Proteomic and functional characterization of the outer membrane vesicles from the gastric pathogen Helicobacter pylori

Proteomics - Clinical Applications

Volumn 3, Issue 7, 2009, Pages 785-796

  Mullaney, Erica ^a   Brown, Paul A ^a   Smith, Sinead M ^a   Botting, Catherine H ^b   Yamaoka, Yoshio Y ^c   Terres, Ana M ^a   Kelleher, Dermot P ^a   Windle, Henry J ^a  

^a ST JAMES S HOSPITAL   (Ireland)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Helicobacter pylori; Outer membrane vesicles

Indexed keywords

CAGA PROTEIN; VACUOLATING TOXIN;

ARTICLE; BACTERIAL OUTER MEMBRANE; CELL PROLIFERATION; HELICOBACTER PYLORI; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MEMBRANE VESICLE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI; OAT MOSAIC VIRUS;

EID: 70350099087     PISSN: 18628346     EISSN: None     Source Type: Journal    
DOI: 10.1002/prca.200800192     Document Type: Article

References (96)

1. Kusters, J. G., van Vliet, A. H. M., Kuipers, E. J., Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 2006, 19, 449-490.
2. Naumann, M., Crabtree, J. E., Helicobacter pylori-induced epithelial cell signalling in gastric carcinogenesis. Trends Microbiol. 2004, 12, 29-36.
3. Pritchard, D. M., Crabtree, J. E., Helicobacter pylori and gastric cancer. Curr. Opin. Gastroenterol. 2006, 22, 620-625.
4. Wilson, K. T., Crabtree, J. E., Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology 2007, 133, 288-308.
5. Kwok, T., Zabler, D., Urman, S., Rohde, M. et al., Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 2007, 449, 862-866.
6. Viala, J., Chaput, C., Boneca, I., Cardona, A. et al., Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 2004, 5, 1166-1174.
7. Backert, S., Selbach, M., Role of type IV secretion in Helicobacter pylori pathogenesis. Cell. Microbiol. 2008, 10, 1573-1581.
8. Selbach, M., Moese, S., Hauck, C. R., Meyer, T. F., Backert, S., Src Is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J. Biol. Chem. 2002, 277, 6775-6778.
9. Moese, S., Selbach, M., Brinkmann, V., Karlas, A. et al., The Helicobacter pylori CagA protein disrupts matrix adhesion of gastric epithelial cells by dephosphorylation of vinculin. Cell. Microbiol. 2007, 9, 1148-1161.
10. Wessler, S., Backert, S., Molecular mechanisms of epithelial-barrier disruption by Helicobacter pylori. Trends Microbiol. 2008, 16, 397-405.
11. Crabtree, J. E., Farmery, S. M., Lindley, I. J., Figura, N. et al., CagA/cytotoxic strains of Helicobacter pylori and interleukin-8 in gastric epithelial cell lines. J. Clin. Pathol. 1994, 47, 945-950.
12. Hynes, S. O., Keenan, J. I., Ferris, J. A., Annuk, H., Moran, A. P., Lewis epitopes on outer membrane vesicles of relevance to Helicobacter pylori pathogenesis. Helicobacter 2005, 10, 146-156.
13. Ismail, S., Hampton, M. B., Keenan, J. I., Helicobacter pylori outer membrane vesicles modulate proliferation and interleukin-8 production by gastric epithelial cells. Infect. Immun. 2003, 71, 5670-5675.
14. Keenan, J., Day, T., Neal, S., Cook, B. et al., A role for the bacterial outer membrane in the pathogenesis of Helicobacter pylori infection. FEMS Microbiol. Lett. 2000, 182, 259-264.
15. Beveridge, T. J., Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 1999, 181, 4725-4733.
16. Mashburn-Warren, L. M., Whiteley, M., Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 2006, 61, 839-846.
17. Alaniz, R. C., Deatherage, B. L., Lara, J. C., Cookson, B. T., Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J. Immunol. 2007, 179, 7692-7701.
