Phosphoproteome analysis of the pathogenic bacterium Helicobacter pylori reveals over-representation of tyrosine phosphorylation and multiply phosphorylated proteins

Proteomics

Volumn 11, Issue 8, 2011, Pages 1449-1461

  Ge, Ruiguang ^a   Sun, Xuesong ^b   Xiao, Chuanle ^b   Yin, Xingfeng ^b   Shan, Weiran ^a   Chen, Zhuo ^a   He, Qing Yu ^b  

^a SUN YAT SEN UNIVERSITY   (China)

^b JINAN UNIVERSITY   (China)

Author keywords

Helicobacter pylori; Membrane; Microbiology; Phosphoproteome; Tyrosine phosphorylation

Indexed keywords

MEMBRANE PROTEIN; PHOSPHOPEPTIDE; PROTEOME; SERINE; THREONINE; TYROSINE;

ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; HELICOBACTER PYLORI; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEOMICS;

BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; HELICOBACTER PYLORI; MASS SPECTROMETRY; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN KINASES; PROTEOME; PROTEOMICS;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI; NEGIBACTERIA;

EID: 79953712602     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000649     Document Type: Article

References (59)

1. Johnson, L. N., The regulation of protein phosphorylation. Biochem. Soc. Trans. 2009, 37, 627-641.
2. Cohen, P., The regulation of protein function by multisite phosphorylation a 25 year update. Trends Biochem. Sci. 2000, 25, 596-601.
3. Mann, M., Ong, S. E., Gronborg, M., Steen, H. et al., Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 2002, 20, 261-268.
4. Ge, R., Sun, H., Metallomics: an integrated biometal science. Sci. China Ser. B Chem. 2009, 52, 2055-2070.
5. Paradela, A., Albar, J. P., Advances in the analysis of protein phosphorylation. J. Proteome Res. 2008, 7, 1809-1818.
6. Li, X., Gerber, S. A., Rudner, A. D., Beausoleil, S. A. et al., Large-scale phosphorylation analysis of alpha-factor-arrested Saccharomyces cerevisiae. J. Proteome Res. 2007, 6, 1190-1197.
7. Marshall, B. J., Warren, J. R., Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984, 1, 1311-1315.
8. Blaser, M. J., Ecology of Helicobacter pylori in the human stomach. J. Clin. Invest. 1997, 100, 759-762.
9. Cover, T. L., The vacuolating cytotoxin of Helicobacter pylori. Mol. Microbiol. 1996, 20, 241-246.
10. Backert, S., Selbach, M., Role of type IV secretion in Helicobacter pylori pathogenesis. Cell. Microbiol. 2008, 10, 1573-1581.
11. Salama, N. R., Otto, G., Tompkins, L., Falkow, S., Vacuolating cytotoxin of Helicobacter pylori plays a role during colonization in a mouse model of infection. Infect. Immun. 2001, 69, 730-736.
12. Costa, A. C., Figueiredo, C., Touati, E., Pathogenesis of Helicobacter pylori infection. Helicobacter 2009, 14, 15-20.
13. Hatakeyama, M., Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 2004, 4, 688-694.
14. Wen, S., Moss, S. F., Helicobacter pylori virulence factors in gastric carcinogenesis. Cancer Lett. 2009, 282, 1-8.
15. Shi, L., Potts, M., Kennelly, P. J., The serine, threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait. FEMS Microbiol. Rev. 1998, 22, 229-253.
16. Grangeasse, C., Pichon, B., Bollen, A., Godfroid, E., Protein kinase activity in Helicobacter pylori. FEMS Microbiol. Lett. 1999, 176, 327-332.
17. Voisin, S., Watson, D. C., Tessier, L., Ding, W. et al., The cytoplasmic phosphoproteome of the Gram-negative bacterium Campylobacter jejuni: evidence for modification by unidentified protein kinases. Proteomics 2007, 7, 4338-4348.
18. 2+ storage in Helicobacter pylori. Biochem. J. 2006, 393, 285-293.
