Tyrosine-kinases in bacteria: From a matter of controversy to the status of key regulatory enzymes

Amino Acids

Volumn 37, Issue 3, 2009, Pages 499-507

  Bechet, Emmanuelle ^a   Guiral, Sébastien ^a   Torres, Sophie ^a   Mijakovic, Ivan ^b   Cozzone, Alain Jean ^a   Grangeasse, Christophe ^a  

^a UNIVERSITÉ DE LYON   (France)

^b CNRS   (France)

Author keywords

Bacterial physiology; BY kinase; Phosphoproteomics; Phosphorylation; Regulatory process; Signaling; Tyrosine kinase

Indexed keywords

ENZYME; PHOSPHOTYROSINE; POLYSACCHARIDE; PROTEIN SERINE KINASE; PROTEIN TYROSINE KINASE;

BACTERIAL CELL; BACTERIUM; CELL FUNCTION; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW;

BACTERIA; BACTERIAL PROTEINS; GRAM-POSITIVE BACTERIA; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEOBACTERIA; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 69249225578     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-009-0237-8     Document Type: Review

References (72)

1. CJ Bakal JE Davies 2000 No longer an exclusive club: eukaryotic signalling domains in bacteria Trends Cell Biol 10 32 38
2. A Becker A Puhler 1998 Specific amino acid substitutions in the proline-rich motif of the Rhizobium meliloti ExoP protein result in enhanced production of low-molecular-weight succinoglycan at the expense of high-molecular-weight succinoglycan J Bacteriol 180 395 399
3. MH Bender RT Cartee J Yother 2003 Positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae J Bacteriol 185 6057 6066
4. K Chow D Ng R Stokes P Johnson 1994 Protein tyrosine phosphorylation in Mycobacterium tuberculosis FEMS Microbiol Lett 124 203 207 (Pubitemid 124012917)
5. RF Collins K Beis BR Clarke RC Ford M Hulley JH Naismith C Whitfield 2006 Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules J Biol Chem 281 2144 2150
6. JC Cortay C Rieul B Duclos AJ Cozzone 1986 Characterization of the phosphoproteins of Escherichia coli cells by electrophoretic analysis Eur J Biochem 159 227 237
7. AJ Cozzone 1993 ATP-dependent protein kinases in bacteria J Cell Biochem 51 7 13
8. AJ Cozzone 1998 Post-translational modification of proteins by reversible phosphorylation in prokaryotes Biochimie 80 43 48
9. J Deutscher MH Saier Jr 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
10. J Deutscher C Francke PW Postma 2006 How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria Microbiol Mol Biol Rev 70 939 1031
11. P Doublet C Vincent C Grangeasse AJ Cozzone B Duclos 1999 On the binding of ATP to the autophosphorylating protein, Ptk, of the bacterium Acinetobacter johnsonii FEBS Lett 445 137 143 (Pubitemid 29101549)
12. P Doublet C Grangeasse B Obadia E Vaganay AJ Cozzone 2002 Structural organization of the protein-tyrosine autokinase Wzc within Escherichia coli cells J Biol Chem 277 37339 37348
13. R Foster J Thorner GS Martin 1989 Nucleotidylation, not phosphorylation, is the major source of the phosphotyrosine detected in enteric bacteria J Bacteriol 171 272 279
14. P Freestone S Grant M Trinei T Onoda V Norris 1998 Protein phosphorylation in Escherichia coli L. form NC-7 Microbiology 144 Pt 12 3289 3295 (Pubitemid 29011958)
15. M Garnak HC Reeves 1979 Phosphorylation of isocitrate dehydrogenase of Escherichia coli Science 203 1111 1112
16. C Grangeasse P Doublet E Vaganay C Vincent G Deleage B Duclos AJ Cozzone 1997 Characterization of a bacterial gene encoding an autophosphorylating protein tyrosine-kinase Gene 204 259 265
