Bordetella pertussis outer membrane vesicle vaccine confers equal efficacy in mice with milder inflammatory responses compared to a whole-cell vaccine

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Raeven, René H M ^a,b   Brummelman, Jolanda ^c   Pennings, Jeroen L A ^c   Van Der Maas, Larissa ^a   Tilstra, Wichard ^a   Helm, Kina ^c   Van Riet, Elly ^a   Jiskoot, Wim ^b   Van Els, Cécile A C M ^c   Han, Wanda G H ^c   Kersten, Gideon F A ^a,b   Metz, Bernard ^a  

^a Institute for Translational Vaccinology (Intravacc)   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; BACTERIUM ANTIBODY; IMMUNOGLOBULIN G; OUTER MEMBRANE PROTEIN;

ANIMAL; BAGG ALBINO MOUSE; BORDETELLA PERTUSSIS; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; HELPER CELL; IMMUNOLOGY; MOUSE;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL VACCINES; BORDETELLA PERTUSSIS; FEMALE; GENE EXPRESSION REGULATION; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84999766471     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep38240     Document Type: Article

References (60)

1. Cherry, J. D. Epidemic pertussis in 2012-the resurgence of a vaccine-preventable disease. The New England journal of medicine 367, 785-787, doi: 10. 1056/NEJMp1209051 (2012).
2. Tan, T. et al. Pertussis Across the Globe: Recent Epidemiologic Trends From 2000 to 2013. The Pediatric infectious disease journal 34, e222-232, doi: 10. 1097/INF. 0000000000000795 (2015).
3. 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 immunology 6, 787-796, doi: 10. 1038/mi. 2012. 117 (2013).
4. Ross, P. J. et al. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS pathogens 9, e1003264, doi: 10. 1371/journal. ppat. 1003264 (2013).
5. Higgins, S. C., Jarnicki, A. G., Lavelle, E. C., Mills, K. H. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol 177, 7980-7989 (2006).
6. Banus, S. et al. The role of Toll-like receptor-4 in pertussis vaccine-induced immunity. BMC immunology 9, 21, doi: 10. 1186/1471-2172-9-21 (2008).
7. Raeven, R. H. M. et al. Immunoproteomic Profiling of Bordetella pertussis Outer Membrane Vesicle Vaccine Reveals Broad and Balanced Humoral Immunogenicity. Journal of proteome research 14, 2929-2942, doi: 10. 1021/acs. jproteome. 5b00258 (2015).
8. Jefferson, T., Rudin, M., DiPietrantonj, C. Systematic review of the effects of pertussis vaccines in children. Vaccine 21, 2003-2014 (2003).
9. David, S., Vermeer-de Bondt, P. E., van der Maas, N. A. Reactogenicity of infant whole cell pertussis combination vaccine compared with acellular pertussis vaccines with or without simultaneous pneumococcal vaccine in the Netherlands. Vaccine 26, 5883-5887, doi: 10. 1016/j. vaccine. 2008. 07. 105 (2008).
10. Miller, D. L., Ross, E. M., Alderslade, R., Bellman, M. H., Rawson, N. S. Pertussis immunisation and serious acute neurological illness in children. British medical journal 282, 1595-1599 (1981).
11. Armstrong, M. E., Loscher, C. E., Lynch, M. A., Mills, K. H. IL-1beta-dependent neurological effects of the whole cell pertussis vaccine: a role for IL-1-associated signalling components in vaccine reactogenicity. Journal of neuroimmunology 136, 25-33 (2003).
12. Klein, N. P., Bartlett, J., Rowhani-Rahbar, A., Fireman, B., Baxter, R. Waning protection after fifth dose of acellular pertussis vaccine in children. The New England journal of medicine 367, 1012-1019, doi: 10. 1056/NEJMoa1200850 (2012).
13. 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. Proceedings of the National Academy of Sciences of the United States of America 111, 787-792, doi: 10. 1073/pnas. 1314688110 (2014).
14. Brummelman, J. et al. Modulation of the CD4(+ ) T cell response after acellular pertussis vaccination in the presence of TLR4 ligation. Vaccine 33, 1483-1491, doi: 10. 1016/j. vaccine. 2015. 01. 063 (2015).
15. Roberts, R. et al. Outer membrane vesicles as acellular vaccine against pertussis. Vaccine 26, 4639-4646, doi: 10. 1016/j. vaccine. 2008. 07. 004 (2008).
16. Gaillard, M. E. et al. Acellular pertussis vaccine based on outer membrane vesicles capable of conferring both long-lasting immunity and protection against different strain genotypes. Vaccine 32, 931-937, doi: 10. 1016/j. vaccine. 2013. 12. 048 (2014).
17. Bottero, D. et al. Characterization of the immune response induced by pertussis OMVs-based vaccine. Vaccine 34, 3303-3309, doi: 10. 1016/j. vaccine. 2016. 04. 079 (2016).
