Protein-tyrosine phosphorylation interaction network in Bacillus subtilis reveals new substrates, kinase activators and kinase cross-talk

Frontiers in Microbiology

Volumn 5, Issue OCT, 2014, Pages

  Shi, Lei ^a,b   Pigeonneau, Nathalie ^a   Ventroux, Magali ^a   Derouiche, Abderahmane ^a,b   Bidnenko, Vladimir ^b   Mijakovic, Ivan ^a,b   Noirot Gros, Marie Françoise ^a  

^a UMR1319 MICALIS   (France)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Bacterial cell division; Bacterial protein kinase; Bacterial signaling; Protein phosphorylation; Protein protein network

Indexed keywords

PHOSPHATASE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE;

AFFINITY CHROMATOGRAPHY; ANTIBIOTIC RESISTANCE; ARTICLE; AUTOPHOSPHORYLATION; BACILLUS SUBTILIS; CARBOHYDRATE METABOLISM; CELL DIVISION; DNA METABOLISM; FAR WESTERN BLOTTING; FLUORESCENCE MICROSCOPY; GENETIC SCREENING; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS;

EID: 84987819734     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00538     Document Type: Article

References (70)

1. Arigoni, F., Duncan, L., Alper, S., Losick, R., and Stragier, P. (1996). SpoIIE governs the phosphorylation state of a protein regulating transcription factor sigma F during sporulation in Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 93, 3238-3242. doi: 10.1073/pnas.93.8.3238
2. Baer, C. E., Iavarone, A. T., Alber, T., and Sassetti, C. M. (2014). Biochemical and spatial coincidence in the provisional Ser/Thr protein kinase interaction network of mycobacterium tuberculosis. J. Biol. Chem. 289, 20422-20433. doi: 10.1074/jbc.M114.559054
3. Ben-Yehuda, S., Rudner, D. Z., and Losick, R. (2003). RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299, 532-536. doi: 10.1126/science.1079914
4. Bidnenko, V., Shi, L., Kobir, A., Ventroux, M., Pigeonneau, N., Henry, C., et al. (2013). Bacillus subtilis serine/threonine protein kinase YabT is involved in spore development via phosphorylation of a bacterial recombinase. Mol. Microbiol. 88, 921-935. doi: 10.1111/mmi.12233
5. Burmann, F., Ebert, N., Van Baarle, S., and Bramkamp, M. (2011). A bacterial dynamin-like protein mediating nucleotide-independent membrane fusion. Mol. Microbiol. 79, 1294-1304. doi: 10.1111/j.1365-2958.2011.07523.x
6. Butala, M., Zgur-Bertok, D., and Busby, S. J. (2009). The bacterial LexA transcriptional repressor. Cell Mol. Life Sci. 66, 82-93. doi: 10.1007/s00018-008-8378-6
7. Dempwolff, F., Wischhusen, H. M., Specht, M., and Graumann, P. L. (2012). The deletion of bacterial dynamin and flotillin genes results in pleiotrophic effects on cell division, cell growth and in cell shape maintenance. BMC Microbiol. 12:298. doi: 10.1186/1471-2180-12-298
8. Derouiche, A., Bidnenko, V., Grenha, R., Pigonneau, N., Ventroux, M., Franz-Wachtel, M., et al. (2013). Interaction of bacterial fatty-acid-displaced regulators with DNA is interrupted by tyrosine phosphorylation in the helix-turn-helix domain. Nucleic Acids Res. 41, 9371-9381. doi: 10.1093/nar/gkt709
9. Duncan, L., Alper, S., Arigoni, F., Losick, R., and Stragier, P. (1995). Activation of cell-specific transcription by a serine phosphatase at the site of asymmetric division. Science 270, 641-644. doi: 10.1126/science.270.5236.641
