Identification of multiple substrates of the StkP Ser/Thr protein kinase in Streptococcus pneumoniae

Journal of Bacteriology

Volumn 192, Issue 14, 2010, Pages 3629-3638

  Nováková, Linda ^a   Bezoušková, Silvia ^a   Pompach, Petr ^a   Špidlová, Petra ^a   Sasková, Lenka ^a   Weiser, Jaroslav ^a   Branny, Pavel ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; INORGANIC PYROPHOSPHATASE; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN; PPAC ENZYME; PROTEIN DIVIVA; PROTEIN SERINE THREONINE KINASE; PROTEIN SPR0334; RNA POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CELL DIVISION; CYTOPLASM; ENZYME ACTIVATION; ENZYME INACTIVATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; STREPTOCOCCUS PNEUMONIAE;

BACTERIAL PROTEINS; CELL DIVISION; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; PROTEIN-SERINE-THREONINE KINASES; STREPTOCOCCUS PNEUMONIAE; SUBSTRATE SPECIFICITY;

EUKARYOTA; PROKARYOTA; STREPTOCOCCUS PNEUMONIAE;

EID: 77954414035     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01564-09     Document Type: Article

References (55)

1. Absalon, C., M. Obuchowski, E. Madec, D. Delattre, I. B. Holland, and S. J. Seror. 2009. CpgA, EF-Tu and the stressosome protein YezB are substrates of the Ser/Thr kinase/phosphatase couple, PrkC/PrpC, in Bacillus subtilis. Microbiology 155:932-943.
2. Avery, O. T., C. M. McLeod, and M. McCarthy. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. J. Exp. Med. 79:137-158.
3. 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.
4. Beltramini, A. M., C. D. Mukhopadhyay, and V. Pancholi. 2009. Modulation of cell wall structure and antimicrobial susceptibility by a Staphylococcus aureus eukaryote-like serine/threonine kinase and phosphatase. Infect. Immun. 77:1406-1416.
5. Canova, M. J., L. Kremer, and V. Molle. 2008. pETPhos: a customized expression vector designed for further characterization of Ser/Thr/Tyr protein kinases and their substrates. Plasmid 60:149-153.
6. Canova, M. J., L. Kremer, and V. Molle. 2009. The Mycobacterium tuberculosis GroEL1 chaperone is a substrate of Ser/Thr protein kinases. J. Bacteriol. 191:2876-2883.
7. Claverys, J. P., A. Dintilhac, E. V. Pestova, B. Martin, and D. A. Morrison. 1995. Construction and evaluation of new drug-resistance cassettes for gene disruption mutagenesis in Streptococcus pneumoniae, using an ami test platform. Gene 164:123-128.
8. Debarbouille, M., S. Dramsi, O. Dussurget, M. A. Nahori, E. Vaganay, G. Jouvion, A. Cozzone, T. Msadek, and B. Duclos. 2009. Characterization of a serine/threonine kinase involved in virulence of Staphylococcus aureus. J. Bacteriol. 191:4070-4081.
9. Echenique, J., A. Kadioglu, S. Romao, P. W. Andrew, and M. C. Trombe. 2004. Protein serine/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae. Infect. Immun. 72:2434-2437.
10. Errington, J., R. A. Daniel, and D. J. Scheffers. 2003. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67:52-65, table.
11. Fadda, D., C. Pischedda, F. Caldara, M. B. Whalen, D. Anderluzzi, E. Domenici, and O. Massidda. 2003. Characterization of divIVA and other genes located in the chromosomal region downstream of the dcw cluster in Streptococcus pneumoniae. J. Bacteriol. 185:6209-6214.
12. Fadda, D., A. Santona, V. D'Ulisse, P. Ghelardini, M. G. Ennas, M. B. Whalen, and O. Massidda. 2007. Streptococcus pneumoniae DivIVA: localization and interactions in a MinCD-free context. J. Bacteriol. 189:1288-1298.
13. Fernandez, P., B. Saint-Joanis, N. Barilone, M. Jackson, B. Gicquel, S. T. Cole, and P. M. Alzari. 2006. The Ser/Thr protein kinase PknB is essential for sustaining mycobacterial growth. J. Bacteriol. 188:7778-7784.
14. Fiuza, M., M. J. Canova, D. Patin, M. Letek, I. Zanella-Cleon, M. Becchi, L. M. Mateos, D. Mengin-Lecreulx, V. Molle, and J. A. Gil. 2008. The MurC ligase essential for peptidoglycan biosynthesis is regulated by the serine/threonine protein kinase PknA in Corynebacterium glutamicum. J. Biol. Chem. 283:36553-36563.
