The Ser/Thr protein kinase PknB is essential for sustaining mycobacterial growth

Journal of Bacteriology

Volumn 188, Issue 22, 2006, Pages 7778-7784

  Fernandez, Pablo ^a   Saint Joanis, Brigitte ^a   Barilone, Nathalie ^a   Jackson, Mary ^a   Gicquel, Brigitte ^a   Cole, Stewart T ^a   Alzari, Pedro M ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE INHIBITOR; PROTEIN PKNB; PROTEIN SERINE THREONINE KINASE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG;

ACTINOBACTERIA; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CELL DIVISION; CELL SHAPE; ENZYME INACTIVATION; GENE OVEREXPRESSION; GRAM POSITIVE BACTERIUM; MINIMUM INHIBITORY CONCENTRATION; MYCOBACTERIUM; MYCOBACTERIUM AURUM; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PKNB GENE; PRIORITY JOURNAL;

DOSE-RESPONSE RELATIONSHIP, DRUG; GENE DELETION; GENES, BACTERIAL; MICROBIAL SENSITIVITY TESTS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; OPERON; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES;

ACTINOBACTERIA; EUKARYOTA; MYCOBACTERIUM AURUM; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA;

EID: 33751075999     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00963-06     Document Type: Article

References (49)

1. Av-Gay, Y., and J. Davies. 1997. Components of eukaryotic-like protein signaling pathways in Mycobacterium tuberculosis. Microb. Comp. Genomics 2:63-73.
2. Av-Gay, Y., and V. Deretic. 2005. Two-component systems, protein kinases and signal transduction in Mycobacterium tuberculosis, p. 359-367. In S. T. Cole, K. D. Eisenach, D. N. McMurray, and W. R. Jacobs, Jr. (ed.), Tuberculosis and the tubercle bacillus. ASM Press, Washington D.C.
3. Av-Gay, Y., and M. Everett. 2000. The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis. Trends Microbiol. 8:238-244.
4. Av-Gay, Y., S. Jamil, and S. J. Drews. 1999. Expression and characterization of the Mycobacterium tuberculosis serine/threonine protein kinase PknB. Infect. Immun. 67:5676-5682.
5. Bange, F. C., F. M. Collins, and W. R. Jacobs, Jr. 1999. Survival of mice infected with Mycobacterium smegmatis containing large DNA fragments from Mycobacterium tuberculosis. Tuber. Lung Dis. 79:171-180.
6. Belanger, A. E., and G. F. Hatfull. 1999. Exponential-phase glycogen recycling is essential for growth of Mycobacterium smegmatis. J. Bacteriol. 181:6670-6678.
7. Bentley, S. D., R. Brosch, S. V. Gordon, D. A. Hopwood, and S. T. Cole. 2004. Genomics of actinobacteria, the high G+C Gram-positive bacteria, p. 333-360. In C. M. Fraser, T. Read, and K. E. Nelson (ed.), Microbial genomes. Humana Press, Inc., Totowa, N.J.
8. Bentley, S. D., K. F. Chater, A. M. Cerdeno-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147.
9. Boitel, B., M. Ortiz-Lombardia, R. Duran, F. Pompeo, S. T. Cole, C. Cervenansky, and P. M. Alzari. 2003. PknB kinase activity is regulated by phosphorylation in two Thr residues and dephosphorylation by PstP, the cognate phospho-Ser/Thr phosphatase, in Mycobacterium tuberculosis. Mol. Microbiol. 49:1493-1508.
10. Cohen, P. 2002. Protein kinases-the major drug targets of the twenty-first century? Nat. Rev. Drug Discov. 1:309-315.
11. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry, 3rd, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McLean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M. A. Quail, M. A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J. E. Sulston, K. Taylor, S. Whitehead, and B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
12. 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.
