Immunoproteomic Profiling of Bordetella pertussis Outer Membrane Vesicle Vaccine Reveals Broad and Balanced Humoral Immunogenicity

Journal of Proteome Research

Volumn 14, Issue 7, 2015, Pages 2929-2942

  Raeven, René H M ^a,b,d   Van Der Maas, Larissa ^a   Tilstra, Wichard ^a   Uittenbogaard, Joost P ^a   Bindels, Tim H E ^a   Kuipers, Betsy ^c   Van Der Ark, Arno ^a   Pennings, Jeroen L A ^c   Van Riet, Elly ^a   Jiskoot, Wim ^b   Kersten, Gideon F A ^a,b   Metz, Bernard ^a  

^a Intravacc   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^d NONE   (Netherlands)

Author keywords

2D electrophoresis; antibody; Bordetella pertussis; humoral; outer membrane vesicle; proteomics; subclass; vaccine; Western blot

Indexed keywords

BACTERIAL ANTIGEN; BRKA PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; LIPOPOLYSACCHARIDE; PERTUSSIS VACCINE; PROTEOME; UNCLASSIFIED DRUG; VAG8 PROTEIN; BACTERIAL VACCINE; BACTERIUM ANTIBODY; OUTER MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN SPECIFICITY; ARTICLE; BORDETELLA PERTUSSIS; FEMALE; HUMORAL IMMUNITY; IMMUNOASSAY; IMMUNOBLOTTING; IMMUNOGENICITY; MASS SPECTROMETRY; MOUSE; NONHUMAN; OUTER MEMBRANE; PERTUSSIS; PRIORITY JOURNAL; PROTEOMICS; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; VACCINATION; ANIMAL; BIOSYNTHESIS; IMMUNOLOGY; LIQUID CHROMATOGRAPHY; METABOLISM; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; WHOOPING COUGH;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL VACCINES; BORDETELLA PERTUSSIS; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MICE; PROTEOME; TANDEM MASS SPECTROMETRY; WHOOPING COUGH;

EID: 84947205237     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00258     Document Type: Article

References (70)

