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Cited by 33HIV Research and TreatmentCell Adhesion Molecules ResearchVirus-based gene therapy research

LFA-1 Engagement Triggers T Cell Polarization at the HIV-1 Virological Synapse

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Starling, Shimona, Jolly, Clare·2016·Journal of Virology
DOI 10.1128/jvi.01152-16PMC PMC5068534
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Abstract

HIV-1 efficiently disseminates by cell-cell spread at intercellular contacts called virological synapses (VS), where the virus preferentially assembles and buds. Cell-cell contact triggers active polarization of organelles and viral proteins within infected cells to the contact site to support efficient VS formation and HIV-1 spread; critically, however, which cell surface protein triggers contact-induced polarization at the VS remains unclear. Additionally, the mechanism by which the HIV-1 envelope glycoprotein (Env) is recruited to the VS remains ill defined. Here, we use a reductionist bead-coupled antibody assay as a model of the VS and show that cross-linking the integrin LFA-1 alone is sufficient to induce active T cell polarization and recruitment of the microtubule organizing center (MTOC) in HIV-1-infected cells. Mutant cell lines coupled with inhibitors demonstrated that LFA-1-induced polarization was dependent on the T cell kinase ZAP70. Notably, immunofluorescent staining of viral proteins revealed an accumulation of surface Env at sites of LFA-1 engagement, with intracellular Env localized to a Golgi compartment proximal to the polarized MTOC. Furthermore, blocking LFA-1-induced MTOC polarization through ZAP70 inhibition prevented intracellular Env polarization. Taken together, these data reveal that LFA-1 is a key determinant in inducing dynamic T cell remodeling to the VS and suggest a model in which LFA-1 engagement triggers active polarization of the MTOC and the associated Env-containing secretory apparatus to sites of cell-cell contact to support polarized viral assembly and egress for efficient cell-cell spread. IMPORTANCE: HIV-1 causes AIDS by spreading within immune cells and depletion of CD4 T lymphocytes. Rapid spread between these cells occurs by highly efficient cell-cell transmission that takes place at virological synapses (VS). VS are characterized by striking T cell remodeling that is spatially associated with polarized virus assembly and budding at sites of cell contact. Here, we show that the integrin LFA-1 triggers organelle polarization and viral protein recruitment, facilitating formation of the VS, and that this requires the T cell kinase ZAP70. Taken together, these data suggest a mechanism by which HIV-1-infected T cells sense and respond to cell contact to polarize viral egress and promote cell-cell spread. Understanding how cell-cell spread is regulated may help reveal therapeutic targets to specifically block this mode of HIV-1 dissemination.

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  • Binding of ICAM-1 to LFA-1 leads to polarization of the MTOC in the infected donor cell towards the recipient target cell.

    “The binding of ICAM-1 to LFA-1 leads to the polarization of the microtubule-organizing center (MTOC) in the infected (donor) cell towards the recipient (target) cell [37,38].”

    From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [38]

  • In contrast to HTLV-1, MTOC polarization in HIV-1-infected T cells is triggered via LFA-1 and activation of the downstream ZAP70 kinase signaling cascade.

    “In contrast to HTLV-1, MTOC polarization in HIV-1-infected T cells is triggered via the LFA-1 molecule, and the activation of a downstream T cell-specific ZAP70 kinase signaling cascade [38].”

    From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [38]

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Sorted by citations

Authors
Starling, S., & Jolly, C.
Affiliations
University College London (GB)
Corresponding author
Jolly, Clare
ORCID
Venue
Journal of Virology
Publisher
American Society for Microbiology
Published
2016-11
Volume
90
Issue
21
Pages
9841-9854
ISSN
  • 0022-538X (ISSN-L)
  • 1098-5514
DOI
10.1128/jvi.01152-16
PMC
PMC5068534
OpenAlex
W2516456642
Cited by
33
References
2
Citations by year
2026: 1 · 2024: 1 · 2023: 5 · 2022: 7 · 2021: 3 · 2020: 3 · 2019: 8 · 2018: 4 · 2017: 1
FWCI
3.00
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Virology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
  • Wellcome Trust (108079/Z/15/Z)
  • Medical Research Council (MR/J008184/1)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
  • Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Keywords
HIV-1, virological synapse, LFA-1, integrins, T cell polarization, ZAP-70, cell-to-cell transmission, HIV-1 envelope glycoprotein, microtubule organizing center, Golgi apparatus
MeSH terms
Humans, Lymphocyte Activation, CD4-Positive T-Lymphocytes, HIV-1, HIV Infections, Lymphocyte Function-Associated Antigen-1, Virus Assembly, Jurkat Cells, Microtubule-Organizing Center, Cell Line, Tumor, Virus Internalization

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