Transcriptional regulation of fatty acid biosynthesis in mycobacteria

Molecular Microbiology

Volumn 89, Issue 2, 2013, Pages 372-387

  Mondino, S ^a   Gago, G ^a   Gramajo, H ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHOSPHOPANTETHEINYLTRANSFERASE; FATTY ACID; FATTY ACID SYNTHASE; MYCOLIC ACID; PROTEIN FASR; TRANSCRIPTION FACTOR; TRANSFERASE; UNCLASSIFIED DRUG;

ACPS GENE; ARTICLE; BACTERIAL VIABILITY; CONTROLLED STUDY; FAS GENE; FATTY ACID SYNTHESIS; GENE; GENE EXPRESSION; GENE FUSION; GENE SEQUENCE; IN VITRO STUDY; MUTANT; MYCOBACTERIUM; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERATOR GENE; OPERON; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; BINDING SITES; FATTY ACID SYNTHASES; FATTY ACIDS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; LIPID METABOLISM; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; OPERON; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

CORYNEBACTERINEAE; MYCOBACTERIUM SP.;

EID: 84880137152     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12282     Document Type: Article

References (63)

1. Arabolaza, A., D'Angelo, M., Comba, S., and Gramajo, H. (2010) FasR, a novel class of transcriptional regulator, governs the activation of fatty acid biosynthesis genes in Streptomyces coelicolor. Mol Microbiol 78: 47-63.
2. Bacon, J., and Marsh, P.D. (2007) Transcriptional responses of Mycobacterium tuberculosis exposed to adverse conditions in vitro. Curr Mol Med 7: 277-286.
3. Bailey, T.L., and Elkan, C. (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3: 21-29.
4. Bailey, T.L., and Gribskov, M. (1998) Methods and statistics for combining motif match scores. J Comput Biol 5: 211-221.
5. Bhatt, A., Fujiwara, N., Bhatt, K., Gurcha, S.S., Kremer, L., Chen, B., etal. (2007a) Deletion of kasB in Mycobacterium tuberculosis causes loss of acid-fastness and subclinical latent tuberculosis in immunocompetent mice. Proc Natl Acad Sci USA 104: 5157-5162.
6. Bhatt, A., Molle, V., Besra, G.S., Jacobs, W.R., Jr, and Kremer, L. (2007b) The Mycobacterium tuberculosis FAS-II condensing enzymes: their role in mycolic acid biosynthesis, acid-fastness, pathogenesis and in future drug development. Mol Microbiol 64: 1442-1454.
7. Bloch, K. (1975) Fatty acid synthases from Mycobacterium phlei. Methods Enzymol 35: 84-90.
8. 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.
9. Brennan, P.J., and Crick, D.C. (2007) The cell-wall core of Mycobacterium tuberculosis in the context of drug discovery. Curr Top Med Chem 7: 475-488.
10. Brennan, P.J., and Nikaido, H. (1995) The envelope of mycobacteria. Annu Rev Biochem 64: 29-63.
11. Butala, M., Zgur-Bertok, D., and Busby, S.J. (2009) The bacterial LexA transcriptional repressor. Cell Mol Life Sci 66: 82-93.
12. Campbell, J.W., and Cronan, J.E., Jr (2001) Escherichia coli FadR positively regulates transcription of the fabB fatty acid biosynthetic gene. J Bacteriol 183: 5982-5990.
13. Chalut, C., Botella, L., de Sousa-D'Auria, C., Houssin, C., and Guilhot, C. (2006) The nonredundant roles of two 4′-phosphopantetheinyl transferases in vital processes of Mycobacteria. Proc Natl Acad Sci USA 103: 8511-8516.
14. Connell, N.D. (1994) Mycobacterium: isolation, maintenance, transformation, and mutant selection. Methods Cell Biol 45: 107-125.
15. Daffe, M. (2008) The global architecture of the mycobacteria cell envelope. In The Mycobacterial Cell Envelope. Daffe, M., and Reyrat, J.M. (eds). Washington, DC: ASM Press, pp. 3-12.
16. Daffe, M., and Draper, P. (1998) The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39: 131-203.
17. Daniel, J., Deb, C., Dubey, V., Sirakova, T., Abomoelak, B., Morbidoni, H., and Kolattukudy, P. (2004) Induction of a novel class of diacylglycerol acyltransferases and triacylglycerol accumulation in Mycobacterium tuberculosis as it goes into a dormancy-like state in culture. J Bacteriol 186: 5017-5030.
