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Vol. 9, No. 3-4, 2005
Issue release date: January 2006
J Mol Microbiol Biotechnol 2005;9:125–131
(DOI:10.1159/000089641)

Ser/Thr/Tyr Protein Phosphorylation in Bacteria – For Long Time Neglected, Now Well Established

Deutscher J. · Saier Jr. M.H.
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Abstract

The first clearly established example of Ser/Thr/Tyr phosphorylation of a bacterial protein was isocitrate dehydrogenase. In 1979, 25 years after the discovery of protein phosphorylation in eukaryotes, this enzyme was reported to become phosphorylated on a serine residue. In subsequent years, numerous other bacterial proteins phosphorylated on Ser, Thr or Tyr were discovered and the corresponding protein kinases and P-protein phosphatases were identified. These protein modifications regulate all kinds of physiological processes. Ser/Thr/Tyr phosphorylation in bacteria therefore seems to play a similar important role as in eukaryotes. Surprisingly, many bacterial protein kinases do not exhibit any similarity to eukaryotic protein kinases, but rather resemble nucleotide-binding proteins or kinases phosphorylating diverse low-molecular-weight substrates.



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References

  1. Allen, G.S., Steinhauer, K., Hillen, W., Stülke, J., Brennan, R.G. 2003. Crystal structure of HPr kinase/phosphatase from Mycoplasma pneumoniae. J Mol Biol 326:1203–1217.
  2. Alzari, P.M. 2004. First structural glimpse at a bacterial Ser/Thr protein phosphatase. Structure 12:1923–1924.
  3. Barford, D. 1995. Protein phosphatases. Curr Opin Struct Biol 5:728–734.
  4. Bender, M.H., Yother, J. 2001. CpsB is a modulator of capsule-associated tyrosine kinase activity in Streptococcus pneumoniae. J Biol Chem 276:47966–47974.
  5. Boël, G., Mijakovic, I., Mazé, A., Poncet, S., Taha, M.-K., Larribe, M., Darbon, E., Khemiri, A., Galinier, A., Deutscher, J. 2003. Transcription regulators potentially controlled by HPr kinase/phosphorylase in gram-negative bacteria. J Mol Microbiol Biotechnol 5:206–215.
  6. Cohen, P., Rylatt, D.B., Nimmo, G.A. 1977. The hormonal control of glycogen metabolism: the amino acid sequence at the phosphorylation site of protein phosphatase inhibitor-1. FEBS Lett 76:182–186.
  7. Cordell, S.C., Lowe, J. 2001. Crystal structure of the bacterial cell division regulator MinD. FEBS Lett 492:160–165.
  8. Cori, G.T., Green, A.A. 1943. Crystalline muscle phosphorylase. II. Prosthetic group. J Biol Chem 151:31–38.
  9. Cortay, J.C., Rieul, C., Duclos, B., Cozzone, A.J. 1986. Characterization of the phosphoproteins of Escherichia coli cells by electrophoretic analysis. Eur J Biochem 159:227–237.
  10. Cozzone, A.J. 2005. Role of protein phosphorylation on serine/threonine and tyrosine in the virulence of bacterial pathogens. J Mol Biol Biotechnol 9:198–213.
  11. Cozzone, A.J., El-Mansi, M. 2005. Control of isocitrate dehydrogenase catalytic activity by protein phosphorylation in Escherichia coli. J Mol Microbiol Biotechnol 9:132–146.
  12. de Verdier, C.-H. 1952. Isolation of phosphothreonine from bovine casein. Nature 170:804–805.
  13. DeLange, R.J., Kemp, R.G., Riley, W.D., Cooper, R.A., Krebs, E.G. 1968. Activation of skeletal muscle phosphorylase kinase by adenosine triphosphate and adenosine 3′,5′-monophosphate. J Biol Chem 243:2200–2208.
  14. Deutscher, J., Galinier, A., Martin-Verstraete, I. 2002. Carbohydrate uptake and metabolism; in Sonenshein, A.L., Hoch, J.A., Losick, R. (eds.): Bacillus subtilis and Its Closest Relatives: From Genes to Cells. Washington, ASM Press, pp 129–150.