10. Elsholz, A. K., Turgay, K., Michalik, S., Hessling, B., Gronau, K., Oertel, D., et al. (2012). Global impact of protein arginine phosphorylation on the physiology of Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 109, 7451-7456. doi: 10.1073/pnas.1117483109
11. Fabret, C., Feher, V. A., and Hoch, J. A. (1999). Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J. Bacteriol. 181, 1975-1983.
12. Feucht, A., and Lewis, P. J. (2001). Improved plasmid vectors for the production of multiple fluorescent protein fusions in Bacillus subtilis. Gene 264, 289-297. doi: 10.1016/S0378-1119(01)00338-9
13. Fleurie, A., Cluzel, C., Guiral, S., Freton, C., Galisson, F., Zanella-Cleon, I., et al. (2012). Mutational dissection of the S/T-kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae. Mol. Microbiol. 83, 746-758. doi: 10.1111/j.1365-2958.2011.07962.x
14. Gaidenko, T. A., Kim, T. J., and Price, C. W. (2002). The PrpC serine-threonine phosphatase and PrkC kinase have opposing physiological roles in stationary-phase Bacillus subtilis cells. J. Bacteriol. 184, 6109-6114. doi: 10.1128/JB.184.22.6109-6114.2002
15. Galinier, A., Kravanja, M., Engelmann, R., Hengstenberg, W., Kilhoffer, M. C., Deutscher, J., et al. (1998). New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc. Natl. Acad. Sci. U.S.A. 95, 1823-1828. doi: 10.1073/pnas.95.4.1823
16. Garsin, D. A., Duncan, L., Paskowitz, D. M., and Losick, R. (1998). The kinase activity of the antisigma factor SpoIIAB is required for activation as well as inhibition of transcription factor sigmaF during sporulation in Bacillus subtilis. J. Mol. Biol. 284, 569-578. doi: 10.1006/jmbi.1998.2202
17. Ge, R., Sun, X., Xiao, C., Yin, X., Shan, W., Chen, Z., et al. (2011). Phosphoproteome analysis of the pathogenic bacterium Helicobacter pylori reveals over-representation of tyrosine phosphorylation and multiply phosphorylated proteins. Proteomics 11, 1449-1461. doi: 10.1002/pmic.201000649
18. Gerwig, J., Kiley, T. B., Gunka, K., Stanley-Wall, N., and Stulke, J. (2014). The protein tyrosine kinases EpsB and PtkA differentially affect biofilm formation in Bacillus subtilis. Microbiology 160, 682-691. doi: 10.1099/mic.0.074971-0
19. Good, M., Tang, G., Singleton, J., Remenyi, A., and Lim, W. A. (2009). The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136, 1085-1097. doi: 10.1016/j.cell.2009.01.049
20. Grangeasse, C., Cozzone, A. J., Deutscher, J., and Mijakovic, I. (2007). Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem. Sci. 32, 86-94. doi: 10.1016/j.tibs.2006.12.004
21. Gueiros-Filho, F. J., and Losick, R. (2002). A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev. 16, 2544-2556. doi: 10.1101/gad.1014102
22. Hanks, S. K., Quinn, A. M., and Hunter, T. (1988). The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52. doi: 10.1126/science.3291115
23. Hempel, A. M., Cantlay, S., Molle, V., Wang, S. B., Naldrett, M. J., Parker, J. L., et al. (2012). The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc. Natl. Acad. Sci. U.S.A. 109, E2371-E2379. doi: 10.1073/pnas.1207409109
24. Jadeau, F., Grangeasse, C., Shi, L., Mijakovic, I., Deleage, G., and Combet, C. (2012). BYKdb: the Bacterial protein tYrosine Kinase database. Nucleic Acids Res. 40, D321-D324. doi: 10.1093/nar/gkr915
25. James, P., Halladay, J., and Craig, E. A. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436.
