Identification and biochemical characterization of a eukaryotic-type serine/threonine kinase and its cognate phosphatase in streptococcus pyogenes: Their biological functions and substrate identification

Journal of Molecular Biology

Volumn 357, Issue 5, 2006, Pages 1351-1372

  Jin, Hong ^a   Pancholi, Vijay ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Group A Streptococcus; phagocytosis and adherence; pharyngeal cells; Ser Thr kinase; Ser Thr protein phosphatase

Indexed keywords

ANTIBODY; HISTONE; HYALURONIC ACID; M PROTEIN; MANGANESE; MEMBRANE PROTEIN; PHOSPHATASE; PROTEIN P10; PROTEIN SERINE THREONINE KINASE; PROTEIN SP STK; PROTEIN SP STP; RECOMBINANT PROTEIN; SECRETORY PROTEIN; THREONINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; BACTERIUM COLONY; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CELL GROWTH; CELL WALL; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; EUKARYOTE; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; IN VITRO STUDY; INDUCED MUTATION; KNOCKOUT GENE; NEUTROPHIL; NONHUMAN; NUCLEOTIDE REPEAT; PHAGOCYTOSIS; PHARYNX; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STREPTOCOCCUS PYOGENES; WILD TYPE;

BACTERIA (MICROORGANISMS); EUKARYOTA; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SP. 'GROUP A';

EID: 33645054791     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.01.020     Document Type: Article

References (78)

