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Research Article

Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1

Adel Benlahrech, Julian Harris, Andrea Meiser, Timos Papagatsias, Julia Hornig, Peter Hayes, Andre Lieber, Takis Athanasopoulos, Veronique Bachy, Eszter Csomor, Rod Daniels, Kerry Fisher, Frances Gotch, Len Seymour, Karen Logan, Romina Barbagallo, Linda Klavinskis, George Dickson, and Steven Patterson
PNAS first published November 16, 2009; https://doi.org/10.1073/pnas.0907898106
Adel Benlahrech
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Julian Harris
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Andrea Meiser
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Timos Papagatsias
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Julia Hornig
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Peter Hayes
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Andre Lieber
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Takis Athanasopoulos
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Veronique Bachy
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Eszter Csomor
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Rod Daniels
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Kerry Fisher
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Frances Gotch
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Len Seymour
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Karen Logan
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Romina Barbagallo
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Linda Klavinskis
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George Dickson
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Steven Patterson
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  • For correspondence: s.patterson@imperial.ac.uk
  1. Edited by Robert C. Gallo, University of Maryland, Baltimore, MD, and approved September 30, 2009 (received for review July 16, 2009)

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Abstract

In the recently halted HIV type 1 (HIV-1) vaccine STEP trial, individuals that were seropositive for adenovirus serotype 5 (Ad5) showed increased rates of HIV-1 infection on vaccination with an Ad5 vaccine. We propose that this was due to activation and expansion of Ad5-specific mucosal-homing memory CD4 T cells. To test this hypothesis, Ad5 and Ad11 antibody titers were measured in 20 healthy volunteers. Dendritic cells (DCs) from these individuals were pulsed with replication defective Ad5 or Ad11 and co-cultured with autologous lymphocytes. Cytokine profiles, proliferative capacity, mucosal migration potential, and susceptibility to HIV infection of the adenovirus-stimulated memory CD4 T cells were measured. Stimulation of T cells from healthy Ad5-seropositive but Ad11-seronegative individuals with Ad5, or serologically distinct Ad11 vectors induced preferential expansion of adenovirus memory CD4 T cells expressing α4β7 integrins and CCR9, indicating a mucosal-homing phenotype. CD4 T-cell proliferation and IFN-γ production in response to Ad stimulation correlated with Ad5 antibody titers. However, Ad5 serostatus did not correlate with total cytokine production upon challenge with Ad5 or Ad11. Expanded Ad5 and Ad11 memory CD4 T cells showed an increase in CCR5 expression and higher susceptibility to infection by R5 tropic HIV-1. This suggests that adenoviral-based vaccination against HIV-1 in individuals with preexisting immunity against Ad5 results in preferential expansion of HIV-susceptible activated CD4 T cells that home to mucosal tissues, increases the number of virus targets, and leads to a higher susceptibility to HIV acquisition.

  • STEP trial
  • vaccine
  • alpha 4 beta 7

Footnotes

  • 1To whom correspondence should be addressed. E-mail: s.patterson{at}imperial.ac.uk
  • Author contributions: A.B., T.A., V.B., E.C., R.D., K.F., F.G., L.S., K.L., R.B., L.K., G.D., and S.P. designed research; A.B., J. Harris, A.M., T.P., J. Hornig, P.H., and G.D. performed research; A.L. contributed new reagents/analytic tools; A.B. and S.P. analyzed data; and A.B. and S.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

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Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1
Adel Benlahrech, Julian Harris, Andrea Meiser, Timos Papagatsias, Julia Hornig, Peter Hayes, Andre Lieber, Takis Athanasopoulos, Veronique Bachy, Eszter Csomor, Rod Daniels, Kerry Fisher, Frances Gotch, Len Seymour, Karen Logan, Romina Barbagallo, Linda Klavinskis, George Dickson, Steven Patterson
Proceedings of the National Academy of Sciences Nov 2009, pnas.0907898106; DOI: 10.1073/pnas.0907898106

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Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1
Adel Benlahrech, Julian Harris, Andrea Meiser, Timos Papagatsias, Julia Hornig, Peter Hayes, Andre Lieber, Takis Athanasopoulos, Veronique Bachy, Eszter Csomor, Rod Daniels, Kerry Fisher, Frances Gotch, Len Seymour, Karen Logan, Romina Barbagallo, Linda Klavinskis, George Dickson, Steven Patterson
Proceedings of the National Academy of Sciences Nov 2009, pnas.0907898106; DOI: 10.1073/pnas.0907898106
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