18. Lee, H. S. W., Boulton, I. C., Reddin, K., Wong, H. et al., Neisserial outer membrane vesicles bind the coinhibitory receptor carcinoembryonic antigen-related cellular adhesion molecule 1 and suppress CD4+T lymphocyte function. Infect. Immun. 2007, 75, 4449-4455.
19. Davis, J. M., Carvalho, H. M., Rasmussen, S. B., O'Brien, A. D., Cytotoxic necrotizing factor type 1 delivered by outer membrane vesicles of uropathogenic Escherichia coli attenuates polymorphonuclear leukocyte antimicrobial activity and chemotaxis. Infect. Immun. 2006, 74, 4401-4408.
20. Kesty, N., Mason, K., Reedy, M., Miller, S., Kuehn, M., Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 2004, 23, 4538-4549.
21. Kouokam, J. C., Wai, S. N., Fallman, M., Dobrindt, U. et al., Active cytotoxic necrotizing factor 1 associated with outer membrane vesicles from uropathogenic Escherichia coli. Infect. Immun. 2006, 74, 2022-2030.
22. Wai, S. N., Lindmark, B., Soderblom, T., Takade, A. et al., Vesicle-mediated export and assembly of pore-forming oligomers of the Enterobacterial ClyA cytotoxin. Cell 2003, 115, 25-35.
23. Kuehn, M., Kesty, N., Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005, 19, 2645-2655.
24. McBroom, A. J., Kuehn, M. J., Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 2007, 63, 545-558.
25. Galka, F., Wai, S. N., Kusch, H., Engelmann, S. et al., Proteomic characterisation of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect. Immun. 2008, 76, 1825-1836.
26. Berlanda Scorza, F., Doro, F., Rodriguez-Ortega, M. J., Stella, M. et al., Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli tolR IHE3034 mutant. Mol. Cell. Proteomics 2008, 7, 473-485.
27. Fisseha, M., Chen, P., Brandt, B., Kijek, T. et al., Characterization of native outer membrane vesicles from lpxL mutant strains of Neisseria meningitidis for use in parenteral vaccination. Infect. Immun. 2005, 73, 4070-4080.
28. Post, D. M. B., Zhang, D., Eastvold, J. S., Teghanemt, A. et al., Biochemical and functional characterization of membrane blebs purified from Neisseria meningitidis serogroup B. J. Biol. Chem. 2005, 280, 38383-38394.
29. Vaughan, T. E., Skipp, P. J., O'Connor, C. D., Hudson, M. J. et al., Proteomic analysis of Neisseria lactamica and Neisseria meningitidis outer membrane vesicle vaccine antigens. Vaccine 2006, 24, 5277-5293.
30. Wheeler, J., Vipond, C., Feavers, I., Exploring the proteome of meningococcal outer membrane vesicle vaccines. Proteomics - Clin. Appl. 2007, 1, 1198-1210.
31. Nally, J., Whitelegge, J., Aguilera, R., Pereira, M. et al., Purification and proteomic analysis of outer membrane vesicles from a clinical isolate of Leptospira interrogans serovar Copenhageni. Proteomics 2005, 5, 144-152.
32. Ayala, G., Torres, L., Espinosa, M., Fierros-Zarate, G. et al., External membrane vesicles from Helicobacter pylori induce apoptosis in gastric epithelial cells. FEMS Microbiol. Lett. 2006, 260, 178-185.
33. Chitcholtan, K., Hampton, M. B., Keenan, J. I., Outer membrane vesicles enhance the carcinogenic potential of Helicobacter pylori. Carcinogenesis 2008, 12, 2400-2405.
34. Heczko, U., Smith, V. C., Mark Meloche, R., Buchan, A. M. J., Finlay, B. B., Characteristics of Helicobacter pylori attachment to human primary antral epithelial cells. Microb. Infect. 2000, 2, 1669-1676.
35. Fiocca, R., Necchi, V., Sommi, P., Ricci, V. et al., Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J. Pathol. 1999, 188, 220-226.
36. Keenan, J., Oliaro, J., Domigan, N., Potter, H. et al., Immune response to an 18-kilodalton outer membrane antigen identifies lipoprotein 20 as a Helicobacter pylori vaccine candidate. Infect. Immun. 2000, 68, 3337-3343.
37. Sommi, P., Ricci, V., Fiocca, R., Necchi, V. et al., Persistence of Helicobacter pylori VacA toxin and vacuolating potential in cultured gastric epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 1998, 275, G681-G688.
