Silencing essential protein secretion in Mycobacterium smegmatis by using tetracycline repressors

Journal of Bacteriology

Volumn 189, Issue 13, 2007, Pages 4614-4623

  Guo, Xinzheng V ^a,b   Monteleone, Mercedes ^a   Klotzsche, Marcus ^a   Kamionka, Annette ^c   Hillen, Wolfgang ^c   Braunstein, Miriam ^d   Ehrt, Sabine ^a,b   Schnappinger, Dirk ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANHYDROTETRACYCLINE; PORIN; PROTEIN MSPA; REPRESSOR PROTEIN; TETRACYCLINE; TETRACYCLINE REPRESSOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BETA GALACTOSIDASE; TRANSACTIVATOR PROTEIN;

ARTICLE; BACTERIAL GROWTH; ENVELOPE GENE; ESSENTIAL GENE; GENE CONSTRUCT; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC ANALYSIS; GROWTH INHIBITION; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SECA1 GENE; DOSE RESPONSE; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROMOTER REGION; TIME; WESTERN BLOTTING;

CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS;

BACTERIAL PROTEINS; BETA-GALACTOSIDASE; BLOTTING, WESTERN; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE SILENCING; KINETICS; MUTATION; MYCOBACTERIUM SMEGMATIS; PROMOTER REGIONS (GENETICS); TETRACYCLINE; TIME FACTORS; TRANS-ACTIVATORS;

EID: 34347402468     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00216-07     Document Type: Article

References (45)