1. Cherry, J. D. Epidemic pertussis in 2012-the resurgence of a vaccine-preventable disease N. Engl. J. Med. 2012, 367 (9) 785-7
2. Baxter, R.; Bartlett, J.; Rowhani-Rahbar, A.; Fireman, B.; Klein, N. P. Effectiveness of pertussis vaccines for adolescents and adults: case-control study Br. Med. J. 2013, 347, f4249
3. Celentano, L. P.; Massari, M.; Paramatti, D.; Salmaso, S.; Tozzi, A. E. Resurgence of pertussis in Europe Pediatr. Infect. Dis. J. 2005, 24 (9) 761-5
4. Kretzschmar, M.; Teunis, P. F.; Pebody, R. G. Incidence and reproduction numbers of pertussis: estimates from serological and social contact data in five European countries PLoS Med. 2010, 7 (6) e1000291
5. Mielcarek, N.; Debrie, A. S.; Raze, D.; Bertout, J.; Rouanet, C.; Younes, A. B.; Creusy, C.; Engle, J.; Goldman, W. E.; Locht, C. Live attenuated B. pertussis as a single-dose nasal vaccine against whooping cough PLoS Pathog. 2006, 2 (7) e65
6. Roberts, R.; Moreno, G.; Bottero, D.; Gaillard, M. E.; Fingermann, M.; Graieb, A.; Rumbo, M.; Hozbor, D. Outer membrane vesicles as acellular vaccine against pertussis Vaccine 2008, 26 (36) 4639-46
7. Bottero, D.; Gaillard, M. E.; Fingermann, M.; Weltman, G.; Fernandez, J.; Sisti, F.; Graieb, A.; Roberts, R.; Rico, O.; Rios, G.; Regueira, M.; Binsztein, N.; Hozbor, D. Pulsed-field gel electrophoresis, pertactin, pertussis toxin S1 subunit polymorphisms, and surfaceome analysis of vaccine and clinical Bordetella pertussis strains Clin. Vaccine Immunol. 2007, 14 (11) 1490-8
8. Altindis, E.; Tefon, B. E.; Yildirim, V.; Ozcengiz, E.; Becher, D.; Hecker, M.; Ozcengiz, G. Immunoproteomic analysis of Bordetella pertussis and identification of new immunogenic proteins Vaccine 2009, 27 (4) 542-8
9. Misegades, L. K.; Winter, K.; Harriman, K.; Talarico, J.; Messonnier, N. E.; Clark, T. A.; Martin, S. W. Association of childhood pertussis with receipt of 5 doses of pertussis vaccine by time since last vaccine dose, California, 2010 JAMA, J. Am. Med. Assoc. 2012, 308 (20) 2126-32
10. Mooi, F. R.; van der Maas, N. A. T.; De Melker, H. E. Pertussis resurgence: waning immunity and pathogen adaptation-two sides of the same coin Epidemiol. Infect. 2013, 1-10
11. Warfel, J. M.; Zimmerman, L. I.; Merkel, T. J. Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model Proc. Natl. Acad. Sci. U.S.A. 2014, 111 (2) 787-92
12. Plotkin, S. A. Correlates of protection induced by vaccination Clin. Vaccine Immunol. 2010, 17 (7) 1055-65
13. Storsaeter, J.; Hallander, H. O.; Gustafsson, L.; Olin, P. Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis Vaccine 1998, 16 (20) 1907-16
14. van den Berg, B. M.; David, S.; Beekhuizen, H.; Mooi, F. R.; van Furth, R. Protection and humoral immune responses against Bordetella pertussis infection in mice immunized with acellular or cellular pertussis immunogens Vaccine 2000, 19 (9-10) 1118-28
15. Mills, K. H.; Ryan, M.; Ryan, E.; Mahon, B. P. A murine model in which protection correlates with pertussis vaccine efficacy in children reveals complementary roles for humoral and cell-mediated immunity in protection against Bordetella pertussis Infect. Immun. 1998, 66 (2) 594-602
16. Gouw, D.; Jonge, M. I.; Hermans, P. W.; Wessels, H. J.; Zomer, A.; Berends, A.; Pratt, C.; Berbers, G. A.; Mooi, F. R.; Diavatopoulos, D. A. Proteomics-identified Bvg-Activated Autotransporters Protect against Bordetella pertussis in a mouse model PLoS One 2014, 9 (8) e105011
17. Warfel, J. M.; Merkel, T. J. Bordetella pertussis infection induces a mucosal IL-17 response and long-lived Th17 and Th1 immune memory cells in nonhuman primates Mucosal Immunol. 2013, 6 (4) 787-96
