Immunoproteomic analysis of the development of natural immunity in subjects colonized by Neisseria meningitidis reveals potential vaccine candidates

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 5080-5089

  Williams, Jeannette N ^a   Skipp, Paul J ^b   O'Connor, C David ^b   Christodoulides, Myron ^a   Heckels, John E ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; MEMBRANE PROTEIN; VACCINE;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; IMMUNOREACTIVITY; INNATE IMMUNITY; MASS SPECTROMETRY; NEISSERIA MENINGITIDIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SERUM; SERUM BACTERICIDAL ACTIVITY; TWO DIMENSIONAL ELECTROPHORESIS;

ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, WESTERN; CARRIER STATE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; MENINGOCOCCAL INFECTIONS; MENINGOCOCCAL VACCINES; NEISSERIA MENINGITIDIS, SEROGROUP B; PROTEOMICS;

EID: 70350451448     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00701-09     Document Type: Article

References (60)

1. Abel, A., S. Sanchez, J. Arenas, M. T. Criado, and C. M. Ferreiros. 2007. Bioinformatic analysis of outer membrane proteome of Neisseria meningitidis and Neisseria lactamica. Int. Microbiol. 10:5-11.
2. Achtman, M., R. A. Wall, M. Bopp, B. Kusecek, G. Morelli, E. Saken, and M. Hassanking. 1991. Variation in class 5 protein expression by serogroup A meningococci during a meningitis epidemic. J. Infect. Dis. 164:375-382.
3. Bernardini, G., G. Renzone, M. Comanducci, R. Mini, S. Arena, C. D'Ambrosio, S. Bambini, L. Trabalzini, G. Grandi, P. Martelli, M. Achtman, A. Scaloni, G. Ratti, and A. Santucci. 2004. Proteome analysis of Neisseria meningitidis serogroup A. Proteomics 4:2893-2926.
4. Beveridge, T. J. 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181:4725-4733.
5. Bjune, G., E. A. Hoiby, J. K. Gronnesby, O. Arnesen, J. Holstfredriksen, A. Halstensen, E. Holten, A. K. Lindbak, H. Nokleby, E. Rosenqvist, L. K. Solberg, O. Closs, J. Eng, L. O. Froholm, A. Lystad, L. S. Bakketeig, and B. Hareide. 1991. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 338:1093-1096.
6. Boslego, J., J. Garcia, C. Cruz, W. Zollinger, B. Brandt, S. Ruiz, M. Martinez, J. Arthur, P. Underwood, W. Silva, E. Moran, W. Hankins, J. Gilly, and J. Mays. 1995. Efficacy, safety, and immunogenicity of a meningococcal group B (15 P1.3) outer membrane protein vaccine in Iquique, Chile. Vaccine 13:821-829.
7. Callaghan, M. J., S. Lewis, S. E. Bailey, H. Chan, D. Ferguson, J. P. Derrick, I. M. Feavers, M. C. Maiden, and A. J. Pollard. 2008. Evaluation of recombinant Opa proteins as vaccine candidates against hyperinvasive meningococci, abstr. 043, p. 59. 16th Int. Pathog. Neisseria Conf., Rotterdam, The Netherlands.
8. Delgado, M., D. Yero, O. Niebla, S. Gonzalez, Y. Climent, Y. Perez, K. Cobas, E. Caballero, D. Garcia, and R. Pajon. 2007. Lipoprotein NMB0928 from Neisseria meningitidis serogroup B as a novel vaccine candidate. Vaccine 25:8420-8431.
9. Ferrari, G., I. Garaguso, J. Adu-Bobie, F. Doro, A. R. Taddei, B. Biolchi, B. Brunelli, M. M. Giuliani, M. Pizza, N. Norais, and G. Grandi. 2006. Outer membrane vesicles from group B Neisseria meningitidis gna33 mutant: proteomic and immunological comparison with detergent-derived outer membrane vesicles. Proteomics 6:1856-1866.
10. Finne, J., M. Leinonen, and P. H. Makela. 1983. Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet ii:355-357.
11. Forgber, M., R. Basu, K. Roychoudhury, S. Theinert, S. Roy, S. Sundar, and P. Walden. 2006. Mapping the antigenicity of the parasites in Leishmania donovani infection by proteome serology. PLoS ONE 1:e40.
12. Frye, S. A., R. Assalkhou, R. F. Collins, R. C. Ford, C. Petersson, J. P. Derrick, and T. Tonjum. 2006. Topology of the outer-membrane secretin PilQ from Neisseria meningitidis. Microbiology 152:3751-3764.