1. Aziz, M. A., and A. Wright. 2005. The World Health Organization/International Union Against Tuberculosis and Lung Disease Global Project on Surveillance for Anti-Tuberculosis Drug Resistance: a model for other infectious diseases. Clin. Infect. Dis. 41(Suppl. 4):S258-S262.
2. Braunstein, M., A. M. Brown, S. Kurtz, and W. R. Jacobs, Jr. 2001. Two nonredundant SecA homologues function in mycobacteria. J. Bacteriol. 183: 6979-6990.
3. Braunstein, M., B. J. Espinosa, J. Chan, J. T. Belisle, and W. R. Jacobs, Jr. 2003. SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol. Microbiol. 48:453-464.
4. Brodin, P., L. Majlessi, L. Marsollier, M. I. de Jonge, D. Bottai, C. Demangel, J. Hinds, O. Neyrolles, P. D. Butcher, C. Leclerc, S. T. Cole, and R. Brosch. 2006. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect. Immun. 74:88-98.
5. Brodin, P., I. Rosenkrands, P. Andersen, S. T. Cole, and R. Brosch. 2004. ESAT-6 proteins: protective antigens and virulence factors? Trends Microbiol. 12:500-508.
6. Cabelli, R. J., L. Chen, P. C. Tai, and D. B. Oliver. 1988. SecA protein is required for secretory protein translocation into E. coli membrane vesicles. Cell 55:683-692.
7. Chen, L., Q. W. Xie, and C. Nathan. 1998. Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates. Mol. Cell 1:795-805.
8. Cole, S. T., K. Eiglmeier, J. Parkhill, K. D. James, N. R. Thomson, P. R. Wheeler, N. Honore, T. Garnier, C. Churcher, D. Harris, K. Mungall, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. M. Davies, K. Devlin, S. Duthoy, T. Feltwell, A. Fraser, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, C. Lacroix, J. Maclean, S. Moule, L. Murphy, K. Oliver, M. A. Quail, M. A. Rajandream, K. M. Rutherford, S. Rutter, K. Seeger, S. Simon, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, K. Taylor, S. Whitehead, J. R. Woodward, and B. G. Barrell. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007-1011.
9. Cunningham, K., and W. Wickner. 1989. Specific recognition of the leader region of precursor proteins is required for the activation of translocation ATPase of Escherichia coli. Proc. Natl. Acad. Sci. USA 86:8630-8634.
10. Ehrt, S., X. V. Guo, C. M. Hickey, M. Ryou, M. Monteleone, L. W. Riley, and D. Schnappinger. 2005. Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res. 33:e21.
11. Ehrt, S., and D. Schnappinger. 2006. Controlling gene expression in mycobacteria. Future Microbiol. 1:177-184.
12. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
13. Fortune, S. M., A. Jaeger, D. A. Sarracino, M. R. Chase, C. M. Sassetti, D. R. Sherman, B. R. Bloom, and E. J. Rubin. 2005. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc. Natl. Acad. Sci. USA 102:10676-10681.
14. Frieden, T. R., T. R. Sterling, S. S. Munsiff, C. J. Watt, and C. Dye. 2003. Tuberculosis. Lancet 362:887-899.
15. Geluk, A., K. E. van Meijgaarden, K. L. Franken, B. Wieles, S. M. Arend, W. R. Faber, B. Naafs, and T. H. Ottenhoff. 2004. Immunological crossreactivity of the Mycobacterium leprae CFP-10 with its homologue in Mycobacterium tuberculosis. Scand. J. Immunol. 59:66-70.
16. Guinn, K. M., M. J. Hickey, S. K. Mathur, K. L. Zakel, J. E. Grotzke, D. M. Lewinsohn, S. Smith, and D. R. Sherman. 2004. Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol. Microbiol. 51:359-370.
17. Hsu, T., S. M. Hingley-Wilson, B. Chen, M. Chen, A. Z. Dai, P. M. Morin, C. B. Marks, J. Padiyar, C. Goulding, M. Gingery, D. Eisenberg, R. G. Russell, S. C. Derrick, F. M. Collins, S. L. Morris, C. H. King, and W. R. Jacobs, Jr. 2003. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc. Natl. Acad. Sci. USA 100:12420-12425.
18. Kamionka, A., R. Bertram, and W. Hillen. 2005. Tetracycline-dependent conditional gene knockout in Bacillus subtilis. Appl. Environ. Microbiol. 71:728-733.
19. Kaps, I., S. Ehrt, S. Seeber, D. Schnappinger, C. Martin, L. W. Riley, and M. Niederweis. 2001. Energy transfer between fluorescent proteins using a coexpression system in Mycobacterium smegmatis. Gene 278:115-124.
20. Kaufmann, S. H., and J. Hess. 1999. Impact of intracellular location of and antigen display by intracellular bacteria: implications for vaccine development. Immunol. Lett. 65:81-84.
21. Kobayashi, K., S. D. Ehrlich, A. Albertini, G. Amati, K. K. Andersen, M. Arnaud, K. Asai, S. Ashikaga, S. Aymerich, P. Bessieres, F. Boland, S. C. Brignell, S. Bron, K. Bunai, J. Chapuis, L. C. Christiansen, A. Danchin, M. Debarbouille, E. Dervyn, E. Deuerling, K. Devine, S. K. Devine, O. Dreesen, J. Errington, S. Fillinger, S. J. Foster, Y. Fujita, A. Galizzi, R. Gardan, C. Eschevins, T. Fukushima, K. Haga, C. R. Harwood, M. Hecker, D. Hosoya, M. F. Hullo, H. Kakeshita, D. Karamata, Y. Kasahara, F. Kawamura, K. Koga, P. Koski, R. Kuwana, D. Imamura, M. Ishimaru, S. Ishikawa, I. Ishio, D. Le Coq, A. Masson, C. Mauel, R. Meima, R. P. Mellado, A. Moir, S. Moriya, E. Nagakawa, H. Nanamiya, S. Nakai, P. Nygaard, M. Ogura, T. Ohanan, M. O'Reilly, M. O'Rourke, Z. Pragai, H. M. Pooley, G. Rapoport, J. P. Rawlins, L. A. Rivas, C. Rivolta, A. Sadaie, Y. Sadaie, M. Sarvas, T. Sato, H. H. Saxild, E. Scanlan, W. Schumann, J. F. Seegers, J. Sekiguchi, A. Sekowska, S. J. Seror, M. Simon, P. Stragier, R. Studer, H. Takamatsu, T. Tanaka, M. Takeuchi, H. B. Thomaides, V. Vagner, J. M. van Dijl, K. Watabe, A. Wipat, H. Yamamoto, M. Yamamoto, Y. Yamamoto, K. Yamane, K. Yata, K. Yoshida, H. Yoshikawa, U. Zuber, and N. Ogasawara. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100:4678-4683.
