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HIV-1 N-Glycan Composition Governs a Balance between Dendritic Cell-Mediated Viral Transmission and Antigen Presentation

Thijs van Montfort, Dirk Eggink, Maikel Boot, Michael Tuen, Catarina E. Hioe, Ben Berkhout and Rogier W. Sanders
J Immunol November 1, 2011, 187 (9) 4676-4685; DOI: https://doi.org/10.4049/jimmunol.1101876
Thijs van Montfort
*Laboratory of Experimental Virology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam, Academic Medical Center of the University of Amsterdam, 1105 AZ Amsterdam, The Netherlands;
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Dirk Eggink
*Laboratory of Experimental Virology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam, Academic Medical Center of the University of Amsterdam, 1105 AZ Amsterdam, The Netherlands;
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Maikel Boot
*Laboratory of Experimental Virology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam, Academic Medical Center of the University of Amsterdam, 1105 AZ Amsterdam, The Netherlands;
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Michael Tuen
†Department of Pathology, New York University School of Medicine, New York, NY 10010; and
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Catarina E. Hioe
†Department of Pathology, New York University School of Medicine, New York, NY 10010; and
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Ben Berkhout
*Laboratory of Experimental Virology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam, Academic Medical Center of the University of Amsterdam, 1105 AZ Amsterdam, The Netherlands;
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Rogier W. Sanders
*Laboratory of Experimental Virology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam, Academic Medical Center of the University of Amsterdam, 1105 AZ Amsterdam, The Netherlands;
‡Department of Microbiology and Immunology, Weill Medical College, Cornell University, New York, NY 10065
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Abstract

The natural function of dendritic cells (DCs) is to capture and degrade pathogens for Ag presentation. However, HIV-1 can evade viral degradation by DCs and hijack DCs for migration to susceptible CD4+ T lymphocytes. It is unknown what factors decide whether a virus is degraded or transmitted to T cells. The interaction of DCs with HIV-1 involves C-type lectin receptors, such as DC-specific ICAM-3–grabbing nonintegrin, which bind to the envelope glycoprotein complex (Env), which is decorated heavily with N-linked glycans. We hypothesized that the saccharide composition of the Env N-glycans is involved in avoiding viral degradation and Ag presentation, as well as preserving infectious virus for the transmission to target cells. Therefore, we studied the fate of normally glycosylated virus versus oligomannose-enriched virus in DCs. Changing the heterogeneous N-linked glycan composition of Env to uniform oligomannose N-glycans increased the affinity of HIV-1 for DC-specific ICAM-3–grabbing nonintegrin and enhanced the capture of HIV-1 by immature DCs; however, it decreased the subsequent transmission to target cells. Oligomannose-enriched HIV-1 was directed more efficiently into the endocytic pathway, resulting in enhanced viral degradation and reduced virus transfer to target cells. Furthermore, Env containing exclusively oligomannose N-glycans was presented to Env-specific CD4+ T cells more efficiently. Taken together, our results showed that the HIV-1 N-glycan composition plays a crucial role in the balance between DC-mediated Ag degradation and presentation and DC-mediated virus transmission to target cells. This finding may have implications for the early events in HIV-1 transmission and the induction of antiviral immune responses.

Footnotes

  • This work was supported by AIDS Fund (Amsterdam) Grants 2005021 (to B.B.) and 2008013 (to R.W.S.). R.W.S. is a recipient of Veni and Vidi fellowships from The Netherlands Organization for Scientific Research and a Mathilde Krim research fellowship from the American Foundation for AIDS Research.

  • Abbreviations used in this article:

    CLR
    C-type lectin receptor
    DC
    dendritic cell
    DCIR
    dendritic cell immunoreceptor
    DC-SIGN
    dendritic cell-specific ICAM-3–grabbing nonintegrin
    EGFP
    enhanced GFP
    Env
    envelope glycoprotein complex
    ER
    endoplasmic reticulum
    GnTI
    GlcNAc transferase I enzyme
    iDC
    immature dendritic cell
    PEI
    polyethylenimine
    Raji–DC-SIGN cell
    Raji cell expressing dendritic cell-specific ICAM-3–grabbing nonintegrin
    TSM
    tris saline magnesium buffer
    wt
    wild-type.

  • Received June 24, 2011.
  • Accepted August 26, 2011.
  • Copyright © 2011 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 187 (9)
The Journal of Immunology
Vol. 187, Issue 9
1 Nov 2011
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HIV-1 N-Glycan Composition Governs a Balance between Dendritic Cell-Mediated Viral Transmission and Antigen Presentation
Thijs van Montfort, Dirk Eggink, Maikel Boot, Michael Tuen, Catarina E. Hioe, Ben Berkhout, Rogier W. Sanders
The Journal of Immunology November 1, 2011, 187 (9) 4676-4685; DOI: 10.4049/jimmunol.1101876

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HIV-1 N-Glycan Composition Governs a Balance between Dendritic Cell-Mediated Viral Transmission and Antigen Presentation
Thijs van Montfort, Dirk Eggink, Maikel Boot, Michael Tuen, Catarina E. Hioe, Ben Berkhout, Rogier W. Sanders
The Journal of Immunology November 1, 2011, 187 (9) 4676-4685; DOI: 10.4049/jimmunol.1101876
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