18. Raeven, R. H. M.; Brummelman, J.; Pennings, J. L.; Nijst, O. E.; Kuipers, B.; Blok, L. E.; Helm, K.; van Riet, E.; Jiskoot, W.; van Els, C. A.; Han, W. G.; Kersten, G. F.; Metz, B. Molecular Signatures of the Evolving Immune Response in Mice following a Bordetella pertussis Infection PLoS One 2014, 9 (8) e104548
19. Stevens, T. L.; Bossie, A.; Sanders, V. M.; Fernandez-Botran, R.; Coffman, R. L.; Mosmann, T. R.; Vitetta, E. S. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells Nature 1988, 334 (6179) 255-8
20. Mitsdoerffer, M.; Lee, Y.; Jager, A.; Kim, H. J.; Korn, T.; Kolls, J. K.; Cantor, H.; Bettelli, E.; Kuchroo, V. K. Proinflammatory T helper type 17 cells are effective B-cell helpers Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (32) 14292-7
21. Redhead, K.; Watkins, J.; Barnard, A.; Mills, K. H. Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity Infect. Immun. 1993, 61 (8) 3190-8
22. Rowe, J.; Macaubas, C.; Monger, T. M.; Holt, B. J.; Harvey, J.; Poolman, J. T.; Sly, P. D.; Holt, P. G. Antigen-specific responses to diphtheria-tetanus-acellular pertussis vaccine in human infants are initially Th2 polarized Infect. Immun. 2000, 68 (7) 3873-7
23. Ross, P. J.; Sutton, C. E.; Higgins, S.; Allen, A. C.; Walsh, K.; Misiak, A.; Lavelle, E. C.; McLoughlin, R. M.; Mills, K. H. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine PLoS Pathog. 2013, 9 (4) e1003264
24. Hellwig, S. M.; van Oirschot, H. F.; Hazenbos, W. L.; van Spriel, A. B.; Mooi, F. R.; van De Winkel, J. G. Targeting to Fcgamma receptors, but not CR3 (CD11b/CD18), increases clearance of Bordetella pertussis J. Infect. Dis. 2001, 183 (6) 871-9
25. Rodriguez, M. E.; Hellwig, S. M.; Hozbor, D. F.; Leusen, J.; van der Pol, W. L.; van de Winkel, J. G. Fc receptor-mediated immunity against Bordetella pertussis J. Immunol. 2001, 167 (11) 6545-51
26. Hellwig, S. M.; Rodriguez, M. E.; Berbers, G. A.; van de Winkel, J. G.; Mooi, F. R. Crucial role of antibodies to pertactin in Bordetella pertussis immunity J. Infect. Dis. 2003, 188 (5) 738-42
27. Taranger, J.; Trollfors, B.; Lagergard, T.; Sundh, V.; Bryla, D. A.; Schneerson, R.; Robbins, J. B. Correlation between pertussis toxin IgG antibodies in postvaccination sera and subsequent protection against pertussis J. Infect. Dis. 2000, 181 (3) 1010-3
28. Zhu, Y. Z.; Cai, C. S.; Zhang, W.; Guo, H. X.; Zhang, J. P.; Ji, Y. Y.; Ma, G. Y.; Wu, J. L.; Li, Q. T.; Lu, C. P.; Guo, X. K. Immunoproteomic analysis of human serological antibody responses to vaccination with whole-cell pertussis vaccine (WCV) PLoS One 2010, 5 (11) e13915
29. Tefon, B. E.; Maass, S.; Ozcengiz, E.; Becher, D.; Hecker, M.; Ozcengiz, G. A comprehensive analysis of Bordetella pertussis surface proteome and identification of new immunogenic proteins Vaccine 2011, 29 (19) 3583-95
30. Ormazabal, M.; Bartel, E.; Gaillard, M. E.; Bottero, D.; Errea, A.; Zurita, M. E.; Moreno, G.; Rumbo, M.; Castuma, C.; Flores, D.; Martin, M. J.; Hozbor, D. Characterization of the key antigenic components of pertussis vaccine based on outer membrane vesicles Vaccine 2014, 32 (46) 6084-90
31. Gaillard, M. E.; Bottero, D.; Errea, A.; Ormazabal, M.; Zurita, M. E.; Moreno, G.; Rumbo, M.; Castuma, C.; Bartel, E.; Flores, D.; van der Ley, P.; van der Ark, A.; Hozbor, D. F. Acellular pertussis vaccine based on outer membrane vesicles capable of conferring both long-lasting immunity and protection against different strain genotypes Vaccine 2014, 32 (8) 931-7
32. Zollinger, W. D.; Donets, M. A.; Schmiel, D. H.; Pinto, V. B.; Labrie, J.; Moran, E. E.; Brandt, B. L.; Ionin, B.; Marques, R.; Wu, M.; Chen, P.; Stoddard, M. B.; Keiser, P. B. Design and evaluation in mice of a broadly protective meningococcal group B native outer membrane vesicle vaccine Vaccine 2010, 28, 5057-67
33. Welch, D. F. Applications of cellular fatty acid analysis Clin. Microbiol. Rev. 1991, 4 (4) 422-38