26. Jers, C., Kobir, A., Sondergaard, E. O., Jensen, P. R., and Mijakovic, I. (2011). Bacillus subtilis two-component system sensory kinase DegS is regulated by serine phosphorylation in its input domain. PLoS ONE 6:e14653. doi: 10.1371/journal.pone.0014653
27. Jers, C., Pedersen, M. M., Paspaliari, D. K., Schutz, W., Johnsson, C., Soufi, B., et al. (2010). Bacillus subtilis BY-kinase PtkA controls enzyme activity and localization of its protein substrates. Mol. Microbiol. 77, 287-299. doi: 10.1111/j.1365-2958.2010.07227.x
28. Kang, C. M., Abbott, D. W., Park, S. T., Dascher, C. C., Cantley, L. C., and Husson, R. N. (2005). The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev. 19, 1692-1704. doi: 10.1101/gad.1311105
29. Kang, C. M., Vijay, K., and Price, C. W. (1998). Serine kinase activity of a Bacillus subtilis switch protein is required to transduce environmental stress signals but not to activate its target PP2C phosphatase. Mol. Microbiol. 30, 189-196. doi: 10.1046/j.1365-2958.1998.01052.x
30. Kawai, Y., and Ogasawara, N. (2006). Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152, 1129-1141. doi: 10.1099/mic.0.28497-0
31. Kiley, T. B., and Stanley-Wall, N. R. (2010). Post-translational control of Bacillus subtilis biofilm formation mediated by tyrosine phosphorylation. Mol. Microbiol. 78, 947-963. doi: 10.1111/j.1365-2958.2010.07382.x
32. Kobayashi, K., Ogura, M., Yamaguchi, H., Yoshida, K., Ogasawara, N., Tanaka, T., et al. (2001). Comprehensive DNA microarray analysis of Bacillus subtilis two-component regulatory systems. J. Bacteriol. 183, 7365-7370. doi: 10.1128/JB.183.24.7365-7370.2001
33. Krishnamurthy, M., Tadesse, S., Rothmaier, K., and Graumann, P. L. (2010). A novel SMC-like protein, SbcE (YhaN), is involved in DNA double-strand break repair and competence in Bacillus subtilis. Nucleic Acids Res. 38, 455-466. doi: 10.1093/nar/gkp909
34. Kunkel, B., Losick, R., and Stragier, P. (1990). The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. Genes Dev. 4, 525-535. doi: 10.1101/gad.4.4.525
35. Lee, C. D., and Wang, T. F. (2009). The N-terminal domain of Escherichia coli RecA have multiple functions in promoting homologous recombination. J. Biomed. Sci. 16:37. doi: 10.1186/1423-0127-16-37
36. Lee, S., and Price, C. W. (1993). The minCD locus of Bacillus subtilis lacks the minE determinant that provides topological specificity to cell division. Mol. Microbiol. 7, 601-610. doi: 10.1111/j.1365-2958.1993.tb01151.x
37. Levin, P. A., Margolis, P. S., Setlow, P., Losick, R., and Sun, D. (1992). Identification of Bacillus subtilis genes for septum placement and shape determination. J. Bacteriol. 174, 6717-6728.
38. Lin, M. H., Hsu, T. L., Lin, S. Y., Pan, Y. J., Jan, J. T., Wang, J. T., et al. (2009). Phosphoproteomics of Klebsiella pneumoniae NTUH-K2044 reveals a tight link between tyrosine phosphorylation and virulence. Mol. Cell. Proteomics 8, 2613-2623. doi: 10.1074/mcp.M900276-MCP200
39. Lusetti, S. L., and Cox, M. M. (2002). The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu. Rev. Biochem. 71, 71-100. doi: 10.1146/annurev.biochem.71.083101.133940
40. Macek, B., Mijakovic, I., Olsen, J. V., Gnad, F., Kumar, C., Jensen, P. R., et al. (2007). The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol. Cell. Proteomics 6, 697-707. doi: 10.1074/mcp.M600464-MCP200
