Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T Cells following human-,simian-,and chimpanzee-derived recombinant adenoviral vector immunization

Kylie M. Quinn, Andreia Da Costa, Ayako Yamamoto, Dana Berry, Ross W B Lindsay, Patricia A. Darrah, Lingshu Wang, Cheng Cheng, Wing Pui Kong, Jason G D Gall, Alfredo Nicosia, Antonella Folgori, Stefano Colloca, Riccardo Cortese, Emma Gostick, David A. Price, Carmen E. Gomez, Mariano Esteban, Linda S. Wyatt, Bernard MossCecilia Morgan, Mario Roederer, Robert T. Bailer, Gary J. Nabel, Richard A. Koup, Robert A. Seder

Research output: Contribution to journalArticle

Abstract

Recombinant adenoviral vectors (rAds) are the most potent recombinant vaccines for eliciting CD8+; T cell-mediated immunity in humans; however, prior exposure from natural adenoviral infection can decrease such responses. In this study we show low seroreactivity in humans against simian- (sAd11, sAd16) or chimpanzee-derived (chAd3, chAd63) compared with human-derived (rAd5, rAd28, rAd35) vectors across multiple geographic regions. We then compared the magnitude, quality, phenotype, and protective capacity of CD8 +; T cell responses in mice vaccinated with rAds encoding SIV Gag. Using a dose range (1 3 107-109 particle units), we defined a hierarchy among rAd vectors based on the magnitude and protective capacity of CD8+; T cell responses, from most to least, as: rAd5 and chAd3, rAd28 and sAd11, chAd63, sAd16, and rAd35. Selection of rAd vector or dose could modulate the proportion and/or frequency of IFN-γ+;TNF- α+;IL-2+; and KLRG1+;CD1272CD8 +; T cells, but strikingly ∼30-80% of memory CD8+; T cells coexpressed CD127 and KLRG1. To further optimize CD8+; T cell responses, we assessed rAds as part of prime-boost regimens. Mice primed with rAds and boosted with NYVAC generated Gag-specific responses that approached ∼60% of total CD8+; T cells at peak. Alternatively, priming with DNA or rAd28 and boosting with rAd5 or chAd3 induced robust and equivalent CD8+; T cell responses compared with prime or boost alone. Collectively, these data provide the immunologic basis for using specific rAd vectors alone or as part of prime-boost regimens to induce CD8+; T cells for rapid effector function or robust long-term memory, respectively.

Original languageEnglish (US)
Pages (from-to)2720-2735
Number of pages16
JournalJournal of Immunology
Volume190
Issue number6
DOIs
StatePublished - Mar 15 2013
Externally publishedYes

Fingerprint

Simian Immunodeficiency Virus
Pan troglodytes
Immunization
T-Lymphocytes
Phenotype
Synthetic Vaccines
Long-Term Memory
Cellular Immunity
Interleukin-2

ASJC Scopus subject areas

  • Immunology

Cite this

Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T Cells following human-,simian-,and chimpanzee-derived recombinant adenoviral vector immunization. / Quinn, Kylie M.; Da Costa, Andreia; Yamamoto, Ayako; Berry, Dana; Lindsay, Ross W B; Darrah, Patricia A.; Wang, Lingshu; Cheng, Cheng; Kong, Wing Pui; Gall, Jason G D; Nicosia, Alfredo; Folgori, Antonella; Colloca, Stefano; Cortese, Riccardo; Gostick, Emma; Price, David A.; Gomez, Carmen E.; Esteban, Mariano; Wyatt, Linda S.; Moss, Bernard; Morgan, Cecilia; Roederer, Mario; Bailer, Robert T.; Nabel, Gary J.; Koup, Richard A.; Seder, Robert A.

In: Journal of Immunology, Vol. 190, No. 6, 15.03.2013, p. 2720-2735.

