A copper-responsive global repressor regulates expression of diverse membrane-associated transporters and bacterial drug resistance in mycobacteria

Journal of Biological Chemistry

Volumn 287, Issue 47, 2012, Pages 39721-39731

  Rao, Muding ^a   Liu, Huicong ^a   Yang, Min ^a   Zhao, Chunchao ^a   He, Zheng Guo ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL GENOMES; COPPER IONS; DNA-BINDING; DRUG RESISTANCE; IN-VIVO; MULTIDRUG RESISTANCE; MUTANT STRAIN; MYCOBACTERIAL; MYCOBACTERIUM SMEGMATIS; PALINDROMIC; SIGNALING PATHWAYS; TARGET GENES; TRANSPORT PROTEINS; WILD-TYPE STRAIN;

BACTERIA; GENES; METAL IONS; TRANSCRIPTION FACTORS;

CELL MEMBRANES;

CARRIER PROTEIN; COPPER ION; GENOMIC DNA; PROTEIN GFCR; PROTEIN MS2173; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE TARGETING; MOLECULAR RECOGNITION; MYCOBACTERIUM SMEGMATIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; WILD TYPE;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CARRIER PROTEINS; COPPER; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; METALLOPROTEINS; MYCOBACTERIUM SMEGMATIS; REPRESSOR PROTEINS; RESPONSE ELEMENTS;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS;

EID: 84869214330     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.383604     Document Type: Article

References (51)

