Tyrosine phosphorylation and bacterial virulence

Protein phosphorylation on tyrosine has emerged as a key device in the control of numerous cellular functions in bacteria. In this article, we review the structure and function of bacterial tyrosine kinases and phosphatases. Phosphorylation is catalyzed by autophosphorylating adenosine triphosphate-dependent enzymes (bacterial tyrosine (BY) kinases) that are characterized by the presence of Walker motifs. The reverse reaction is catalyzed by three classes of enzymes: the eukaryotic-like phosphatases (PTPs) and dual-specific phosphatases; the low molecular weight protein-tyrosine phosphatases (LMW-PTPs); and the polymerase–histidinol phosphatases (PHP). Many BY kinases and tyrosine phosphatases can utilize host cell proteins as substrates, thereby contributing to bacterial pathogenicity. Bacterial tyrosine phosphorylation/dephosphorylation is also involved in biofilm formation and community development. The Porphyromonas gingivalis tyrosine phosphatase Ltp1 is involved in a restraint pathway that regulates heterotypic community development with Streptococcus gordonii. Ltp1 is upregulated by contact with S. gordonii and Ltp1 activity controls adhesin expression and levels of the interspecies signal AI-2.

[1]  S. Moréra,et al.  Structure Analysis of the Staphylococcus aureus UDP-N-acetyl-mannosamine Dehydrogenase Cap5O Involved in Capsular Polysaccharide Biosynthesis* , 2011, The Journal of Biological Chemistry.

[2]  J. Stülke.  More than just activity control: phosphorylation may control all aspects of a protein's properties , 2010, Molecular microbiology.

[3]  K. Rittinger,et al.  Sequestering of Rac by the Yersinia Effector YopO Blocks Fcγ Receptor-mediated Phagocytosis* , 2009, The Journal of Biological Chemistry.

[4]  A. Cozzone,et al.  Endogenous protein phosphorylation in Escherichia coli extracts. , 1982, Biochemical and biophysical research communications.

[5]  M. Noda,et al.  A novel tyrosine-phosphorylated protein inhibiting the growth of Streptomyces cells. , 2009, Biochemical and biophysical research communications.

[6]  T. Wood,et al.  Connecting Quorum Sensing, c-di-GMP, Pel Polysaccharide, and Biofilm Formation in Pseudomonas aeruginosa through Tyrosine Phosphatase TpbA (PA3885) , 2009, PLoS pathogens.

[7]  M. Tomita,et al.  Ser/Thr/Tyr phosphoproteome analysis of pathogenic and non‐pathogenic Pseudomonas species , 2009, Proteomics.

[8]  B. Finlay,et al.  Bacterial Effector Binding to Ribosomal Protein S3 Subverts NF-κB Function , 2009, PLoS pathogens.

[9]  A. Cozzone.  Bacterial tyrosine kinases: novel targets for antibacterial therapy? , 2009, Trends in microbiology.

[10]  A. Becker,et al.  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 , 2001, Journal of bacteriology.

[11]  Jörg Stülke,et al.  The Phosphoproteome of the Minimal Bacterium Mycoplasma pneumoniae , 2010, Molecular & Cellular Proteomics.

[12]  H. Baker,et al.  Role of Porphyromonas gingivalis SerB in Gingival Epithelial Cell Cytoskeletal Remodeling and Cytokine Production , 2008, Infection and Immunity.

[13]  A. Becker,et al.  Production of succinoglycan polymer in Sinorhizobium meliloti is affected by SMb21506 and requires the N-terminal domain of ExoP. , 2009, Molecular plant-microbe interactions : MPMI.

[14]  C. Whitfield,et al.  Phosphorylation of Wzc, a Tyrosine Autokinase, Is Essential for Assembly of Group 1 Capsular Polysaccharides in Escherichia coli* , 2001, The Journal of Biological Chemistry.

[15]  S. Foote,et al.  The cytoplasmic phosphoproteome of the Gram‐negative bacterium Campylobacter jejuni: Evidence for modification by unidentified protein kinases , 2007, Proteomics.

[16]  Qing‐Yu He,et al.  Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. , 2010, Journal of proteome research.