13. Cowley, S., M. Ko, N. Pick, R. Chow, K. J. Downing, B. G. Gordhan, J. C. Betts, V. Mizrahi, D. A. Smith, R. W. Stokes, and Y. Av-Gay. 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.
14. Dasgupta, A., P. Datta, M. Kundu, and J. Basu. 2006. The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 152:493-504.
15. Deol, P., R. Vohra, A. K. Saini, A. Singh, H. Chandra, P. Chopra, T. K. Das, A. K. Tyagi, and Y. Singh. 2005. Role of Mycobacterium tuberculosis Ser/Thr kinase PknF: implications in glucose transport and cell division. J. Bacteriol. 187:3415-3420.
16. Drews, S. J., F. Hung, and Y. Av-Gay. 2001. A protein kinase inhibitor as an antimycobacterial agent. FEMS Microbiol. Lett. 205:369-374.
17. Duran, R., A. Villarino, M. Bellinzoni, A. Wehenkel, P. Fernandez, B. Boitel, S. T. Cole, P. M. Alzari, and C. Cervenansky. 2005. Conserved autophosphorylation pattern in activation loops and juxtamembrane regions of Mycobacterium tuberculosis Ser/Thr protein kinases. Biochem. Biophys. Res. Commun. 333:858-867.
18. Fabret, C., and J. A. Hoch. 1998. A two-component signal transduction system essential for growth of Bacillus subtilis: implications for anti-infective therapy. J. Bacteriol. 180:6375-6383.
19. Fontan, P., S. Walters, and I. Smith. 2004. Cellular signaling pathways and transcriptional regulation in Mycobacterium tuberculosis: stress control and virulence. Curr. Sci. 86:122-134.
20. Fsihi, H., E. De Rossi, L. Salazar, R. Cantoni, M. Labo, G. Riccardi, H. E. Takiff, K. Eiglmeier, S. Bergh, and S. T. Cole. 1996. Gene arrangement and organisation in a ∼76 kilobase fragment encompassing the oriC region of the chromosome of Mycobacterium leprae. Microbiology 142:3147-3161.
21. Fukuchi, K., Y. Kasahara, K. Asai, K. Kobayashi, S. Moriya, and N. Ogasawara. 2000. The essential two-component regulatory system encoded by yycF and yycG modulates expression of the ftsAZ operon in Bacillus subtilis. Microbiology 146:1573-1583.
22. Jackson, M., F. X. Berthet, I. Otal, J. Rauzier, C. Martin, B. Gicquel, and C. Guilhot. 1996. The Mycobacterium tuberculosis purine biosynthetic pathway: isolation and characterization of the purC and purL genes. Microbiology 142:2439-2447.
23. Jackson, M., L. Camacho, B. Gicquel, and C. Guilhot. 2001. p. 59-75. In T. Parish and N. Stocker (ed.), Mycobacterium tuberculosis protocols, vol. 54. Humana Press, Inc., Totowa, N.J.
24. Jackson, M., D. Portnoi, D. Catheline, L. Dumail, J. Rauzier, P. Legrand, and B. Gicquel. 1997. Mycobacterium tuberculosis Des protein: an immunodominant target for the humoral response of tuberculous patients. Infect. Immun. 65:2883-2889.
25. Kang, C. M., D. W. Abbott, S. T. Park, C. C. Dascher, L. C. Cantley, and R. N. Husson. 2005. The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev. 19:1692-1704.
26. Kennelly, P. J. 2002. Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. FEMS Microbiol. Lett. 206:1-8.
27. Madec, E., A. Laszkiewicz, A. Iwanicki, M. Obuchowski, and S. Seror. 2002. Characterization of a membrane-linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes. Mol. Microbiol. 46:571-586.
28. Martin, A., M. Camacho, F. Portaels, and J. C. Palomino. 2003. Resazurin microtiter assay plate testing of Mycobacterium tuberculosis susceptibilities to second-line drugs: rapid, simple, and inexpensive method. Antimicrob. Agents Chemother. 47:3616-3619.
29. Nguyen, L., A. Walburger, E. Houben, A. Koul, S. Muller, M. Morbitzer, B. Klebl, G. Ferrari, and J. Pieters. 2005. Role of protein kinase G in growth and glutamine metabolism of Mycobacterium bovis BCG. J. Bacteriol. 187:5852-5856.
30. Niebisch, A., A. Kabus, C. Schultz, B. Weil, and M. Bott. 2006. Corynebacterial protein kinase G controls 2-oxoglutarate dehydrogenase activity via the phosphorylation status of the OdhI protein. J. Biol. Chem. 281:12300-12307.
