Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli ΔtolR IHE3034 mutant

Molecular and Cellular Proteomics

Volumn 7, Issue 3, 2008, Pages 473-485

  Scorza, Francesco Berlanda ^a   Doro, Francesco ^a   Rodríguez Ortega, Manuel José ^a,b   Stella, Maria ^a   Liberatori, Sabrina ^a   Taddei, Anna Rita ^c   Serino, Laura ^a   Moriel, Danilo Gomes ^a   Nesta, Barbara ^a   Fontana, Maria Rita ^a   Spagnuolo, Angela ^a   Pizza, Mariagrazia ^a   Norais, Nathalia ^a   Grandi, Guido ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b UNIVERSITY OF CÓRDOBA   (Spain)

^c UNIVERSITY OF TUSCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; VACCINE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOLOGICAL ACTIVITY; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CYTOPLASM; DRUG RESEARCH; DRUG TARGETING; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE SEQUENCE; GENETIC DATABASE; HOST CELL; MEMBRANE VESICLE; MOLECULAR MECHANICS; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEOMICS; SUPERNATANT; TWO DIMENSIONAL ELECTROPHORESIS;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL TOXINS; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOME, BACTERIAL; MEMBRANE PROTEINS; MUTATION; PEPTIDES; PERIPLASMIC PROTEINS; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEOMICS; SOFTWARE;

ANIMALIA; BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 41549137780     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700295-MCP200     Document Type: Article

References (78)

1. Johnson, J. R., and Russo, T. A. (2002) Uropathogenic Escherichia coli as agents of diverse non-urinary tract extraintestinal infections. J. Infect. Dis. 186, 859-864
2. Johnson, J. R., and Russo, T. A. (2002) Extraintestinal pathogenic Escherichia coli: "the other bad E coli". J. Lab. Clin. Med. 139, 155-162
3. Xie, Y., Kim, K. J., and Kim, K. S. (2004) Current concepts on Escherichia coli K1 translocation of the blood-brain barrier. FEMS Immunol. Med. Microbiol. 42, 271-279
4. Minino, A. M., Heron, M. P., and Smith, B. L. (2006) Deaths: preliminary data for 2004. Natl. Vital Stat. Rep. 54, 1-49
5. Minino, A. M., and Smith, B. L. (2001) Deaths: preliminary data for 2000. Natl. Vital Stat. Rep. 49, 1-40
6. Russo, T. A., and Johnson, J. R. (2006) Extraintestinal isolates of Escherichia coli: identification and prospects for vaccine development. Expert Rev. Vaccines 5, 45-54
7. Grischke, E. M., and Ruttgers, H. (1987) Treatment of bacterial infections of the female urinary tract by immunization of the patients. Urol. Int. 42, 338-341
8. Uehling, D. T., Hopkins, W. J., Elkahwaji, J. E., Schmidt, D. M., and Leverson, G. E. (2003) Phase 2 clinical trial of a vaginal mucosal vaccine for urinary tract infections. J. Urol. 170, 867-869
9. Huber, M., Krauter, K., Winkelmann, G., Bauer, H. W., Rahlfs, V. W., Lauener, P. A., Blessmann, G. S., and Bessler, W. G. (2000) Immunostimulation by bacterial components: II. Efficacy studies and meta-analysis of the bacterial extract OM-89. Int. J. Immunopharmacol., 22, 1103-1111
10. Bauer, H. W., Alloussi, S., Egger, G., Blumlein, H. M., Cozma, G., and Schulman, C. C. (2005) A long-term, multicenter, double-blind study of an Escherichia coli extract (OM-89) in female patients with recurrent urinary tract infections. Eur. Urol. 47, 542-548
11. Bauer, H. W., Rahlfs, V. W., Lauener, P. A., and Blessmann, G. S. (2002) Prevention of recurrent urinary tract infections with immuno-active E. coli fractions: a meta-analysis of five placebo-controlled double-blind studies. Int. J. Antimicrob. Agents 19, 461-456
12. Koukalova, D., Krocova, Z., Vitek, P., Macela, A., and Hajek, V. (1999) Immunostimulatory activity of the vaccine used in the treatment of recurrent urinary infections. II. Bratisl. Lek. Listy 100, 215-217
