Antigen Discovery for Next-Generation Pertussis Vaccines Using Immunoproteomics and Transposon-Directed Insertion Sequencing

Kelsey A. Gregg; Yihui Wang; Jason Warfel; Elizabeth Schoenfeld; Ewa Jankowska; John F. Cipollo; Matthew Mayho; Christine Boinett; Deepika Prasad; Timothy J. Brickman; Sandra K. Armstrong; Julian Parkhill; Ricardo Da Silva Antunes; Alessandro Sette; James F. Papin; Roman Wolf; Tod J. Merkel

doi:10.1093/infdis/jiac502

Antigen Discovery for Next-Generation Pertussis Vaccines Using Immunoproteomics and Transposon-Directed Insertion Sequencing

Kelsey A. Gregg, Yihui Wang, Jason Warfel, Elizabeth Schoenfeld, Ewa Jankowska, John F. Cipollo, Matthew Mayho, Christine Boinett, Deepika Prasad, Timothy J. Brickman, Sandra K. Armstrong, Julian Parkhill, Ricardo Da Silva Antunes, Alessandro Sette, James F. Papin, Roman Wolf, Tod J. Merkel

Microbiology

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

Background. Despite high vaccination rates, the United States has experienced a resurgence in reported cases of pertussis after switching to the acellular pertussis vaccine, indicating a need for improved vaccines that enhance infection control. Methods. Bordetella pertussis antigens recognized by convalescent-baboon serum and nasopharyngeal wash were identified by immunoproteomics and their subcellular localization predicted. Genes essential or important for persistence in the baboon airway were identified by transposon-directed insertion-site sequencing (TraDIS) analysis. Results. In total, 314 B. pertussis antigens were identified by convalescent baboon serum and 748 by nasopharyngeal wash. Thirteen antigens were identified as immunogenic in baboons, essential for persistence in the airway by TraDIS, and membrane-localized: BP0840 (OmpP), Pal, OmpA2, BP1485, BamA, Pcp, MlaA, YfgL, BP2197, BP1569, MlaD, ComL, and BP0183. Conclusions. The B. pertussis antigens identified as immunogenic, essential for persistence in the airway, and membrane-localized warrant further investigation for inclusion in vaccines designed to reduce or prevent carriage of bacteria in the airway of vaccinated individuals.

Original language	English (US)
Pages (from-to)	583-591
Number of pages	9
Journal	Journal of Infectious Diseases
Volume	227
Issue number	4
DOIs	https://doi.org/10.1093/infdis/jiac502
State	Published - Feb 15 2023

Bibliographical note

Funding Information:
We acknowledge the expert support provided by the Food and Drug Administration, Center for Biologics Evaluation and Research vivarium staff, and the Sanger Institute core sequencing and informatics teams. This work was supported by the United States Food and Drug Administration and the National Institutes of Health (interagency agreement 032521, and grant numbers U01 AI141995 and 75N93019C00066). Sequencing and analysis was supported by the Wellcome Trust (grant number 098051).

Publisher Copyright:
© 2023 Authors. All rights reserved.

Keywords

Bordetella pertussis
TraDIS
antigen
baboon
immunization
immunoproteomics
vaccine
whooping cough

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1093/infdis/jiac502

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Gregg, K. A., Wang, Y., Warfel, J., Schoenfeld, E., Jankowska, E., Cipollo, J. F., Mayho, M., Boinett, C., Prasad, D., Brickman, T. J., Armstrong, S. K., Parkhill, J., Da Silva Antunes, R., Sette, A., Papin, J. F., Wolf, R., & Merkel, T. J. (2023). Antigen Discovery for Next-Generation Pertussis Vaccines Using Immunoproteomics and Transposon-Directed Insertion Sequencing. Journal of Infectious Diseases, 227(4), 583-591. https://doi.org/10.1093/infdis/jiac502

Gregg, KA, Wang, Y, Warfel, J, Schoenfeld, E, Jankowska, E, Cipollo, JF, Mayho, M, Boinett, C, Prasad, D, Brickman, TJ, Armstrong, SK, Parkhill, J, Da Silva Antunes, R, Sette, A, Papin, JF, Wolf, R & Merkel, TJ 2023, 'Antigen Discovery for Next-Generation Pertussis Vaccines Using Immunoproteomics and Transposon-Directed Insertion Sequencing', Journal of Infectious Diseases, vol. 227, no. 4, pp. 583-591. https://doi.org/10.1093/infdis/jiac502

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title = "Antigen Discovery for Next-Generation Pertussis Vaccines Using Immunoproteomics and Transposon-Directed Insertion Sequencing",

abstract = "Background. Despite high vaccination rates, the United States has experienced a resurgence in reported cases of pertussis after switching to the acellular pertussis vaccine, indicating a need for improved vaccines that enhance infection control. Methods. Bordetella pertussis antigens recognized by convalescent-baboon serum and nasopharyngeal wash were identified by immunoproteomics and their subcellular localization predicted. Genes essential or important for persistence in the baboon airway were identified by transposon-directed insertion-site sequencing (TraDIS) analysis. Results. In total, 314 B. pertussis antigens were identified by convalescent baboon serum and 748 by nasopharyngeal wash. Thirteen antigens were identified as immunogenic in baboons, essential for persistence in the airway by TraDIS, and membrane-localized: BP0840 (OmpP), Pal, OmpA2, BP1485, BamA, Pcp, MlaA, YfgL, BP2197, BP1569, MlaD, ComL, and BP0183. Conclusions. The B. pertussis antigens identified as immunogenic, essential for persistence in the airway, and membrane-localized warrant further investigation for inclusion in vaccines designed to reduce or prevent carriage of bacteria in the airway of vaccinated individuals.",

