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Productive HIV-1 infection of tissue macrophages by fusion with infected CD4+ T cells. 2023
Rémi Mascarau, and
Marie Woottum, and
Léa Fromont, and
Rémi Gence, and
Vincent Cantaloube-Ferrieu, and
Zoï Vahlas, and
Kevin Lévêque, and
Florent Bertrand, and
Thomas Beunon, and
Arnaud Métais, and
Hicham El Costa, and
Nabila Jabrane-Ferrat, and
Yohan Gallois, and
Nicolas Guibert, and
Jean-Luc Davignon, and
Gilles Favre, and
Isabelle Maridonneau-Parini, and
Renaud Poincloux, and
Bernard Lagane, and
Serge Bénichou, and
Brigitte Raynaud-Messina, and
Christel Vérollet
Institut de Pharmacologie et Biologie Structurale (IPBS), Université de Toulouse, Centre National de la Recherche Scientifique, Université Toulouse III - Paul Sabatier (UPS) , Toulouse, France.
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.
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