13. Koukalova, D., Reif, R., Hajek, V., Mucha, Z., Vesely, J., Viktorinova, M., and Lochman, I. (1999) Immunomodulation of recurrent urinary tract infections with Urvakol vaccine. Bratisl. Lek. Listy 100, 246-251
14. Marinova, S., Nenkov, P., Markova, R., Nikolaeva, S., Kostadinova, R., Mitov, I., and Vretenarska, M. (2005) Cellular and humoral systemic and mucosal immune responses stimulated by an oral polybacterial immunomodulator in patients with chronic urinary tract infections. Int. J. Immunopathol. Pharmacol. 18, 457-473
15. Nenkov, P., Mitov, I., Marinova, S., and Markova, R. (1995) Experimental investigations on the immunomodulating activity of polybacterial preparation for peroral immunotherapy and immunoprophylaxis of uroinfections. Int. J. Immunopharmacol. 17, 489-496
16. Jann, B., and Jann, K. (1990) Structure and biosynthesis of the capsular antigens of Escherichia coli. Curr. Top. Microbiol. Immunol. 150, 19-42
17. Linggood, M. A., and Ingram, P. L. (1982) The role of a haemolysin in the virulence of Escherichia coli for mice. J. Med. Microbiol. 15, 23-30
18. O'Hanley, P., Lalonde, G., and Ji, G. (1991) α-Hemolysin contributes to the pathogenicity of piliated digalactoside-binding Escherichia coli in the kidney: efficacy of an α-hemolysin vaccine in preventing renal injury in the BALB/c mouse model of pyelonephritis. Infect. Immun. 59, 1153-1161
19. O'Hanley, P., Marcus, R., Baek, K. H., Denich, K., and Ji, G. E. (1993) Genetic conservation of hlyA determinants and serologicall conservation of HlyA: basis for developing a broadly cross-reactive subunit Escherichia coli α-hemolysin vaccine. Infect. Immun. 61, 1091-1097
20. 1) attenuates the virulence of uropathogenic Escherichia coli. Infect. Immun. 69, 3954-3964
21. Johnson, W. M., and Lior, H. (1988) A new heat-labile cytolethal distending toxin (CLDT) produced by Escherichia coli isolates from clinical material. Microb. Pathog. 4, 103-113
22. Kesty, N. C., Mason, K. M., Reedy, M., Miller, S. E., and Kuehn, M. J. (2004) Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23, 4538-4549
23. Russo, T. A., Beanan, J. M., Olson, R., Genagon, S. A., Macdonald, U., Cope, J. J., Davidson, B. A., Johnston, B., and Johnson, J. R. (2007) A killed, genetically engineered derivative of a wild-type extraintestinal pathogenic E. coli strain is a vaccine candidate. Vaccine 25, 3859-3870
24. Evans, D. J., Jr., Ruiz-Palacios, G., Evans, D. E., DuPont, H. L., Pickering, L. K., and Olarte, J. (1977) Humoral immune response to the heat-labile enterotoxin of Escherichia coli in naturally acquired diarrhea and antitoxin determination by passive immune hemolysis. Infect. Immun. 16, 781-788
25. Greatorex, J. S., and Thorne, G. M. (1994) Humoral immune responses to Shiga-like toxins and Escherichia coli O157 lipopolysaccharide in hemolytic-uremic syndrome patients and healthy subjects. J. Clin. Microbiol. 32, 1172-1178
26. Leblanc, J., Fliss, I., and Matar, C. (2004) Induction of a humoral immune response following an Escherichia coli O157:H7 infection with an immunomodulatory peptidic fraction derived from Lactobacillus helveticus-fermented milk. Clin. Diagn. Lab. Immunol. 11, 1171-1181
27. Cordwell, S. J. (2006) Technologies for bacterial surface proteomics. Curr. Opin. Microbiol. 9, 320-329
28. Ferrari, G., Garaguso, I., Adu-Bobie, J., Doro, F., Taddei, A. R., Biolchi, A., Brunelli, B., Giuliani, M. M., Pizza, M., Norais, N., and Grandi, G. (2006) Outer membrane vesicles from group B Neisseria meningitidis ΔAgna33 mutant: proteomic and immunological comparison with detergent-derived outer membrane vesicles. Proteomics 6, 1856-1866
