Gluconeogenic carbon flow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 21, 2010, Pages 9819-9824

  Marrero, Joeli ^a   Rhee, Kyu Y ^a   Schnappinger, Dirk ^a   Pethe, Kevin ^b   Ehrt, Sabine ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

Author keywords

Carbon metabolism; Gluconeogenesis; Metabolomics; Microbial pathogenesis; Phosphoenolpyruvate carboxykinase

Indexed keywords

CARBON 13; FATTY ACID; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP);

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; BIOSYNTHESIS; CARBON SOURCE; CITRIC ACID CYCLE; GLUCONEOGENESIS; IMMUNE RESPONSE; LUNG TUBERCULOSIS; MACROPHAGE; METABOLITE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

ANIMALS; CARBON; CITRIC ACID CYCLE; FATTY ACIDS; GLUCONEOGENESIS; MACROPHAGES; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); TUBERCULOSIS; VIRUS REPLICATION;

BACTERIA (MICROORGANISMS); MURINAE; MUS; MYCOBACTERIUM TUBERCULOSIS;

EID: 77953105101     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1000715107     Document Type: Article

References (38)

1. Harries AD, Dye C (2006) Tuberculosis. Ann Trop Med Parasitol 100:415-431.
2. Fischbach MA, Walsh CT (2009) Antibiotics for emerging pathogens. Science 325: 1089-1093.
3. Boshoff HI, Barry CE, 3rd (2005) Tuberculosis-metabolism and respiration in the absence of growth. Nat Rev Microbiol 3:70-80.
4. Muñoz-Elías EJ, McKinney JD (2006) Carbon metabolism of intracellular bacteria. Cell Microbiol 8:10-22.
5. Sauer U, Eikmanns BJ (2005) The PEP-pyruvate-oxaloacetate node as the switch point for carbon flux distribution in bacteria. FEMS Microbiol Rev 29:765-794.
6. Muñoz-Elías 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.
7. Bloch H, Segal W (1956) Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J Bacteriol 72:132-141.
8. Cole ST, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
9. Schnappinger D, et al. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: Insights into the phagosomal environment. J Exp Med 198:693-704.
10. Dubnau E, Smith I (2003) Mycobacterium tuberculosis gene expression in macrophages. Microbes Infect 5:629-637.
11. Timm J, 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 USA 100:14321-14326.
12. Gould TA, van de Langemheen H, Muñoz-Elías EJ, McKinney JD, Sacchettini JC (2006) Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis. Mol Microbiol 61:940-947.
13. Muñoz-Elías 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.
14. Upton AM, McKinney JD (2007) Role of the methylcitrate cycle in propionate metabolism and detoxification in Mycobacterium smegmatis. Microbiology 153: 3973-3982.
15. Matte A, Tari LW, Goldie H, Delbaere LT (1997) Structure and mechanism of phosphoenolpyruvate carboxykinase. J Biol Chem 272:8105-8108.
16. Hanson RW (2009) Thematic minireview series: A perspective on the biology of phosphoenolpyruvate carboxykinase 55 years after its discovery. J Biol Chem 284: 27021-27023.
17. Mukhopadhyay B, Concar EM, Wolfe RS (2001) A GTP-dependent vertebrate-type phosphoenolpyruvate carboxykinase from Mycobacterium smegmatis. J Biol Chem 276:16137-16145.
18. Collins DM, et al. (2002) Production of avirulent mutants of Mycobacterium bovis with vaccine properties by the use of illegitimate recombination and screening of stationary-phase cultures. Microbiology 148:3019-3027.
19. Liu KY, Yu JZ, Russell DG (2003) pckA-deficient Mycobacterium bovis BCG shows attenuated virulence in mice and in macrophages. Microbiology 149:1829-1835.
20. Klotzsche M, Ehrt S, Schnappinger D (2009) Improved tetracycline repressors for gene silencing in mycobacteria. Nucleic Acids Res 37:1778-1788.
21. Ehrt S, et al. (2005) Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res 33:e21.
22. Rej R (1985) Oxaloacetate, UV-method. Methods of Enzymatic Analysis, ed Bergmeyer HU (Verlag Chemie, Weinheim), 3rd Ed, Vol VII, pp 59-67.
23. Petersen S, et al. (2001) Metabolic consequences of altered phosphoenolpyruvate carboxykinase activity in Corynebacterium glutamicum reveal anaplerotic regulation mechanisms in vivo. Metab Eng 3:344-361.
24. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34:257-267.
25. 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. (Pubitemid 129621653)
26. Domenech P, Reed MB (2009) Rapid and spontaneous loss of phthiocerol dimycocerosate (PDIM) from Mycobacterium tuberculosis grown in vitro: Implications for virulence studies. Microbiology 155:3532-3543.
27. Kana BD, et al. (2008) The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol Microbiol 67:672-684.
28. Manjunatha UH, et al. (2006) Identification of a nitroimidazo-oxazine- specific protein involved in PA-824 resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103:431-436.
29. Gandotra S, Schnappinger D, Monteleone M, Hillen W, Ehrt S (2007) In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 13:1515-1520.
30. Savvi S, 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 190:3886-3895.
31. Gengenbacher M, Rao SP, Pethe K, Dick T (2009) Nutrient-starved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability. Microbiology 156:81-87.
32. Barry CE, 3rd (2001) Interpreting cell wall 'virulence factors' of Mycobacterium tuberculosis. Trends Microbiol 9:237-241.
33. Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64: 29-63.
34. Brauer MJ, et al. (2006) Conservation of the metabolomic response to starvation across two divergent microbes. Proc Natl Acad Sci USA 103:19302-19307.
35. Bardarov S, et al. (1997) Conditionally replicating mycobacteriophages: A system for transposon delivery to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 94: 10961-10966.
36. 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.
37. Vandal OH, Nathan CF, Ehrt S (2009) Acid resistance in Mycobacterium tuberculosis. J Bacteriol 191:4714-4721.
38. Pesek JJ, Matyska MT, Fischer SM, Sana TR (2008) Analysis of hydrophilic metabolites by high-performance liquid chromatography-mass spectrometry using a silica hydride-based stationary phase. J Chromatogr A 1204:48-55.