34. Caroff, M.; Brisson, J.; Martin, A.; Karibian, D. Structure of the Bordetella pertussis 1414 endotoxin FEBS Lett. 2000, 477 (1-2) 8-14
35. Stenger, R. M.; Smits, M.; Kuipers, B.; Kessen, S. F.; Boog, C. J.; van Els, C. A. Fast, antigen-saving multiplex immunoassay to determine levels and avidity of mouse serum antibodies to pertussis, diphtheria, and tetanus antigens Clin. Vaccine Immunol. 2011, 18 (4) 595-603
36. Hijnen, M.; van Gageldonk, P. G.; Berbers, G. A.; van Woerkom, T.; Mooi, F. R. The Bordetella pertussis virulence factor P.69 pertactin retains its immunological properties after overproduction in Escherichia coli Protein Expression Purif. 2005, 41 (1) 106-12
37. Yan, J. X.; Wait, R.; Berkelman, T.; Harry, R. A.; Westbrook, J. A.; Wheeler, C. H.; Dunn, M. J. A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry Electrophoresis 2000, 21 (17) 3666-72
38. van de Waterbeemd, B.; Mommen, G. P.; Pennings, J. L.; Eppink, M. H.; Wijffels, R. H.; van der Pol, L. A.; de Jong, A. P. Quantitative proteomics reveals distinct differences in the protein content of outer membrane vesicle vaccines J. Proteome Res. 2013, 12 (4) 1898-908
39. Meiring, H. D.; Van Der Heeft, E.; Ten Hove, G. J.; De Jong, A. P. J. M. Nanoscale LC-MS(n): Technical design and applications to peptide and protein analysis J. Sep. Sci. 2002, 25 (Issue 9) 557-68
40. Bart, M. J.; van Gent, M.; van der Heide, H. G.; Boekhorst, J.; Hermans, P.; Parkhill, J.; Mooi, F. R. Comparative genomics of prevaccination and modern Bordetella pertussis strains BMC Genomics 2010, 11, 627
41. Silva, J. C.; Gorenstein, M. V.; Li, G. Z.; Vissers, J. P.; Geromanos, S. J. Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition Mol. Cell. Proteomics 2006, 5 (1) 144-56
42. Huang da, W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2009, 4 (1) 44-57
43. Canthaboo, C.; Williams, L.; Xing, D. K.; Corbel, M. J. Investigation of cellular and humoral immune responses to whole cell and acellular pertussis vaccines Vaccine 2000, 19 (6) 637-43
44. Germann, T.; Bongartz, M.; Dlugonska, H.; Hess, H.; Schmitt, E.; Kolbe, L.; Kolsch, E.; Podlaski, F. J.; Gately, M. K.; Rude, E. Interleukin-12 profoundly up-regulates the synthesis of antigen-specific complement-fixing IgG2a, IgG2b and IgG3 antibody subclasses in vivo Eur. J. Immunol. 1995, 25 (3) 823-9
45. Quintana, F. J.; Solomon, A.; Cohen, I. R.; Nussbaum, G. Induction of IgG3 to LPS via Toll-like receptor 4 co-stimulation PLoS One 2008, 3 (10) e3509
46. Bachmann, M. F.; Jennings, G. T. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns Nat. Rev. Immunol. 2010, 10 (11) 787-96
47. Kuehn, M. J.; Kesty, N. C. Bacterial outer membrane vesicles and the host-pathogen interaction Genes Dev. 2005, 19 (22) 2645-55
48. Akira, S.; Takeda, K. Toll-like receptor signalling Nat. Rev. Immunol. 2004, 4 (7) 499-511
49. Bekeredjian-Ding, I.; Jego, G. Toll-like receptors - sentries in the B-cell response Immunology 2009, 128 (3) 311-23
50. Hogenesch, H. Mechanism of immunopotentiation and safety of aluminum adjuvants Front. Immunol. 2012, 3, 406
51. Brummelman, J.; Helm, K.; Hamstra, H. J.; van der Ley, P.; Boog, C. J.; Han, W. G.; van Els, C. A. Modulation of the CD4 T cell response after acellular pertussis vaccination in the presence of TLR4 ligation Vaccine 2015, 33, 1483-91
52. Gracia, A.; Polewicz, M.; Halperin, S. A.; Hancock, R. E.; Potter, A. A.; Babiuk, L. A.; Gerdts, V. Antibody responses in adult and neonatal BALB/c mice to immunization with novel Bordetella pertussis vaccine formulations Vaccine 2011, 29 (8) 1595-604