38. Keenan, J. I., Allardyce, R. A., Bagshaw, P. F., Dual silver staining to characterise Helicobacter spp. outer membrane components. J. Immunol. Method 1997, 209, 17-24.
39. Keenan, J., Allardyce, R., Iron influences the expression of Helicobacter pylori outer membrane vesicle-associated virulence factors. Eur. J. Gastroenterol. Hepatol. 2000.
40. Asahi, M., Azuma, T., Ito, S., Ito, Y. et al., Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J. Exp. Med. 2000, 191, 593-602.
41. Alm, R. A., Ling, L.-S. L., Moir, D. T., King, B. L. et al., Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999, 397, 176-180.
42. Bradford, M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
43. Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680-685.
44. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., Mann, M., In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protocols 2007, 1, 2856-2860.
45. Keenan, J. I., Allardyce, R. A., Bagshaw, P. F., Lack of protection following immunisation with H. pylori outer membrane vesicles highlights antigenic differences between H. felis and H. pylori. FEMS Microbiol. Lett. 1998, 161, 21-27.
46. Ricci, V., Chiozzi, V., Necchi, V., Oldani, A. et al., Free-soluble and outer membrane vesicle-associated VacA from Helicobacter pylori: two forms of release, a different activity. Biochem. Biophys. Res. Commun. 2005, 337, 173-178.
47. Grenier, D., Mayrand, D., Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect. Immun. 1987, 55, 111-117.
48. Moe, G. R., Zuno-Mitchell, P., Hammond, S. N., Granoff, D. M., Sequential immunization with vesicles prepared from heterologous Neisseria meningitidis strains elicits broadly protective serum antibodies to Group B strains. Infect. Immun. 2002, 70, 6021-6031.
49. Backert, S., Kwok, T., Schmid, M., Selbach, M. et al., Subproteomes of soluble and structure-bound Helicobacter pylori proteins analyzed by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2005, 5, 1331-1345.
50. Gardy, J. L., Brinkman, F. S. L., Methods for predicting bacterial protein subcellular localization. Nat. Rev. Microbiol. 2006, 4, 741-751.
51. Gardy, J. L., Laird, M. R., Chen, F., Rey, S. et al., PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 2005, 21, 617-623.
52. Alm, R. A., Bina, J., Andrews, B. M., Doig, P. et al., Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect. Immun. 2000, 68, 4155-4168.
53. Salama, N., Guillemin, K., McDaniel, T. K., Sherlock, G. et al., A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl. Acad. Sci. 2000, 97, 14668-14673.
54. Jungblut, P., Bumann, D., Haas, G., Zimny-Arndt, U. et al., Comparative proteome analysis of Helicobacter pylori. Mol. Microbiol. 2000, 36, 710-725.
55. Yamaoka, Y., Ojo, O., Fujimoto, S., Odenbreit, S. et al., Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut 2006, 55, 775-781.
56. Forsyth, M. H., Atherton, J. C., Blaser, M. J., Cover, T. L., Heterogeneity in levels of vacuolating cytotoxin gene (vacA) transcription among Helicobacter pylori strains. Infect. Immun. 1998, 66, 3088-3094.
57. Cover, T. L., Cao, P., Lind, C. D., Tham, K. T., Blaser, M. J., Correlation between vacuolating cytotoxin production by Helicobacter pylori isolates in vitro and in vivo. Infect. Immun. 1993, 61, 5008-5012.
58. Hennig, E. E., Mernaugh, R., Edl, J., Cao, P., Cover, T. L., Heterogeneity among Helicobacter pylori strains in expression of the outer membrane protein BabA. Infect. Immun. 2004, 72, 3429-3435.
59. Ilver, D., Arnqvist, A., Ogren, J., Frick, I.-M. et al., Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998, 279, 373-377.