41. Machida, K., and Mayer, B. J. (2009). Detection of protein-protein interactions by far-western blotting. Methods Mol. Biol. 536, 313-329. doi: 10.1007/978-1-59745-542-8_34
42. Madec, E., Laszkiewicz, A., Iwanicki, A., Obuchowski, M., and Seror, S. (2002). Characterization of a membrane-linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes. Mol. Microbiol. 46, 571-586. doi: 10.1046/j.1365-2958.2002.03178.x
43. Marchadier, E., Carballido-Lopez, R., Brinster, S., Fabret, C., Mervelet, P., Bessieres, P., et al. (2011). An expanded protein-protein interaction network in Bacillus subtilis reveals a group of hubs: exploration by an integrative approach. Proteomics 11, 2981-2991. doi: 10.1002/pmic.201000791
44. Marston, A. L., Thomaides, H. B., Edwards, D. H., Sharpe, M. E., and Errington, J. (1998). Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev. 12, 3419-3430. doi: 10.1101/gad.12.21.3419
45. Mijakovic, I., Musumeci, L., Tautz, L., Petranovic, D., Edwards, R. A., Jensen, P. R., et al. (2005a). In vitro characterization of the Bacillus subtilis protein tyrosine phosphatase YwqE. J. Bacteriol. 187, 3384-3390. doi: 10.1128/JB.187.10.3384-3390.2005
46. Mijakovic, I., Petranovic, D., Bottini, N., Deutscher, J., and Ruhdal Jensen, P. (2005b). Protein-tyrosine phosphorylation in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 9, 189-197. doi: 10.1159/000089647
47. Mijakovic, I., Petranovic, D., Macek, B., Cepo, T., Mann, M., Davies, J., et al. (2006). Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine. Nucleic Acids Res. 34, 1588-1596. doi: 10.1093/nar/gkj514
48. Mijakovic, I., Poncet, S., Boel, G., Maze, A., Gillet, S., Jamet, E., et al. (2003). Transmembrane modulator-dependent bacterial tyrosine kinase activates UDP-glucose dehydrogenases. EMBO J. 22, 4709-4718. doi: 10.1093/emboj/cdg458
49. Musumeci, L., Bongiorni, C., Tautz, L., Edwards, R. A., Osterman, A., Perego, M., et al. (2005). Low-molecular-weight protein tyrosine phosphatases of Bacillus subtilis. J. Bacteriol. 187, 4945-4956. doi: 10.1128/JB.187.14.4945-4956.2005
50. Nicolas, P., Mader, U., Dervyn, E., Rochat, T., Leduc, A., Pigeonneau, N., et al. (2012). Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335, 1103-1106. doi: 10.1126/science.1206848
51. Noirot-Gros, M. F., Dervyn, E., Wu, L. J., Mervelet, P., Errington, J., Ehrlich, S. D., et al. (2002). An expanded view of bacterial DNA replication. Proc. Natl. Acad. Sci. U.S.A. 99, 8342-8347. doi: 10.1073/pnas.122040799
52. Obuchowski, M., Madec, E., Delattre, D., Boel, G., Iwanicki, A., Foulger, D., et al. (2000). Characterization of PrpC from Bacillus subtilis, a member of the PPM phosphatase family. J. Bacteriol. 182, 5634-5638. doi: 10.1128/JB.182.19.5634-5638.2000
53. Orchard, S., Ammari, M., Aranda, B., Breuza, L., Briganti, L., Broackes-Carter, F., et al. (2014). The MIntAct project-IntAct as a common curation platform for 11 molecular interaction databases. Nucleic Acids Res. 42, D358-D363. doi: 10.1093/nar/gkt1115
54. Pane-Farre, J., Lewis, R. J., and Stulke, J. (2005). The RsbRST stress module in bacteria: a signalling system that may interact with different output modules. J. Mol. Microbiol. Biotechnol. 9, 65-76. doi: 10.1159/000088837