15. Fiuza, M., M. J. Canova, I. Zanella-Cleon, M. Becchi, A. J. Cozzone, L. M. Mateos, L. Kremer, J. A. Gil, and V. Molle. 2008. From the characterization of the four serine/threonine protein kinases (PknA/B/G/L) of Corynebacterium glutamicum toward the role of PknA and PknB in cell division. J. Biol. Chem. 283:18099-18112.
16. Gaidenko, T. A., T. J. Kim, and C. W. Price. 2002. The PrpC serine-threonine phosphatase and PrkC kinase have opposing physiological roles in stationary-phase Bacillus subtilis cells. J. Bacteriol. 184:6109-6114.
17. Giefing, C., A. L. Meinke, M. Hanner, T. Henics, M. D. Bui, D. Gelbmann, U. Lundberg, B. M. Senn, M. Schunn, A. Habel, B. Henriques-Normark, A. Ortqvist, M. Kalin, A. von Gabain, and E. Nagy. 2008. Discovery of a novel class of highly conserved vaccine antigens using genomic scale antigenic fingerprinting of pneumococcus with human antibodies. J. Exp. Med. 205:117-131.
18. Gordon, E., N. Mouz, E. Duee, and O. Dideberg. 2000. The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance. J. Mol. Biol. 299:477-485.
19. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
20. Hussain, H., P. Branny, and E. Allan. 2006. A eukaryotic-type serine/threonine protein kinase is required for biofilm formation, genetic competence, and acid resistance in Streptococcus mutans. J. Bacteriol. 188:1628-1632.
21. Jin, H., and V. Pancholi. 2006. Identification and biochemical characterization of a eukaryotic-type serine/threonine kinase and its cognate phosphatase in Streptococcus pyogenes: their biological functions and substrate identification. J. Mol. Biol. 357:1351-1372.
22. Jones, G., and P. Dyson. 2006. Evolution of transmembrane protein kinases implicated in coordinating remodeling of gram-positive peptidoglycan: inside versus outside. J. Bacteriol. 188:7470-7476. (Pubitemid 44646246)
23. 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.
24. Kristich, C. J., C. L. Wells, and G. M. Dunny. 2007. A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc. Natl. Acad. Sci. U. S. A. 104:3508-3513.
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Lahti, R. 1983. Microbial inorganic pyrophosphatases. Microbiol. Rev. 47:169-178.
27. Levine, A., F. Vannier, C. Absalon, L. Kuhn, P. Jackson, E. Scrivener, V. Labas, J. Vinh, P. Courtney, J. Garin, and S. J. Seror. 2006. Analysis of the dynamic Bacillus subtilis Ser/Thr/Tyr phosphoproteome implicated in a wide variety of cellular processes. Proteomics 6:2157-2173.
28. Lin, W. J., D. Walthers, J. E. Connelly, K. Burnside, K. A. Jewell, L. J. Kenney, and L. Rajagopal. 2009. Threonine phosphorylation prevents promoter DNA binding of the group B Streptococcus response regulator CovR. Mol. Microbiol. 71:1477-1495.
29. Macek, B., F. Gnad, B. Soufi, C. Kumar, J. V. Olsen, I. Mijakovic, and M. Mann. 2008. Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol. Cell. Proteomics 7:299-307.
30. Macek, B., I. Mijakovic, J. V. Olsen, F. Gnad, C. Kumar, P. R. Jensen, and M. Mann. 2007. The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol. Cell. Proteomics 6:697-707.
31. 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.
32. Marston, A. L., and J. Errington. 1999. Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol. Microbiol. 33:84-96.
33. Molle, V., A. K. Brown, G. S. Besra, A. J. Cozzone, and L. Kremer. 2006. The condensing activities of the Mycobacterium tuberculosis type II fatty acid synthase are differentially regulated by phosphorylation. J. Biol. Chem. 281:30094-30103.
34. Morrison, D. A., S. A. Lacks, W. R. Guild, and J. M. Hageman. 1983. Isolation and characterization of three new classes of transformation-deficient mutants of Streptococcus pneumoniae that are defective in DNA transport and genetic recombination. J. Bacteriol. 156:281-290.
35. Novakova, L., L. Saskova, P. Pallova, J. Janecek, J. Novotna, A. Ulrych, J. Echenique, M. C. Trombe, and P. Branny. 2005. Characterization of a eukaryotic type serine/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates. FEBS J. 272:1243-1254.