  15. Deutscher, J., Herro, R., Bourand, A., Mijakovic, I., Poncet, P. 2005. P-Ser-HPr – a link between carbon metabolism and the virulence of certain pathogenic bacteria. Biochim Biophys Acta [epub ahead of print].
  16. Deutscher, J., Küster, E., Bergstedt, U., Charrier, V., Hillen, W. 1995. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol Microbiol 15:1049–1053.
  17. Deutscher, J., Saier, M.H. 1983. ATP-dependent protein kinase-catalyzed phosphorylation of a seryl residue in HPr, a phosphate carrier protein of the phosphotransferase system in Streptococcus pyogenes. Proc Natl Acad Sci USA 80:6790–6794.
  18. Duclos, B., Grangeasse, C., Vaganay, E., Riberty, M., Cozzone, A.J. 1996. Autophosphorylation of a bacterial protein at tyrosine. J Mol Biol 259:891–895.
  19. Duncan, L., Alper, S., Arigoni, F., Losick, R., Stragier, P. 1995. Activation of cell-specific transcription by a serine phosphatase at the site of asymmetric division. Science 270:641–644.
  20. Durocher, D., Taylor, I.A., Sarbassova, D., Haire, L.F., Westcott, S.L., Jackson, S.P., Smerdon, S.J., Yaffe, M.B. 2000. The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol Cell 6:1169–1182.
  21. Fieulaine, S., Morera, S., Poncet, S., Mijakovic, I., Galinier, A., Janin, J., Deutscher, J., Nessler, S. 2002. X-ray structure of a bifunctional protein kinase in complex with its protein substrate HPr. Proc Natl Acad Sci USA 99:13437–13441.
  22. Fieulaine, S., Morera, S., Poncet, S., Monedero, V., Gueguen-Chaignon, V., Galinier, A., Janin, J., Deutscher, J., Nessler, S. 2001. X-ray structure of HPr kinase: A bacterial protein kinase with a P-loop nucleotide binding domain. EMBO J 20:3917–3927.
  23. Fischer, E.H., Krebs, E.G. 1955. Conversion of phosphorylase b to phosphorylase a in muscle extracts. J Biol Chem 216:121–132.
  24. Fujita, Y., Miwa, Y., Galinier, A., Deutscher, J. 1995. Specific recognition of the Bacillus subtilisgntcis-acting catabolite-responsive element by a protein complex formed between CcpA and seryl-phosphorylated HPr. Mol Microbiol 17:953–960.
  25. Galinier, A., Kravanja, M., Engelmann, R., Hengstenberg, W., Kilhoffer, M.-C., Deutscher, J., Haiech, J. 1998. New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc Natl Acad Sci USA 95:1823–1828.
  26. Garnak, M., Reeves, H.C. 1979. Phosphorylation of isocitrate dehydrogenase of Escherichia coli. Science 203:1111–1112.
  27. Gonzalez, C.F., Stonestrom, A.J., Lorca, G.L., Saier, M.H., Jr. 2005. Biochemical characterization of phosphoryl transfer involving HPr of the phosphoenolpyruvate-dependent phosphotransferase system in Treponema denticola, an organism that lacks PTS permeases. Biochemistry 44:598–608.
  28. Grangeasse, C., Obadia, B., Mijakovic, I., Deutscher, J., Cozzone, A.J., Doublet, P. 2003. Autophosphorylation of the Escherichia coli protein kinase Wzc regulates tyrosine phosphorylation of Ugd, a UDP-glucose dehydrogenase. J Biol Chem 278:39323–39329.
  29. Greenstein, A.E., Grundner, C., Echols, N., Gay, L.M., Lombana, T.N., Miecskowski, C.A., Pullen, K.E., Sung, P., Alber, T. 2005. Structure/function studies of Ser/Thr/Tyr protein phosphorylation in Mycobacterium tuberculosis. J Mol Microbiol Biotechnol 9:167–181.
  30. Hanks, S.K., Quinn, A.M., Hunter, T. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52.
  31. Hayashi, I., Oyama, T., Morikawa, K. 2001. Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus. EMBO J 20:1819–1828.