18. Deb, C., Lee, C.M., Dubey, V.S., Daniel, J., Abomoelak, B., Sirakova, T.D., etal. (2009) A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS ONE 4: e6077.
19. DiRusso, C.C., Heimert, T.L., and Metzger, A.K. (1992) Characterization of FadR, a global transcriptional regulator of fatty acid metabolism in Escherichia coli. Interaction with the fadB promoter is prevented by long chain fatty acyl coenzyme A. J Biol Chem 267: 8685-8691.
20. Dubnau, E., Chan, J., Raynaud, C., Mohan, V.P., Laneelle, M.A., Yu, K., etal. (2000) Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol Microbiol 36: 630-637.
21. Dussurget, O., Timm, J., Gomez, M., Gold, B., Yu, S., Sabol, S.Z., etal. (1999) Transcriptional control of the iron-responsive fxbA gene by the mycobacterial regulator IdeR. J Bacteriol 181: 3402-3408.
22. Feng, Y., and Cronan, J.E. (2011) Complex binding of the FabR repressor of bacterial unsaturated fatty acid biosynthesis to its cognate promoters. Mol Microbiol 80: 195-218.
23. Glickman, M.S., Cox, J.S., and Jacobs, W.R., Jr (2000) A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol Cell 5: 717-727.
24. 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.
25. Grkovic, S., Brown, M.H., Roberts, N.J., Paulsen, I.T., and Skurray, R.A. (1998) QacR is a repressor protein that regulates expression of the Staphylococcus aureus multidrug efflux pump QacA. J Biol Chem 273: 18665-18673.
26. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
27. Henry, M.F., and Cronan, J.E., Jr (1991) Escherichia coli transcription factor that both activates fatty acid synthesis and represses fatty acid degradation. J Mol Biol 222: 843-849.
28. Higo, A., Horinouchi, S., and Ohnishi, Y. (2011) Strict regulation of morphological differentiation and secondary metabolism by a positive feedback loop between two global regulators AdpA and BldA in Streptomyces griseus. Mol Microbiol 81: 1607-1622.
29. Jerga, A., and Rock, C.O. (2009) Acyl-Acyl carrier protein regulates transcription of fatty acid biosynthetic genes via the FabT repressor in Streptococcus pneumoniae. J Biol Chem 284: 15364-15368.
30. Jourlin-Castelli, C., Mani, N., Nakano, M.M., and Sonenshein, A.L. (2000) CcpC, a novel regulator of the LysR family required for glucose repression of the citB gene in Bacillus subtilis. J Mol Biol 295: 865-878.
31. Kaur, D., Guerin, M.E., Skovierova, H., Brennan, P.J., and Jackson, M. (2009) Biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv Appl Microbiol 69: 23-78.
32. Kremer, L., Douglas, J.D., Baulard, A.R., Morehouse, C., Guy, M.R., Alland, D., etal. (2000) Thiolactomycin and related analogues as novel anti-mycobacterial agents targeting KasA and KasB condensing enzymes in Mycobacterium tuberculosis. J Biol Chem 275: 16857-16864.
33. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
34. Lambalot, R.H., Gehring, A.M., Flugel, R.S., Zuber, P., LaCelle, M., Marahiel, M.A., etal. (1996) A new enzyme superfamily - the phosphopantetheinyl transferases. Chem Biol 3: 923-936.
35. Lu, Y.J., and Rock, C.O. (2006) Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol Microbiol 59: 551-566.
36. 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.
37. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. Molle, V., Brown, A.K., Besra, G.S., Cozzone, A.J., and Kremer, L. (2006) The condensing activities of the Mycobacterium tuberculosis type II fatty acid synthase are differentially regulated by phosphorylation. J Biol Chem 281: 30094-30103.
39. Munoz-Elias, E.J., and McKinney, J.D. (2006) Carbon metabolism of intracellular bacteria. Cell Microbiol 8: 10-22.
40. Nickel, J., Irzik, K., van Ooyen, J., and Eggeling, L. (2010) The TetR-type transcriptional regulator FasR of Corynebacterium glutamicum controls genes of lipid synthesis during growth on acetate. Mol Microbiol 78: 253-265.