18. Nakaya, H. I. et al. Systems biology of vaccination for seasonal influenza in humans. Nature immunology 12, 786-795, doi: 10. 1038/ni. 2067 (2011).
19. Furman, D. et al. Apoptosis and other immune biomarkers predict influenza vaccine responsiveness. Molecular systems biology 9, 659, doi: 10. 1038/msb. 2013. 15 (2013).
20. Querec, T. D. et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nature immunology 10, 116-125, doi: 10. 1038/ni. 1688 (2009).
21. Obermoser, G. et al. Systems scale interactive exploration reveals quantitative and qualitative differences in response to influenza and pneumococcal vaccines. Immunity 38, 831-844, doi: 10. 1016/j. immuni. 2012. 12. 008 (2013).
22. Li, S. et al. Molecular signatures of antibody responses derived from a systems biology study of five human vaccines. Nature immunology 15, 195-204, doi: 10. 1038/ni. 2789 (2014).
23. Mizukami, T. et al. System vaccinology for the evaluation of influenza vaccine safety by multiplex gene detection of novel biomarkers in a preclinical study and batch release test. PloS one 9, e101835, doi: 10. 1371/journal. pone. 0101835 (2014).
24. Raeven, R. H. M. et al. Molecular Signatures of the Evolving Immune Response in Mice following a Bordetella pertussis Infection. PloS one 9, e104548, doi: 10. 1371/journal. pone. 0104548 (2014).
25. Zollinger, W. D. et al. Design and evaluation in mice of a broadly protective meningococcal group B native outer membrane vesicle vaccine. Vaccine 28, 5057-5067, doi: 10. 1016/j. vaccine. 2010. 05. 006 (2010).
26. Benjamini, Y., Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57, 289-300. (1995).
27. Samarajiwa, S. A., Forster, S., Auchettl, K., Hertzog, P. J. INTERFEROME: the database of interferon regulated genes. Nucleic acids research 37, D852-857, doi: 10. 1093/nar/gkn732 (2009).
28. Pereira-Lopes, S. et al. The exonuclease Trex1 restrains macrophage proinflammatory activation. J Immunol 191, 6128-6135, doi: 10. 4049/jimmunol. 1301603 (2013).
29. Chen, G. Y. et al. Broad and direct interaction between TLR and Siglec families of pattern recognition receptors and its regulation by Neu1. eLife 3, e04066, doi: 10. 7554/eLife. 04066 (2014).
30. He, Y., Franchi, L., Nunez, G. The protein kinase PKR is critical for LPS-induced iNOS production but dispensable for inflammasome activation in macrophages. European journal of immunology 43, 1147-1152, doi: 10. 1002/eji. 201243187 (2013).
31. Jozefowski, S., Biedron, R., Srottek, M., Chadzinska, M., Marcinkiewicz, J. The class A scavenger receptor SR-A/CD204 and the class B scavenger receptor CD36 regulate immune functions of macrophages differently. Innate immunity 20, 826-847, doi: 10. 1177/1753425913510960 (2014).
32. Dufton, N. et al. Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J Immunol 184, 2611-2619, doi: 10. 4049/jimmunol. 0903526 (2010).
33. Inoue, A. et al. Murine tumor necrosis factor alpha-induced adipose-related protein (tumor necrosis factor alpha-induced protein 9) deficiency leads to arthritis via interleukin-6 overproduction with enhanced NF-kappaB, STAT-3 signaling, and dysregulated apoptosis of macrophages. Arthritis and rheumatism 64, 3877-3885, doi: 10. 1002/art. 34666 (2012).
34. Jin, F. Y., Nathan, C., Radzioch, D., Ding, A. Secretory leukocyte protease inhibitor: a macrophage product induced by and antagonistic to bacterial lipopolysaccharide. Cell 88, 417-426 (1997).
35. Lu, B., Moser, A., Shigenaga, J. K., Grunfeld, C., Feingold, K. R. The acute phase response stimulates the expression of angiopoietin like protein 4. Biochemical and biophysical research communications 391, 1737-1741, doi: 10. 1016/j. bbrc. 2009. 12. 145 (2010).
36. Zhu, P., Goh, Y. Y., Chin, H. F., Kersten, S., Tan, N. S. Angiopoietin-like 4: a decade of research. Bioscience reports 32, 211-219, doi: 10. 1042/BSR20110102 (2012).
37. Vigne, S. et al. IL-36R ligands are potent regulators of dendritic and T cells. Blood 118, 5813-5823, doi: 10. 1182/blood-2011-05-356873 (2011).
38. Lee, M. S., Kim, B., Oh, G. T., Kim, Y. J. OASL1 inhibits translation of the type I interferon-regulating transcription factor IRF7. Nature immunology 14, 346-355, doi: 10. 1038/ni. 2535 (2013).