36. Oliver, A. W., S. Knapp, and L. H. Pearl. 2007. Activation segment exchange: a common mechanism of kinase autophosphorylation? Trends Biochem. Sci. 32:351-356.
37. Pallova, P., K. Hercik, L. Saskova, L. Novakova, and P. Branny. 2007. A eukaryotic-type serine/threonine protein kinase StkP of Streptococcus pneumoniae acts as a dimer in vivo. Biochem. Biophys. Res. Commun. 355:526-530.
38. Perez, J., A. Castaneda-Garcia, H. Jenke-Kodama, R. Muller, and J. Munoz-Dorado. 2008. Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome. Proc. Natl. Acad. Sci. U. S. A. 105:15950-15955.
39. Pike, A. C., P. Rellos, F. H. Niesen, A. Turnbull, A. W. Oliver, S. A. Parker, B. E. Turk, L. H. Pearl, and S. Knapp. 2008. Activation segment dimerization: a mechanism for kinase autophosphorylation of non-consensus sites. EMBO J. 27:704-714.
40. Rais, I., M. Karas, and H. Schagger. 2004. Two-dimensional electrophoresis for the isolation of integral membrane proteins and mass spectrometric identification. Proteomics 4:2567-2571.
41. Rajagopal, L., A. Clancy, and C. E. Rubens. 2003. A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. J. Biol. Chem. 278:14429-14441.
42. Rajagopal, L., A. Vo, A. Silvestroni, and C. E. Rubens. 2005. Regulation of purine biosynthesis by a eukaryotic-type kinase in Streptococcus agalactiae. Mol. Microbiol. 56:1329-1346.
43. Rajagopal, L., A. Vo, A. Silvestroni, and C. E. Rubens. 2006. Regulation of cytotoxin expression by converging eukaryotic-type and two-component signalling mechanisms in Streptococcus agalactiae. Mol. Microbiol. 62:941-957.
44. Rantanen, M. K., L. Lehtio, L. Rajagopal, C. E. Rubens, and A. Goldman. 2007. Structure of the Streptococcus agalactiae family II inorganic pyrophosphatase at 2.80 A resolution. Acta Crystallogr. Sect. D Biol. Crystallogr. 63:738-743.
45. Saskova, L., L. Novakova, M. Basler, and P. Branny. 2007. Eukaryotic-type serine/threonine protein kinase StkP is a global regulator of gene expression in Streptococcus pneumoniae. J. Bacteriol. 189:4168-4179. (Pubitemid 46847365)
46. Schultz, C., A. Niebisch, A. Schwaiger, U. Viets, S. Metzger, M. Bramkamp, and M. Bott. 2009. Genetic and biochemical analysis of the serine/threonine protein kinases PknA, PknB, PknG and PknL of Corynebacterium glutamicum: evidence for non-essentiality and for phosphorylation of OdhI and FtsZ by multiple kinases. Mol. Microbiol. 74:724-741.
47. Shah, I. M., M. H. Laaberki, D. L. Popham, and J. Dworkin. 2008. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135:486-496.
48. Sharma, K., M. Gupta, A. Krupa, N. Srinivasan, and Y. Singh. 2006. EmbR, a regulatory protein with ATPase activity, is a substrate of multiple serine/threonine kinases and phosphatase in Mycobacterium tuberculosis. FEBS J. 273:2711-2721.
49. Silvestroni, A., K. A. Jewell, W. J. Lin, J. E. Connelly, M. M. Ivancic, W. A. Tao, and L. Rajagopal. 2009. Identification of serine/threonine kinase substrates in the human pathogen group B streptococcus. J. Proteome Res. 8:2563-2574.
50. Thakur, M., and P. K. Chakraborti. 2006. GTPase activity of mycobacterial FtsZ is impaired due to its transphosphorylation by the eukaryotic-type Ser/Thr kinase, PknA. J. Biol. Chem. 281:40107-40113.
51. Thakur, M., and P. K. Chakraborti. 2008. Ability of PknA, a mycobacterial eukaryotic-type serine/threonine kinase, to transphosphorylate MurD, a ligase involved in the process of peptidoglycan biosynthesis. Biochem. J. 415:27-33.
52. Ulijasz, A. T., S. P. Falk, and B. Weisblum. 2009. Phosphorylation of the RitR DNA-binding domain by a Ser-Thr phosphokinase: implications for global gene regulation in the streptococci. Mol. Microbiol. 71:382-390.
53. Williams, T. I., J. C. Combs, A. P. Thakur, H. J. Strobel, and B. C. Lynn. 2006. A novel Bicine running buffer system for doubled sodium dodecyl sulfate-polyacrylamide gel electrophoresis of membrane proteins. Electrophoresis 27:2984-2995.
54. Yeats, C., R. D. Finn, and A. Bateman. 2002. The PASTA domain: a betalactam-binding domain. Trends Biochem. Sci. 27:438.
55. 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.