19. Sun, X., Ge, F., Xiao, C. L., Yin, X. F. et al., Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. J. Proteome Res. 2010, 9, 275-282.
20. Haas, W., Faherty, B. K., Gerber, S. A., Elias, J. E. et al., Optimization and use of peptide mass measurement accuracy in shotgun proteomics. Mol. Cell. Proteomics 2006, 5, 1326-1337.
21. Villen, J., Beausoleil, S. A., Gygi, S. P., Evaluation of the utility of neutral-loss-dependent MS3 strategies in large-scale phosphorylation analysis. Proteomics 2008, 8, 4444-4452.
22. Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L. J., Gygi, S. P., Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2003, 2, 43-50.
23. Macek, B., Gnad, F., Soufi, B., Kumar, C. et al., Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol. Cell. Proteomics 2008, 7, 299-307.
24. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B. et al., Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127, 635-648.
25. Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J. et al., Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21, 3674-3676.
26. Gardy, J. L., Spencer, C., Wang, K., Ester, M. et al., PSORT-B: Improving protein subcellular localization prediction for Gram-negative bacteria. Nucleic Acids Res. 2003, 31, 3613-3617.
27. Tomb, J. F., White, O., Kerlavage, A. R., Clayton, R. A. et al., The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997, 388, 539-547.
28. Rain, J. C., Selig, L., De Reuse, H., Battaglia, V. et al., The protein-protein interaction map of Helicobacter pylori. Nature 2001, 409, 211-215.
29. Bradshaw, R. A., Burlingame, A. L., Carr, S., Aebersold, R., Reporting protein identification data: the next generation of guidelines. Mol. Cell. Proteomics 2006, 5, 787-788.
30. Parker, J. L., Jones, A. M., Serazetdinova, L., Saalbach, G. 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. Proteomics 2010, 10, 2486-2497.
31. Lin, M. H., Hsu, T. L., Lin, S. Y., Pan, Y. J. et al., Phosphoproteomics of Klebsiella pneumoniae NTUH-K2044 reveals a tight link between tyrosine phosphorylation and virulence. Mol. Cell. Proteomics 2009, 8, 2613-2623.
32. Ravichandran, A., Sugiyama, N., Tomita, M., Swarup, S., Ishihama, Y., Ser/Thr/Tyr phosphoproteome analysis of pathogenic and non-pathogenic Pseudomonas species. Proteomics 2009, 9, 2764-2775.
33. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D. J. et al., Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 1997, 91, 511-520.
34. Segal, E. D., Cha, J., Lo, J., Falkow, S., Tompkins, L. S., Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc. Natl. Acad. Sci. USA 1999, 96, 14559-14564.
35. Clifton, D. R., Fields, K. A., Grieshaber, S. S., Dooley, C. A. et al., A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc. Natl. Acad. Sci. USA 2004, 101, 10166-10171.
36. Schulein, R., Guye, P., Rhomberg, T. A., Schmid, M. C. et al., A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc. Natl. Acad. Sci. USA 2005, 102, 856-861.
37. Cozzone, A. J., Bacterial tyrosine kinases: novel targets for antibacterial therapy? Trends Microbiol. 2009, 17, 536-543.
38. Mazmanian, S. K., Kasper, D. L., The love-hate relationship between bacterial polysaccharides and the host immune system. Nat. Rev. Immunol. 2006, 6, 849-858.
39. Grangeasse, C., Cozzone, A. J., Deutscher, J., Mijakovic, I., Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem. Sci. 2007, 32, 86-94.
40. Jadeau, F., Bechet, E., Cozzone, A. J., Deleage, G. et al., Identification of the idiosyncratic bacterial protein tyrosine kinase (BY-kinase) family signature. Bioinformatics 2008, 24, 2427-2430.
