Cross-phosphorylation of bacterial serine/threonine and tyrosine protein kinases on key regulatory residues

Frontiers in Microbiology

Volumn 5, Issue SEP, 2014, Pages

  Shi, Lei ^a   Pigeonneau, Nathalie ^b   Ravikumar, Vaishnavi ^c   Dobrinic, Paula ^d   Macek, Boris ^c   Franjevic, Damjan ^d   Noirot Gros, Marie Francoise ^b   Mijakovic, Ivan ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b UMR1319 MICALIS   (France)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

bacterial protein kinase; kinase activation; phosphorylation cascade; protein kinase cross talk; Protein phosphorylation

Indexed keywords

AMINO ACID; PRKC KINASE; PRKD KINASE; PROTEIN HISTIDINE KINASE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; PTKA KINASE; SPOIIAB; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; YABT KINASE;

ARTICLE; AUTOPHOSPHORYLATION; AUTORADIOGRAPHY; BACILLUS SUBTILIS; DNA SEQUENCE; ENZYME PHOSPHORYLATION; ESCHERICHIA COLI; GENETIC ANALYSIS; MAP KINASE ASSAY; MASS SPECTROMETRY; MOLECULAR BIOLOGY; MOLECULAR MODEL; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PEPTIDE ANALYSIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS);

EID: 84907614613     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00495     Document Type: Article

References (44)

