| Title: |
HIV-1 budding requires cortical actin disassembly by the oxidoreductase MICAL1 |
| Authors: |
Serrano, Thomas; Casartelli, Nicoletta; Ghasemi, Foad; Wioland, Hugo; Cuvelier, Frédérique; Salles, Audrey; Moya-Nilges, Maryse; Welker, Lisa; Bernacchi, Serena; Ruff, Marc; Jégou, Antoine; Romet-Lemonne, Guillaume; Schwartz, Olivier; Frémont, Stéphane; Echard, Arnaud |
| Contributors: |
Trafic membranaire et Division cellulaire - Membrane Traffic and Cell Division; Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité); Virus et immunité - Virus and immunity; Institut Pasteur Paris (IP)-Université Paris Cité (UPCité); Institut Jacques Monod (IJM (UMR_7592)); Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité); BioImagerie Photonique – Photonic BioImaging (UTechS PBI); Plate-forme de bioimagerie ultrastructurale - Ultrastructural BioImaging Core Facility; Architecture et Réactivité de l'ARN (ARN); Institut de biologie moléculaire et cellulaire (IBMC); Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS); Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg (UNISTRA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS); This work has been supported by Institut Pasteur, CNRS, Agence Nationale de la Recherche (ANR) RedoxActin, and Fondation pour la Recherche Médicale (EQU202103012627) to A.E.; ANRS-21020 AP2020-2 to S.F.; Institut Pasteur, Urgence COVID-19 Fundraising Campaign of Institut Pasteur, Fondation pour la Recherche Médicale (FRM), ANRS, the Vaccine Research Institute (ANR-10-LABX-77), Labex Integrative Biology for Emerging Infectious Disease (IBEID) (ANR-10-LABX-62-IBEID), ANR/FRM Flash Covid PROTEO-SARS-CoV-2, ANR Coronamito, HERA European funding (Durable consortium), Learning and Adaptive European Pandemic Preparedness System funding, and ANRS-21020 AP2020-2 to N.C. and O.S.; and ANR Redoxactin and Fondation pour la Recherche Medicale (EQU202203014630) to G.R.-L.; T.S. received a PhD fellowship from SIDACTION 2021-1-FJC-13007. We thank the Ecole Doctorale Frontières de l’Innovation en Recherche et Education—Programme Bettencourt to T.S.; F.G. received a postdoctoral fellowship from FRM (EQU202203014630). UTechS PBI and UTechS UBI are part of the France–BioImaging infrastructure network (FBI) supported by the French National Research Agency (ANR-10-INBS-04; Investments for the Future), and acknowledges support from Institut Pasteur, ANR/FBI, the Région Ile-de-France (program “Domaine d’Intérêt Majeur-Malinf” and DIM1HEALTH) and the French Government Investissement d’Avenir Programme—Laboratoire d’Excellence “Integrative Biology of Emerging Infectious Diseases” (ANR-10-LABX-62-IBEID) for the use of ELYRA PS1 LSM780 and ELYRA7 microscopes.; ANR-19-CE13-0018,RedoxActin,Régulation du cytosquelette d'actine par le contrôle de son oxydation(2019); ANR-10-LABX-0077,VRI,Initiative for the creation of a Vaccine Research Institute(2010); ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010); ANR-10-INBS-0004,France-BioImaging,Développment d'une infrastructure française distribuée coordonnée(2010) |
| Source: |
ISSN: 0027-8424. |
| Publisher Information: |
CCSD; National Academy of Sciences |
| Publication Year: |
2024 |
| Collection: |
Institut Pasteur: HAL |
| Subject Terms: |
HIV-1 budding; actin; Arp2/3; MICAL1; ESCRT; [SDV]Life Sciences [q-bio] |
| Description: |
International audience ; Many enveloped viruses bud from the plasma membrane that is tightly associated with a dense and thick actin cortex. This actin network represents a significant challenge for membrane deformation and scission, and how it is remodeled during the late steps of the viral cycle is largely unknown. Using superresolution microscopy, we show that HIV-1 buds in areas of the plasma membrane with low cortical F-actin levels. We find that the cellular oxidoreductase MICAL1 locally depolymerizes actin at budding sites to promote HIV-1 budding and release. Upon MICAL1 depletion, F-actin abnormally remains at viral budding sites, incompletely budded viruses accumulate at the plasma membrane and viral release is impaired. Remarkably, normal viral release can be restored in MICAL1-depleted cells by inhibiting Arp2/3-dependent branched actin networks. Mechanistically, we find that MICAL1 directly disassembles branched-actin networks and controls the timely recruitment of the Endosomal Sorting Complexes Required for Transport scission machinery during viral budding. In addition, the MICAL1 activator Rab35 is recruited at budding sites, functions in the same pathway as MICAL1, and is also required for viral release. This work reveals a role for oxidoreduction in triggering local actin depolymerization to control HIV-1 budding, a mechanism that may be widely used by other viruses. The debranching activity of MICAL1 could be involved beyond viral budding in various other cellular functions requiring local plasma membrane deformation. |
| Document Type: |
article in journal/newspaper |
| Language: |
English |
| Relation: |
info:eu-repo/semantics/altIdentifier/pmid/39556735; PUBMED: 39556735; PUBMEDCENTRAL: PMC11621841 |
| DOI: |
10.1073/pnas.2407835121 |
| Availability: |
https://hal.science/hal-04796735; https://hal.science/hal-04796735v1/document; https://hal.science/hal-04796735v1/file/serrano-et-al-hiv-1-budding-requires-cortical-actin-disassembly-by-the-oxidoreductase-mical1.pdf; https://doi.org/10.1073/pnas.2407835121 |
| Rights: |
http://creativecommons.org/licenses/by-nc-nd/ ; info:eu-repo/semantics/OpenAccess |
| Accession Number: |
edsbas.37B922 |
| Database: |
BASE |