41. Orth, P., Schnappinger, D., Hillen, W., Saenger, W., and Hinrichs, W. (2000) Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat Struct Biol 7: 215-219.
42. Pelicic, V., Jackson, M., Reyrat, J.M., Jacobs, W.R., Jr, Gicquel, B., and Guilhot, C. (1997) Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 94: 10955-10960.
43. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
44. Ramos, J.L., Martinez-Bueno, M., Molina-Henares, A.J., Teran, W., Watanabe, K., Zhang, X., etal. (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69: 326-356.
45. Rao, V., Gao, F., Chen, B., Jacobs, W.R., Jr, and Glickman, M.S. (2006) Trans-cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis-induced inflammation and virulence. J Clin Invest 116: 1660-1667.
46. Salzman, V., Mondino, S., Sala, C., Cole, S.T., Gago, G., and Gramajo, H. (2010) Transcriptional regulation of lipid homeostasis in mycobacteria. Mol Microbiol 78: 64-77.
47. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
48. Schnappinger, D., Ehrt, S., Voskuil, M.I., Liu, Y., Mangan, J.A., Monahan, I.M., etal. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198: 693-704.
49. Schujman, G.E., Paoletti, L., Grossman, A.D., and de Mendoza, D. (2003) FapR, a bacterial transcription factor involved in global regulation of membrane lipid biosynthesis. Dev Cell 4: 663-672.
50. Schujman, G.E., Guerin, M., Buschiazzo, A., Schaeffer, F., Llarrull, L.I., Reh, G., etal. (2006) Structural basis of lipid biosynthesis regulation in Gram-positive bacteria. EMBO J 25: 4074-4083.
51. Schweizer, E., and Hofmann, J. (2004) Microbial type I fatty acid synthases (FAS): major players in a network of cellular FAS systems. Microbiol Mol Biol Rev 68: 501-517.
52. Simons, R.W., Egan, P.A., Chute, H.T., and Nunn, W.D. (1980) Regulation of fatty acid degradation in Escherichia coli: isolation and characterization of strains bearing insertion and temperature-sensitive mutations in gene fadR. J Bacteriol 142: 621-632.
53. Slama, N., Leiba, J., Eynard, N., Daffe, M., Kremer, L., Quemard, A., and Molle, V. (2011) Negative regulation by Ser/Thr phosphorylation of HadAB and HadBC dehydratases from Mycobacterium tuberculosis type II fatty acid synthase system. Biochem Biophys Res Commun 412: 401-406.
54. Snapper, S.B., Melton, R.E., Mustafa, S., Kieser, T., and Jacobs, W.R., Jr (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4: 1911-1919.
55. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
56. Takayama, K., Wang, C., and Besra, G.S. (2005) Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin Microbiol Rev 18: 81-101.
57. Veyron-Churlet, R., Molle, V., Taylor, R.C., Brown, A.K., Besra, G.S., Zanella-Cleon, I., etal. (2009) The Mycobacterium tuberculosis beta-ketoacyl-acyl carrier protein synthase III activity is inhibited by phosphorylation on a single threonine residue. J Biol Chem 284: 6414-6424.
58. Walsh, C.T., Gehring, A.M., Weinreb, P.H., Quadri, L.E., and Flugel, R.S. (1997) Post-translational modification of polyketide and nonribosomal peptide synthases. Curr Opin Chem Biol 1: 309-315.
59. Zhang, Y. (2005) The magic bullets and tuberculosis drug targets. Annu Rev Pharmacol Toxicol 45: 529-564.
60. Zhang, Y.M., and Rock, C.O. (2009) Transcriptional regulation in bacterial membrane lipid synthesis. J Lipid Res 50: S115-S119.
61. Zhang, Y.M., White, S.W., and Rock, C.O. (2006) Inhibiting bacterial fatty acid synthesis. J Biol Chem 281: 17541-17544.
62. Zhu, K., Zhang, Y.M., and Rock, C.O. (2009) Transcriptional regulation of membrane lipid homeostasis in Escherichia coli. J Biol Chem 284: 34880-34888.
63. Zimhony, O., Vilcheze, C., and Jacobs, W.R., Jr (2004) Characterization of Mycobacterium smegmatis expressing the Mycobacterium tuberculosis fatty acid synthase I (fas1) gene. J Bacteriol 186: 4051-4055.