13. Gardy, J. L., M. R. Laird, F. Chen, S. Rey, C. J. Walsh, M. Ester, and F. S. Brinkman. 2005. PSORTb v. 2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21:617-623.
14. Goldschneider, I., E. C. Gotschlich, and M. S. Artenstein. 1969. Human immunity to the meningococcus. I. The role of humoral antibodies. J. Exp. Med. 129:1307-1326.
15. Gorg, A., W. Weiss, and M. J. Dunn. 2004. Current two-dimensional electrophoresis technology for proteomics. Proteomics 4:3665-3685. (Pubitemid 39657447)
16. Grifantini, R., E. Bartolini, A. Muzzi, M. Draghi, E. Frigimelica, J. Berger, F. Randazzo, and G. Grandi. 2002. Gene expression profile in Neisseria meningitidis and Neisseria lactamica upon host-cell contact: from basic research to vaccine development. Ann. N. Y. Acad. Sci. 975:202-216.
17. Guttormsen, H. K., L. M. Wetzler, and A. Naess. 1993. Humoral immune response to the class 3 outer membrane protein during the course of meningococcal disease. Infect. Immun. 61:4734-4742.
18. Haas, G., G. Karaali, K. Ebermayer, W. G. Metzger, S. Lamer, U. Zimny- Arndt, S. Diescher, U. B. Goebel, K. Vogt, A. B. Roznowski, B. J. Wiedenmann, T. F. Meyer, T. Aebischer, and P. R. Jungblut. 2002. Immunoproteomics of Helicobacter pylori infection and relation to gastric disease. Proteomics 2:313-324.
19. Halperin, S. A., J. M. Langley, B. Smith, P. Wunderli, L. Kaufman, A. Kimura, and D. Martin. 2007. Phase 1 first-in-human studies of the reactogenicity and immunogenicity of a recombinant NspA vaccine in healthy adults. Vaccine 25:450-457. (Pubitemid 44856095)
20. Harrison, L. H. 2006. Prospects for vaccine prevention of meningococcal infection. Clin. Microbiol. Rev. 19:142-164.
21. Jacobsson, S., S. T. Hedberg, P. Molling, M. Unemo, M. Comanducci, R. Rappuoli, and P. Olcen. 2009. Prevalence and sequence variations of the genes encoding the five antigens included in the novel 5CVMB vaccine covering group B meningococcal disease. Vaccine 27:1579-1584.
22. Jolley, K., L. Appleby, J. C. Wright, M. Christodoulides, and J. E. Heckels. 2001. Immunization with recombinant Opc outer membrane protein from Neisseria meningitidis: influence of sequence variation and levels of expression on the bactericidal immune response against meningococci. Infect. Immun. 69:3809-3916.
23. Jones, G. R., M. Christodoulides, J. L. Brooks, A. R. O. Miller, K. A. V. Cartwright, and J. E. Heckels. 1998. Dynamics of carriage of Neisseria meningitidis in a group of military recruits: subtype stability and specificity of the immune response following colonisation. J. Infect. Dis. 178:451-459.
24. Jones, G. R., J. N. Williams, M. Christodoulides, K. Jolley, and J. E. Heckels. 2000. Lack of immunity in university students prior to an outbreak of serogroup C meningococcal infection. J. Infect. Dis. 181:1172-1175.
25. Jordens, J. Z., J. N. Williams, G. R. Jones, and J. E. Heckels. 2002. Detection of meningococcal carriage by culture and PCR of throat swabs and mouth gargles. J. Clin. Microbiol. 40:75-79.
26. Jordens, J. Z., J. N. Williams, G. R. Jones, M. Christodoulides, and J. E. Heckels. 2004. Development of immunity to serogroup B meningococci during carriage of Neisseria meningitidis in a cohort of university students. Infect. Immun. 72:6503-6510.
27. Khemiri, A., A. Galland, D. Vaudry, S. P. Chan Tchi, H. Vaudry, T. Jouenne, and P. Cosette. 2008. Outer-membrane proteomic maps and surface-exposed proteins of Legionella pneumophila using cellular fractionation and fluorescent labelling. Anal. Bioanal. Chem. 390:1861-1871.
28. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
29. Lee, E. Y., J. Y. Bang, G. W. Park, D. S. Choi, J. S. Kang, H. J. Kim, K. S. Park, J. O. Lee, Y. K. Kim, K. H. Kwon, K. P. Kim, and Y. S. Gho. 2007. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7:3143-3153.
