Characterization of the transcriptional regulator Rv3124 of Mycobacterium tuberculosis identifies it as a positive regulator of molybdopterin biosynthesis and defines the functional consequences of a non-synonymous SNP in the Mycobacterium bovis BCG orthologue

Microbiology

Volumn 156, Issue 7, 2010, Pages 2112-2123

  Lopez, Pablo Mendoza ^a,b   Golby, Paul ^b   Wooff, Esen ^b   Garcia, Javier Nunez ^b   Garcia Pelayo, M Carmen ^b   Conlon, Kevin ^e   Camacho, Ana Gema ^a   Hewinson, R Glyn ^b   Polaina, Julio ^c   García, Antonio Suárez ^d   Gordon, Stephen V ^b,e  

^a VIRCELL S L   (Spain)

^b TB Research Group   (United Kingdom)

^c INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^d Centro de Investigacion Biomedica   (Spain)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BCG VACCINE; GLUTAMIC ACID; GLYCINE; MOLYBDOPTERIN; PROTEIN MOAR1; PROTEIN RV3124; TRANSCRIPTOME; UNCLASSIFIED DRUG; COENZYME; METALLOPROTEIN; MOLYBDENUM COFACTOR; PTERIDINE DERIVATIVE; TRANSCRIPTION FACTOR;

ALPHA HELIX; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOLOGICAL MONITORING; BIOSYNTHESIS; CONTROLLED STUDY; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENE OVEREXPRESSION; GENE SEQUENCE; MICROARRAY ANALYSIS; MODEL; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SINGLE NUCLEOTIDE POLYMORPHISM; SITE DIRECTED MUTAGENESIS; TETRATRICOPEPTIDE REPEAT; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; CHEMISTRY; COENZYME; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN MOTIF;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; COENZYMES; GENE EXPRESSION REGULATION, BACTERIAL; METALLOPROTEINS; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PTERIDINES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM BOVIS BCG; MYCOBACTERIUM TUBERCULOSIS;

EID: 77954579484     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.037200-0     Document Type: Article

References (39)

