Antiviral responses induced by Tdap-IPV vaccination are associated with persistent humoral immunity to Bordetella pertussis

Joshua Gillard, Madeleine Suffiotti, Peter Brazda, Prashanna B. Venkatasubramanian, Pauline Versteegen, Marien I. Jonge, Dominic Kelly, Sagida Bibi, Marta Valente Pinto, Elles Simonetti, Mihaela Babiceanu, Andrew Kettring, Cristina Teodosio, Ronald Groot, Guy Berbers, Hendrik G. Stunnenberg, Brian Schanen, Craig Fenwick, Martijn A. Huynen and Dimitri A. Diavatopoulos ()
Additional contact information
Joshua Gillard: Radboud University Medical Center
Madeleine Suffiotti: University of Lausanne
Peter Brazda: Princess Máxima Center for Pediatric Oncology
Prashanna B. Venkatasubramanian: Radboud University Medical Center
Pauline Versteegen: National Institute for Public Health and the Environment
Marien I. Jonge: Radboud University Medical Center
Dominic Kelly: University of Oxford
Sagida Bibi: University of Oxford
Marta Valente Pinto: University of Oxford
Elles Simonetti: Radboud University Medical Center
Mihaela Babiceanu: Sanofi Pasteur VaxDesign
Andrew Kettring: Sanofi Pasteur VaxDesign
Cristina Teodosio: Immunohematology & Blood Transfusion
Ronald Groot: Radboud University Medical Center
Guy Berbers: National Institute for Public Health and the Environment
Hendrik G. Stunnenberg: Princess Máxima Center for Pediatric Oncology
Brian Schanen: Sanofi Pasteur VaxDesign
Craig Fenwick: University of Lausanne
Martijn A. Huynen: Radboud University Medical Center
Dimitri A. Diavatopoulos: Radboud University Medical Center

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Many countries continue to experience pertussis epidemics despite widespread vaccination. Waning protection after booster vaccination has highlighted the need for a better understanding of the immunological factors that promote durable protection. Here we apply systems vaccinology to investigate antibody responses in adolescents in the Netherlands (N = 14; NL) and the United Kingdom (N = 12; UK) receiving a tetanus-diphtheria-acellular pertussis-inactivated poliovirus (Tdap-IPV) vaccine. We report that early antiviral and interferon gene expression signatures in blood correlate to persistence of pertussis-specific antibody responses. Single-cell analyses of the innate response identified monocytes and myeloid dendritic cells (MoDC) as principal responders that upregulate antiviral gene expression and type-I interferon cytokine production. With public data, we show that Tdap vaccination stimulates significantly lower antiviral/type-I interferon responses than Tdap-IPV, suggesting that IPV may promote antiviral gene expression. Subsequent in vitro stimulation experiments demonstrate TLR-dependent, IPV-specific activation of the pro-inflammatory p38 MAP kinase pathway in MoDCs. Together, our data provide insights into the molecular host response to pertussis booster vaccination and demonstrate that IPV enhances innate immune activity associated with persistent, pertussis-specific antibody responses.

Date: 2024
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DOI: 10.1038/s41467-024-46560-w

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