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Pathogenesis and Immunity

Cooperativity of HIV-Specific Cytolytic CD4 T Cells and CD8 T Cells in Control of HIV Viremia

Susan Johnson, Michael Eller, Jeffrey E. Teigler, Sebastien M. Maloveste, Bruce T. Schultz, Damien Z. Soghoian, Richard Lu, Alexander F. Oster, Agnès-Laurence Chenine, Galit Alter, Ulf Dittmer, Mary Marovich, Merlin L. Robb, Nelson L. Michael, Diane Bolton, Hendrik Streeck
G. Silvestri, Editor
Susan Johnson
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Michael Eller
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Jeffrey E. Teigler
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Sebastien M. Maloveste
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Bruce T. Schultz
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Damien Z. Soghoian
cRagon Institute of MGH, MIT, and Harvard, Boston, Massachusetts, USA
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Richard Lu
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Alexander F. Oster
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Agnès-Laurence Chenine
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Galit Alter
cRagon Institute of MGH, MIT, and Harvard, Boston, Massachusetts, USA
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Ulf Dittmer
dInstitute of Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany
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Mary Marovich
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Merlin L. Robb
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Nelson L. Michael
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Diane Bolton
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
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Hendrik Streeck
aU.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
bHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, USA
eInstitute for Medical Biology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany
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G. Silvestri
Roles: Editor
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DOI: 10.1128/JVI.00438-15
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ABSTRACT

CD4+ T cells play a pivotal role in the control of chronic viral infections. Recently, nontraditional CD4+ T cell functions beyond helper effects have been described, and a role for cytolytic CD4+ T cells in the control of HIV infection has been suggested. We define here the transcriptional, phenotypic, and functional profiles of HIV-specific cytolytic CD4+ T cells. Fluidigm BioMark and multiparameter flow cytometric analysis of HIV-specific cytolytic CD4+ T cells revealed a distinct transcriptional signature compared to Th1 CD4+ cells but shared similar features with HIV-specific cytolytic CD8+ T cells. Furthermore, HIV-specific cytolytic CD4+ T cells showed comparable killing activity relative to HIV-specific CD8+ T cells and worked cooperatively in the elimination of virally infected cells. Interestingly, we found that cytolytic CD4+ T cells emerge early during acute HIV infection and tightly follow acute viral load trajectory. This emergence was associated to the early viral set point, suggesting an involvement in early control, in spite of CD4 T cell susceptibility to HIV infection. Our data suggest cytolytic CD4+ T cells as an independent subset distinct from Th1 cells that show combined activity with CD8+ T cells in the long-term control of HIV infection.

IMPORTANCE The ability of the immune system to control chronic HIV infection is of critical interest to both vaccine design and therapeutic approaches. Much research has focused on the effect of the ability of CD8+ T cells to control the virus, while CD4+ T cells have been overlooked as effectors in HIV control due to the fact that they are preferentially infected. We show here that a subset of HIV-specific CD4+ T cells cooperate in the cytolytic control of HIV replication. Moreover, these cells represent a distinct subset of CD4+ T cells showing significant transcriptional and phenotypic differences compared to HIV-specific Th1 cells but with similarities to CD8+ T cells. These findings are important for our understanding of HIV immunopathology.

FOOTNOTES

    • Received 17 February 2015.
    • Accepted 27 April 2015.
    • Accepted manuscript posted online 13 May 2015.
  • Address correspondence to Hendrik Streeck, hendrik.streeck{at}uk-essen.de.
  • ↵* Present address: Sebastien M. Maloveste, Amplimmune, Inc., Gaithersburg, Maryland, USA; Mary Marovich, NIAID, Division of AIDS, Bethesda, Maryland, USA.

  • Citation Johnson S, Eller M, Teigler JE, Maloveste SM, Schultz BT, Soghoian DZ, Lu R, Oster AF, Chenine A-L, Alter G, Dittmer U, Marovich M, Robb ML, Michael NL, Bolton D, Streeck H. 2015. Cooperativity of HIV-specific cytolytic CD4 T cells and CD8 T cells in control of HIV viremia. J Virol 89:7494–7505. doi:10.1128/JVI.00438-15.

  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/JVI.00438-15.

  • Copyright © 2015, American Society for Microbiology. All Rights Reserved.
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Cooperativity of HIV-Specific Cytolytic CD4 T Cells and CD8 T Cells in Control of HIV Viremia
Susan Johnson, Michael Eller, Jeffrey E. Teigler, Sebastien M. Maloveste, Bruce T. Schultz, Damien Z. Soghoian, Richard Lu, Alexander F. Oster, Agnès-Laurence Chenine, Galit Alter, Ulf Dittmer, Mary Marovich, Merlin L. Robb, Nelson L. Michael, Diane Bolton, Hendrik Streeck
Journal of Virology Jul 2015, 89 (15) 7494-7505; DOI: 10.1128/JVI.00438-15

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Cooperativity of HIV-Specific Cytolytic CD4 T Cells and CD8 T Cells in Control of HIV Viremia
Susan Johnson, Michael Eller, Jeffrey E. Teigler, Sebastien M. Maloveste, Bruce T. Schultz, Damien Z. Soghoian, Richard Lu, Alexander F. Oster, Agnès-Laurence Chenine, Galit Alter, Ulf Dittmer, Mary Marovich, Merlin L. Robb, Nelson L. Michael, Diane Bolton, Hendrik Streeck
Journal of Virology Jul 2015, 89 (15) 7494-7505; DOI: 10.1128/JVI.00438-15
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