keywords = "Bordetella pertussis, TraDIS, antigen, baboon, immunization, immunoproteomics, vaccine, whooping cough",

author = "Gregg, {Kelsey A.} and Yihui Wang and Jason Warfel and Elizabeth Schoenfeld and Ewa Jankowska and Cipollo, {John F.} and Matthew Mayho and Christine Boinett and Deepika Prasad and Brickman, {Timothy J.} and Armstrong, {Sandra K.} and Julian Parkhill and {Da Silva Antunes}, Ricardo and Alessandro Sette and Papin, {James F.} and Roman Wolf and Merkel, {Tod J.}",

note = "Funding Information: We acknowledge the expert support provided by the Food and Drug Administration, Center for Biologics Evaluation and Research vivarium staff, and the Sanger Institute core sequencing and informatics teams. This work was supported by the United States Food and Drug Administration and the National Institutes of Health (interagency agreement 032521, and grant numbers U01 AI141995 and 75N93019C00066). Sequencing and analysis was supported by the Wellcome Trust (grant number 098051). Publisher Copyright: {\textcopyright} 2023 Authors. All rights reserved.",

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doi = "10.1093/infdis/jiac502",

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T1 - Antigen Discovery for Next-Generation Pertussis Vaccines Using Immunoproteomics and Transposon-Directed Insertion Sequencing

AU - Gregg, Kelsey A.

AU - Wang, Yihui

AU - Warfel, Jason

AU - Schoenfeld, Elizabeth

AU - Jankowska, Ewa

AU - Cipollo, John F.

AU - Mayho, Matthew

AU - Boinett, Christine

AU - Prasad, Deepika

AU - Brickman, Timothy J.

AU - Armstrong, Sandra K.

AU - Parkhill, Julian

AU - Da Silva Antunes, Ricardo

AU - Sette, Alessandro

AU - Papin, James F.

AU - Wolf, Roman

AU - Merkel, Tod J.

N1 - Funding Information: We acknowledge the expert support provided by the Food and Drug Administration, Center for Biologics Evaluation and Research vivarium staff, and the Sanger Institute core sequencing and informatics teams. This work was supported by the United States Food and Drug Administration and the National Institutes of Health (interagency agreement 032521, and grant numbers U01 AI141995 and 75N93019C00066). Sequencing and analysis was supported by the Wellcome Trust (grant number 098051). Publisher Copyright: © 2023 Authors. All rights reserved.

PY - 2023/2/15

Y1 - 2023/2/15

N2 - Background. Despite high vaccination rates, the United States has experienced a resurgence in reported cases of pertussis after switching to the acellular pertussis vaccine, indicating a need for improved vaccines that enhance infection control. Methods. Bordetella pertussis antigens recognized by convalescent-baboon serum and nasopharyngeal wash were identified by immunoproteomics and their subcellular localization predicted. Genes essential or important for persistence in the baboon airway were identified by transposon-directed insertion-site sequencing (TraDIS) analysis. Results. In total, 314 B. pertussis antigens were identified by convalescent baboon serum and 748 by nasopharyngeal wash. Thirteen antigens were identified as immunogenic in baboons, essential for persistence in the airway by TraDIS, and membrane-localized: BP0840 (OmpP), Pal, OmpA2, BP1485, BamA, Pcp, MlaA, YfgL, BP2197, BP1569, MlaD, ComL, and BP0183. Conclusions. The B. pertussis antigens identified as immunogenic, essential for persistence in the airway, and membrane-localized warrant further investigation for inclusion in vaccines designed to reduce or prevent carriage of bacteria in the airway of vaccinated individuals.

AB - Background. Despite high vaccination rates, the United States has experienced a resurgence in reported cases of pertussis after switching to the acellular pertussis vaccine, indicating a need for improved vaccines that enhance infection control. Methods. Bordetella pertussis antigens recognized by convalescent-baboon serum and nasopharyngeal wash were identified by immunoproteomics and their subcellular localization predicted. Genes essential or important for persistence in the baboon airway were identified by transposon-directed insertion-site sequencing (TraDIS) analysis. Results. In total, 314 B. pertussis antigens were identified by convalescent baboon serum and 748 by nasopharyngeal wash. Thirteen antigens were identified as immunogenic in baboons, essential for persistence in the airway by TraDIS, and membrane-localized: BP0840 (OmpP), Pal, OmpA2, BP1485, BamA, Pcp, MlaA, YfgL, BP2197, BP1569, MlaD, ComL, and BP0183. Conclusions. The B. pertussis antigens identified as immunogenic, essential for persistence in the airway, and membrane-localized warrant further investigation for inclusion in vaccines designed to reduce or prevent carriage of bacteria in the airway of vaccinated individuals.

KW - Bordetella pertussis

KW - TraDIS

KW - antigen

KW - baboon

KW - immunization

KW - immunoproteomics

KW - vaccine

KW - whooping cough

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SN - 0022-1899

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JO - Journal of Infectious Diseases

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Antigen Discovery for Next-Generation Pertussis Vaccines Using Immunoproteomics and Transposon-Directed Insertion Sequencing

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

UN SDGs

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