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Mucosal application of the broadly neutralizing antibody 10-1074 protects macaques from cell-associated SHIV vaginal exposure

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  • Karunasinee Suphaphiphat

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

  • Delphine Desjardins

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

  • Valérie Lorin

    (Université Paris Cité, INSERM U1222)

  • Nastasia Dimant

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

  • Kawthar Bouchemal

    (CNRS, Institut de Recherche de Chimie Paris, CNRS UMR 8247)

  • Laetitia Bossevot

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

  • Maxence Galpin-Lebreau

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

  • Nathalie Dereuddre-Bosquet

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

  • Hugo Mouquet

    (Université Paris Cité, INSERM U1222)

  • Roger Grand

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

  • Mariangela Cavarelli

    (Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial diseases (IMVA-HB/IDMIT))

Abstract

Passive immunization using broadly neutralizing antibodies (bNAbs) is investigated in clinical settings to inhibit HIV-1 acquisition due to the lack of a preventive vaccine. However, bNAbs efficacy against highly infectious cell-associated virus transmission has been overlooked. HIV-1 transmission mediated by infected cells present in body fluids likely dominates infection and aids the virus in evading antibody-based immunity. Here, we show that the anti-N-glycans/V3 loop HIV-1 bNAb 10-1074 formulated for topical vaginal application in a microbicide gel provides significant protection against repeated cell-associated SHIV162P3 vaginal challenge in non-human primates. The treated group has a significantly lower infection rate than the control group, with 5 out of 6 animals fully protected from the acquisition of infection. The findings suggest that mucosal delivery of potent bnAbs may be a promising approach for preventing transmission mediated by infected cells and support the use of anti-HIV-antibody-based strategies as potential microbicides in human clinical trials.

Suggested Citation

  • Karunasinee Suphaphiphat & Delphine Desjardins & Valérie Lorin & Nastasia Dimant & Kawthar Bouchemal & Laetitia Bossevot & Maxence Galpin-Lebreau & Nathalie Dereuddre-Bosquet & Hugo Mouquet & Roger Gr, 2023. "Mucosal application of the broadly neutralizing antibody 10-1074 protects macaques from cell-associated SHIV vaginal exposure," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41966-4
    DOI: 10.1038/s41467-023-41966-4
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    1. Masashi Shingai & Yoshiaki Nishimura & Florian Klein & Hugo Mouquet & Olivia K. Donau & Ronald Plishka & Alicia Buckler-White & Michael Seaman & Michael Piatak & Jeffrey D. Lifson & Dimiter Dimitrov &, 2013. "Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia," Nature, Nature, vol. 503(7475), pages 277-280, November.
    2. Sung-Youl Ko & Amarendra Pegu & Rebecca S. Rudicell & Zhi-yong Yang & M. Gordon Joyce & Xuejun Chen & Keyun Wang & Saran Bao & Thomas D. Kraemer & Timo Rath & Ming Zeng & Stephen D. Schmidt & John-Pau, 2014. "Enhanced neonatal Fc receptor function improves protection against primate SHIV infection," Nature, Nature, vol. 514(7524), pages 642-645, October.
    3. Timothée Bruel & Florence Guivel-Benhassine & Sonia Amraoui & Marine Malbec & Léa Richard & Katia Bourdic & Daniel Aaron Donahue & Valérie Lorin & Nicoletta Casartelli & Nicolas Noël & Olivier Lambott, 2016. "Elimination of HIV-1-infected cells by broadly neutralizing antibodies," Nature Communications, Nature, vol. 7(1), pages 1-12, April.
    4. Pilar Mendoza & Henning Gruell & Lilian Nogueira & Joy A. Pai & Allison L. Butler & Katrina Millard & Clara Lehmann & Isabelle Suárez & Thiago Y. Oliveira & Julio C. C. Lorenzi & Yehuda Z. Cohen & Chr, 2018. "Combination therapy with anti-HIV-1 antibodies maintains viral suppression," Nature, Nature, vol. 561(7724), pages 479-484, September.
    5. Marina Caskey & Florian Klein & Julio C. C. Lorenzi & Michael S. Seaman & Anthony P. West & Noreen Buckley & Gisela Kremer & Lilian Nogueira & Malte Braunschweig & Johannes F. Scheid & Joshua A. Horwi, 2015. "Viraemia suppressed in HIV-1-infected humans by broadly neutralizing antibody 3BNC117," Nature, Nature, vol. 522(7557), pages 487-491, June.
    6. Ann J. Hessell & Lars Hangartner & Meredith Hunter & Carin E. G. Havenith & Frank J. Beurskens & Joost M. Bakker & Caroline M. S. Lanigan & Gary Landucci & Donald N. Forthal & Paul W. H. I. Parren & P, 2007. "Fc receptor but not complement binding is important in antibody protection against HIV," Nature, Nature, vol. 449(7158), pages 101-104, September.
    7. Rajeev Gautam & Yoshiaki Nishimura & Amarendra Pegu & Martha C. Nason & Florian Klein & Anna Gazumyan & Jovana Golijanin & Alicia Buckler-White & Reza Sadjadpour & Keyun Wang & Zachary Mankoff & Steph, 2016. "A single injection of anti-HIV-1 antibodies protects against repeated SHIV challenges," Nature, Nature, vol. 533(7601), pages 105-109, May.
    8. Qingsheng Li & Lijie Duan & Jacob D. Estes & Zhong-Min Ma & Tracy Rourke & Yichuan Wang & Cavan Reilly & John Carlis & Christopher J. Miller & Ashley T. Haase, 2005. "Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells," Nature, Nature, vol. 434(7037), pages 1148-1152, April.
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