Research output: Contribution to journalArticle

Quinn, KM, Da Costa, A, Yamamoto, A, Berry, D, Lindsay, RWB, Darrah, PA, Wang, L, Cheng, C, Kong, WP, Gall, JGD, Nicosia, A, Folgori, A, Colloca, S, Cortese, R, Gostick, E, Price, DA, Gomez, CE, Esteban, M, Wyatt, LS, Moss, B, Morgan, C, Roederer, M, Bailer, RT, Nabel, GJ, Koup, RA & Seder, RA 2013, 'Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T Cells following human-,simian-,and chimpanzee-derived recombinant adenoviral vector immunization', Journal of Immunology, vol. 190, no. 6, pp. 2720-2735. https://doi.org/10.4049/jimmunol.1202861
Quinn, Kylie M. ; Da Costa, Andreia ; Yamamoto, Ayako ; Berry, Dana ; Lindsay, Ross W B ; Darrah, Patricia A. ; Wang, Lingshu ; Cheng, Cheng ; Kong, Wing Pui ; Gall, Jason G D ; Nicosia, Alfredo ; Folgori, Antonella ; Colloca, Stefano ; Cortese, Riccardo ; Gostick, Emma ; Price, David A. ; Gomez, Carmen E. ; Esteban, Mariano ; Wyatt, Linda S. ; Moss, Bernard ; Morgan, Cecilia ; Roederer, Mario ; Bailer, Robert T. ; Nabel, Gary J. ; Koup, Richard A. ; Seder, Robert A. / Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T Cells following human-,simian-,and chimpanzee-derived recombinant adenoviral vector immunization. In: Journal of Immunology. 2013 ; Vol. 190, No. 6. pp. 2720-2735.
@article{4576473dd10e4bd3ad26a021297a09d8,
title = "Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T Cells following human-,simian-,and chimpanzee-derived recombinant adenoviral vector immunization",
abstract = "Recombinant adenoviral vectors (rAds) are the most potent recombinant vaccines for eliciting CD8+; T cell-mediated immunity in humans; however, prior exposure from natural adenoviral infection can decrease such responses. In this study we show low seroreactivity in humans against simian- (sAd11, sAd16) or chimpanzee-derived (chAd3, chAd63) compared with human-derived (rAd5, rAd28, rAd35) vectors across multiple geographic regions. We then compared the magnitude, quality, phenotype, and protective capacity of CD8 +; T cell responses in mice vaccinated with rAds encoding SIV Gag. Using a dose range (1 3 107-109 particle units), we defined a hierarchy among rAd vectors based on the magnitude and protective capacity of CD8+; T cell responses, from most to least, as: rAd5 and chAd3, rAd28 and sAd11, chAd63, sAd16, and rAd35. Selection of rAd vector or dose could modulate the proportion and/or frequency of IFN-γ+;TNF- α+;IL-2+; and KLRG1+;CD1272CD8 +; T cells, but strikingly ∼30-80{\%} of memory CD8+; T cells coexpressed CD127 and KLRG1. To further optimize CD8+; T cell responses, we assessed rAds as part of prime-boost regimens. Mice primed with rAds and boosted with NYVAC generated Gag-specific responses that approached ∼60{\%} of total CD8+; T cells at peak. Alternatively, priming with DNA or rAd28 and boosting with rAd5 or chAd3 induced robust and equivalent CD8+; T cell responses compared with prime or boost alone. Collectively, these data provide the immunologic basis for using specific rAd vectors alone or as part of prime-boost regimens to induce CD8+; T cells for rapid effector function or robust long-term memory, respectively.",
author = "Quinn, {Kylie M.} and {Da Costa}, Andreia and Ayako Yamamoto and Dana Berry and Lindsay, {Ross W B} and Darrah, {Patricia A.} and Lingshu Wang and Cheng Cheng and Kong, {Wing Pui} and Gall, {Jason G D} and Alfredo Nicosia and Antonella Folgori and Stefano Colloca and Riccardo Cortese and Emma Gostick and Price, {David A.} and Gomez, {Carmen E.} and Mariano Esteban and Wyatt, {Linda S.} and Bernard Moss and Cecilia Morgan and Mario Roederer and Bailer, {Robert T.} and Nabel, {Gary J.} and Koup, {Richard A.} and Seder, {Robert A.}",
year = "2013",
month = "3",
day = "15",
doi = "10.4049/jimmunol.1202861",
language = "English (US)",
volume = "190",
pages = "2720--2735",
journal = "Journal of Immunology",
issn = "0022-1767",
publisher = "American Association of Immunologists",
number = "6",

}

TY - JOUR

T1 - Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T Cells following human-,simian-,and chimpanzee-derived recombinant adenoviral vector immunization

AU - Quinn, Kylie M.

AU - Da Costa, Andreia

AU - Yamamoto, Ayako

AU - Berry, Dana

AU - Lindsay, Ross W B

AU - Darrah, Patricia A.