39. Takaoka, A. et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448, 501-505, doi: 10. 1038/nature06013 (2007).
40. Pollpeter, D., Komuro, A., Barber, G. N., Horvath, C. M. Impaired cellular responses to cytosolic DNA or infection with Listeria monocytogenes and vaccinia virus in the absence of the murine LGP2 protein. PloS one 6, e18842, doi: 10. 1371/journal. pone. 0018842 (2011).
41. Arthur, J. C. et al. Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity. J Immunol 185, 4515-4519, doi: 10. 4049/jimmunol. 1002227 (2010).
42. Shi, M. et al. TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nature immunology 9, 369-377, doi: 10. 1038/ni1577 (2008).
43. Traves, P. G. et al. Pivotal role of protein tyrosine phosphatase 1B (PTP1B) in the macrophage response to pro-inflammatory and anti-inflammatory challenge. Cell death & disease 5, e1125, doi: 10. 1038/cddis. 2014. 90 (2014).
44. Lechmann, M., Shuman, N., Wakeham, A., Mak, T. W. The CD83 reporter mouse elucidates the activity of the CD83 promoter in B, T, and dendritic cell populations in vivo. Proceedings of the National Academy of Sciences of the United States of America 105, 11887-11892, doi: 10. 1073/pnas. 0806335105 (2008).
45. Riley, J. P. et al. PARP-14 binds specific DNA sequences to promote Th2 cell gene expression. PloS one 8, e83127, doi: 10. 1371/journal. pone. 0083127 (2013).
46. Cho, S. H. et al. B cell-intrinsic and-extrinsic regulation of antibody responses by PARP14, an intracellular (ADP-ribosyl) transferase. J Immunol 191, 3169-3178, doi: 10. 4049/jimmunol. 1301106 (2013).
47. Loscher, C. E., Donnelly, S., McBennett, S., Lynch, M. A., Mills, K. H. Proinflammatory cytokines in the adverse systemic and neurologic effects associated with parenteral injection of a whole cell pertussis vaccine. Annals of the New York Academy of Sciences 856, 274-277 (1998).
48. O'Neill, L. A. How Toll-like receptors signal: what we know and what we don't know. Current opinion in immunology 18, 3-9, doi: 10. 1016/j. coi. 2005. 11. 012 (2006).
49. Shi, Y., HogenEsch, H., Regnier, F. E., Hem, S. L. Detoxification of endotoxin by aluminum hydroxide adjuvant. Vaccine 19, 1747-1752 (2001).
50. Bufe, B. et al. Recognition of bacterial signal peptides by mammalian formyl peptide receptors: a new mechanism for sensing pathogens. The Journal of biological chemistry 290, 7369-7387, doi: 10. 1074/jbc. M114. 626747 (2015).
51. Fu, H. et al. Ligand recognition and activation of formyl peptide receptors in neutrophils. Journal of leukocyte biology 79, 247-256, doi: 10. 1189/jlb. 0905498 (2006).
52. Rajakariar, R. et al. Hematopoietic prostaglandin D2 synthase controls the onset and resolution of acute inflammation through PGD2 and 15-deoxyDelta12 14 PGJ2. Proceedings of the National Academy of Sciences of the United States of America 104, 20979-20984, doi: 10. 1073/pnas. 0707394104 (2007).
53. Sato, M. et al. Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS letters 441, 106-110 (1998).
54. McNab, F., Mayer-Barber, K., Sher, A., Wack, A., O'Garra, A. Type I interferons in infectious disease. Nature reviews. Immunology 15, 87-103, doi: 10. 1038/nri3787 (2015).
55. Huber, J. P., Farrar, J. D. Regulation of effector and memory T-cell functions by type I interferon. Immunology 132, 466-474, doi: 10. 1111/j. 1365-2567. 2011. 03412. x (2011).
56. Reynolds, J. M. et al. Toll-like receptor 2 signaling in CD4(+ ) T lymphocytes promotes T helper 17 responses and regulates the pathogenesis of autoimmune disease. Immunity 32, 692-702, doi: 10. 1016/j. immuni. 2010. 04. 010 (2010).
57. Dunne, A. et al. A novel TLR2 agonist from Bordetella pertussis is a potent adjuvant that promotes protective immunity with an acellular pertussis vaccine. Mucosal immunology 8, 607-617, doi: 10. 1038/mi. 2014. 93 (2015).
58. Martin, S. W. et al. Pertactin-negative Bordetella pertussis strains: evidence for a possible selective advantage. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 60, 223-227, doi: 10. 1093/cid/ciu788 (2015).
59. Lam, C. et al. Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerging infectious diseases 20, 626-633, doi: 10. 3201/eid2004. 131478 (2014).
60. Quintana, F. J., Solomon, A., Cohen, I. R., Nussbaum, G. Induction of IgG3 to LPS via Toll-like receptor 4 co-stimulation. PloS one 3, e3509, doi: 10. 1371/journal. pone. 0003509 (2008).