[17]  J. Turner,et al.  Enteropathogenic E. coli non‐LEE encoded effectors NleH1 and NleH2 attenuate NF‐κB activation , 2010, Molecular microbiology.

[18]  X. Zhao,et al.  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* , 2002, The Journal of Biological Chemistry.

[19]  S. South,et al.  Tyrosine kinase activity in Pseudomonas aeruginosa , 1994, Molecular microbiology.

[20]  J. Bliska.  Yop effectors of Yersinia spp. and actin rearrangements. , 2000, Trends in microbiology.

[21]  Jason A. Rosenzweig,et al.  The Ser/Thr kinase activity of the Yersinia protein kinase A (YpkA) is necessary for full virulence in the mouse, mollifying phagocytes, and disrupting the eukaryotic cytoskeleton. , 2006, Microbial pathogenesis.

[22]  C. Whitfield,et al.  Functional Analysis of Conserved Gene Products Involved in Assembly of Escherichia coli Capsules and Exopolysaccharides: Evidence for Molecular Recognition between Wza and Wzc for Colanic Acid Biosynthesis , 2005, Journal of bacteriology.

[23]  J Wu,et al.  A novel bacterial tyrosine kinase essential for cell division and differentiation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[24]  A. Cozzone,et al.  Isolation and characterization of a protein-tyrosine kinase and a phosphotyrosine-protein phosphatase from Klebsiella pneumoniae. , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[25]  A. Ullrich,et al.  Cloning and Characterization of Secretory Tyrosine Phosphatases of Mycobacterium tuberculosis , 2000, Journal of bacteriology.

[26]  B. Maček,et al.  Bacillus subtilis BY‐kinase PtkA controls enzyme activity and localization of its protein substrates , 2010, Molecular microbiology.

[27]  D. Petranovic,et al.  Protein-Tyrosine Phosphorylation in Bacillus subtilis , 2006, Journal of Molecular Microbiology and Biotechnology.

[28]  R. Lamont,et al.  Community signalling between Streptococcus gordonii and Porphyromonas gingivalis is controlled by the transcriptional regulator CdhR , 2010, Molecular microbiology.

[29]  M. Schell,et al.  A complex network regulates expression of eps and other virulence genes of Pseudomonas solanacearum , 1995, Journal of bacteriology.

[30]  K. Geider,et al.  Protein tyrosine kinases in bacterial pathogens are associated with virulence and production of exopolysaccharide , 1999, The EMBO journal.

[31]  V. Trajković,et al.  Intracellular expression of Mycobacterium tuberculosis‐specific 10‐kDa antigen down‐regulates macrophage B7·1 expression and nitric oxide release , 2003, Clinical and experimental immunology.

[32]  Ivan Mijakovic,et al.  Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. , 2007, Trends in biochemical sciences.

[33]  Hong Soon-Kwang,et al.  Phosphorylation of the AfsR protein involved in secondary metabolism in Streptomyces species by a eukary otic-type protein kinase , 1994 .

[34]  R. Lamont,et al.  Role of Porphyromonas gingivalis Phosphoserine Phosphatase Enzyme SerB in Inflammation, Immune Response, and Induction of Alveolar Bone Resorption in Rats , 2010, Infection and Immunity.

[35]  D. S. Cowen,et al.  SptP, a Salmonella typhimurium type III‐secreted protein, inhibits the mitogen‐activated protein kinase pathway by inhibiting Raf activation , 2003, Cellular microbiology.

[36]  M. Selbach,et al.  Tyrosine-phosphorylated bacterial effector proteins: the enemies within. , 2005, Trends in microbiology.

[37]  R. Morona,et al.  Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in Streptococcus pneumoniae , 2000, Molecular microbiology.

[38]  R. Lamont,et al.  A Porphyromonas gingivalis haloacid dehalogenase family phosphatase interacts with human phosphoproteins and is important for invasion. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  T. Wood,et al.  Tyrosine phosphatase TpbA of Pseudomonas aeruginosa controls extracellular DNA via cyclic diguanylic acid concentrations. , 2010, Environmental microbiology reports.

[40]  A. Cozzone,et al.  Functional characterization of the low-molecular-mass phosphotyrosine-protein phosphatase of Acinetobacter johnsonii. , 1998, Journal of molecular biology.