31. Ortiz-Lombardia, M., F. Pompeo, B. Boitel, and P. M. Alzari. 2003. Crystal structure of the catalytic domain of the PknB serine/threonine kinase from Mycobacterium tuberculosis. J. Biol. Chem. 278:13094-13100.
32. Papavinasasundaram, K. G., B. Chan, J. H. Chung, M. J. Colston, E. O. Davis, and Y. Av-Gay. 2005. Deletion of the Mycobacterium tuberculosis pknH gene confers a higher bacillary load during the chronic phase of infection in BALB/c mice. J. Bacteriol. 187:5751-5760.
33. Parish, T., D. A. Smith, S. Kendall, N. Casali, G. J. Bancroft, and N. G. Stoker. 2003. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect. Immun. 71:1134-1140.
34. Parish, T., D. A. Smith, G. Roberts, J. Betts, and N. G. Stoker. 2003. The senX3-regX3 two-component regulatory system of Mycobacterium tuberculosis is required for virulence. Microbiology 149:1423-1435.
35. Pelicic, V., M. Jackson, J. M. Reyrat, W. R. Jacobs, Jr., B. Gicquel, and C. Guilhot. 1997. Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 94:10955-10960.
36. Perez, E., S. Samper, Y. Bordas, C. Guilhot, B. Gicquel, and C. Martin. 2001. An essential role for phoP in Mycobacterium tuberculosis virulence. Mol. Microbiol. 41:179-187.
37. Perez, J., R. Garcia, H. Bach, J. H. de Waard, W. R. Jacobs, Jr., Y. Av-Gay, J. Bubis, and H. E. Takiff. 2006. Mycobacterium tuberculosis transporter MmpL7 is a potential substrate for kinase PknD. Biochem. Biophys. Res. Commun. 348:6-12.
38. Rickman, L., J. W. Saldanha, D. M. Hunt, D. N. Hoar, M. J. Colston, J. B. Millar, and R. S. Buxton. 2004. A two-component signal transduction system with a PAS domain-containing sensor is required for virulence of Mycobacterium tuberculosis in mice. Biochem. Biophys. Res. Commun. 314:259-267.
39. Sassetti, C. M., D. H. Boyd, and E. J. Rubin. 2003. Genes required for mycobacterial growth denned by high density mutagenesis. Mol. Microbiol. 48:77-84.
40. Singh, A., Y. Singh, R. Pine, L. Shi, R. Chandra, and K. Drlica. 2006. Protein kinase I of Mycobacterium tuberculosis: cellular localization and expression during infection of macrophage-like cells. Tuberculosis (Edinburgh) 86:28-33.
41. 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.
42. Supply, P., J. Magdalena, S. Himpens, and C. Locht. 1997. Identification of novel intergenic repetitive units in a mycobacterial two-component system operon. Mol. Microbiol. 26:991-1003.
43. Villarino, A., R. Duran, A. Wehenkel, P. Fernandez, P. England, P. Brodin, S. T. Cole, U. Zimny-Arndt, P. R. Jungblut, C. Cervenansky, and P. M. Alzari. 2005. Proteomic identification 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.
44. Walburger, A., A. Koul, G. Ferrari, L. Nguyen, C. Prescianotto-Baschong, K. Huygen, B. Klebl, C. Thompson, G. Bacher, and J. Pieters. 2004. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304:1800-1804.
45. West, A. H., and A. M. Stock. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26:369-376.
46. Yeats, C., R. D. Finn, and A. Bateman. 2002. The PASTA domain: a beta-lactam-binding domain. Trends Biochem. Sci. 27:438.
47. Young, T. A., B. Delagoutte, J. A. Endrizzi, A. M. Falick, and T. Alber. 2003. Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat. Struct. Biol. 10:168-174.
48. Zahrt, T. C., and V. Deretic. 2000. An essential two-component signal transduction system in Mycobacterium tuberculosis. J. Bacteriol. 182:3832-3838.
49. Zahrt, T. C., and V. Deretic. 2001. Mycobacterium tuberculosis signal transduction system required for persistent infections. Proc. Natl. Acad. Sci. USA 98:12706-12711.