17. C Grangeasse P Doublet C Vincent E Vaganay M Riberty B Duclos AJ Cozzone 1998 Functional characterization of the low-molecular-mass phosphotyrosine- protein phosphatase of Acinetobacter johnsonii J Mol Biol 278 339 347
18. C Grangeasse P Doublet AJ Cozzone 2002 Tyrosine phosphorylation of protein kinase Wzc from Escherichia coli K12 occurs through a two-step process J Biol Chem 277 7127 7135
19. C Grangeasse B Obadia I Mijakovic J Deutscher AJ Cozzone P Doublet 2003 Autophosphorylation of the Escherichia coli protein kinase Wzc regulates tyrosine phosphorylation of Ugd, a UDP-glucose dehydrogenase J Biol Chem 278 39323 39329
20. C Grangeasse AJ Cozzone J Deutscher I Mijakovic 2007 Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology Trends Biochem Sci 32 86 94
21. T Hunter 2000 Signaling-2000 and beyond Cell 100 113 127
22. F Jadeau E Bechet AJ Cozzone G Deleage C Grangeasse C Combet 2008 Identification of the idiosyncratic bacterial protein-tyrosine kinase (BY-kinase) family signature Bioinformatics 24 2427 2430
23. K Kelly-Wintenberg SL South TC Montie 1993 Tyrosine phosphate in a- and b-type flagellins of Pseudomonas aeruginosa J Bacteriol 175 2458 2461
24. PJ Kennelly M Potts 1996 Fancy meeting you here! A fresh look at "prokaryotic" protein phosphorylation J Bacteriol 178 4759 4764
25. J Kirstein K Turgay 2005 A new tyrosine phosphorylation mechanism involved in signal transduction in Bacillus subtilis J Mol Microbiol Biotechnol 9 182 188
26. G Klein C Dartigalongue S Raina 2003 Phosphorylation-mediated regulation of heat shock response in Escherichia coli Mol Microbiol 48 269 285
27. S Klumpp J Krieglstein 2002 Phosphorylation and dephosphorylation of histidine residues in proteins Eur J Biochem 269 1067 1071
28. M Kolot R Gorovits N Silberstein B Fichtman E Yagil 2008 Phosphorylation of the integrase protein of coliphage HK022 Virology 375 383 390
29. S Lacour P Doublet B Obadia AJ Cozzone C Grangeasse 2006 A novel role for protein-tyrosine-kinase Etk from Escherichia coli K-12 related to polymyxin resistance Res Microbiol 157 637 641
30. S Lacour E Bechet AJ Cozzone I Mijakovic C Grangeasse 2008 Tyrosine phosphorylation of the UDP-glucose dehydrogenase of Escherichia coli is at the crossroads of colanic acid synthesis and polymyxin resistance PLoS ONE 3 e3053
31. DC Lee J Zheng YM She Z Jia 2008 Structure of Escherichia coli tyrosine-kinase Etk reveals a novel activation mechanism Embo J 27 1758 1766
32. DD Leipe YI Wolf EV Koonin L Aravind 2002 Classification and evolution of P-loop GTPases and related ATPases J Mol Biol 317 41 72
33. DD Leipe EV Koonin L Aravind 2003 Evolution and classification of P-loop kinases and related proteins J Mol Biol 333 781 815
34. CJ Leonard L Aravind EV Koonin 1998 Novel families of putative protein kinases in bacteria and archaea:evolution of the "eukaryotic" protein kinase superfamily Genome Res 8 1038 1047
35. B Macek I Mijakovic JV Olsen F Gnad C Kumar PR Jensen M Mann 2007 The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis Mol Cell Proteomics 4 697 707
36. B Macek F Gnad B Soufi C Kumar JV Olsen I Mijakovic M Mann 2008 Phosphoproteome analysis of E coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation Mol Cell Proteomics 7 299 307