55. Pawson, T., and Scott, J. D. (1997). Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2075-2080. doi: 10.1126/science.278.5346.2075
56. Pereira, S. F., Goss, L., and Dworkin, J. (2011). Eukaryote-like serine/threonine kinases and phosphatases in bacteria. Microbiol. Mol. Biol. Rev. 75, 192-212. doi: 10.1128/MMBR.00042-10
57. Petranovic, D., Michelsen, O., Zahradka, K., Silva, C., Petranovic, M., Jensen, P. R., et al. (2007). Bacillus subtilis strain deficient for the protein-tyrosine kinase PtkA exhibits impaired DNA replication. Mol. Microbiol. 63, 1797-1805. doi: 10.1111/j.1365-2958.2007.05625.x
58. Pietack, N., Becher, D., Schmidl, S. R., Saier, M. H., Hecker, M., Commichau, F. M., et al. (2010). In vitro phosphorylation of key metabolic enzymes from Bacillus subtilis: PrkC phosphorylates enzymes from different branches of basic metabolism. J. Mol. Microbiol. Biotechnol. 18, 129-140. doi: 10.1159/000308512
59. Pompeo, F., Luciano, J., Brochier-Armanet, C., and Galinier, A. (2011). The GTPase function of YvcJ and its subcellular relocalization are dependent on growth conditions in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 20, 156-167. doi: 10.1159/000329298
60. Saalbach, G., Hempel, A. M., Vigouroux, M., Flardh, K., Buttner, M. J., and Naldrett, M. J. (2013). Determination of phosphorylation sites in the DivIVA cytoskeletal protein of Streptomyces coelicolor by targeted LC-MS/MS. J. Proteome Res. 12, 4187-4192. doi: 10.1021/pr400524d
61. Shi, L., Kobir, A., Jers, C., and Mijakovic, I. (2010). Bacterial Protein-Tyrosine Kinases. Curr. Proteomics 7, 188-194. doi: 10.2174/157016410792928198
62. Shi, L., Pigeonneau, N., Ravikumar, V., Dobrinic, P., Macek, B., Franjevic, D., et al. (2014). Cross-phosphorylation of bacterial serine/threonine and tyrosine protein kinases on key regulatory residues. Front. Microbiol. 5:495. doi: 10.3389/fmicb.2014.00495
63. Soufi, B., Kumar, C., Gnad, F., Mann, M., Mijakovic, I., and Macek, B. (2010). Stable isotope labeling by amino acids in cell culture (SILAC) applied to quantitative proteomics of Bacillus subtilis. J. Proteome Res. 9, 3638-3646. doi: 10.1021/pr100150w
64. Sun, X., Ge, F., Xiao, C. L., Yin, X. F., Ge, R., Zhang, L. H., et al. (2010). Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. J. Proteome Res. 9, 275-282. doi: 10.1021/pr900612v
65. Surdova, K., Gamba, P., Claessen, D., Siersma, T., Jonker, M. J., Errington, J., et al. (2013). The conserved DNA-binding protein WhiA is involved in cell division in Bacillus subtilis. J. Bacteriol. 195, 5450-5460. doi: 10.1128/JB.00507-13
66. Vagner, V., Dervyn, E., and Ehrlich, S. D. (1998). A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144 (Pt 11), 3097-3104. doi: 10.1099/00221287-144-11-3097
67. Weir, M., and Keeney, J. B. (2014). PCR mutagenesis and gap repair in yeast. Methods Mol. Biol. 1205, 29-35. doi: 10.1007/978-1-4939-1363-3_3
68. Whitfield, C. (2006). Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75, 39-68. doi: 10.1146/annurev.biochem.75.103004.142545
69. Wu, L. J., and Errington, J. (2003). RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol. Microbiol. 49, 1463-1475. doi: 10.1046/j.1365-2958.2003.03643.x
70. Wu, Y., Li, Q., and Chen, X. Z. (2007). Detecting protein-protein interactions by Far western blotting. Nat Protoc. 2, 3278-3284. doi: 10.1038/nprot.2007.459