1. S.K. Hanks, A.M. Quinn, and T. Hunter The protein kinase family: conserved features and deduced phylogeny of the catalytic domains Science 241 1988 42 52
2. T. Hunter Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling Cell 80 1995 225 236
3. S.K. Hanks, and T. Hunter Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification FASEB J. 9 1995 576 596
4. L. Shi, M. Potts, and P.J. Kennelly The serine, threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait FEMS Microbiol. Rev. 22 1998 229 253
5. C.J. Bakal, and J.E. Davies No longer an exclusive club: eukaryotic signalling domains in bacteria Trends Cell Biol. 10 2000 32 37
6. P.J. Kennelly Archeal protein kinases and protein phosphatases - insights from genomics and biochemistry Biochem. J. 370 2003 373 389
7. P.J. Kennelly Protein kinases and protein phosphatases in prokaryotes: a genomic perspective FEMS Microbiol. Letters 206 2002 1 8
8. J. Munoz-Dorado, S. Inouye, and M. Inouye A gene encoding a protein serine/threonine kinase is required for normal development of M. xanthus, a Gram-negative bacterium Cell 67 1991 995 1006
9. K. Petrickova, and M. Petricek Eukaryotic-type protein kinases in Streptomyces coelicolor: variations on a common theme Microbiol.-Sgm 149 2003 1609 1621
10. L. Yang, W. Zhang, J. Chiao, G. Zhao, and W. Jiang An eukaryotic-type serine/threonine protein kinase involved in the carbon source-dependent pigmant biosynthesis in Amycolatopsis mediterranei U32 Biochem. Biophys. Res. Commun. 284 2001 357 362
11. L. Gonzalez, V. Phalip, and C.C. Zhang Characterization of PknC, a Ser/Thr kinase with broad substrate specificity from the cyanobacterium Anabaena sp. strain PCC 7120 Eur. J. Biochem. 268 2001 1869 1875
12. L. Janda, P. Tichy, J. Spiek, and M. Patiek A deduced Thermomonospora curvata protein containing serine/threonine protein kinase and WD-repeat domains J. Bacteriol. 178 1996 1487 1489
13. E. Madec, A. Laszkiewicz, A. Iwanicki, M. Obuchowski, and S. Seror Characterization of a membrane-linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes Mol. Microbiol. 46 2002 571 586
14. Y. Av-Gay, and M. Everett The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis Trends Microbiol. 8 2000 238 244
15. S. Mukhopadhyay, V. Kapatral, W. Xu, and A.M. Chakrabarty Characterization of a Hank's type serine/threonine kinase and serine/threonine phosphoprotein phosphatase in Pseudomonas aeruginosa J. Bacteriol. 181 1999 6615 6622
16. G.R. Cornelis The Yersinia deadly kiss J. Bacteriol. 180 1998 5495 5504
17. A. Verma, and A.T. Maurelli Identification of two eukaryote-like serine/threonine kinases encoded by Chlamydia trachomatis serovar L2 and characterization of interacting partners of Pkn1 Infect. Immun. 71 2003 5772 5784
18. L. Rajagopal, A. Clancy, and C.E. Rubens 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 2003 14429 14441
19. L. Novakova, L. Saskova, P. Pallova, J. Janecek, J. Novotna, and A. Ulrych Characterization of a eukaryotic type serine/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates FEBS Letters 272 2005 1243 1254
20. L. Shi Manganese-dependent protein O-phosphatases in prokaryotes and their biological functions Front. Biosci. 9 2004 1382 1397
21. P. Bork, N.P. Brown, H. Hegyi, and J. Schultz The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues Protein Sci. 5 1996 1421 1425
22. E. Adler, A. Donella-Deana, F. Arigoni, L.A. Pinna, and P. Stragier Strctural relationship between a bacterial developmental protein and eukaryotic PP2C protein phosphatases Mol. Microbiol. 23 1997 57 62
23. M. Obuchowski, E. Madec, D. Delattre, G. Boel, A. Iwannicki, and D. Foulger Characterization of PrpC from Bacillus subtilis, a member of the PPM phosphatase family J. Bacteriol. 182 2000 5634 5638
24. J.J. Ferretti, W.M. McShan, D. Ajdic, D.J. Savic, G. Savic, and K. Lyon Complete genome sequence of an M1 strain of Streptococcus pyogenes Proc. Natl Acad. Sci. USA 98 2001 4658 4663
25. J.C. Smoot, K.D. Barbian, J.J. Van Gompel, L.M. Smoot, M.S. Chaussee, and G.L. Sylva Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks Proc. Natl Acad. Sci. USA 99 2002 4668 4673
26. S.B. Beres, G.L. Sylva, K.D. Barbian, B. Lei, J.S. Hoff, and N.D. Mammarella Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence Proc. Natl Acad. Sci. USA 99 2002 10078 10083