37. M Manai AJ Cozzone 1979 Analysis of the protein-kinase activity of Escherichia coli cells Biochem Biophys Res Commun 91 819 826
38. I Mijakovic S Poncet G Boel A Maze S Gillet E Jamet P Decottignies C Grangeasse P Doublet P Le Marechal J Deutscher 2003 Transmembrane modulator-dependent bacterial tyrosine-kinase activates UDP-glucose dehydrogenases EMBO J 22 4709 4718
39. I Mijakovic D Petranovic B Macek T Cepo M Mann J Davies PR Jensen D Vujaklija 2006 Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine Nucleic Acids Res 34 1588 1596
40. Z Minic C Marie C Delorme JM Faurie G Mercier D Ehrlich P Renault 2007 Control of EpsE, the phosphoglycosyltransferase initiating exopolysaccharide synthesis in Streptococcus thermophilus, by EpsD tyrosine-kinase J Bacteriol 189 1351 1357
41. JK Morona JC Paton DC Miller R Morona 2000 Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in streptococcus pneumoniae Mol Microbiol 35 1431 1442
42. R Morona L Van Den Bosch C Daniels 2000 Evaluation of Wzz/MPA1/MPA2 proteins based on the presence of coiled-coil regions Microbiology 146 Pt 1 1 4
43. JK Morona R Morona DC Miller JC Paton 2003 Mutational analysis of the carboxy-terminal (YGX)(4) repeat domain of CpsD, an autophosphorylating tyrosine-kinase required for capsule biosynthesis in Streptococcus pneumoniae J Bacteriol 185 3009 3019
44. J Munoz-Dorado S Inouye M Inouye 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
45. D Nakar DL Gutnick 2003 Involvement of a protein tyrosine-kinase in production of the polymeric bioemulsifier emulsan from the oil-degrading strain Acinetobacter lwoffii RAG-1 J Bacteriol 185 1001 1009
46. D Niemeyer A Becker 2001 The molecular weight distribution of succinoglycan produced by Sinorhizobium meliloti is influenced by specific tyrosine phosphorylation and ATPase activity of the cytoplasmic domain of the ExoP protein J Bacteriol 183 5163 5170
47. B Obadia S Lacour P Doublet H Baubichon-Cortay AJ Cozzone C Grangeasse 2007 Influence of tyrosine-kinase Wzc activity on colanic acid production in Escherichia coli K12 cells J Mol Biol 367 42 53
48. V Olivares-Illana P Meyer E Bechet V Gueguen-Chaignon D Soulat S Lazereg-Riquier I Mijakovic J Deutscher AJ Cozzone O Laprevote S Morera C Grangeasse S Nessler 2008 Structural basis for the regulation mechanism of the tyrosine-kinase CapB from Staphylococcus aureus PLoS Biol 6 e143
49. PC Ostrovsky S Maloy 1995 Protein phosphorylation on serine, threonine, and tyrosine residues modulates membrane-protein interactions and transcriptional regulation in Salmonella typhimurium Genes Dev 9 2034 2041
50. A Paiment J Hocking C Whitfield 2002 Impact of phosphorylation of specific residues in the tyrosine autokinase, Wzc, on its activity in assembly of group 1 capsules in Escherichia coli J Bacteriol 184 6437 6447
51. T Pawson JD Scott 2005 Protein phosphorylation in signaling-50 years and counting Trends Biochem Sci 30 286 290
52. A Peleg Y Shifrin O Ilan C Nadler-Yona S Nov S Koby K Baruch S Altuvia M Elgrably-Weiss CM Abe S Knutton MA Saper I Rosenshine 2005 Identification of an Escherichia coli operon required for formation of the O-antigen capsule J Bacteriol 187 5259 5266
53. D Petranovic O Michelsen K Zahradka C Silva M Petranovic PR Jensen I Mijakovic 2007 Bacillus subtilis strain deficient for the protein tyrosine-kinase PtkA exhibits impaired DNA replication Mol Microbiol 63 1797 1805
