Immunization with whole cell but not acellular pertussis vaccines primes CD4 T_RM cells that sustain protective immunity against nasal colonization with Bordetella pertussis

References

• Tan T, Dalby T, Forsyth K, et al. Pertussis across the globe. Pediatr Infect Dis J. 2015;34:e222–e232. doi: 10.1097/INF.0000000000000795
   PubMed Web of Science ®Google Scholar
• Mills KH, Ross PJ, Allen AC, et al. Do we need a new vaccine to control the re-emergence of pertussis? Trends Microbiol. 2014;22:49–52. doi: 10.1016/j.tim.2013.11.007
   PubMed Web of Science ®Google Scholar
• Safarchi A, Octavia S, Luu LDW, et al. Pertactin negative Bordetella pertussis demonstrates higher fitness under vaccine selection pressure in a mixed infection model. Vaccine. 2015;33:6277–6281. doi: 10.1016/j.vaccine.2015.09.064
   PubMed Web of Science ®Google Scholar
• Dorji D, Mooi F, Yantorno O, et al. Bordetella pertussis virulence factors in the continuing evolution of whooping cough vaccines for improved performance. Med Microbiol Immunol. 2018;207:3–26. doi: 10.1007/s00430-017-0524-z
   PubMed Web of Science ®Google Scholar
• van der Zee A, Schellekens JF, Mooi FR. Laboratory diagnosis of pertussis. Clin Microbiol Rev. 2015;28:1005–1026. doi: 10.1128/CMR.00031-15
   PubMed Web of Science ®Google Scholar
• Winter K, Zipprich J, Harriman K, et al. Risk factors associated with infant deaths from pertussis: a case-control study. Clin Infect Dis. 2015;61:1099–1106. doi: 10.1093/cid/civ472
   PubMed Web of Science ®Google Scholar
• Amirthalingam G, Andrews N, Campbell H, et al. Effectiveness of maternal pertussis vaccination in England: an observational study. Lancet. 2014;384:1521–1528. doi: 10.1016/S0140-6736(14)60686-3
   PubMed Web of Science ®Google Scholar
• Greco D, Salmaso S, Mastrantonio P, et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. Progetto Pertosse working group. N Engl J Med. 1996;334:341–349. doi: 10.1056/NEJM199602083340601
   PubMed Web of Science ®Google Scholar
• Gustafsson L, Hallander HO, Olin P, et al. A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. N Engl J Med. 1996;334:349–356. doi: 10.1056/NEJM199602083340602
   PubMed Web of Science ®Google Scholar
• Cherry JD, Gornbein J, Heininger U, et al. A search for serologic correlates of immunity to Bordetella pertussis cough illnesses. Vaccine. 1998;16:1901–1906. doi: 10.1016/S0264-410X(98)00226-6
   PubMed Web of Science ®Google Scholar
• Storsaeter J, Hallander HO, Gustafsson L, et al. Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis. Vaccine. 1998;16:1907–1916. doi: 10.1016/S0264-410X(98)00227-8
   PubMed Web of Science ®Google Scholar
• Ryan M, Murphy G, Gothefors L, et al. Bordetella pertussis respiratory infection in children is associated with preferential activation of type 1T helper cells. J Infect Dis. 1997;175:1246–1250. doi: 10.1086/593682
   PubMed Web of Science ®Google Scholar
• Ryan M, Murphy G, Ryan E, et al. Distinct T-cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology. 1998;93:1–10. doi: 10.1046/j.1365-2567.1998.00401.x
   PubMed Web of Science ®Google Scholar
• Ausiello CM, Urbani F, la Sala A, et al. Vaccine- and antigen-dependent type 1 and type 2 cytokine induction after primary vaccination of infants with whole-cell or acellular pertussis vaccines. Infect Immun. 1997;65:2168–2174.