27. I. Nakagawa, K. Kurokawa, A. Yamashita, M. Nakata, Y. Tomiyasu, and N. Okahashi Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution Genome Res. 13 2003 1042 1055
28. D.R. Johnson, D.L. Stevens, and E.L. Kaplan Epidemiologic analysis of group A streptococcal serotypes associated with systemic infection, rheumatic fever, or uncomplicated pharyngitis J. Infect. Dis. 166 1992 374 382
29. L.A. Cone, D.R. Woodard, P.M. Schlievert, and G.S. Tomory Clinical and bacteriologic observations of a toxic shock-like syndrome due to Streptoccoccus pyogenes N. Engl. J. Med. 317 1987 146 149
30. D.L. Stevens Streptococcal toxic-shock syndrome: specturm of disease, pathogenesis, and new concepts in treatment Emerg. Infect. Dis. 1 1995 69 78
31. M.W. Cunningham Pathogenesis of a group A streptococcal infections Clin. Microbiol. Rev. 13 2000 470 511
32. W.W. Navarre, and O. Schneewind Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope Microbiol. Mol. Biol. Rev. 63 1999 174 229
33. B. Kreikemeyer, K.S. McIver, and A. Podbielski Virulence factors regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions Trends Microbiol. 11 2003 224 232
34. J. Wang, C. Li, H. Yang, A. Mushegian, and S. Jin A novel serine/threonine protein kinase homologue of Pseudomonas aeruginosa is specifically inducible within the host infection site and is required for full virulence in neutropenic mice J. Bacteriol. 180 1998 6764 6768
35. P. Peirs, L. De Wit, M. Braibant, K. Huygen, and J. Content A serine/threonine protein kinase from Mycobacterium tuberculosis Eur J. Biochem. 244 1997 604 612
36. C. Yeats, R.D. Finn, and A. Bateman The PASTA domain: a β-lactam-binding protein Trends Biochem. Sci. 27 2002 438 440
37. V. Pancholi, and V.A. Fischetti Regulation of the phosphorylation of human pharyngeal cell proteins by group A streptococcal surface dehydrogenase(SDH): signal transduction between streptococci and pharyngeal cells J. Expt. Med. 186 1997 1633 1643
38. V. Pancholi, P.A. Fontan, and H. Jin Plasminogen-mediated group A streptococcal adherence to and pericellular invasion of human pharyngeal cells Microb. Pathog. 35 2003 293 303
39. P.A. Ryan, V. Pancholi, and V.A. Fischetti Group A streptococci bind to mucin and human pharyngeal cells through sialic acid-containing receptors Infect. Immun. 69 2002 7402 7412
40. R. Lancefield Differentiation of group A streptococci with a common R antigen into three serological types, with special reference to the bactericidal test J. Expt. Med. 106 1957 525 544
41. V.A. Fischetti Streptococcal M protein: molecular design and biological behavior Clin. Microbiol. Rev. 2 1989 285 314
42. + lineage J. Immunol. 160 1998 860 869
43. J. Perez-Casal, N. Okada, M.G. Caparon, and J.R. Scott Role of the conserved C-repeat region of the M protein of Streptococcus pyogenes Mol. Microbiol. 15 1995 907 916
44. K.F. Jones, B.N. Manjula, K.H. Johnston, S.K. Hollingshead, J.R. Scott, and V.A. Fischetti Location of variable and conserved epitopes among the multiple serotypes of streptococcal M protein J. Expt. Med. 161 1985 623 628
45. V.A. Fischetti, K.F. Jones, B.N. Manjula, and J.R. Scott Streptococcal M6 protein expressed in Escherichia coli J. Expt. Med. 159 1984 1083 1095
46. M.R. Wessels, A.E. Moses, J.B. Goldberg, and T.J. DiCesare Hyaluronic acid capsule is a virulence factor for mucoid group A streptococci Proc. Natl Acad. Sci. USA 88 1991 8317 8321
47. H.M. Schrager, J.G. Rheinwald, and M.R. Wessels Hyaluronic acid capsule and the role of streptococcal entry into keratinocytes in invasive skin infection J. Clin. Invest. 98 1996 1954 1958
48. J. Munoz-Dorado, S. Inouye, and M. Inouye Eukaryotic-like protein serine/threonine kinases in Myxococcus xanthus, a developmental bacterium exhibiting social behavior J. Cell Biochem. 51 1993 29 33
49. K. Drlica, and J. Rouviere-Yaniv Histone-like proteins of bacteria Microbiol. Rev. 51 1987 310 319
50. B. Boitel, M. Ortiz-Lombardia, R. Duran, F. Pompeo, S.W. Cole, C. Cervenansky, and P.M. Alzari 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 2003 1493 1508
51. C.-M. Kang, D.A. Abbott, S.T. Park, C.C. Dascher, L.C. Cantley, and R.N. Husson The Mycobacterium tuberculosis serine/threonine kinase PknA and PknB: substrate identification and regulation of cell shape Genes Dev. 19 2005 1692 1704
52. A. Villarino, R. Duran, A. Wehenkel, P. Fernandez, P. England, and P. Brodin Proteomic identification of M. tuberculosis portein kinase substrates: PknB recruits GarA, a FHA domain-containing protein, through activation loop-mediated interactions J. Mol. Biol. 350 2005 953 963