54. G Rafter 1964 Identification of a new form of bound phosphoserine in Escherichia coli J Biol Chem 239 1044 1047
55. MK Ray GS Kumar S Shivaji 1994 Tyrosine phosphorylation of a cytoplasmic protein from the antartic psychrotrophic bacterium Pseudomonas syringae FEMS Microbiol Lett 122 49 54
56. L Shi M Potts PJ Kennelly 1998 The serine, threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait FEMS Microbiol Rev 22 229 253
57. B Soufi F Gnad PR Jensen D Petranovic M Mann I Mijakovic B Macek 2008 The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins Proteomics 8 3486 3493
58. D Soulat JM Jault B Duclos C Geourjon AJ Cozzone C Grangeasse 2006 Staphylococcus aureus operates protein-tyrosine phosphorylation through a specific mechanism J Biol Chem 281 14048 14056
59. D Soulat C Grangeasse E Vaganay AJ Cozzone B Duclos 2007 UDP-acetyl-mannosamine dehydrogenase is an endogenous protein substrate of Staphylococcus aureus protein-tyrosine-kinase activity J Mol Microbiol Biotechnol 13 45 54
60. SR Thomas TJ Trust 1995 Tyrosine phosphorylation of the tetragonal paracrystalline array of Aeromonas hydrophila: molecular cloning and high-level expression of the S-layer protein gene J Mol Biol 245 568 581
61. B Thomasson J Link AG Stassinopoulos N Burke L Plamann PL Hartzell 2002 MglA, a small GTPase, interacts with a tyrosine-kinase to control type IV pili-mediated motility and development of Myxococcus xanthus Mol Microbiol 46 1399 1413
62. A Tocilj C Munger A Proteau R Morona L Purins E Ajamian J Wagner M Papadopoulos L Van Den Bosch JL Rubinstein J Fethiere A Matte M Cygler 2008 Bacterial polysaccharide co-polymerases share a common framework for control of polymer length Nat Struct Mol Biol 15 130 138
63. H van Tilbeurgh N Declerck 2001 Structural insights into the regulation of bacterial signalling proteins containing PRDs Curr Opin Struct Biol 11 685 693
64. C Vincent P Doublet C Grangeasse E Vaganay AJ Cozzone B Duclos 1999 Cells of Escherichia coli contain a protein-tyrosine-kinase, Wzc, and a phosphotyrosine-protein phosphatase, Wzb J Bacteriol 181 3472 3477
65. JY Wang DE Koshland Jr 1978 Evidence for protein kinase activities in the prokaryote Salmonella typhimurium J Biol Chem 253 7605 7608
66. KM Warner GS Bullerjahn 1994 Light-dependent tyrosine phosphorylation in the cyanobacterium Prochlorothrix hollandica Plant Physiol 105 629 633
67. C Whitfield 2006 Biosynthesis and assembly of capsular polysaccharides in Escherichia coli Annu Rev Biochem 75 39 68
68. C Whitfield K Larue 2008 Stop and go: regulation of chain length in the biosynthesis of bacterial polysaccharides Nat Struct Mol Biol 15 121 123
69. J Wu N Ohta JL Zhao A Newton 1999 A novel bacterial tyrosine-kinase essential for cell division and differentiation Proc Natl Acad Sci USA 96 13068 13073
70. T Wugeditsch A Paiment J Hocking J Drummelsmith C Forrester C Whitfield 2001 Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli J Biol Chem 276 2361 2371
71. X Zhao JS Lam 2002 WaaP of Pseudomonas aeruginosa is a novel eukaryotic type protein-tyrosine-kinase as well as a sugar kinase essential for the biosynthesis of core lipopolysaccharide J Biol Chem 277 4722 4730 (Pubitemid 34968503)
72. J Zheng C He VK Singh NL Martin Z Jia 2007 Crystal structure of a novel prokaryotic Ser/Thr kinase and its implication in the Cpx stress response pathway Mol Microbiol 63 1360 1371