29. Adu-Bobie, J., Lupetti, P., Brunelli, B., Granoff, D., Norais, N., Ferrari, G., Grandi, G., Rappuoli, R., and Pizza, M. (2004) GNA33 of Neisseria meningitidis is a lipoprotein required for cell separation, membrane architecture, and virulence. Infect. Immun. 72, 1914-1919
30. Kuehn, M. J., and Kesty, N. C. (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19, 2645-2655
31. Mashburn-Warren, L. M., and Whiteley, M. (2006) Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61, 839-846
32. Bernadac, A., Gavioli, M., Lazzaroni, J. C., Raina, S., and Lloubes, R. (1998) Escherichia coli tol-pal mutants form outer membrane vesicles. J. Bacteriol. 180, 4872-4878
33. Suzuki, H., Nishimura, Y., Yasuda, S., Nishimura, A., Yamada, M., and Hirota, Y. (1978) Murein-lipoprotein of Escherichia coli: a protein involved in the stabilization of bacterial cell envelope. Mol. Gen. Genet. 167, 1-9
34. Yem, D. W., and Wu, H. C. (1978) Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein. J. Bacteriol. 133, 1419-1426
35. Cascales, E., Bemadac, A., Gavioli, M., Lazzaroni, J. C., and Lloubes, R. (2002) Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J. Bacteriol. 184, 754-759
36. Kouokam, J. C., Wai, S. N., Fallman, M., Dobrindt, U., Hacker, J., and Uhlin, B. E. (2006) Active cytotoxic necrotizing factor 1 associated with outer membrane vesicles from uropathogenic Escherichia coli. Infect. Immun. 74, 2022-2030
37. Derbise, A., Lesic, B., Dacheux, D., Ghigo, J. M., and Camiel, E. (2003) A rapid and simple method for inactivating chromosomal genes in Yersinia. FEMS Immunol. Med. Microbiol. 38, 113-116
38. Taylor, L. A., and Rose, R. E. (1988) A correction in the nucleotide sequence of the Tn903 kanamycin resistance determinant in pUC4K. Nucleic Acids Res. 16, 358
39. Maxson, M. E., and Darwin, A. J. (2004) Identification of inducers of the Yersinia enterocolitica phage shock protein system and comparison to the regulation of the RpoE and Cpx extracytoplasmic stress responses. J. Bacteriol. 186, 4199-4208
40. Achtman, M., Mercer, A., Kusecek, B., Pohl, A., Hauzenroeder, M., Aaronson, W., Sutton, A., and Silver, R. P. (1983) Six widespread bacterial clones among Escherichia cali K1 isolates. Infect. Immun. 39, 315-335
41. Mobley, H. L., Green, D. M., Trifillis, A. L., Johnson, D. E., Chippendale, G. R., Lockatell, C. V., Jones, B. D., and Warren, J. W. (1990) Pyelone-phritogenic Escherichia coli and killing of cultured human renal proximal tubular epitheliall cells: role of hemolysin in some strains. Infect. Immun. 58, 1281-1289
42. Doherty, N. S., Littman, B. H., Reilly, K., Swindell, A. C., Buss, J. M., and Anderson, N. L (1998) Analysis of changes in acute-phase plasma proteins in an acute inflammatory response and in rheumatoid arthritis using two-dimensional gel electrophoresis. Electrophoresis 19, 355-363
43. Blattner, F. R., Plunkett, G., III, Bloch, C. A., Perna, N. T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J. D., Rode, C. K., Mayhew, G. F., Gregor, J., Davis, N. W., Kirkpatrick, H. A., Goeden, M. A., Rose, D. J., Mau, B., and Shao, Y. (1997) The complete genome sequence of Escherichia coli K-12. Science 277, 1453-1474
44. Riley, M., Abe, T., Arnaud, M. B., Berlyn, M. K., Blattner, F. R., Chaudhuri, R. R., Glasner, J. D., Horiuchi, T., Keseler, I. M., Kosuge, T., Mori, H., Perna, N. T., Plunkett, G., III, Rudd, K. E., Serres, M. H., Thomas, G. H., Thomson, N. R., Wishart, D., and Wenner, B. L (2006) Escherichia coli K-12: a cooperatively developed annotation snapshot - 2005. Nucleic Acids Res. 34, 1-9
45. Welch, R. A., Burland, V., Plunkett, G., III, Redford, P., Roesch, P., Rasko, D., Buckles, E. L., Liou, S. R., Boutin, A., Hackett, J., Stroud, D., Mayhew, G. F., Rose, D. J., Zhou, S., Schwartz, D. C., Pema, N. T., Mobley, H. L., Donnenberg, M. S., and Blattner, F. R. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99, 17020-17024
