-scale metabolic reconstructions. Mol Syst Biol 5:320
60. Covert MW, Knight EM, Reed JL, Herrgard MJ, Palsson BO (2004) Integrating high-throughput and computational data elucidates bacterial networks. Nature 429:92-96
61. Cappelli G, Volpe E, Grassi M, Liseo B, Colizzi V, Mariani F (2006) profiling of Mycobacterium tuberculosis gene expression during human macrophage infection: upregulation of the alternative sigma factor G, a group of transcriptional regulators, and proteins with unknown function. Res Microbiol 157:445-455
62. Raju B, Hoshino Y, Belitskaya-Levy I, Dawson R, Ress S, Gold JA, Condos R, Pine R, Brown S, Nolan A et al (2008) Gene expression profiles of bronchoalveolar cells in pulmonary TB. Tuberculosis (Edinb) 88:39-51
63. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C et al (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198:693-704
64. Tailleux L, Waddell SJ, Pelizzola M, Mortellaro A, Withers M, Tanne A, Castagnoli PR, Gicquel B, Stoker NG, Butcher PD et al (2008) Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS One 3:e1403
65. Talaat AM, Lyons R, Howard ST, Johnston SA (2004) The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc Natl Acad Sci USA 101:4602-4607
66. Salmon K, Hung SP, Mekjian K, Baldi P, Hatfield GW, Gunsalus RP (2003) Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J Biol Chem 278:29837-29855
67. Kacser H, Burns JA (1995) The control of flux. Biochem Soc Trans 23:341-366
68. Heinrich R, Rapoport TA (1974) A linear steady-state treatment of enzymatic chains. Critique of the crossover theorem and a general procedure to identify interaction sites with an effector. Eur J Biochem 42:97-105
69. Patil KR, Nielsen J (2005) Uncovering transcriptional regulation of metabolism by using metabolic network topology. Proc Natl Acad Sci USA 102:2685-2689
70. Shlomi T, Cabili MN, Herrgard MJ, Palsson BO, Ruppin E (2008) Network-based prediction of human tissue-speci fi c metabolism. Nat Biotechnol 26:1003-1010
71. Colijn C, Brandes A, Zucker J, Lun DS, Weiner B, Farhat MR, Cheng TY, Moody DB, Murray M, Galagan JE (2009) Interpreting expression data with metabolic flux models: predicting Mycobacterium tuberculosis mycolic acid production. PLoS Comput Biol 5:e1000489
72. Boshoff HI, Myers TG, Copp BR, McNeil MR, Wilson MA, Barry CE III (2004) The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J Biol Chem 279:40174-40184
73. Shi L, Sohaskey CD, Pfeiffer C, Datta P, Parks M, McFadden J, North RJ, Gennaro ML (2010) Carbon flux rerouting during Mycobacterium tuberculosis growth arrest. Mol Microbiol 78:1199-1215
74. Bonde BK, Beste D, Laing E, Kierzek A, McFadden J (2011) Differential Producibility Analysis (DPA) of transcriptomic data with metabolic networks: deconstructing the metabolic response of M. tuberculosis. PLoS Comput Biol 7:e1002060
75. Garton NJ, Waddell SJ, Sherratt AL, Lee SM, Smith RJ, Senner C, Hinds J, Rajakumar K, Adegbola RA, Besra GS et al (2008) Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med 5:e75
76. de Carvalho LP, Fischer SM, Marrero J, Nathan C, Ehrt S, Rhee KY (2010) Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem Biol 17:1122-1131
77. Thomas ST, Vanderven BC, Sherman DR, Russell DG, Sampson NS (2011) Pathway profiling in Mycobacterium tuberculosis: elucidation of cholesterol-derived catabolite and enzymes that catalyze its metabolism. J Biol Chem 286:43668-43678
78. Marrero J, Rhee KY, Schnappinger D, Pethe K, Ehrt S (2010) Gluconeogenic carbon fl ow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection. Proc Natl Acad Sci USA 107:9819-9824
79. Zamboni N, Fendt SM, Ruhl M, Sauer U (2009) (13)C-based metabolic flux analysis. Nat Protoc 4:878-892
80. Munoz-Elias EJ, McKinney JD (2006) Carbon metabolism of intracellular bacteria. Cell Microbiol 8:10-22