GarA is an essential regulator of metabolism in mycobacterium tuberculosis

Molecular Microbiology

Volumn 90, Issue 2, 2013, Pages 356-366

  Ventura, Marcello ^a   Rieck, Barbara ^b   Boldrin, Francesca ^a   Degiacomi, Giulia ^a   Bellinzoni, Marco ^c   Barilone, Nathalie ^c   Alzaidi, Faisal ^b   Alzari, Pedro M ^c   Manganelli, Riccardo ^a   O'Hare, Helen M ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLUTAMIC ACID; OXOGLUTARATE DEHYDROGENASE; PROTEIN GARA; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CITRIC ACID CYCLE; CONTROLLED STUDY; GARA GENE; GENE DELETION; IN VITRO STUDY; METABOLIC REGULATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS;

CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

BACTERIAL PROTEINS; CELL LINE, TUMOR; CITRIC ACID CYCLE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GLUTAMIC ACID; HUMANS; KETOGLUTARIC ACIDS; MACROPHAGES; MUTAGENESIS, SITE-DIRECTED; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; PHOSPHORYLATION; RECOMBINANT PROTEINS;

EID: 84885388067     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12368     Document Type: Article

References (36)

1. Argyrou, A., and Blanchard, J.S. (2001) Mycobacterium tuberculosis lipoamide dehydrogenase is encoded by Rv0462 and not by the lpdA or lpdB genes. Biochemistry 40: 11353-11363.
2. Bange, F.C., Collins, F.M., and Jacobs, W.R., Jr. (1999) Survival of mice infected with Mycobacterium smegmatis containing large DNA fragments from Mycobacterium tuberculosis. Tuber Lung Dis 79: 171-180.
3. Barthe, P., Roumestand, C., Canova, M.J., Kremer, L., Hurard, C., Molle, V., and Cohen-Gonsaud, M. (2009) Dynamic and structural characterization of a bacterial FHA protein reveals a new autoinhibition mechanism. Structure 17: 568-578.
4. Belanger, A.E., and Hatfull, G.F. (1999) Exponential-phase glycogen recycling is essential for growth of Mycobacterium smegmatis. J Bacteriol 181: 6670-6678.
5. Beste, D.J., Hooper, T., Stewart, G., Bonde, B., Avignone-Rossa, C., Bushell, M.E., etal. (2007) GSMN-TB: a web-based genome-scale network model of Mycobacterium tuberculosis metabolism. Genome Biol 8: R89.
6. Boldrin, F., Casonato, S., Dainese, E., Sala, C., Dhar, N., Palu, G., etal. (2010) Development of a repressible mycobacterial promoter system based on two transcriptional repressors. Nucleic Acids Res 38: e134.
7. Bunik, V.I., and Fernie, A.R. (2009) Metabolic control exerted by the 2-oxoglutarate dehydrogenase reaction: a cross-kingdom comparison of the crossroad between energy production and nitrogen assimilation. Biochem J 422: 405-421.
8. Burkovski, A. (2007) Nitrogen control in Corynebacterium glutamicum: proteins, mechanisms, signals. J Microbiol Biotechnol 17: 187-194.
9. Carroll, P., Waddell, S.J., Butcher, P.D., and Parish, T. (2011) Methionine sulfoximine resistance in Mycobacterium tuberculosis is due to a single nucleotide deletion resulting in increased expression of the major glutamine synthetase, GlnA1. Microb Drug Resist 17: 351-355.
10. Cowley, S., Ko, M., Pick, N., Chow, R., Downing, K.J., Gordhan, B.G., etal. (2004) The Mycobacterium tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Mol Microbiol 52: 1691-1702.
11. Durocher, D., Henckel, J., Fersht, A.R., and Jackson, S.P. (1999) The FHA domain is a modular phosphopeptide recognition motif. Mol Cell 4: 387-394.
12. England, P., Wehenkel, A., Martins, S., Hoos, S., Andre-Leroux, G., Villarino, A., and Alzari, P.M. (2009) The FHA-containing protein GarA acts as a phosphorylation-dependent molecular switch in mycobacterial signaling. FEBS Lett 583: 301-307.
13. Gould, T.A., van de Langemheen, H., Munoz-Elias, E.J., McKinney, J.D., and Sacchettini, J.C. (2006) Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis. Mol Microbiol 61: 940-947.
14. Griffin, J.E., Gawronski, J.D., Dejesus, M.A., Ioerger, T.R., Akerley, B.J., and Sassetti, C.M. (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7: e1002251.
15. Gunka, K., and Commichau, F.M. (2012) Control of glutamate homeostasis in Bacillus subtilis: a complex interplay between ammonium assimilation, glutamate biosynthesis and degradation. Mol Microbiol 85: 213-224.