  32. Herro, R., Poncet, S., Cossart, P., Buchrieser, C., Gouin, E., Glaser, P., Deutscher, J. 2005. How seryl-phosphorylated HPr inhibits PrfA, a transcription activator of Listeria monocytogenes virulence genes. J Mol Microbiol Biotechnol 9:224–234.
  33. Hofmann, K., Bucher, P. 1995. The FHA domain: a putative nuclear signalling domain found in protein kinases and transcription factors. Trends Biochem Sci 20:347–349.
  34. Hu, K.-Y., Saier, M.H., Jr. 2002. Phylogeny of phosphoryl transfer proteins of the phosphoenolpyruvate-dependent sugar transporting phosphotransferase system. Res Microbiol 153:405–415.
  35. Hunter, T., Sefton, B.M. 1980. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci USA 77:1311–1315.
  36. Iwanicki, A., Herman-Antosiewicz, A., Pierechod, M., Seror, S.J., Obuchowski, M. 2002. PrpE, a PPP protein phosphatase from Bacillus subtilis with unusual substrate specificity. Biochem J 366:929–936.
  37. Kennelly, P.J. 2002. Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. FEMS Microbiol Lett 206:1–8.
  38. Kim, C., Xuong, N.H., Taylor, S.S. 2005. Crystal structure of a complex between the catalytic and regulatory (RIα) subunits of PKA. Science 307:690–696.
  39. Kirstein, J., Turgay, K. 2005. A new tyrosine phosphorylation mechanism involved in signal transduction in Bacillus subtilis. J Mol Microbiol Biotechnol 9:182–188.
  40. Kirstein, J., Zühlke, D., Gerth, U., Turgay, K., Hecker, M. 2005. A tyrosine kinase and its activator control the activity of the CtsR heat shock repressor in B. subtilis. EMBO J 24: 3435–3445.
  41. Klein, G., Dartigalongue, C., Raina, S. 2003. Phosphorylation-mediated regulation of heat shock response in Escherichia coli. Mol Microbiol 48:269–285.
  42. Knighton, D.R., Zheng, J.H., Ten Eyck, L.F., Ashford, V.A., Xuong, N.H., Taylor, S.S., Sowadski, J.M. 1991a. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253:407–414.
  43. Knighton, D.R., Zheng, J.H., Ten Eyck, L.F., Xuong, N.H., Taylor, S.S., Sowadski, J.M. 1991b. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253:414–420.
  44. Kravanja, M., Engelmann, R., Dossonnet, V., Blüggel, M., Meyer, H.E., Frank, R., Galinier, A., Deutscher, J., Schnell, N., Hengstenberg, W. 1999. The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: the HPr kinase/phosphatase. Mol Microbiol 31:59–66.
  45. LaPorte, D.C., Chung, T. 1985. A single gene codes for the kinase and phosphatase which regulate isocitrate dehydrogenase. J Biol Chem 260:15291–15297.
  46. Lipmann, F.A., Levene, P.A. 1932. Serinephosphoric acid obtained on hydrolysis of vitellinic acid. J Biol Chem 98:109–114.
  47. Manai, M., Cozzone, A.J. 1979. Analysis of the protein-kinase activity of Escherichia coli cells. Biochem Biophys Res Commun 91:819–826.
  48. Marquez, J.A., Hasenbein, S., Koch, B., Fieulaine, S., Nessler, S., Russell, R.B., Hengstenberg, W., Scheffzek, K. 2002. Structure of the full-length HPr kinase/phosphatase from Staphylococcus xylosus at 1.95 Å resolution: mimicking the product/substrate of the phospho transfer reactions. Proc Natl Acad Sci USA 99:3458–3463.
  49. Matsumoto, A., Hong, S.K., Ishizuka, H., Horinouchi, S., Beppu, T. 1994. Phosphorylation of the AfsR protein involved in secondary metabolism in Streptomyces species by a eukaryotic-type protein kinase. Gene 146:47–56.