60. Yamaoka, Y., Souchek, J., Odenbreit, S., Haas, R. et al., Discrimination between cases of duodenal ulcer and gastritis on the basis of putative virulence factors of Helicobacter pylori. J. Clin. Microbiol. 2002, 40, 2244-2246.
61. Carlsohn, E., Nystrom, J., Karlsson, H., Svennerholm, A. M., Nilsson, C. L., Characterization of the outer membrane protein profile from disease-related Helicobacter pylori isolates by subcellular fractionation and nano-LC FT-ICR MS analysis. J. Proteome Res. 2006, 5, 3197-3204.
62. Lee, E., Bang, J., Park, G., Choi, D. et al., Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 2007, 7, 3143-3153.
63. Chong, P. K., Gan, C. S., Pham, T. K., Wright, P. C., isobaric tags for relative and absolute quantitation (iTRAQ) reproducibility: implication of multiple injections. J. Proteome Res. 2006, 5, 1232-1240.
64. Censini, S., Lange, C., Xiang, Z., Crabtree, J. E. et al., cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. PNAS USA 1996, 93, 14648-14653.
65. Tufano, M. A., Rossano, F., Catalanotti, P., Liguori, G. et al., Immunobiological activities of Helicobacter pylori porins. Infect. Immun. 1994, 62, 1392-1399.
66. Fan, X., Gunasena, H., Cheng, Z., Espejo, R. et al., H. pylori urease binds to class II MHC on gastric epithelial cells and induces their apoptosis. J. Immunol. 2000, 165, 1918-1924.
67. Gobert, A. P., Mersey, B. D., Cheng, Y., Blumberg, D. R. et al., Urease release by Helicobacter pylori stimulates macrophage inducible nitric oxide synthase. J. Immunol. 2002, 168, 6002-6006.
68. Voland, P., Hafsi, N., Zeitner, M., Laforsch, S. et al., Antigenic properties of HpaA and Omp18, two outer membrane proteins of Helicobacter pylori. Infect. Immun. 2003, 71, 3837-3843.
69. Rathinavelu, S., Kao, J. Y., Zavros, Y., Merchant, J. L., Helicobacter pylori outer membrane protein 18 (Hp1125) induces dendritic cell maturation and function. Helicobacter 2005, 10, 424-432.
70. Amedei, A., Cappon, A., Codolo, G., Cabrelle, A. et al., The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J. Clin. Invest. 2006, 116, 1092-1101.
71. Montemurro, P., Nishioka, H., Dundon, W., de Bernard, M. et al., The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a potent stimulant of mast cells. Eur. J. Immunol. 2002, 32, 671-676.
72. Pathak, S. K., Basu, S., Bhattacharyya, A., Pathak, S. et al., TLR4-dependent NF-kB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-Isomerase (HP0175)-mediated induction of IL-6 release from macrophages. J. Immunol. 2006, 177, 7950-7958.
73. Kim, K.-M., Lee, S.-G., Park, M.-G., Song, J.-Y. et al., [gamma]-Glutamyltranspeptidase of Helicobacter pylori induces mitochondria-mediated apoptosis in AGS cells. Biochem. Biophys. Res. Commun. 2007, 355, 562-567.
74. Tabassam, F. H., Graham, D. Y., Yamaoka, Y., OipA plays a role in Helicobacter pylori-induced focal adhesion kinase activation and cytoskeletal re-organization. Cell. Microbiol. 2008, 10, 1008-1020.
75. Gobert, A. P., Bambou, J.-C., Werts, C., Balloy, V. et al., Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a Toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism. J. Biol. Chem. 2004, 279, 245-250.
76. Ferrari, G., Garaguso, I., Adu-Bobie, J., Doro, F. et al., Outer membrane vesicles from group B Neisseria meningitidis delta gna33 mutant: proteomic and immunological comparison with detergent-derived outer membrane vesicles. Proteomics 2006, 6, 1856-1866.
77. Vipond, C., Suker, J., Jones, C., Tang, C. et al., Proteomic analysis of a meningococcal outer membrane vesicle vaccine prepared from the group B strain NZ98/254. Proteomics 2006, 6, 3400-3413.