1. Alderwick, L. J., Molle, V., Kremer, L., Cozzone, A. J., Dafforn, T. R., Besra, G. S. & Futterer, K. (2006). Molecular structure of EmbR, a response element of Ser/Thr kinase signaling in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 103, 2558-2563. (Pubitemid 43306588)
2. Baker, K. P. & Boxer, D. H. (1991). Regulation of the chlA locus of Escherichia coli K12: involvement of molybdenum cofactor. Mol Microbiol 5, 901-907.
3. Bardarov, S., Bardarov, S., Jr, Pavelka, M. S., Jr, Sambandamurthy, V., Larsen, M., Tufariello, J., Chan, J., Hatfull, G. & Jacobs, W. R., Jr (2002). Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148, 3007-3017. (Pubitemid 35243700)
4. Behr, M. A., Wilson, M. A., Gill, W. P., Salamon, H., Schoolnik, G. K., Rane, S. & Small, P. M. (1999). Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284, 1520-1523. (Pubitemid 129524431)
5. Behr, M. A., Schroeder, B. G., Brinkman, J. N., Slayden, R. A. & Barry, C. E., III (2000). A point mutation in the mma3 gene is responsible for impaired methoxymycolic acid production in Mycobacterium bovis BCG strains obtained after 1927. J Bacteriol 182, 3394-3399.
6. Belanger, A. E., Besra, G. S., Ford, M. E., Mikusova, K., Belisle, J. T., Brennan, P. J. & Inamine, J. M. (1996). The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol. Proc Natl Acad Sci U S A 93, 11919-11924. (Pubitemid 26347224)
7. Belley, A., Alexander, D., Di Pietrantonio, T., Girard, M., Jones, J., Schurr, E., Liu, J., Sherman, D. R. & Behr, M. A. (2004). Impact of methoxymycolic acid production by Mycobacterium bovis BCG vaccines. Infect Immun 72, 2803-2809. (Pubitemid 38542408)
8. Brosch, R., Gordon, S. V., Garnier, T., Eiglmeier, K., Frigui, W., Valenti, P., Dos Santos, S., Duthoy, S., Lacroix, C. & other authors (2007). Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci U S A 104, 5596-5601. (Pubitemid 47175726)
9. Bryson, K., McGuffin, L. J., Marsden, R. L., Ward, J. J., Sodhi, J. S. & Jones, D. T. (2005). Protein structure prediction servers at University College London. Nucleic Acids Res 33, W36-W38.
10. Calmette, A. (1927). La Vaccination Preventive Contre la Tuberculose. Paris: Masson et cie.
11. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S. & other authors (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544. (Pubitemid 28319235)
12. D'Andrea, L. D. & Regan, L. (2003). TPR proteins: the versatile helix. Trends Biochem Sci 28, 655-662.
13. Dussurget, O., Timm, J., Gomez, M., Gold, B., Yu, S., Sabol, S. Z., Holmes, R. K., Jacobs, W. R., Jr & Smith, I. (1999). Transcriptional control of the iron-responsive fxbA gene by the mycobacterial regulator IdeR. J Bacteriol 181, 3402-3408.
14. Garcia Pelayo, M. C., Uplekar, S., Keniry, A., Mendoza Lopez, P., Garnier, T., Nunez Garcia, J., Boschiroli, L., Zhou, X., Parkhill, J. & other authors (2009). A comprehensive survey of single nucleotide polymorphisms (SNPs) across Mycobacterium bovis strains and M. bovis BCG vaccine strains refines the genealogy and defines a minimal set of SNPs that separate virulent M. bovis strains and M. bovis BCG strains. Infect Immun 77, 2230-2238.
15. Golby, P., Hatch, K. A., Bacon, J., Cooney, R., Riley, P., Allnutt, J., Hinds, J., Nunez, J., Marsh, P. D. & other authors (2007). Comparative transcriptomics reveals key gene expression differences between the human and bovine pathogens of the Mycobacterium tuberculosis complex. Microbiology 153, 3323-3336.
16. Golby, P., Nunez, J., Cockle, P. J., Ewer, K., Logan, K., Hogarth, P., Vordermeier, H. M., Hinds, J., Hewinson, R. G. & Gordon, S. V. (2008). Characterization of two in vivo-expressed methyltransferases of the Mycobacterium tuberculosis complex: antigenicity and genetic regulation. Microbiology 154, 1059-1067.
17. Gordon, S. V., Brosch, R., Billault, A., Garnier, T., Eiglmeier, K. & Cole, S. T. (1999). Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays. Mol Microbiol 32, 643-655.
18. Hunt, D. M., Saldanha, J. W., Brennan, J. F., Benjamin, P., Strom, M., Cole, J. A., Spreadbury, C. L. & Buxton, R. S. (2008). Single nucleotide polymorphisms that cause structural changes in the cyclic AMP receptor protein transcriptional regulator of the tuberculosis vaccine strain Mycobacterium bovis BCG alter global gene expression without attenuating growth. Infect Immun 76, 2227-2234.
19. Jones, D. T. (1999). Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292, 195-202. (Pubitemid 29435759)
20. Keating, L. A., Wheeler, P. R., Mansoor, H., Inwald, J. K., Dale, J., Hewinson, R. G. & Gordon, S. V. (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. (Pubitemid 40461496)
21. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L. & Schwede, T. (2009). The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 37, D387-D392.
22. Lewis, K. N., Liao, R., Guinn, K. M., Hickey, M. J., Smith, S., Behr, M. A. & Sherman, D. R. (2003). Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guérin attenuation. J Infect Dis 187, 117-123. (Pubitemid 36034479)
23. Mahairas, G. G., Sabo, P. J., Hickey, M. J., Singh, D. C. & Stover, C. K. (1996). Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 178, 1274-1282.
24. Martinez-Hackert, E. & Stock, A. M. (1997a). The DNA-binding domain of OmpR: crystal structures of a winged helix transcription factor. Structure 5, 109-124. (Pubitemid 27102862)
25. Martinez-Hackert, E. & Stock, A. M. (1997b). Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269, 301-312. (Pubitemid 27267754)
26. Miller, J. M. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
27. Mostowy, S., Tsolaki, A. G., Small, P. M. & Behr, M. A. (2003). The in vitro evolution of BCG vaccines. Vaccine 21, 4270-4274.
28. Muttucumaru, D. G., Roberts, G., Hinds, J., Stabler, R. A. & Parish, T. (2004). Gene expression profile of Mycobacterium tuberculosis in a non-replicating state. Tuberculosis (Edinb) 84, 239-246. (Pubitemid 38857856)
29. Parish, T. & Brown, A. (2008). Mycobacterium: Genomics and Molecular Biology. Norwich, Caister Academic Press.
30. Pym, A. S., Brodin, P., Brosch, R., Huerre, M. & Cole, S. T. (2002). Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 46, 709-717. (Pubitemid 35365606)
31. Rachman, H., Strong, M., Ulrichs, T., Grode, L., Schuchhardt, J., Mollenkopf, H., Kosmiadi, G. A., Eisenberg, D. & Kaufmann, S. H. (2006). Unique transcriptome signature of Mycobacterium tuberculosis in pulmonary tuberculosis. Infect Immun 74, 1233-1242. (Pubitemid 43185563)
32. Sala, C., Forti, F., Magnoni, F. & Ghisotti, D. (2008). The katG mRNA of Mycobacterium tuberculosis and Mycobacterium smegmatis is processed at its 5′ end and is stabilized by both a polypurine sequence and translation initiation. BMC Mol Biol 9, 33. (Pubitemid 351619146)
33. Sassetti, C. M. & Rubin, E. J. (2003). Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100, 12989-12994.
34. Schwarz, G., Mendel, R. R. & Ribbe, M. W. (2009). Molybdenum cofactors, enzymes and pathways. Nature 460, 839-847.
35. Self, W. T., Grunden, A. M., Hasona, A. & Shanmugam, K. T. (1999). Transcriptional regulation of molybdoenzyme synthesis in Escherichia coli in response to molybdenum: ModE-molybdate, a repressor of the modABCD (molybdate transport) operon is a secondary transcriptional activator for the hyc and nar operons. Microbiology 145, 41-55. (Pubitemid 29043576)
36. Sheldon, P. J., Busarow, S. B. & Hutchinson, C. R. (2002). Mapping the DNA-binding domain and target sequences of the Streptomyces peucetius daunorubicin biosynthesis regulatory protein, DnrI. Mol Microbiol 44, 449-460.
37. Tanaka, A., Takano, Y., Ohnishi, Y. & Horinouchi, S. (2007). AfsR recruits RNA polymerase to the afsS promoter: a model for transcriptional activation by SARPs. J Mol Biol 369, 322-333. (Pubitemid 46678042)
38. Wayne, L. G. & Hayes, L. G. (1996). An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64, 2062-2069.
39. Wooff, E., Michell, S. L., Gordon, S. V., Chambers, M. A., Bardarov, S., Jacobs, W. R., Jr, Hewinson, R. G. & Wheeler, P. R. (2002). Functional genomics reveals the sole sulphate transporter of the Mycobacterium tuberculosis complex and its relevance to the acquisition of sulphur in vivo. Mol Microbiol 43, 653-663. (Pubitemid 34597260)