41. Selbach, M., Moese, S., Backert, S., Jungblut, P. R., Meyer, T. F., The Helicobacter pylori CagA protein induces tyrosine dephosphorylation of ezrin. Proteomics 2004, 4, 2961-2968.
42. Bayle, D., Wangler, S., Weitzenegger, T., Steinhilber, W. et al., Properties of the P-type ATPases encoded by the copAP operons of Helicobacter pylori and Helicobacter felis. J. Bacteriol. 1998, 180, 317-329.
43. Rosen, R., Becher, D., Buttner, K., Biran, D. et al., Highly phosphorylated bacterial proteins. Proteomics 2004, 4, 3068-3077.
44. Soufi, B., Gnad, F., Jensen, P. R., Petranovic, D. et al., The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins. Proteomics 2008, 8, 3486-3493.
45. Jers, C., Soufi, B., Grangeasse, C., Deutscher, J., Mijakovic, I., Phosphoproteomics in bacteria: towards a systemic understanding of bacterial phosphorylation networks. Expert Rev. Proteomics 2008, 5, 619-627.
46. Ge, R., Sun, X., Gu, Q., Watt, R. M. et al., A proteomic approach for the identification of bismuth-binding proteins in Helicobacter pylori. J. Biol. Inorg. Chem. 2007, 12, 831-842.
47. Sun, X., Ge, R., Chiu, J. F., Sun, H., He, Q. Y., Identification of proteins related to nickel homeostasis in Helicobater pylori by immobilized metal affinity chromatography and two-dimensional gel electrophoresis. Metal Based Drugs 2008, 2008, 289490.
48. Zhu, K., Zhao, J., Lubman, D. M., Miller, F. R., Barder, T. J., Protein pI shifts due to posttranslational modifications in the separation and characterization of proteins. Anal. Chem. 2005, 77, 2745-2755.
49. Gnad, F., Ren, S., Cox, J., Olsen, J. V. et al., PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol. 2007, 8, R250.
50. Macek, B., Mijakovic, I., Olsen, J. V., Gnad, F. et al., The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol. Cell. Proteomics 2007, 6, 697-707.
51. Miller, M. L., Soufi, B., Jers, C., Blom, N. et al., NetPhosBac - a predictor for Ser/Thr phosphorylation sites in bacterial proteins. Proteomics 2009, 9, 116-125.
52. Telford, J. L., Ghiara, P., Dell'Orco, M., Comanducci, M. et al., Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J. Exp. Med. 1994, 179, 1653-1658.
53. Cover, T. L., Blanke, S. R., Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat. Rev. Microbiol. 2005, 3, 320-332.
54. Ilver, D., Barone, S., Mercati, D., Lupetti, P., Telford, J. L., Helicobacter pylori toxin VacA is transferred to host cells via a novel contact-dependent mechanism. Cell. Microbiol. 2004, 6, 167-174.
55. Endo, A., Kurusu, Y., Identification of in vivo substrates of the chaperonin GroEL from Bacillus subtilis. Biosci. Biotechnol. Biochem. 2007, 71, 1073-1077.
56. Dai, Z., Lackland, H., Stein, S., Li, Q. et al., Molecular mimicry in Lyme disease: monoclonal antibody H9724 to B. burgdorferi flagellin specifically detects chaperonin-HSP60. Biochim. Biophys. Acta 1993, 1181, 97-100.
57. Suerbaum, S., Thiberge, J. M., Kansau, I., Ferrero, R. L., Labigne, A., Helicobacter pylori hspA-hspB heat-shock gene cluster: nucleotide sequence, expression, putative function and immunogenicity. Mol. Microbiol. 1994, 14, 959-974.
58. Sherman, M., Goldberg, A. L., Heat shock-induced phosphorylation of GroEL alters its binding and dissociation from unfolded proteins. J. Biol. Chem. 1994, 269, 31479-31483.
59. Kumar, C. M., Khare, G., Srikanth, C. V., Tyagi, A. K. et al., Facilitated oligomerization of mycobacterial GroEL: evidence for phosphorylation-mediated oligomerization. J. Bacteriol. 2009, 191, 6525-6538.