  50. Mijakovic, I., Musumeci, L., Tautz, L., Petranovic, D., Edwards, R.A., Jensen, P.R., Mustelin, T., Deutscher, J., Bottini, N. 2005a. In vitro characterization of the Bacillus subtilis protein tyrosine phosphatase YwqE. J Bacteriol 187:3384–3390.
  51. Mijakovic, I., Petranovic, D., Bottini, N., Deutscher, J., Jensen, P.R. 2005b. Protein-tyrosine phosphorylation in Bacillus subtilis. J Mol Microbiol Biotechnol 9:189–197.
  52. Mijakovic, I., Poncet, S., Boël, G., Mazé, A., Gillet, S., Jamet, E., Decottignies, P., Grangeasse, C., Doublet, P., Le Maréchal, P., Deutscher, J. 2003. Transmembrane modulator-dependent bacterial tyrosine kinase activates UDP-glucose dehydrogenases. EMBO J 22:4709–4718.
  53. Mijakovic, I., Poncet, S., Galinier, A., Monedero, V., Fieulaine, S., Janin, J., Nessler, S., Marquez, J.A., Scheffzek, K., Hasenbein, S., Hengstenberg, W., Deutscher, J. 2002. Pyrophosphate-producing protein dephosphorylation by HPr kinase/phosphorylase: a relic of early life? Proc Natl Acad Sci USA 99:13442–13447.
  54. Molle, V., Soulat, D., Jault, J.M., Grangeasse, C., Cozzone, A.J., Prost, J.F. 2004. Two FHA domains on an ABC transporter, Rv1747, mediate its phosphorylation by PknF, a Ser/Thr protein kinase from Mycobacterium tuberculosis. FEMS Microbiol Lett 234:215–223.
  55. Munoz-Dorado, J., Inouye, S., Inouye, M. 1991. A gene encoding a protein serine/threonine kinase is required for normal development of M. xanthus, a gram-negative bacterium. Cell 67:995–1006.
  56. Najafi, S.M., Willis, A.C., Yudkin, M.D. 1995. Site of phosphorylation of SpoIIAA, the anti-anti-sigma factor for sporulation-specific sigma F of Bacillus subtilis. J Bacteriol 177:2912–2913.
  57. Nariya, H., Inouye, S. 2005. Factors that modulate the Pkn4 kinase cascade in Myxococcus xanthus. J Mol Microbiol Biotechnol 9:147–153.
  58. Nimmo, G.A., Cohen, P. 1978. The regulation of glycogen metabolism. Phosphorylation of inhibitor-1 from rabbit skeletal muscle, and its interaction with protein phosphatases-III and -II. Eur J Biochem 15:353–365.
  59. Obuchowski, M., Madec, E., Delattre, D., Boël, G., Iwanicki, A., Foulger, D., Seror, S.J. 2000. Characterization of PrpC from Bacillus subtilis, a member of the PPM phosphatase family. J Bacteriol 182:5634–5638.
  60. Ortiz-Lombardia, M., Pompeo, F., Boitel, B., Alzari, P.M. 2003. Crystal structure of the catalytic domain of the PknB serine/threonine kinase from Mycobacterium tuberculosis. J Biol Chem 278:13094–13100.
  61. Pallen, M., Chaudhuri, R., Khan, A. 2002. Bacterial FHA domains: neglected players in the phospho-threonine signalling game? Trends Microbiol 10:556–563.
  62. Pawson, T., Gish, G.D. 1992. SH2 and SH3 domains: from structure to function. Cell 71:359–362.
  63. Postma, P.W., Lengeler, J.W., Jacobson, G.R. 1993. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57:543–594.
  64. Pullen, K.E., Ng, H.L., Sung, P.Y., Good, M.C., Smith, S.M., Alber, T. 2004. An alternate conformation and a third metal in PstP/Ppp, the M. tuberculosis PP2C-family Ser/Thr protein phosphatase. Structure 12:1947–1954.
  65. Rafter, G.W. 1964. Identification of a new form of bound phosphoserine in Escherichia coli. J Biol Chem 239:1044–1047.
  66. Rahmsdorf, H.-J., Pai, S.H., Ponta, H., Herrlich, P., Roskoski, J.R., Schweiger, M., Studier, F.W. 1974. Protein kinase induction in Escherichia coli by bacteriophage T7. Proc Natl Acad Sci USA 71:586–589.