[41]  M. Mann,et al.  The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins , 2008, Proteomics.

[42]  Zhon-Yin Zhang,et al.  Functional studies of protein tyrosine phosphatases with chemical approaches. , 2005, Biochimica et biophysica acta.

[43]  Dong Wook Kim,et al.  An injected bacterial effector targets chromatin access for transcription factor NF-κB to alter transcription of host genes involved in immune responses , 2007, Nature Immunology.

[44]  Henry M Epino,et al.  Changes in Availability of Oxygen Accentuate Differences in Capsular Polysaccharide Expression by Phenotypic Variants and Clinical Isolates of Streptococcus pneumoniae , 2001, Infection and Immunity.

[45]  P. Cossart,et al.  LipA, a Tyrosine and Lipid Phosphatase Involved in the Virulence of Listeria monocytogenes , 2011, Infection and Immunity.

[46]  H. Bach,et al.  Mycobacterium tuberculosis virulence is mediated by PtpA dephosphorylation of human vacuolar protein sorting 33B. , 2008, Cell host & microbe.

[47]  Jason M. Link,et al.  MglA, a small GTPase, interacts with a tyrosine kinase to control type IV pili‐mediated motility and development of Myxococcus xanthus , 2002, Molecular microbiology.

[48]  D. Gutnick,et al.  Involvement of a Protein Tyrosine Kinase in Production of the Polymeric Bioemulsifier Emulsan from the Oil-Degrading Strain Acinetobacter lwoffii RAG-1 , 2003, Journal of bacteriology.

[49]  Ivan Mijakovic,et al.  Structural Basis for the Regulation Mechanism of the Tyrosine Kinase CapB from Staphylococcus aureus , 2008, PLoS biology.

[50]  A. Cozzone,et al.  Cells of Escherichia coli Contain a Protein-Tyrosine Kinase, Wzc, and a Phosphotyrosine-Protein Phosphatase, Wzb , 1999, Journal of bacteriology.

[51]  S. Shizukuishi,et al.  A Porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes , 2008, Molecular microbiology.

[52]  Y. Av‐Gay,et al.  Expression and localization of the Mycobacterium tuberculosis protein tyrosine phosphatase PtpA. , 2002, Research in microbiology.

[53]  S. Horinouchi,et al.  Phosphorylation of the AfsR protein involved in secondary metabolism in Streptomyces species by a eukaryotic-type protein kinase. , 1994, Gene.

[54]  M. Simionato,et al.  Porphyromonas gingivalis Genes Involved in Community Development with Streptococcus gordonii , 2006, Infection and Immunity.

[55]  D. Petranovic,et al.  Insights from site-specific phosphoproteomics in bacteria. , 2008, Biochimica et biophysica acta.

[56]  Florian Gnad,et al.  Ser/Thr/Tyr Protein Phosphorylation in the Archaeon Halobacterium salinarum—A Representative of the Third Domain of Life , 2009, PloS one.

[57]  K. Khoo,et al.  Phosphoproteomics of Klebsiella pneumoniae NTUH-K2044 Reveals a Tight Link between Tyrosine Phosphorylation and Virulence* , 2009, Molecular & Cellular Proteomics.

[58]  T. Tiganis.  Protein Tyrosine Phosphatases: Dephosphorylating the Epidermal Growth Factor Receptor , 2002, IUBMB life.

[59]  H. Wolf‐Watz,et al.  Localization of the Yersinia PTPase to focal complexes is an important virulence mechanism , 1999, Molecular microbiology.

[60]  M. Mann,et al.  Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine , 2006, Nucleic acids research.

[61]  R. Morona,et al.  Mutational Analysis of the Carboxy-Terminal (YGX)4 Repeat Domain of CpsD, an Autophosphorylating Tyrosine Kinase Required for Capsule Biosynthesis in Streptococcus pneumoniae , 2003, Journal of bacteriology.

[62]  J. Yother,et al.  CpsB Is a Modulator of Capsule-associated Tyrosine Kinase Activity in Streptococcus pneumoniae * , 2001, The Journal of Biological Chemistry.