22. Kremer, L. and G. S. Besra. 2002. Re-emergence of tuberculosis: strategies and treatment. Expert Opin. Investig. Drugs. 11:153-157.
23. Kurtz, S., K. P. McKinnon, M. S. Runge, J. P. Ting, and M. Braunstein. 2006. The SecA2 secretion factor of Mycobacterium tuberculosis promotes growth in macrophages and inhibits the host immune response. Infect. Immun. 74:6855-6864.
24. Lamichhane, G., M. Zignol, N. J. Blades, D. E. Geiman, A. Dougherty, J. Grosset, K. W. Broman, and W. R. Bishai. 2003. A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 100:7213-7218.
25. Lill, R., K. Cunningham, L. A. Brundage, K. Ito, D. Oliver, and W. Wickner. 1989. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. EMBO J. 8:961-966.
26. Majlessi, L., P. Brodin, R. Brosch, M. J. Rojas, H. Khun, M. Huerre, S. T. Cole, and C. Leclerc. 2005. Influence of ESAT-6 secretion system 1 (RD1) of Mycobacterium tuberculosis on the interaction between mycobacteria and the host immune system. J. Immunol. 174:3570-3579.
27. McDonough, J. A., K. E. Hacker, A. R. Flores, M. S. Pavel ka, Jr., and M. Braunstein. 2005. The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for the export of mycobacterial p-lactamases. J. Bacteriol. 187:7667-7679.
28. Meyer, T. H., J. F. Menetret, R. Breitling, K. R. Miller, C. W. Akey, and T. A. Rapoport. 1999. The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex. J. Mol. Biol. 285:1789-1800.
29. Niederweis, M., S. Ehrt, C. Heinz, U. Klocker, S. Karosi, K. M. Swiderek, L. W. Riley, and R. Benz. 1999. Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Mol. Microbiol. 33:933-945.
30. Nikaido, H., and J. Reid. 1990. Biogenesis of prokaryotic pores. Experientia 46:174-180.
31. Nouwen, N., and A. J. Driessen. 2002. SecDFyajC forms a heterotetrameric complex with YidC. Mol. Microbiol. 44:1397-1405.
32. Pook, E., S. Grimm, A. Bonin, T. Winkler, and W. Hillen. 1998. Affinities of mAbs to Tet repressor complexed with operator or tetracycline suggest conformational changes associated with induction. Eur. J. Biochem. 258:915-922.
33. Posey, J. E., T. M. Shinnick, and F. D. Quinn. 2006. Characterization of the twin-arginine translocase secretion system of Mycobacterium smegmatis. J. Bacteriol. 188:1332-1340.
34. Primm, T. P., C. A. Lucero, and J. O. Falkinham III. 2004. Health impacts of environmental mycobacteria. Clin. Microbiol. Rev. 17:98-106.
35. Rowland, B., A. Purkayastha, C. Monserrat, Y. Casart, H. Takiff, and K. A. McDonough. 1999. Fluorescence-based detection of lacZ reporter gene expression in intact and viable bacteria including Mycobacterium species. FEMS Microbiol. Lett. 179:317-325.
36. Saint-Joanis, B., C. Demangel, M. Jackson, P. Brodin, L. Marsollier, H. Boshoff, and S. T. Cole. 2006. Inactivation of Rv2525c, a substrate of the twin arginine translocation (Tat) system of Mycobacterium tuberculosis, increases p-lactam susceptibility and virulence. J. Bacteriol. 188:6669-6679.
37. Sassetti, C. M., D. H. Boyd, and E. J. Rubin. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48:77-84.
38. Scholz, O., E. M. Henssler, J. Bail, P. Schubert, J. Bogdanska-Urbaniak, S. Sopp, M. Reich, S. Wisshak, M. Kostner, R. Bertram, and W. Hillen. 2004. Activity reversal of Tet repressor caused by single amino acid exchanges. Mol. Microbiol. 53:777-789.
39. Sharma, V., A. Arockiasamy, D. R. Ronning, C. G. Sawa, A. Holzenburg, M. Braunstein, W. R. Jacobs, Jr., and J. C. Sacchettini. 2003. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc. Natl. Acad. Sci. USA 100:2243-2248.
40. Snapper, S. B., R. E. Melton, S. Mustafa, T. Kieser, and W. R. Jacobs, Jr. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4:1911-1919.
41. Stahl, C., S. Kubetzko, I. Kaps, S. Seeber, H. Engelhardt, and M. Niederweis. 2001. MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 40:451-464.
42. Stanley, S. A., S. Raghavan, W. W. Hwang, and J. S. Cox. 2003. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc. Natl. Acad. Sci. USA 100:13001- 13006.
43. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. Benson, L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, et al. 1991. New use of BCG for recombinant vaccines. Nature 351:456-460.
44. Tortoli, E. 2006. The new mycobacteria: an update. FEMS Immunol. Med. Microbiol. 48:159-178.
45. van der Laan, M., M. L. Urbanus, C. M. Ten Hagen-Jongman, N. Nouwen, B. Oudega, N. Harms, A. J. Driessen, and J. Luirink. 2003. A conserved function of YidC in the biogenesis of respiratory chain complexes. Proc. Natl. Acad. Sci. USA 100:5801-5806.