   PubMed Web of Science ®Google Scholar
• Ross PJ, Sutton CE, Higgins S, 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 Pathog. 2013;9:e1003264. doi: 10.1371/journal.ppat.1003264
   PubMed Web of Science ®Google Scholar
• Mahon BP, Sheahan BJ, Griffin F, et al. Atypical disease after Bordetella pertussis respiratory infection of mice with targeted disruptions of interferon-gamma receptor or immunoglobulin mu chain genes. J Exp Med. 1997;186:1843–1851. doi: 10.1084/jem.186.11.1843
   PubMed Web of Science ®Google Scholar
• Warfel JM, Zimmerman LI, Merkel TJ. 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;111:787–792. doi: 10.1073/pnas.1314688110
   PubMed Web of Science ®Google Scholar
• Althouse BM, Scarpino SV. Asymptomatic transmission and the resurgence of Bordetella pertussis. BMC Med. 2015;13:146. doi: 10.1186/s12916-015-0382-8
   PubMed Web of Science ®Google Scholar
• Klein NP, Bartlett J, Rowhani-Rahbar A, et al. Waning protection after fifth dose of acellular pertussis vaccine in children. N Engl J Med. 2012;367:1012–1019. doi: 10.1056/NEJMoa1200850
   PubMed Web of Science ®Google Scholar
• Witt MA, Katz PH, Witt DJ. Unexpectedly limited durability of immunity following acellular pertussis vaccination in preadolescents in a North American outbreak. Clin Infect Dis. 2012;54:1730–1735. doi: 10.1093/cid/cis287
   PubMed Web of Science ®Google Scholar
• McGirr A, Fisman DN. Duration of pertussis immunity after DTaP immunization: a meta-analysis. Pediatrics. 2015;135:331–343. doi: 10.1542/peds.2014-1729
   PubMed Web of Science ®Google Scholar
• Klein NP, Bartlett J, Fireman B, et al. Comparative effectiveness of acellular versus whole-cell pertussis vaccines in teenagers. Pediatrics. 2013;131:e1716–e1722. doi: 10.1542/peds.2012-3836
   PubMed Web of Science ®Google Scholar
• Witt MA, Arias L, Katz PH, et al. Reduced risk of pertussis among persons ever vaccinated with whole cell pertussis vaccine compared to recipients of acellular pertussis vaccines in a large US cohort. Clin Infect Dis. 2013;56:1248–1254. doi: 10.1093/cid/cit046
   PubMed Web of Science ®Google Scholar
• van der Lee S, Hendrikx LH, Sanders EAM, et al. Whole-cell or acellular pertussis primary immunizations in infancy determines adolescent cellular immune profiles. Front Immunol. 2018;9:51. doi: 10.3389/fimmu.2018.00051
   PubMed Web of Science ®Google Scholar
• da Silva Antunes R, Babor M, Carpenter C, et al. Th1/Th17 polarization persists following whole-cell pertussis vaccination despite repeated acellular boosters. J Clin Invest. 2018;128:3853–3865. doi: 10.1172/JCI121309
   PubMed Web of Science ®Google Scholar
• Pizzolla A, Nguyen THO, Smith JM, et al. Resident memory CD8(+) T cells in the upper respiratory tract prevent pulmonary influenza virus infection. Sci Immunol. 2017;2 (12). pii: eaam6970. doi: 10.1126/sciimmunol.aam6970
   PubMed Web of Science ®Google Scholar
• Mueller SN, Mackay LK. Tissue-resident memory T cells: local specialists in immune defence. Nat Rev Immunol. 2016;16:79–89. doi: 10.1038/nri.2015.3
   PubMed Web of Science ®Google Scholar
• Wilk MM, Mills KHG. CD4 TRM cells following infection and immunization: implications for more effective vaccine design. Front Immunol. 2018;9:1860. doi: 10.3389/fimmu.2018.01860
   PubMed Web of Science ®Google Scholar
• Wilk MM, Misiak A, McManus RM, et al. Lung CD4 tissue-resident memory T cells mediate adaptive immunity induced by previous infection of mice with Bordetella pertussis. J Immunol. 2017;199:233–243. doi: 10.4049/jimmunol.1602051
   PubMed Web of Science ®Google Scholar
• Wirsing von Konig CH, Postels-Multani S, Bock HL, et al. Pertussis in adults: frequency of transmission after household exposure. Lancet. 1995;346:1326–1329. doi: 10.1016/S0140-6736(95)92343-8
   PubMed Web of Science ®Google Scholar
• Cassone A, Ausiello CM, Urbani F, et al. Cell-mediated and antibody responses to Bordetella pertussis antigens in children vaccinated with acellular or whole-cell pertussis vaccines. The Progetto Pertosse-CMI working group. Arch Pediatr Adolesc Med. 1997;151:283–289. doi: 10.1001/archpedi.1997.02170400069013
   PubMed Web of Science ®Google Scholar
• Marcellini V, Piano Mortari E, Fedele G, et al. Protection against pertussis in humans correlates to elevated serum antibodies and memory B cells. Front Immunol. 2017;8:1158. doi: 10.3389/fimmu.2017.01158
   PubMed Web of Science ®Google Scholar
• Taranger J, Trollfors B, Lagergård T, et al. Correlation between pertussis toxin IgG antibodies in postvaccination sera and subsequent protection against pertussis. J Infect Dis. 2000;181:1010–1013. doi: 10.1086/315318
   PubMed Web of Science ®Google Scholar
• Kapil P, Papin JF, Wolf RF, et al. Maternal vaccination with a monocomponent pertussis toxoid vaccine is sufficient to protect infants in a baboon model of whooping cough. J Infect Dis. 2018;217:1231–1236. doi: 10.1093/infdis/jiy022
   PubMed Web of Science ®Google Scholar
• Mills KH, Barnard A, Watkins J, et al. Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect Immun. 1993;61:399–410.