[63]  Ivan Mijakovic,et al.  The Serine/Threonine/Tyrosine Phosphoproteome of the Model Bacterium Bacillus subtilis*S , 2007, Molecular & Cellular Proteomics.

[64]  A. Cozzone,et al.  Tyrosine phosphatase MptpA of Mycobacterium tuberculosis inhibits phagocytosis and increases actin polymerization in macrophages. , 2005, Research in microbiology.

[65]  J. Bliska,et al.  A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurlum , 1996, Molecular microbiology.

[66]  M. Wessels,et al.  Identification of cpsD, a gene essential for type III capsule expression in group B streptococci , 1993, Molecular microbiology.

[67]  S. Maloy,et al.  Protein phosphorylation on serine, threonine, and tyrosine residues modulates membrane-protein interactions and transcriptional regulation in Salmonella typhimurium. , 1995, Genes & development.

[68]  M. Bibb,et al.  Analysis of the phosphoproteome of the multicellular bacterium Streptomyces coelicolor A3(2) by protein/peptide fractionation, phosphopeptide enrichment and high‐accuracy mass spectrometry , 2010, Proteomics.

[69]  M. Schell,et al.  Molecular characterization of the eps gene cluster of Pseudomonas solanacearum and its transcriptional regulation at a single promoter , 1995, Molecular microbiology.

[70]  P. Renault,et al.  Control of EpsE, the Phosphoglycosyltransferase Initiating Exopolysaccharide Synthesis in Streptococcus thermophilus, by EpsD Tyrosine Kinase , 2006, Journal of bacteriology.

[71]  Klaus Geider,et al.  Characterization of the amsI gene product as a low molecular weight acid phosphatase controlling exopolysaccharide synthesis of Erwinia amylovora , 1997, FEBS letters.

[72]  Zongchao Jia,et al.  Structure of Escherichia coli tyrosine kinase Etk reveals a novel activation mechanism , 2008, The EMBO journal.

[73]  Maria Fällman,et al.  The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions , 1997, The EMBO journal.

[74]  J. Samuel,et al.  Coxiella burnetii Acid Phosphatase Inhibits the Release of Reactive Oxygen Intermediates in Polymorphonuclear Leukocytes , 2010, Infection and Immunity.

[75]  C. Arrieumerlou,et al.  Shigella flexneri type III secreted effector OspF reveals new crosstalks of proinflammatory signaling pathways during bacterial infection. , 2011, Cellular signalling.

[76]  M. Popoff,et al.  Molecular characterization of the Salmonella typhi StpA protein that is related to both Yersinia YopE cytotoxin and YopH tyrosine phosphatase. , 1997, Research in microbiology.

[77]  Liem Nguyen,et al.  Protein Kinase G from Pathogenic Mycobacteria Promotes Survival Within Macrophages , 2004, Science.

[78]  Qing‐Yu He,et al.  Phosphoproteome analysis of the pathogenic bacterium Helicobacter pylori reveals over‐representation of tyrosine phosphorylation and multiply phosphorylated proteins , 2011, Proteomics.

[79]  J. Suh,et al.  Binding study of AfsK, a Ser/Thr kinase from Streptomyces coelicolor A3(2) and S-adenosyl-L-methionine. , 2007, FEMS microbiology letters.

[80]  J. Bliska,et al.  Identification of an amino‐terminal substrate‐binding domain in the Yersinia tyrosine phosphatase that is required for efficient recognition of focal adhesion targets , 1998, Molecular microbiology.

[81]  A. Cozzone,et al.  Protein phosphorylation on tyrosine in bacteria , 2004, Archives of Microbiology.

[82]  J. Galán,et al.  Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells , 2001, Cellular microbiology.

[83]  G. Curley,et al.  Protein-tyrosine phosphatase activity of Coxiella burnetii that inhibits human neutrophils. , 1996, Acta virologica.

[84]  A. Cozzone.  Role of Protein Phosphorylation on Serine/Threonine and Tyrosine in the Virulence of Bacterial Pathogens , 2006, Journal of Molecular Microbiology and Biotechnology.

[85]  Ivan Mijakovic,et al.  MATERIALS AND METHODS , 1981, Green Corrosion Inhibitors: Reviews and Applications.