30. Lopez, J. E., W. F. Siems, G. H. Palmer, K. A. Brayton, T. C. McGuire, J. Norimine, and W. C. Brown. 2005. Identification of novel antigenic proteins in a complex Anaplasma marginale outer membrane immunogen by mass spectrometry and genomic mapping. Infect. Immun. 73:8109-8118.
31. McGuinness, B. T., I. N. Clarke, P. R. Lambden, A. K. Barlow, J. T. Poolman, D. M. Jones, and J. E. Heckels. 1991. Point mutation in meningococcal porA gene associated with increased endemic disease. Lancet 337:514-517.
32. Mendum, T. A., J. Newcombe, C. L. McNeilly, and J. Mcfadden. 2009. Towards the immunoproteome of Neisseria meningitidis. PLoS ONE 4:e5940.
33. Milagres, L. G., S. R. Ramos, C. T. Sacchi, C. E. A. Melles, V. S. D. Vieira, H. Sato, G. S. Brito, J. C. Moraes, and C. E. Frasch. 1994. Immune response of Brazilian children to a Neisseria meningitidis serogroup B outer membrane protein vaccine: comparison with efficacy. Infect. Immun. 62:4419-4424.
34. Noah, N., and B. Henderson. 2002. Surveillance of bacterial meningitis in Europe 1999/2000. Communicable Disease Surveillance Centre, Public Health Laboratory Service, London, United Kingdom.
35. Oster, P., D. Lennon, J. O'Hallahan, K. Mulholland, S. Reid, and D. Martin. 2005. MeNZB: a safe and highly immunogenic tailor-made vaccine against the New Zealand Neisseria meningitidis serogroup B disease epidemic strain. Vaccine 23:2191-2196.
36. Pitarch, A., J. Abian, M. Carrascal, M. Sanchez, C. Nombela, and C. Gil. 2004. Proteomics-based identification of novel Candida albicans antigens for diagnosis of systemic candidiasis in patients with underlying hematological malignancies. Proteomics 4:3084-3106.
37. Post, D. M., D. Zhang, J. S. Eastvold, A. Teghanemt, B. W. Gibson, and J. P. Weiss. 2005. Biochemical and functional characterization of membrane blebs purified from Neisseria meningitidis serogroup B. J. Biol. Chem. 280:38383-38394.
38. Rosenqvist, E., E. A. Hoiby, E. Wedege, K. Bryn, J. Kolberg, A. Klem, E. Ronnild, G. Bjune, and H. Nokleby. 1995. Human antibody responses to meningococcal outer membrane antigens after three doses of the Norwegian group B meningococcal vaccine. Infect. Immun. 63:4642-4652.
39. Rosenqvist, E., E. A. Hoiby, E. Wedege, B. Kusecek, and M. Achtman. 1993. The 5c protein of Neisseria meningitidis is highly immunogenic in humans and induces bactericidal antibodies. J. Infect. Dis. 167:1065-1073.
40. Santoni, V., M. Molloy, and T. Rabilloud. 2000. Membrane proteins and proteomics: un amour impossible? Electrophoresis 21:1054-1070.
41. Saunders, N. J., A. C. Jeffries, J. F. Peden, D. W. Hood, H. Tettelin, R. Rappuoli, and E. R. Moxon. 2000. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol. Microbiol. 37:207-215.
42. Schoen, C., J. Blom, H. Claus, A. Schramm-Gluck, P. Brandt, T. Muller, A. Goesmann, B. Joseph, S. Konietzny, O. Kurzai, C. Schmitt, T. Friedrich, B. Linke, U. Vogel, and M. Frosch. 2008. Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 105:3473-3478. (Pubitemid 351723577)
43. Shevchenko, A., O. N. Jensen, A. V. Podtelejnikov, F. Sagliocco, M. Wilm, O. Vorm, P. Mortensen, A. Shevchenko, H. Boucherie, and M. Mann. 1996. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. USA 93:14440-14445.
44. Shin, Y. S., G. W. Shin, Y. R. Kim, E. Y. Lee, H. H. Yang, K. J. Palaksha, H. J. Youn, J. H. Kim, D. Y. Kim, A. E. Marsh, J. Lakritz, and T. S. Jung. 2005. Comparison of proteome and antigenic proteome between two Neospora caninum isolates. Vet. Parasitol. 134:41-52.
45. Sierra, G. V. G., H. C. Campa, N. M. Varcacel, I. L. Garcia, P. L. Izquierdo, P. F. Sotolongo, G. V. Casanueva, C. O. Rico, C. R. Rodriguez, and M. H. Terry. 1991. Vaccine against group B Neisseria meningitidis: protection trial and mass vaccination results in Cuba. Natl. Inst. Public Health Ann. (Oslo) 14:195-210.