1. Absalon, C., Obuchowski, M., Madec, E., Delattre, D., Holland, I. B., and Séror, S. J. (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. doi: 10.1099/mic.0.022475-0
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. Barthe, P., Mukamolova, G. V., Roumestand, C., and Cohen-Gonsaud, M. (2010). The structure of PknB extracellular PASTA domain from Mycobacterium tuberculosis suggests a ligand-dependent kinase activation. Structure 18, 606-615. doi: 10.1016/j.str.2010.02.013
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. Bordoli, L., Kiefer, F., Arnold, K., Benkert, P., Battey, J., and Schwede, T. (2009). Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4, 1-13. doi: 10.1038/nprot.2008.197
6. Burbulys, D., Trach, K. A., and Hoch, J. A. (1991). Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64, 545-552. doi: 10.1016/0092-8674(91)90238-T
7. Campbell, E. A., Masuda, S., Sun, J. L., Muzzin, O., Olson, C. A., Wang, S., et al. (2002). Crystal structure of the Bacillus stearothermophilus anti-sigma factor SpoIIAB with the sporulation sigma factor sigmaF. Cell 108, 795-807. doi: 10.1016/S0092-8674(02)00662-1
8. Colinge, J., César-Razquin, A., Huber, K., Breitwieser, F. P., Májek, P., and Superti-Furga, G. (2014). Building and exploring an integrated human kinase network: global organization and medical entry points. J. Proteomics 107, 113-127. doi: 10.1016/j.jprot.2014.03.028
9. Cousin, C., Derouiche, A., Shi, L., Pagot, Y., Poncet, S., and Mijakovic, I. (2013). Protein-serine/threonine/tyrosine kinases in bacterial signaling and regulation. FEMS Microbiol. Lett. 346, 11-19. doi: 10.1111/1574-6968.12189
10. 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
11. Gerwig, J., Kiley, T. B., Gunka, K., Stanley-Wall, N., and Stülke, 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
12. Goulian, M. (2010). Two-component signaling circuit structure and properties. Curr. Opin. Microbiol. 13, 184-189. doi: 10.1016/j.mib.2010.01.009
13. Grundner, C., Gay, L. M., and Alber, T. (2005). Mycobacterium tuberculosis serine/threonine kinases PknB, PknD, PknE, and PknF phosphorylate multiple FHA domains. Protein Sci. 14, 1918-1921. doi: 10.1110/ps.051413405
14. Hanson, K. G., Steinhauer, K., Reizer, J., Hillen, W., and Stülke, J. (2002). HPr kinase/phosphatase of Bacillus subtilis: expression of the gene and effects of mutations on enzyme activity, growth and carbon catabolite repression. Microbiology 148, 1805-1811. Available online at: http://mic.sgmjournals.org/content/148/6/1805.long
15. 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.
16. Jers, C., Kobir, A., Søndergaard, 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
17. Jers, C., Pedersen, M. M., Paspaliari, D. K., Schütz, 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
18. Joseph, P., Guiseppi, A., Sorokin, A., and Denizot, F. (2004). Characterization of the Bacillus subtilis YxdJ response regulator as the inducer of expression for the cognate ABC transporter YxdLM. Microbiology 150, 2609-2617. doi: 10.1099/mic.0.27155-0
19. 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
20. Katoh, K., and Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9, 286-298. doi: 10.1093/bib/bbn013
21. Kobir, A., Poncet, S., Bidnenko, V., Delumeau, O., Jers, C., Zouhir, S., et al. (2014). Phosphorylation of Bacillus subtilis gene regulator AbrB modulates its DNA-binding properties. Mol. Microbiol. 92, 1129-1141. doi: 10.1111/mmi.12617
22. 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. Proteom. 6, 697-707. doi: 10.1074/mcp.M600464-MCP200
23. Madec, E., Laszkiewicz, A., Iwanicki, A., Obuchowski, M., and Séror, 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
24. Márquez, J. A., Hasenbein, S., Koch, B., Fieulaine, S., Nessler, S., Russell, R. B., et al. (2002). Structure of the full-length HPr kinase/phosphatase from Staphylococcus xylosus at 1.95 A resolution: mimicking the product/substrate of the phospho transfer reactions. Proc. Natl. Acad. Sci. U.S.A. 99, 3458-3463. doi: 10.1073/pnas.052461499
25. Marshall, C. J. (1994). MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4, 82-89. doi: 10.1016/0959-437X(94)90095-7
26. Masuda, S., Murakami, K. S., Wang, S., Anders Olson, C., Donigian, J., Leon, F., et al. (2004). Crystal structures of the ADP and ATP bound forms of the Bacillus anti-sigma factor SpoIIAB in complex with the anti-anti-sigma SpoIIAA. J. Mol. Biol. 340, 941-956. doi: 10.1016/j.jmb.2004.05.040
27. Mijakovic, I., Musumeci, L., Tautz, L., Petranovic, D., Edwards, R. A., Jensen, P. R., et al. (2005). 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
28. Mijakovic, I., Poncet, S., Boël, G., Maz,é, 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
29. Min, K. T., Hilditch, C. M., Diederich, B., Errington, J., and Yudkin, M. D. (1993). Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase. Cell 74, 735-742. doi: 10.1016/0092-8674(93)90520-Z
30. Molle, V., and Kremer, L. (2010). Division and cell envelope regulation by Ser/Thr phosphorylation: Mycobacterium shows the way. Mol. Microbiol. 75, 1064-1077. doi: 10.1111/j.1365-2958.2009.07041.x
31. 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
32. Nicolas, P., Mäder, 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
33. 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
34. Olivares-Illana, V., Meyer, P., Bechet, E., Gueguen-Chaignon, V., Soulat, D., Lazereg-Riquier, S., et al. (2008). Structural basis for the regulation mechanism of the tyrosine kinase CapB from Staphylococcus aureus. PLoS Biol. 6:e143. doi: 10.1371/journal.pbio.0060143
35. 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
36. Petranovic, D., Grangeasse, C., Macek, B., Abdillatef, M., Gueguen-Chaignon, V., Nessler, S., et al. (2009). Activation of Bacillus subtilis Ugd by the BY-kinase PtkA proceeds via phosphorylation of its residue tyrosine 70. J. Mol. Microbiol. Biotechnol. 17, 83-89. doi: 10.1159/000206635
37. Podgornaia, A. I., and Laub, M. T. (2013). Determinants of specificity in two-component signal transduction. Curr. Opin. Microbiol. 16, 156-162. doi: 10.1016/j.mib.2013.01.004
38. Rakette, S., Donat, S., Ohlsen, K., and Stehle, T. (2012). Structural analysis of Staphylococcus aureus serine/threonine kinase PknB. PLoS ONE 7:e39136. doi: 10.1371/journal.pone.0039136
39. Ravikumar, V., Shi, L., Krug, K., Derouiche, A., Jers, C., Cousin, C., et al. (2014). Quantitative phosphoproteome analysis of Bacillus subtilis reveals novel substrates of the kinase PrkC and phosphatase PrpC. Mol. Cell. Proteom. 13, 1965-1978. doi: 10.1074/mcp.M113.035949
40. Ravikumar, V., Shi, L., Krug, K., Derouiche, A., Jers, C., Cousin, C., et al. (2014). Quantitative phosphoproteome analysis of Bacillus subtilis reveals novel substrates of the kinase PrkC and phosphatase PrpC. Mol. Cell. Proteom. 13, 1965-1978. doi: 10.1074/mcp.M113.035949
41. Shah, I. M., Laaberki, M. H., Popham, D. L., and Dworkin, J. (2008). A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135, 486-496. doi: 10.1016/j.cell.2008.08.039
42. Shi, L., Ji, B., Kolar-Znika, L., Boskovic, A., Jadeau, F., Combet, C., et al. (2014). Evolution of bacterial protein-tyrosine kinases and their relaxed specificity toward substrates. Genome Biol. Evol. 6, 800-817. doi: 10.1093/gbe/evu056
43. Yang, X., Kang, C. M., Brody, M. S., and Price, C. W. (1996). Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev. 10, 2265-2275. doi: 10.1101/gad.10.18.2265
44. Young, T. A., Delagoutte, B., Endrizzi, J. A., Falick, A. M., and Alber, T. (2003). Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat. Struct. Biol. 10, 168-174. doi: 10.1038/nsb897