46. Pappin, D. J. (2003) Peptide mass fingerprinting using MALDI-TOF mass spectrometry. Methods Mol. Biol. 211, 211-219
47. Gardy, J. L., Laird, M. R., Chen, F., Rey, S., Walsh, C. J., Ester, M., and Brinkman, F. S. (2005) PSORTb v. 2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21, 617-623
48. Berven, F. S., Karlsen, O. A., Straume, A. H., Flikka, K., Murrell, J. C., Fjellbirkeland, A., Lillehaug, J. R., Eidhammer, I., and Jensen, H. B. (2006) Analysing the outer membrane subproteome of Methylococcus capsutatus (Bath) using proteomics and novel biocomputing tools. Arch. Microbiol. 184, 362-377
49. Horton, R. M., Hunt, H. D., Ho, S. N., Pullen, J. K., and Pease, L. R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene (Amst.) 77, 61-68
50. Wach, A. (1996) PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12, 259-265
51. Lopatin, D. E., Combs, A., Sweier, D. G., Fenno, J. C., and Dhamija, S. (2000) Characterization of heat-inducible expression and cloning of HtpG (Hsp90 homologue) of Porphyromonas gingivalls. Infect. Immun. 68, 1980-1987
52. Johnson, W. M., and Lior, H. (1988) A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. Microb. Pathog. 4, 115-126
53. Okuda, J., Fukumoto, M., Takeda, Y., and Nishibuchi, M. (1997) Examination of diarrheagenicity of cytolethal distending toxin: suckling mouse response to the products of the cdtABC genes of Shigella dysenteriae. Infect Immun. 65, 428-433
54. Whitehouse, C. A., Balbo, P. B., Pesci, E. C., Cottle, D. L., Mirabito, P. M., and Pickett, C. L. (1998) Campylobacter jejuni cytolethal distending toxin causes a G2-phase cell cycle block. Infect. Immun. 66, 1934-1940
55. Coll, J. L., Heyde, M., and Portalier, R. (1994) Expression of the nmpC gene of Escherichia coll K-12 is modulated by external pH. Identification of cis-acting regulatory sequences involved in this regulation. Mol. Microbiol. 12, 83-93
56. Courtney, H. S., Dale, J. B., and Hasty, D. L. (2002) Strategies for preventing Group A streptococcal adhesion and infection, in Handbook of Bacterial Adhesion: Principles, Methods and Applications (An, Y. H., and Friedman, R. J., eds) pp. 553-579, Human Press Inc., Totowa, NJ
57. Lin, J., Huang, S., and Zhang, Q. (2002) Outer membrane proteins: key players for bacterial adaptation in host niches. Microbes Infect. 4, 325-331
58. Lindahl, G., Stalhammar-Carlemalm, M., and Areschoug, T. (2005) Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin. Microbiol. Rev. 18, 102-127
59. Niemann, H. H., Schubert, W. D., and Heinz, D. W. (2004) Adhesins and invasins of pathogenic bacteria: a structural view. Microbes Infect. 6, 101-112
60. Ton-That, H., Marraffini, L A., and Schneewind, O. (2004) Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim. Biophys. Acta 1694, 269-278
61. Galperin, M. Y., and Koonin, E. V. (1999) Searching for drug targets in microbial genomes. Curr. Opin. Biotechnol. 10, 571-578
62. Fujiki, Y., Hubbard, A. L., Fowler, S., and Lazarow, P. B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102
63. Rhomberg, T. A., Karlberg, O., Mini, T., Zimny-Arndt, U., Wickenberg, U., Rottgen, M., Jungblut, P. R., Jeno, P., Andersson, S. G., and Dehio, C. (2004) Proteomic analysis of the sarcosine-insoluble outer membrane fraction of the bacterial pathogen Bartorrella henselae. Proteomics 4, 3021-3033
64. Molloy, M. P., Herbert, B. R., Slade, M. B., Rabilloud, T., Nouwens, A. S., Williams, K. L., and Gooley, A. A. (2000) Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem. 267, 2871-2881