46. Stephens, D. S., B. Greenwood, and P. Brandtzaeg. 2007. Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369:2196-2210.
47. Tala, A., M. De Stefano, C. Bucci, and P. Alifano. 2008. Reverse transcriptase- PCR differential display analysis of meningococcal transcripts during infection of human cells: up-regulation of priA and its role in intracellular replication. BMC Microbiol. 8:131.
48. Tam, R., and M. H. Saier, Jr. 1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57:320-346.
49. Tappero, J. W., R. Lagos, and A. M. Ballesteros. 1999. Immunogenicity of 2 serogroup B outer-membrane protein meningococcal vaccines: a randomized controlled trial in Chile. JAMA 281:1520-1527.
50. Tettelin, H., N. J. Saunders, J. Heidelberg, A. C. Jeffries, K. E. Nelson, J. A. Eisen, K. A. Ketchum, D. W. Hood, J. F. Peden, R. J. Dodson, W. C. Nelson, M. L. Gwinn, R. DeBoy, J. D. Peterson, E. K. Hickey, D. H. Haft, S. L. Salzberg, O. White, R. D. Fleischmann, B. A. Dougherty, T. Mason, A. Ciecko, D. S. Parksey, E. Blair, H. Cittone, E. B. Clark, M. D. Cotton, T. R. Utterback, H. Khouri, H. Y. Qin, J. Vamathevan, J. Gill, V. Scarlato, V. Masignani, M. Pizza, G. Grandi, L. Sun, H. O. Smith, C. M. Fraser, E. R. Moxon, R. Rappuoli, and J. C. Venter. 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287:1809-1815.
51. Trotter, C. L., M. Chandra, R. Cano, A. Larrauri, M. E. Ramsay, C. Brehony, K. A. Jolley, M. C. Maiden, S. Heuberger, and M. Frosch. 2007. A surveillance network for meningococcal disease in Europe. FEMS Microbiol. Rev. 31:27-36.
52. Uli, L., L. Castellanos-Serra, L. Betancourt, F. Dominguez, R. Barbera, F. Sotolongo, G. Guillen, and F. R. Pajon. 2006. Outer membrane vesicles of the VA-MENGOC-BC vaccine against serogroup B of Neisseria meningitidis: analysis of protein components by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 6:3389-3399.
53. Vaughan, T. E., P. J. Skipp, C. D. O'Connor, M. J. Hudson, R. Vipond, M. J. Elmore, and A. R. Gorringe. 2006. Proteomic analysis of Neisseria lactamica and Neisseria meningitidis outer membrane vesicle vaccine antigens. Vaccine 24:5277-5293.
54. Vipond, C., J. Suker, C. Jones, C. Tang, I. M. Feavers, and J. X. Wheeler. 2006. Proteomic analysis of a meningococcal outer membrane vesicle vaccine prepared from the group B strain NZ98/254. Proteomics 6:4203.
55. Vipond, C., J. X. Wheeler, C. Jones, I. M. Feavers, and J. Suker. 2005. Characterization of the protein content of a meningococcal outer membrane vesicle vaccine by polyacrylamide gel electrophoresis and mass spectrometry. Hum. Vaccin. 1:80-84.
56. Wedege, E., E. A. Hoiby, E. Rosenqvist, and G. Bjune. 1998. Immune responses against major outer membrane antigens of Neisseria meningitidis in vaccinees and controls who contracted meningococcal disease during the Norwegian serogroup B protection trial. Infect. Immun. 66:3223-3231.
57. West, D., K. Reddin, M. Matheson, R. Heath, S. Funnell, M. Hudson, A. Robinson, and A. Gorringe. 2001. Recombinant Neisseria meningitidis transferrin binding protein A protects against experimental meningococcal infection. Infect. Immun. 69:1561-1567.
58. Williams, J. N., G. R. Jones, M. Christodoulides, and J. E. Heckels. 2003. Serological correlates of protection against meningococci in a cohort of university students before and during an outbreak of serogroup C infection. J. Infect. Dis. 187:1433-1441.
59. Williams, J. N., P. J. Skipp, H. E. Humphries, M. Christodoulides, C. D. O'Connor, and J. E. Heckels. 2007. Proteomic analysis of outer membranes and vesicles from wild-type serogroup B Neisseria meningitidis and a lipopolysaccharide deficient mutant. Infect. Immun. 75:1364-1372.
60. Zollinger, W. D., and R. E. Mandrell. 1983. Importance of complement source in bactericidal activity of human antibody and murine monoclonal antibody to meningococcal group B polysaccharide. Infect. Immun. 40:257-264.