78. Vipond, C., Wheeler, J., Jones, C., Feavers, I., Suker, J., Characterization of the protein content of a meningococcal outer membrane vesicle vaccine by polyacrylamide gel electrophoresis and mass spectrometry. Hum. Vaccin. 2005, 1, 80-84.
79. Rodríguez-Ortega, M., Norais, N., Bensi, G., Liberatori, S. et al., Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat. Biotechnol. 2006, 24, 191-197.
80. Severin, A., Nickbarg, E., Wooters, J., Quazi, S. A. et al., Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J. Bacteriol. 2007, 189, 1514-1522.
81. Tjalsma, H., Lambooy, L., Hermans, P., Swinkels, D., Shedding & shaving: disclosure of proteomic expressions on a bacterial face. Proteomics 2008, 8, 1415-1428.
82. Herskovits, A. A., Shimoni, E., Minsky, A., Bibi, E., Accumulation of endoplasmic membranes and novel membrane-bound ribosome-signal recognition particle receptor complexes in Escherichia coli. J. Cell Biol. 2002, 159, 403-410.
83. Lee, E., Choi, D., Kim, K., Gho, Y., Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom. Rev. 2008, 27, 535-555.
84. Franzén, B., Becker, S., Mikkola, R., Tidblad, K. et al., Characterization of periplasmic Escherichia coli protein expression at high cell densities. Electrophoresis 1999, 20, 790-797.
85. Chi, A., Valenzuela, L., Beard, S., Mackey, A. J. et al., Periplasmic proteins of the extremophile Acidithiobacillus ferrooxidans: a high throughput proteomics analysis. Mol. Cell. Proteomics 2007, 6, 2239-2251.
86. Harris, A. G., Hazell, S. L., Localisation of Helicobacter pylori catalase in both the periplasm and cytoplasm, and its dependence on the twin-arginine target protein, KapA, for activity. FEMS Microbiol. Lett. 2003, 229, 283-289.
87. Baik, S.-C., Kim, K.-M., Song, S.-M., Kim, D.-S. et al., Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Helicobacter pylori strain 26695. J. Bacteriol. 2004, 186, 949-955.
88. Pyndiah, S., Lasserre, J. P., Menard, A., Claverol, S. et al., Two-dimensional blue native/sds gel electrophoresis of multiprotein complexes from Helicobacter pylori. Mol. Cell. Proteomics 2007, 6, 193-206.
89. Fujita, Y., Yamaguchi, K., Kamegaya, T., Sato, H. et al., A novel mechanism of autolysis in Helicobacter pylori: possible involvement of peptidergic substances. Helicobacter 2005, 10, 567-576.
90. Phadnis, S. H., Parlow, M. H., Levy, M., Ilver, D. et al., Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect. Immun. 1996, 64, 905-912.
91. Schraw, W., McClain, M. S., Cover, T. L., Kinetics and mechanisms of extracellular protein release by Helicobacter pylori. Infect. Immun. 1999, 67, 5247-5252.
92. Vanet, A., Labigne, A., Evidence for specific secretion rather than autolysis in the release of some Helicobacter pylori proteins. Infect. Immun. 1998, 66, 1023-1027.
93. Hawtin, P., Stacey, A., Newell, D., Investigation of the structure and localization of the urease of Helicobacter pylori using monoclonal antibodies. J. Gen Microbiol. 1990, 136, 1995-2000.
94. Dunn, B. E., Vakil, N. B., Schneider, B. G., Miller, M. M. et al., Localization of Helicobacter pylori urease and heat shock protein in human gastric biopsies. Infect. Immun. 1997, 65, 1181-1188.
95. Eschweiler, B., Bohrmann, B., Gerstenecker, B., Schiltz, E., Kist, M., In situ localization of the 60 k protein of Helicobacter pylori, which belongs to the family of heat shock proteins, by immuno-electron microscopy. Zentralbl Bakteriol. 1993, 280, 73-85.
96. Spiegelhalder, C., Gerstenecker, B., Kersten, A., Schiltz, E., Kist, M., Purification of Helicobacter pylori superoxide dismutase and cloning and sequencing of the gene. Infect. Immun. 1993, 61, 5315-5325.