   PubMed Web of Science ®Google Scholar
• Redhead K, Watkins J, Barnard A, et al. Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity. Infect Immun. 1993;61:3190–3198.
   PubMed Web of Science ®Google Scholar
• Byrne P, McGuirk P, Todryk S, et al. Depletion of NK cells results in disseminating lethal infection with Bordetella pertussis associated with a reduction of antigen-specific Th1 and enhancement of Th2, but not Tr1 cells. Eur J Immunol. 2004;34:2579–2588. doi: 10.1002/eji.200425092
   PubMed Web of Science ®Google Scholar
• Klein NP, Bartlett J, Fireman B, et al. Waning Tdap effectiveness in adolescents. Pediatrics. 2016;137:e20153326. doi: 10.1542/peds.2015-3326
   PubMed Web of Science ®Google Scholar
• Mahon BP, Brady MT, Mills KH. Protection against Bordetella pertussis in mice in the absence of detectable circulating antibody: implications for long-term immunity in children. J Infect Dis. 2000;181:2087–2091. doi: 10.1086/315527
   PubMed Web of Science ®Google Scholar
• Perdomo C, Zedler U, Kühl AA, et al. Mucosal BCG vaccination induces protective lung-resident memory T cell populations against tuberculosis. mBio. 2016;7 (6). pii: e01686-16. doi: 10.1128/mBio.01686-16
   PubMed Web of Science ®Google Scholar
• Allen AC, Wilk MM, Misiak A, et al. Sustained protective immunity against Bordetella pertussis nasal colonization by intranasal immunization with a vaccine-adjuvant combination that induces IL-17-secreting TRM cells. Mucosal Immunol. 2018;11:1763–1776. doi: 10.1038/s41385-018-0080-x
   PubMed Web of Science ®Google Scholar
• Barnard A, Mahon BP, Watkins J, et al. Th1/Th2 cell dichotomy in acquired immunity to Bordetella pertussis: variables in the in vivo priming and in vitro cytokine detection techniques affect the classification of T-cell subsets as Th1, Th2 or Th0. Immunology. 1996;87:372–380. doi: 10.1046/j.1365-2567.1996.497560.x
   PubMed Web of Science ®Google Scholar
• McGuirk P, Mahon BP, Griffin F, et al. Compartmentalization of T cell responses following respiratory infection with Bordetella pertussis: hyporesponsiveness of lung T cells is associated with modulated expression of the co-stimulatory molecule CD28. Eur J Immunol. 1998;28:153–163. doi: 10.1002/(SICI)1521-4141(199801)28:01<153::AID-IMMU153>3.0.CO;2-#
   PubMed Web of Science ®Google Scholar
• Anderson KG, Mayer-Barber K, Sung H, et al. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat Protoc. 2014;9:209–222. doi: 10.1038/nprot.2014.005
   PubMed Web of Science ®Google Scholar
• Mills KH, Ryan M, Ryan E, et al. 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;66:594–602.
   PubMed Web of Science ®Google Scholar