AU - Wang, Lingshu

AU - Cheng, Cheng

AU - Kong, Wing Pui

AU - Gall, Jason G D

AU - Nicosia, Alfredo

AU - Folgori, Antonella

AU - Colloca, Stefano

AU - Cortese, Riccardo

AU - Gostick, Emma

AU - Price, David A.

AU - Gomez, Carmen E.

AU - Esteban, Mariano

AU - Wyatt, Linda S.

AU - Moss, Bernard

AU - Morgan, Cecilia

AU - Roederer, Mario

AU - Bailer, Robert T.

AU - Nabel, Gary J.

AU - Koup, Richard A.

AU - Seder, Robert A.

PY - 2013/3/15

Y1 - 2013/3/15

N2 - Recombinant adenoviral vectors (rAds) are the most potent recombinant vaccines for eliciting CD8+; T cell-mediated immunity in humans; however, prior exposure from natural adenoviral infection can decrease such responses. In this study we show low seroreactivity in humans against simian- (sAd11, sAd16) or chimpanzee-derived (chAd3, chAd63) compared with human-derived (rAd5, rAd28, rAd35) vectors across multiple geographic regions. We then compared the magnitude, quality, phenotype, and protective capacity of CD8 +; T cell responses in mice vaccinated with rAds encoding SIV Gag. Using a dose range (1 3 107-109 particle units), we defined a hierarchy among rAd vectors based on the magnitude and protective capacity of CD8+; T cell responses, from most to least, as: rAd5 and chAd3, rAd28 and sAd11, chAd63, sAd16, and rAd35. Selection of rAd vector or dose could modulate the proportion and/or frequency of IFN-γ+;TNF- α+;IL-2+; and KLRG1+;CD1272CD8 +; T cells, but strikingly ∼30-80% of memory CD8+; T cells coexpressed CD127 and KLRG1. To further optimize CD8+; T cell responses, we assessed rAds as part of prime-boost regimens. Mice primed with rAds and boosted with NYVAC generated Gag-specific responses that approached ∼60% of total CD8+; T cells at peak. Alternatively, priming with DNA or rAd28 and boosting with rAd5 or chAd3 induced robust and equivalent CD8+; T cell responses compared with prime or boost alone. Collectively, these data provide the immunologic basis for using specific rAd vectors alone or as part of prime-boost regimens to induce CD8+; T cells for rapid effector function or robust long-term memory, respectively.

AB - Recombinant adenoviral vectors (rAds) are the most potent recombinant vaccines for eliciting CD8+; T cell-mediated immunity in humans; however, prior exposure from natural adenoviral infection can decrease such responses. In this study we show low seroreactivity in humans against simian- (sAd11, sAd16) or chimpanzee-derived (chAd3, chAd63) compared with human-derived (rAd5, rAd28, rAd35) vectors across multiple geographic regions. We then compared the magnitude, quality, phenotype, and protective capacity of CD8 +; T cell responses in mice vaccinated with rAds encoding SIV Gag. Using a dose range (1 3 107-109 particle units), we defined a hierarchy among rAd vectors based on the magnitude and protective capacity of CD8+; T cell responses, from most to least, as: rAd5 and chAd3, rAd28 and sAd11, chAd63, sAd16, and rAd35. Selection of rAd vector or dose could modulate the proportion and/or frequency of IFN-γ+;TNF- α+;IL-2+; and KLRG1+;CD1272CD8 +; T cells, but strikingly ∼30-80% of memory CD8+; T cells coexpressed CD127 and KLRG1. To further optimize CD8+; T cell responses, we assessed rAds as part of prime-boost regimens. Mice primed with rAds and boosted with NYVAC generated Gag-specific responses that approached ∼60% of total CD8+; T cells at peak. Alternatively, priming with DNA or rAd28 and boosting with rAd5 or chAd3 induced robust and equivalent CD8+; T cell responses compared with prime or boost alone. Collectively, these data provide the immunologic basis for using specific rAd vectors alone or as part of prime-boost regimens to induce CD8+; T cells for rapid effector function or robust long-term memory, respectively.

UR - http://www.scopus.com/inward/record.url?scp=84874860188&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84874860188&partnerID=8YFLogxK

U2 - 10.4049/jimmunol.1202861

DO - 10.4049/jimmunol.1202861

M3 - Article

C2 - 23390298

AN - SCOPUS:84874860188

VL - 190

SP - 2720

EP - 2735

JO - Journal of Immunology

JF - Journal of Immunology

SN - 0022-1767

IS - 6

ER -