Maternal acellular pertussis vaccination in mice impairs cellular immunity to Bordetella pertussis infection in offspring
Violaine Dubois, Jonathan Chatagnon, Manon Depessemier, Camille Locht
Violaine Dubois, Jonathan Chatagnon, Manon Depessemier, Camille Locht
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Research Article Infectious disease Vaccines

Maternal acellular pertussis vaccination in mice impairs cellular immunity to Bordetella pertussis infection in offspring

Abstract

Given the resurgence of pertussis, several countries have introduced maternal tetanus, diphtheria, and acellular pertussis (aP) vaccination during pregnancy to protect young infants against severe pertussis. Although protective against the disease, the effect of maternal aP vaccination on bacterial colonization of the offspring is unknown. Here, we used a mouse model to demonstrate that maternal aP immunization, either before or during pregnancy, protects pups from lung colonization by Bordetella pertussis. However, maternal aP vaccination resulted in significantly prolonged nasal carriage of B. pertussis by inhibiting the natural recruitment of IL-17–producing resident memory T cells and ensuing neutrophil influx in the nasal tissue, especially of those with proinflammatory and cytotoxic properties. Prolonged nasal carriage after aP vaccination is due to IL-4 signaling, as prolonged nasal carriage is abolished in IL-4Rα–/– mice. The effect of maternal aP vaccination can be transferred transplacentally to the offspring or via breastfeeding and is long-lasting, as it persists into adulthood. Maternal aP vaccination may, thus, augment the B. pertussis reservoir.

Authors

Violaine Dubois, Jonathan Chatagnon, Manon Depessemier, Camille Locht

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Figure 1

Antenatal aP immunization prevents lung colonization in offspring while enhancing nasal carriage.

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Antenatal aP immunization prevents lung colonization in offspring while ...
(A) Female BALB/c mice were immunized twice s.c. with 1/10 human dose of Infanrix (aP). Control mice received PBS. Mice were mated 28 days after priming and boosted on the day of the mating (preconception [pre-con.] boost) or 10 days later (post-con. boost). For post-con. boosting, fertilization occurred at the day of mating — i.e., 10 days before boosting (D–10) — or 6 days after mating — i.e., 4 days before boosting (D–4). For the preconception boosting, fertilization occurred 1 (D+1), 14 (D+14), or 20 (D+20) after boosting. Five to 9 days after birth, the pups were nasally infected with 5 × 103 CFU B1917. At the indicated time points after challenge, lungs and noses were harvested for CFU counting and blood was collected to measure maternally transferred anti–B. pertussis IgG. (B) CFU counts in lungs (upper panel) and noses (lower panel) from pups born to mothers boosted 10 days after fertilization (D–10) compared with control mice (Ctr) at indicated time points after challenge. (C) CFU counts in lungs (upper panel) and noses (lower panel) from pups born to mothers boosted 1 day before fertilization (D+1) compared with control mice (Ctr) at indicated time points after challenge. (D) CFU counts in lungs (left panel) and noses (right panel) of male (M) and female (F) pups born to nonvaccinated mothers 28 days (left panel) or 56 days (right panel) after challenge. (E) CFU counts in the noses of male (left panel) and female (right panel) pups born to nonvaccinated (Ctr) or aP-vaccinated (aP) mothers 56 days after challenge. Results shown are geometric means ± SD. n = 3–6 for the Ctr groups and n = 3–5 for the aP groups in (B and C). Mann-Whitney tests were performed to compare Ctr and aP offspring. *P < 0.05; **P < 0.01.