Simultaneous Cell-to-Cell Transmission of Human Immunodeficiency Virus to Multiple Targets through Polysynapses

Rudnicka, Dominika; Feldmann, Jérôme; Porrot, Françoise; Wietgrefe, Steve; Guadagnini, Stéphanie; Prévost, Marie-Christine; Estaquier, Jérôme; Haase, Ashley T.; Sol-Foulon, Nathalie; Schwartz, Olivier

doi:10.1128/jvi.00282-09

Cited by 229HIV Research and TreatmentT-cell and Retrovirus StudiesHIV/AIDS Research and Interventions

Simultaneous Cell-to-Cell Transmission of Human Immunodeficiency Virus to Multiple Targets through Polysynapses

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Rudnicka, Dominika, Feldmann, Jérôme, Porrot, Françoise, Wietgrefe, Steve, Guadagnini, Stéphanie, Prévost, Marie-Christine, Estaquier, Jérôme, Haase, Ashley T. +2 more·2009·Journal of Virology

DOI 10.1128/jvi.00282-09PMC PMC2687379

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Abstract

Human immunodeficiency virus type 1 (HIV-1) efficiently propagates through cell-to-cell contacts, which include virological synapses (VS), filopodia, and nanotubes. Here, we quantified and characterized further these diverse modes of contact in lymphocytes. We report that viral transmission mainly occurs across VS and through “polysynapses,” a rosette-like structure formed between one infected cell and multiple adjacent recipients. Polysynapses are characterized by simultaneous HIV clustering and transfer at multiple membrane regions. HIV Gag proteins often adopt a ring-like supramolecular organization at sites of intercellular contacts and colocalize with CD63 tetraspanin and raft components GM1, Thy-1, and CD59. In donor cells engaged in polysynapses, there is no preferential accumulation of Gag proteins at contact sites facing the microtubule organizing center. The LFA-1 adhesion molecule, known to facilitate viral replication, enhances formation of polysynapses. Altogether, our results reveal an underestimated mode of viral transfer through polysynapses. In HIV-infected individuals, these structures, by promoting concomitant infection of multiple targets in the vicinity of infected cells, may facilitate exponential viral growth and escape from immune responses.

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HIV-1-infected T cells can form multiple synapses, with Gag accumulated in ring-shaped structures at sites of intercellular contact without MTOC polarization.
“It has also been reported that HIV-1-infected T cells can form multiple synapses [45]. In this case, the Gag protein accumulated in ring-shaped structures at sites of intercellular contact without MTOC polarization.”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [45]

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Authors: Rudnicka, D., Feldmann, J., Porrot, F., Wietgrefe, S., Guadagnini, S., Prévost, M.-C., Estaquier, J., Haase, A. T., Sol-Foulon, N., & Schwartz, O.
Affiliations: Centre National de la Recherche Scientifique (FR)
Virus and Immunity Unit, Department of Virology, Institut Pasteur, URA CNRS 3015, 28 rue du Dr. Roux, 75724 Paris Cedex 15, France
University of Minnesota (US)
Electron Microscopy Core Facility, Institut Pasteur, Paris, France
INSERM U841, Faculté de Médecine Henri Mondor, 8 rue du Général Sarrail, 94010 Créteil, France
Corresponding author: Schwartz, Olivier
ORCID: Haase, Ashley T.
Schwartz, Olivier
Venue: Journal of Virology
Publisher: American Society for Microbiology
Published: 2009-06-15
Volume: 83
Issue: 12
Pages: 6234-6246
ISSN: 0022-538X (ISSN-L)
1098-5514
DOI: 10.1128/jvi.00282-09
PMC: PMC2687379
OpenAlex: W2065794926
Cited by: 229
References: 54
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2023: 6 · 2022: 13 · 2021: 10 · 2020: 11 · 2019: 8 · 2018: 10 · 2017: 7 · 2016: 14 · 2015: 10 · 2014: 26 · 2013: 26 · 2012: 22
FWCI: 10.04
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Virology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
Life Sciences › Immunology and Microbiology › Immunology › T-cell and Retrovirus Studies
Health Sciences › Medicine › Infectious Diseases › HIV/AIDS Research and Interventions
Keywords: HIV-1, cell-to-cell transmission, virological synapse, filopodia, nanotubes, CD63, lipid rafts, LFA-1, lymphocytes
MeSH terms: Animals, Female, Humans, Macaca, Microscopy, Electron, Scanning, Pseudopodia, Virus Replication, CD4-Positive T-Lymphocytes, HIV-1, HIV Infections, Lymphocyte Function-Associated Antigen-1, Jurkat Cells, Microscopy, Electron, Transmission, env Gene Products, Human Immunodeficiency Virus, gag Gene Products, Human Immunodeficiency Virus

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Simultaneous Cell-to-Cell Transmission of Human Immunodeficiency Virus to Multiple Targets through Polysynapses

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