1. World Health Organization (WHO). Global Tuberculosis Control WHO Report 2011, 10-11
2. Davies, J. E. (1997) in Antibiotic Resistance. Origins, Evolution, Selection and Spread (Chadwick, D.J. and Goode, J., ed.) John Wiley and Sons Ltd., Chichester, United Kingdom
3. Grkovic, S., Brown, M. H., and Skurray, R. A. (2002) Regulation of bacterial drug export systems. Microbiol. Mol. Biol. Rev. 66, 671-701 (Pubitemid 35425113)
4. Walsh, C. (2000) Molecular mechanisms that confer antibacterial drug resistance. Nature 406, 775-781
5. Alekshun, M. N., and Levy, S. B. (2007) Molecular mechanisms of antibacterial multidrug resistance. Cell 128, 1037-1050 (Pubitemid 46427883)
6. Hillen, W., and Berens, C. (1994) Mechanisms underlying expression of Tn10-encoded tetracycline resistance. Annu. Rev. Microbiol. 48, 345-369 (Pubitemid 24334101)
7. Lomovskaya, O., Lewis, K., and Matin, A. (1995) EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB. J. Bacteriol. 177, 2328-2334
8. 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 (Pubitemid 28334800)
9. Ahmed, M., Borsch, C. M., Taylor, S. S., Vázquez-Laslop, N., and Neyfakh, A. A. (1994) A protein that activates expression of a multidrug efflux transporter upon binding the transporter substrates. J. Biol. Chem. 269, 28506-28513 (Pubitemid 24354599)
10. Alekshun, M. N., and Levy, S. B. (1999) Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro. J. Bacteriol. 181, 4669-4672 (Pubitemid 29357952)
11. Paulsen, I. T., Chen, J., Nelson, K. E., and Saier, M. H. Jr. (2001) Comparative genomics of microbial drug efflux systems. J. Mol. Microbiol. Biotechnol. 3, 145-150 (Pubitemid 32257896)
12. Yang, M., Gao, C., Wang, Y., Zhang, H., and He, Z. G. (2010) Characterization of the interaction and cross-regulation of three Mycobacterium tuberculosis RelBE modules. PLoS ONE 5, e10672
13. Li, Y., Zeng, J., Zhang, H., and He, Z. G. (2010) The characterization of conserved binding motifs and potential target genes for M. tuberculosis MtrAB reveals a link between the two-component system and the drug resistance of M. smegmatis. BMC Microbiol. 10, 242
14. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., 3rd., Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (Pubitemid 28319235)
15. Li, X. Z., Zhang, L., and Nikaido, H. (2004) Efflux pump-mediated intrinsic drug resistance in Mycobacterium smegmatis. Antimicrob. Agents Chemother. 48, 2415-2423 (Pubitemid 38823405)
16. De Rossi, E., Aínsa, J. A., and Riccardi, G. (2006) Role of mycobacterial efflux transporters in drug resistance. An unresolved question. FEMS Microbiol. Rev. 30, 36-52
17. Louw, G. E., Warren, R. M., Gey van Pittius, N. C., McEvoy, C. R., Van Helden, P. D., and Victor, T. C. (2009) A balancing act: efflux/influx in mycobacterial drug resistance. Antimicrob. Agents Chemother. 53, 3181-3189
18. Li, X. Z., and Nikaido, H. (2009) Efflux-mediated drug resistance in bacteria. An update. Drugs. 69, 1555-1623
19. Haydon, D. J., and Guest, J. R. (1991) A new family of bacterial regulatory proteins. FEMS Microbiol. Lett. 79, 291-295
20. Vindal, V., Ranjan, S., and Ranjan, A. (2007) In silico analysis and characterization of GntR family of regulators from Mycobacterium tuberculosis. Tuberculosis 87, 242-247 (Pubitemid 46551847)
21. Vindal, V., Suma, K., and Ranjan, A. (2007) GntR family of regulators in Mycobacterium smegmatis. A sequence and structure based characterization. BMC Genomics 8, 289
22. Rigali, S., Derouaux, A., Giannotta, F., and Dusart, J. (2002) Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J. Biol. Chem. 277, 12507-12515 (Pubitemid 34952608)
23. Lee, M. H., Scherer, M., Rigali, S., and Golden, J. W. (2003) PlmA, a new member of the GntR family, has plasmid maintenance functions in Anabaena sp. strain PCC 7120. J. Bacteriol. 185, 4315-4325 (Pubitemid 36896158)
24. Franco, I. S., Mota, L. J., Soares, C. M., and de Sá-Nogueira, I. (2006) Functional domains of the Bacillus subtilis transcription factor AraR and identification of amino acids important for nucleoprotein complex assembly and effector binding. J. Bacteriol. 188, 3024-3036
25. Aguilera, L., Campos, E., Giménez, R., Badía, J., Aguilar, J., and Baldoma, L. (2008) Dual role of LldR in regulation of the lldPRD operon, involved in L-lactate metabolism in Escherichia coli. J. Bacteriol. 190, 2997-3005 (Pubitemid 351508200)
26. 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
27. van Aalten, D. M., DiRusso, C. C., Knudsen, J., and Wierenga, R. K. (2000) Crystal structure of FadR, a fatty acid-responsive transcription factor with a novel acyl coenzyme A-binding fold. EMBO J. 19, 5167-5177
28. van Aalten, D. M., DiRusso, C. C., and Knudsen, J. (2001) The structural basis of acyl coenzyme A-dependent regulation of the transcription factor FadR. EMBO J. 20, 2041-2050 (Pubitemid 32397405)