53. Michaelsen, T. E.; Kolberg, J.; Aase, A.; Herstad, T. K.; Hoiby, E. A. The four mouse IgG isotypes differ extensively in bactericidal and opsonophagocytic activity when reacting with the P1.16 epitope on the outer membrane PorA protein of Neisseria meningitidis Scand. J. Immunol. 2004, 59 (1) 34-9
54. Geurtsen, J.; Fae, K. C.; van den Dobbelsteen, G. P. Importance of (antibody-dependent) complement-mediated serum killing in protection against Bordetella pertussis Expert Rev. Vaccines 2014, 1-12
55. Bruhns, P. Properties of mouse and human IgG receptors and their contribution to disease models Blood 2012, 119 (24) 5640-9
56. Hazenbos, W. L.; Heijnen, I. A.; Meyer, D.; Hofhuis, F. M.; Renardel de Lavalette, C. R.; Schmidt, R. E.; Capel, P. J.; van de Winkel, J. G.; Gessner, J. E.; van den Berg, T. K.; Verbeek, J. S. Murine IgG1 complexes trigger immune effector functions predominantly via Fc gamma RIII (CD16) J. Immunol. 1998, 161 (6) 3026-32
57. Nimmerjahn, F.; Bruhns, P.; Horiuchi, K.; Ravetch, J. V. FcgammaRIV: a novel FcR with distinct IgG subclass specificity Immunity 2005, 23 (1) 41-51
58. Andreasen, C.; Carbonetti, N. H. Role of neutrophils in response to Bordetella pertussis infection in mice Infect. Immun. 2009, 77 (3) 1182-8
59. Kirimanjeswara, G. S.; Agosto, L. M.; Kennett, M. J.; Bjornstad, O. N.; Harvill, E. T. Pertussis toxin inhibits neutrophil recruitment to delay antibody-mediated clearance of Bordetella pertussis J. Clin. Invest. 2005, 115 (12) 3594-601
60. Hamstra, H. J.; Kuipers, B.; Schijf-Evers, D.; Loggen, H. G.; Poolman, J. T. The purification and protective capacity of Bordetella pertussis outer membrane proteins Vaccine 1995, 13 (8) 747-52
61. Oliver, D. C.; Fernandez, R. C. Antibodies to BrkA augment killing of Bordetella pertussis Vaccine 2001, 20 (1-2) 235-41
62. Marr, N.; Oliver, D. C.; Laurent, V.; Poolman, J.; Denoel, P.; Fernandez, R. C. Protective activity of the Bordetella pertussis BrkA autotransporter in the murine lung colonization model Vaccine 2008, 26 (34) 4306-11
63. Finn, T. M.; Stevens, L. A. Tracheal colonization factor: a Bordetella pertussis secreted virulence determinant Mol. Microbiol. 1995, 16 (4) 625-34
64. Chen, I.; Finn, T. M.; Yanqing, L.; Guoming, Q.; Rappuoli, R.; Pizza, M. A recombinant live attenuated strain of Vibrio cholerae induces immunity against tetanus toxin and Bordetella pertussis tracheal colonization factor Infect. Immun. 1998, 66 (4) 1648-53
65. Burns, D. L.; Gould-Kostka, J. L.; Kessel, M.; Arciniega, J. L. Purification and immunological characterization of a GroEL-like protein from Bordetella pertussis Infect. Immun. 1991, 59 (4) 1417-22
66. Mountzouros, K. T.; Kimura, A.; Cowell, J. L. A bactericidal monoclonal antibody specific for the lipooligosaccharide of Bordetella pertussis reduces colonization of the respiratory tract of mice after aerosol infection with B. pertussis Infect. Immun. 1992, 60 (12) 5316-8
67. Gotto, J.; Eckhardt, T.; Scott, J.; Woods, D. Protective effect of Bordetella pertussis lipopolysaccharide in the rat intratracheal challenge model of pertussis Abstracts of the General Meeting of the American Society for Microbiology 1992, Abstr. 92nd (abstr. E-15) 146
68. Weiss, A. A.; Mobberley, P. S.; Fernandez, R. C.; Mink, C. M. Characterization of human bactericidal antibodies to Bordetella pertussis Infect. Immun. 1999, 67 (3) 1424-31
69. Kubler-Kielb, J.; Vinogradov, E.; Lagergard, T.; Ginzberg, A.; King, J. D.; Preston, A.; Maskell, D. J.; Pozsgay, V.; Keith, J. M.; Robbins, J. B.; Schneerson, R. Oligosaccharide conjugates of Bordetella pertussis and bronchiseptica induce bactericidal antibodies, an addition to pertussis vaccine Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (10) 4087-92
70. Finn, T. M.; Amsbaugh, D. F. Vag8, a Bordetella pertussis bvg-regulated protein Infect. Immun. 1998, 66 (8) 3985-9