16. Harth, G., and Horwitz, M.A. (1999) An inhibitor of exported Mycobacterium tuberculosis glutamine synthetase selectively blocks the growth of pathogenic mycobacteria in axenic culture and in human monocytes: extracellular proteins as potential novel drug targets. J Exp Med 189: 1425-1436.
17. Harth, G., and Horwitz, M.A. (2003) Inhibition of Mycobacterium tuberculosis glutamine synthetase as a novel antibiotic strategy against tuberculosis: demonstration of efficacy in vivo. Infect Immun 71: 456-464.
18. Jenkins, V.A., Barton, G.R., Robertson, B.D., and Williams, K.J. (2013) Genome wide analysis of the complete GlnR nitrogen-response regulon in Mycobacterium smegmatis. BMC Genomics 14: 301.
19. Lee, W., Vanderven, B.C., Fahey, R.J., and Russell, D.G. (2013) Intracellular Mycobacterium tuberculosis exploits host-derived fatty acids to limit metabolic stress. J Biol Chem 288: 6788-6800.
20. Lyon, R.H., Hall, W.H., and Costas-Martinez, C. (1974) Effect of L-asparagine on growth of Mycobacterium tuberculosis and on utilization of other amino acids. J Bacteriol 117: 151-156.
21. McKinney, J.D., Honer zu Bentrup, K., Munoz-Elias, E.J., Miczak, A., Chen, B., Chan, W.T., etal. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738.
22. Manganelli, R., Voskuil, M.I., Schoolnik, G.K., and Smith, I. (2001) The Mycobacterium tuberculosis ECF sigma factor SigE: role in global gene expression and survival in macrophages. Mol Microbiol 41: 423-437.
23. Marrero, J., Rhee, K.Y., Schnappinger, D., Pethe, K., and Ehrt, S. (2010) Gluconeogenic carbon flow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection. Proc Natl Acad Sci USA 107: 9819-9824.
24. Middlebrook, G., Cohn, M.L., and Schaefer, W.B. (1954) Studies on isoniazid and tubercle bacilli. III. The isolation, drug-susceptibility, and catalase-testing of tubercle bacilli from isoniazid-treated patients. Am Rev Tuberc 70: 852-872.
25. Munoz-Elias, E.J., Upton, A.M., Cherian, J., and McKinney, J.D. (2006) Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol Microbiol 60: 1109-1122.
26. Niebisch, A., Kabus, A., Schultz, C., Weil, B., and Bott, M. (2006) Corynebacterial protein kinase G controls 2-oxoglutarate dehydrogenase activity via the phosphorylation status of the OdhI protein. J Biol Chem 281: 12300-12307.
27. Nott, T.J., Kelly, G., Stach, L., Li, J., Westcott, S., Patel, D., etal. (2009) An intramolecular switch regulates phosphoindependent FHA domain interactions in Mycobacterium tuberculosis. Sci Signal 2: ra12.
28. O'Hare, H.M., Duran, R., Cervenansky, C., Bellinzoni, M., Wehenkel, A.M., Pritsch, O., etal. (2008) Regulation of glutamate metabolism by protein kinases in mycobacteria. Mol Microbiol 70: 1408-1423.
29. Parish, T., and Stoker, N.G. (2000) Use of a flexible cassette method to generate a double unmarked Mycobacterium tuberculosis tlyA plcABC mutant by gene replacement. Microbiology 146 (Part 8): 1969-1975.
30. Reuther, J., and Wohlleben, W. (2007) Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 12: 139-146.
31. Sassetti, C.M., Boyd, D.H., and Rubin, E.J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
32. Tian, J., Bryk, R., Shi, S., Erdjument-Bromage, H., Tempst, P., and Nathan, C. (2005) Mycobacterium tuberculosis appears to lack alpha-ketoglutarate dehydrogenase and encodes pyruvate dehydrogenase in widely separated genes. Mol Microbiol 57: 859-868.
33. Tullius, M.V., Harth, G., and Horwitz, M.A. (2003) Glutamine synthetase GlnA1 is essential for growth of Mycobacterium tuberculosis in human THP-1 macrophages and guinea pigs. Infect Immun 71: 3927-3936.
34. Upton, A.M., and McKinney, J.D. (2007) Role of the methylcitrate cycle in propionate metabolism and detoxification in Mycobacterium smegmatis. Microbiology 153: 3973-3982.
35. Villarino, A., Duran, R., Wehenkel, A., Fernandez, P., England, P., Brodin, P., etal. (2005) Proteomic identifica tion of M. tuberculosis protein kinase substrates: PknB recruits GarA, a FHA domain-containing protein, through activation loop-mediated interactions. J Mol Biol 350: 953-963.
36. Wagner, T., Bellinzoni, M., Wehenkel, A., O'Hare, H.M., and Alzari, P.M. (2011) Functional plasticity and allosteric regulation of alpha-ketoglutarate decarboxylase in central mycobacterial metabolism. Chem Biol 18: 1011-1020.