65. Xu, C., Lin, X., Ren, H., Zhang, Y., Wang, S., and Peng, X. (2006) Analysis of outer membrane proteome of Escherichia coli related to resistance to ampicillin and tetracycline. Proteomics 6, 462-473
66. Alteri, C. J., and Mobley, H. L. (2007) Quantitative profile of the uropathogenic Escherichia coli outer membrane proteome during growth in human urine. Infect Immun. 75, 2679-2688
67. Lee, E. Y., Bang, J. Y., Park, G. W., Choi, D. S., Kang, J. S., Kim, H. J., Park, K. S., Lee, J. O., Kim, Y. K., Kwon, K. H., Kim, K. P., and Gho, Y. S. (2007) Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7, 3143-3153
68. Maione, D., Margarit, I., Rinaudo, C. D., Masignani, V., Mora, M., Scarselli, M., Tettelin, H., Brettoni, C., Iacobini, E. T., Rosini, R., D'Agostino, N., Miorin, L., Buccato, S., Mariani, M., Galli, G., Nogarotto, R., Nardi Dei, V., Vegni, F., Fraser, C., Mancuso, G., Teti, G., Madoff, L. C., Paoletti, L C., Rappuoli, R., Kasper, D. L., Telford, J. L., and Grandi, G. (2005) Identification of a universal Group B streptococcus vaccine by multiple genome screen. Science 309, 148-150
69. Pizza, M., Scarlato, V., Masignani, V., Giuliani, M. M., Arico, B., Comanducci, M., Jennings, G. T., Baldi, L., Bartolini, E., Capecchi, B., Galeotti, C. L., Luzzi, E., Manetti, R., Marchetti, E., Mora, M., Nuti, S., Ratti, G., Santini, L., Savino, S., Scarselli, M., Storni, E., Zuo, P., Broeker, M., Hundt, E., Knapp, B., Blair, E., Mason, T., Tettelin, H., Hood, D. W., Jeffries, A. C., Saunders, N. J., Granoff, D. M., Venter, J. C., Moxon, E. R., Grandi, G., and Rappuoli, R. (2000) Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 287, 1816-1820
70. Giuliani, M. M., Adu-Bobie, J., Comanducci, M., Arico, B., Savino, S., Santini, L., Brunelli, B., Bambini, S., Biolchi, A., Capecchi, B., Cartocci, E., Ciucchi, Di Marcello, F., Ferlicca, F., Galli, B., Luzzi, E., Masignani, V., Serruto, Veggi, D., Contorni, M., Morandi, M., Bartalesi, A., Cinotti, V., Mannuci, D., Titta, F., Ovidi, E., Weisch, J. A., Granoff, D., Rappuoli, R., and Pizza, M. (2006) A universal vaccine for serogroup B meningococcus. Proc. Natl. Acad. Sci. U. S. A. 103, 10834-10839
71. Achtman, M., Heuzenroeder, M., Kusecek, B., Ochman, H., Caugant, D., Selander, R. K., Vaisanen-Rhen, V., Korhonen, T. K., Stuart, S., and Orsikov, F.(1986) Clonal analysis of Escherichia coli O2:K1 isolated from diseased h mans and animals. Infect. Immun. 51, 268-276
72. Cherifi, A., Contrepois, M., Picard, B., Goullet, P., Orskov, I., and Orskov, F. (1994) Clonal relationships among Escherichia coli serogroup O78 isolates from human and animal infections. J. Clin. Microbiol. 32, 1197-1202
73. Johnson, J. R., Murray, A. C., Gajewski, A., Sullivan, M., Snippes, P., Kuskowski, M. A., and Smith, K. E. (2003) Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrob. Agents Chemother. 47, 2161-2168
74. Heywood, W., Henderson, B., and Nair, S. P. (2005) Cytolethal distending toxin: creating a gap in the cell cycle. J. Med. Microbiol. 54, 207-216
75. Thelestam, M., and Frisan, T. (2004) Cytolethal distending toxins. Rev. Physiol. Biochem. Pharmacol. 152, 111-133
76. McSweeney, L. A., and Dreyfus, L. A. (2005) Carbohydrate-binding specificity of the Escherichia coli cytolethal distending toxin CdtA-II and CdtC-II subunits. Infect. Immun. 73, 2051-2060
77. Nishikubo, S., Ohara, M., Ueno, Y., Ikura, M., Kurihara, H., Komatsuzawa, H., Oswald, E., and Sugai, M. (2003) An N-terminal segment of the active component of the bacterial genotoxin cytolethal distending toxin B (CDTB) directs CDTB into the nucleus. J. Biol. Chem. 278, 50671-60681
78. McSweeney, L. A., and Dreyfus, L. A. (2004) Nuclear localization of the Escherichia coli cytolethal distending toxin CdtB subunit. Cell. Microbiol. 6, 447-458