Cargando…

Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells

Macrophages are essential for HIV-1 pathogenesis and represent major viral reservoirs. Therefore, it is critical to understand macrophage infection, especially in tissue macrophages, which are widely infected in vivo, but poorly permissive to cell-free infection. Although cell-to-cell transmission o...

Descripción completa

Detalles Bibliográficos
Autores principales: Mascarau, Rémi, Woottum, Marie, Fromont, Léa, Gence, Rémi, Cantaloube-Ferrieu, Vincent, Vahlas, Zoï, Lévêque, Kevin, Bertrand, Florent, Beunon, Thomas, Métais, Arnaud, El Costa, Hicham, Jabrane-Ferrat, Nabila, Gallois, Yohan, Guibert, Nicolas, Davignon, Jean-Luc, Favre, Gilles, Maridonneau-Parini, Isabelle, Poincloux, Renaud, Lagane, Bernard, Bénichou, Serge, Raynaud-Messina, Brigitte, Vérollet, Christel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10067447/
https://www.ncbi.nlm.nih.gov/pubmed/36988579
http://dx.doi.org/10.1083/jcb.202205103
_version_ 1785018472547221504
author Mascarau, Rémi
Woottum, Marie
Fromont, Léa
Gence, Rémi
Cantaloube-Ferrieu, Vincent
Vahlas, Zoï
Lévêque, Kevin
Bertrand, Florent
Beunon, Thomas
Métais, Arnaud
El Costa, Hicham
Jabrane-Ferrat, Nabila
Gallois, Yohan
Guibert, Nicolas
Davignon, Jean-Luc
Favre, Gilles
Maridonneau-Parini, Isabelle
Poincloux, Renaud
Lagane, Bernard
Bénichou, Serge
Raynaud-Messina, Brigitte
Vérollet, Christel
author_facet Mascarau, Rémi
Woottum, Marie
Fromont, Léa
Gence, Rémi
Cantaloube-Ferrieu, Vincent
Vahlas, Zoï
Lévêque, Kevin
Bertrand, Florent
Beunon, Thomas
Métais, Arnaud
El Costa, Hicham
Jabrane-Ferrat, Nabila
Gallois, Yohan
Guibert, Nicolas
Davignon, Jean-Luc
Favre, Gilles
Maridonneau-Parini, Isabelle
Poincloux, Renaud
Lagane, Bernard
Bénichou, Serge
Raynaud-Messina, Brigitte
Vérollet, Christel
author_sort Mascarau, Rémi
collection PubMed
description Macrophages are essential for HIV-1 pathogenesis and represent major viral reservoirs. Therefore, it is critical to understand macrophage infection, especially in tissue macrophages, which are widely infected in vivo, but poorly permissive to cell-free infection. Although cell-to-cell transmission of HIV-1 is a determinant mode of macrophage infection in vivo, how HIV-1 transfers toward macrophages remains elusive. Here, we demonstrate that fusion of infected CD4(+) T lymphocytes with human macrophages leads to their efficient and productive infection. Importantly, several tissue macrophage populations undergo this heterotypic cell fusion, including synovial, placental, lung alveolar, and tonsil macrophages. We also find that this mode of infection is modulated by the macrophage polarization state. This fusion process engages a specific short-lived adhesion structure and is controlled by the CD81 tetraspanin, which activates RhoA/ROCK-dependent actomyosin contractility in macrophages. Our study provides important insights into the mechanisms underlying infection of tissue-resident macrophages, and establishment of persistent cellular reservoirs in patients.
format Online
Article
Text
id pubmed-10067447
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-100674472023-04-04 Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells Mascarau, Rémi Woottum, Marie Fromont, Léa Gence, Rémi Cantaloube-Ferrieu, Vincent Vahlas, Zoï Lévêque, Kevin Bertrand, Florent Beunon, Thomas Métais, Arnaud El Costa, Hicham Jabrane-Ferrat, Nabila Gallois, Yohan Guibert, Nicolas Davignon, Jean-Luc Favre, Gilles Maridonneau-Parini, Isabelle Poincloux, Renaud Lagane, Bernard Bénichou, Serge Raynaud-Messina, Brigitte Vérollet, Christel J Cell Biol Article Macrophages are essential for HIV-1 pathogenesis and represent major viral reservoirs. Therefore, it is critical to understand macrophage infection, especially in tissue macrophages, which are widely infected in vivo, but poorly permissive to cell-free infection. Although cell-to-cell transmission of HIV-1 is a determinant mode of macrophage infection in vivo, how HIV-1 transfers toward macrophages remains elusive. Here, we demonstrate that fusion of infected CD4(+) T lymphocytes with human macrophages leads to their efficient and productive infection. Importantly, several tissue macrophage populations undergo this heterotypic cell fusion, including synovial, placental, lung alveolar, and tonsil macrophages. We also find that this mode of infection is modulated by the macrophage polarization state. This fusion process engages a specific short-lived adhesion structure and is controlled by the CD81 tetraspanin, which activates RhoA/ROCK-dependent actomyosin contractility in macrophages. Our study provides important insights into the mechanisms underlying infection of tissue-resident macrophages, and establishment of persistent cellular reservoirs in patients. Rockefeller University Press 2023-03-29 /pmc/articles/PMC10067447/ /pubmed/36988579 http://dx.doi.org/10.1083/jcb.202205103 Text en © 2023 Mascarau et al. https://creativecommons.org/licenses/by/4.0/This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Mascarau, Rémi
Woottum, Marie
Fromont, Léa
Gence, Rémi
Cantaloube-Ferrieu, Vincent
Vahlas, Zoï
Lévêque, Kevin
Bertrand, Florent
Beunon, Thomas
Métais, Arnaud
El Costa, Hicham
Jabrane-Ferrat, Nabila
Gallois, Yohan
Guibert, Nicolas
Davignon, Jean-Luc
Favre, Gilles
Maridonneau-Parini, Isabelle
Poincloux, Renaud
Lagane, Bernard
Bénichou, Serge
Raynaud-Messina, Brigitte
Vérollet, Christel
Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells
title Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells
title_full Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells
title_fullStr Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells
title_full_unstemmed Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells
title_short Productive HIV-1 infection of tissue macrophages by fusion with infected CD4(+) T cells
title_sort productive hiv-1 infection of tissue macrophages by fusion with infected cd4(+) t cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10067447/
https://www.ncbi.nlm.nih.gov/pubmed/36988579
http://dx.doi.org/10.1083/jcb.202205103
work_keys_str_mv AT mascarauremi productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT woottummarie productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT fromontlea productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT genceremi productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT cantaloubeferrieuvincent productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT vahlaszoi productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT levequekevin productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT bertrandflorent productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT beunonthomas productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT metaisarnaud productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT elcostahicham productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT jabraneferratnabila productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT galloisyohan productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT guibertnicolas productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT davignonjeanluc productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT favregilles productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT maridonneaupariniisabelle productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT poinclouxrenaud productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT laganebernard productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT benichouserge productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT raynaudmessinabrigitte productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells
AT verolletchristel productivehiv1infectionoftissuemacrophagesbyfusionwithinfectedcd4tcells