  67. Rahmsdorf, H.J., Herrlich, P., Pai, S.H., Schweiger, M., Wittmann, H.G. 1973. Ribosomes after infection with bacteriophage T4 and T7. Mol Gen Genet 127:259–271.
  68. Reizer, J., Novotny, M.J., Panos, C., Saier, M.H., Jr. 1983. Mechanism of inducer expulsion in Streptococcus pyogenes: A two-step process activated by ATP. J Bacteriol 156:354–361.
  69. Riley, W.D., DeLange, R.J., Bratvold, G.E., Krebs, E.G. 1968. Reversal of phosphorylase kinase activation. J Biol Chem 243:2209–2215.
  70. Rouached, H., Berthomieu, P., El Kassis, E., Cathala, N., Catherinot, V., Labesse, G., Davidian, J.C., Fourcroy, P. 2005. Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1.2. J Biol Chem 280:15976–15983.
  71. Saier, M.H., Jr. 1987. Enzymes in Metabolic Pathways. A Comparative Study of Mechanism, Structure, Evolution, and Control. Harper & Row, New York.
  72. Schumacher, M.A., Allen, G.S., Diel, M., Seidel, G., Hillen, W., Brennan, R.G. 2004. Structural basis for allosteric control of the transcription regulator CcpA by the phosphoprotein HPr-Ser46-P. Cell 118:731–741.
  73. Sefton, B.M., Hunter, T., Beemon, K. 1979. Product of in vitro translation of the Rous sarcoma virus src gene has protein kinase activity. J Virol 30:311–318.
  74. Shi, L., Carmichael, W.W., Kennelly, P.J. 1999. Cyanobacterial PPP family protein phosphatases possess multifunctional capabilities and are resistant to microcystin-LR. J Biol Chem 274:10039–10046.
  75. Stonestrom, A., Gonzalez, C., Saier, M.H., Jr. 2005. Bioinformatic analyses of bacterial HPr kinase homologues. Res Microbiol 156:443–451.
  76. Sutherland, E.W., Wosilait, W.D. 1955. Inactivation and activation of liver phosphorylase. Nature 175:169–170.
  77. Villarino, A., Duran, R., Wehenkel, A., Fernandez, P., England, P., Brodin, P., Cole, S.T., Zimny-Arndt, U., Jungblut, P.R., Cervenansky, C., Alzari, P.M. 2005. Proteomic identification of Mycobacterium tuberculosis protein kinase substrates: PknB recruits GarA, a FHA domain-containing protein, through activation loop-mediated interactions. J Mol Biol 350:953–963.
  78. Wang, J.Y., Koshland, D.E. 1978. Evidence for protein kinase activities in the prokaryote Salmonella typhimurium. J Biol Chem 253:7605–7608.
  79. Wu, J., Ohta, N., Zhao, J.L., Newton, A. 1999. A novel bacterial tyrosine kinase essential for cell division and differentiation. Proc Natl Acad Sci USA 96:13068–13073.
  80. Young, T.A., Delagoutte, B., Endrizzi, J.A., Falick, A.M., Alber, T. 2003. Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat Struct Biol 10:168–174.
  81. Yuan, M., Deleuil, F., Fällman, M. 2005. Interaction between the Yersinia tyrosine phosphatase YopH and its macrophage substrate, Fyn binding protein, FYB. J Mol Microbiol Biotechnol 9:214–223.
  82. Zhang, C.-C., Jang, J., Sakr, S., Wang, L. 2005. Protein phosphorylation on Ser, Thr and Tyr residues in cyanobacteria. J Mol Microbiol Biotechnol 9:154–166.
  83. Zillig, W., Fujiki, H., Blum, W., Janekovic, D., Schweiger, M., Rahmsdorf, H.-J., Ponta, H., Hirsch-Kauffmann, M. 1975. In vivo and in vitro phosphorylation of DNA-dependent RNA polymerase of Escherichia coli by bacteriophage-T7-induced protein kinase. Proc Natl Acad Sci USA 72:2506–2510.


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