29. Xu, Y., Heath, R. J., Li, Z., Rock, C. O., and White, S. W. (2001) The FadR.DNA complex. Transcriptional control of fatty acid metabolism in Escherichia coli. J. Biol. Chem. 276, 17373-17379
30. Blokpoel, M. C., Murphy, H. N., O'Toole, R., Wiles, S., Runn, E. S., Stewart, G. R., Young, D. B., and Robertson, B. D. (2005) Tetracycline-inducible gene regulation in mycobacteria. Nucleic Acids Res. 33, e22
31. Wang, Y., Huang, Y., Xue, C., He, Y., and He, Z. G. (2011) ClpR protein-like regulator specifically recognizes RecA protein-independent promoter motif and broadly regulates expression of DNA damage-inducible genes in mycobacteria. J. Biol. Chem. 286, 31159-31167
32. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace. A web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (Pubitemid 43205406)
33. Snapper, S. B., Melton, R. E., Mustafa, S., Kieser, T., and Jacobs, W. R. (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4, 1911-1919
34. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408 (Pubitemid 34164012)
35. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo. A sequence logo generator. Genome Res. 14, 1188-1190
36. Kendall, S. L., Withers, M., Soffair, C. N., Moreland, N. J., Gurcha, S., Sidders, B., Frita, R., Ten Bokum, A., Besra, G. S., Lott, J. S., and Stoker, N. G. (2007) A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis. Mol. Microbiol. 65, 684-699 (Pubitemid 47077235)
37. Yang, M., Gao, C., Cui, T., An, J., and He, Z. G. (2012) A TetR-like regulator broadly affects the expressions of diverse genes in Mycobacterium smegmatis. Nucleic Acids Res. 40, 1009-1020
38. Casali, N., White, A. M., and Riley, L. W. (2006) Regulation of the Mycobacterium tuberculosis mce1 operon. J. Bacteriol. 188, 441-449 (Pubitemid 43100531)
39. Tojo, S., Satomura, T., Matsuoka, H., Hirooka, K., and Fujita, Y. (2011) Catabolite repression of the Bacillus subtilis FadR regulon, which is involved in fatty acid catabolism. J. Bacteriol. 193, 2388-2395
40. Lubelski, J., Konings, W. N., and Driessen, A. J. (2007) Distribution and physiology of ABC-type transporters contributing to multidrug resistance in bacteria. Microbiol. Mol. Biol. Rev. 71, 463-476 (Pubitemid 47429281)
41. Locher, K. P. (2009) Review. Structure and mechanism of ATP-binding cassette transporters. Phil. Trans. R. Soc. B. 364, 239-245
42. Colangeli, R., Helb, D., Sridharan, S., Sun, J., Varma-Basil, M., Hazbón, M. H., Harbacheuski, R., Megjugorac, N. J., Jacobs, W. R. Jr., Holzenburg, A., Sacchettini, J. C., and Alland, D. (2005) The Mycobacterium tuberculosis iniA gene is essential for activity of an efflux pump that confers drug tolerance to both isoniazid and ethambutol. Mol. Microbiol. 55, 1829-1840 (Pubitemid 40445216)
43. Alland, D., Steyn, A. J., Weisbrod, T., Aldrich, K., and Jacobs, W. R., Jr. (2000) Characterization of the Mycobacterium tuberculosis iniBAC promoter, a promoter that responds to cell wall biosynthesis inhibition. J. Bacteriol. 182, 1802-1811 (Pubitemid 30165365)
44. Agranoff, D., and Krishna, S. (2004) Metal ion transport and regulation in Mycobacterium tuberculosis. Front Biosci. 9, 2996-3006
45. Spagnolo, L., Törö, I., D'Orazio, M., O'Neill, P., Pedersen, J. Z., Carugo, O., Rotilio, G., Battistoni, A., and Djinovic-Carugo, K. (2004) Unique features of the sodC-encoded superoxide dismutase from Mycobacterium tuberculosis, a fully functional copper-containing enzyme lacking zinc in the active site. J. Biol. Chem. 279, 33447-33455 (Pubitemid 39062994)
46. Strausak, D., and Solioz, M. (1997) CopY is a copper-inducible repressor of the Enterococcus hirae copper ATPases. J. Biol. Chem. 272, 8932-8936 (Pubitemid 27154890)
47. Stoyanov, J. V., Hobman, J. L., and Brown, N. L. (2001) CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol. Microbiol. 39, 502-511 (Pubitemid 32113519)
48. Gaballa, A., Cao, M., and Helmann, J. D. (2003) Two MerR homologues that affect copper induction of the Bacillus subtilis copZA operon. Microbiology 149, 3413-3421 (Pubitemid 38016670)
49. Liu, T., Ramesh, A., Ma, Z., Ward, S. K., Zhang, L., George, G. N., Talaat, A. M., Sacchettini, J. C., and Giedroc, D. P. (2007) CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. Nat. Chem. Biol. 3, 60-68 (Pubitemid 46005700)
50. Zheng, M., Cooper, D. R., Grossoehme, N. E., Yu, M., Hung, L. W., Cieslik, M., Derewenda, U., Lesley, S. A., Wilson, I. A., Giedroc, D. P., and Derewenda, Z. S. (2009) Structure of Thermotoga maritima TM0439: implication for the mechanism of bacterial GntR transcription regulators with Zn2+-binding FCD domains. Acta Crystallogr. D Biol. Crystallogr. 65, 356-365
51. Festa, R. A., Jones, M. B., Butler-Wu, S., Sinsimer, D., Gerads, R., Bishai, W. R., Peterson, S. N., and Darwin, K. H. (2011)Anovel copper-responsive regulon in Mycobacterium tuberculosis. Mol. Microbiol. 79, 133-148