53. R.C. Lancefield Current knowledge of the type specific M antigens of group A streptococci J. Immunol. 89 1962 307 313
54. A.E. Moses, M.R. Wessels, K. Zalcman, S. Alberti, S. Natanson-Yaron, and T. Menes Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of the group A Streptococcus Infect. Immun. 65 1997 64 71
55. J.B. Dale, R.G. Washburn, M.B. Marques, and M.R. Wessels Hyaluronate capsule and suface M protein in resistance to opsonization of group A streptococci Infect. Immun. 64 1996 1495 1501
56. G.L. Darmstadt, L. Mentele, A. Podbielski, and C. Rubens Role of group A streptococcal virulence factors in adherence to keratinocytes Infect. Immun. 68 2000 1215 1221
57. M.G. Caparon, D.S. Stephens, A. Olsen, and J.R. Scott Role of M protein in adherence of group A streptococci Infect. Immun. 59 1991 1811 1817
58. L. Rajagopal, A. Va, and C. Rubens Regulation of purine biosynthesis by a eukaryotic-type kinase in Streptococcus agalactiae Mol. Microbiol. 56 2005 1329 1346
59. H. Nariya, and S. Inouye An effective sporulation of Myxococcus xanthus requires glycogen consumption via Pkn4-activated 6-phosphofructokinase Mol. Microbiol. 49 2003 517 528
60. D. Durocher, I.A. Taylor, D. Sarbassova, L.F. Haire, S.L. Westcott, and S.P. Jackson The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms Mol. Cell 6 2000 1169 1182
61. H. Udo, C.K. Lam, S. Mori, M. Inouye, and S. Inouye Identification of a substrate for Pkn2, a protein Ser/Thr kinase from Myxococcus xanthus by a novel method for substrate identification J. Mol. Microbiol. Biotechnol. 2 2000 557 563
62. L. Zhang, T.A. Ignatowski, R.N. Spengler, B. Noble, and M.W. Stinson Streptococcal histone induces murine macrophages to produce interleukin-1 and tumor necrosis factor alpha Infect. Immun. 67 1999 6473 6477
63. M.W. Stinson, R. McLaughlin, S.K. Choi, Z.E. Juarez, and J. Bernard Streptococcal histone-like protein: primary structure of hlpA and protein binding to lipoteichoic acid and epithelial cells Infect. Immun. 66 1998 259 265
64. C.J. Dorman, and P. Deighan Regulation of geneexpression by histone-like proteins in bacteria Curr. Opin. Genet. Dev. 13 2003 179 184
65. C. Robinow, and E. Kellenberger The bacterial nucleoid revisited Microbiol. Rev. 58 1994 211 232
66. S. Rimsky Structure of the histone-like protein H-NS and its role in regulation and genome superstructure Curr. Opin. Microbiol. 7 2004 109 114
67. W. Fischle, Y. Wang, and C.D. Allis Histones and chromatin cross-talk Curr. Opin. Cell Biol. 15 2003 172 183
68. S.J. Nowak, and V.G. Corces Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation Trends Genet. 20 2004 214 220
69. A. Wlaburger, A. Koul, G. Ferrari, L. Nguyen, C. Prescianotto-Baschong, and K. Huygen Protein kinase G from pathogenic mycobacteria promotes survival within macrophages Science 304 2004 1800 1804
70. H. Jin, Y.P. Song, G. Boel, J. Kochar, and V. Pancholi Group A streptococcal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells J. Mol. Biol. 350 2005 27 41
71. A. Derbise, Y.P. Song, S. Parikh, V.A. Fischetti, and V. Pancholi Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci Infect. Immun. 72 2004 94 105
72. D.O. Chaffin, and C.E. Rubens Blue/white screening of recombinant plasmids in Gram-positive bacteria by interruption of alkaline phosphatase gene (phoZ) expression Gene 219 1998 91 99
73. J. Sambrook, and D.W. Russel Molecular Cloning: A Laboratory Manual 2001 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
74. V. Pancholi, and V.A. Fischetti A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate dehydrogenase with multiple binding activity J. Expt. Med. 176 1992 415 426
75. A. Podbielski, B. Spellerberg, M. Woischnik, B. Pohl, and R. Lutticken Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS) Gene 177 1996 137 147
76. D. Simon, and J.J. Ferretti Electrotransformation of Streptococcus pyogenes with plasmid and linear DNA FEMS Microbiol. Letters 82 1991 219 224
77. V. Pancholi, and V.A. Fischetti α-Enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci J. Biol. Chem. 273 1998 14503 14515
78. B. Duclos, S. Marcandier, and A.J. Cozzone Chemical properties and separation of phosphoamino acids by thin-layer chromatography and/or electrophoresis Methods Enzymol. 201 1991 10 21