SAMD9L acts as an antiviral factor against HIV-1 and primate lentiviruses by restricting viral and cellular translation

PLoS Biol. 2024 Jul 3;22(7):e3002696. doi: 10.1371/journal.pbio.3002696. eCollection 2024 Jul.

Abstract

Sterile alpha motif domain-containing proteins 9 and 9-like (SAMD9/9L) are associated with life-threatening genetic diseases in humans and are restriction factors of poxviruses. Yet, their cellular function and the extent of their antiviral role are poorly known. Here, we found that interferon-stimulated human SAMD9L restricts HIV-1 in the late phases of replication, at the posttranscriptional and prematuration steps, impacting viral translation and, possibly, endosomal trafficking. Surprisingly, the paralog SAMD9 exerted an opposite effect, enhancing HIV-1. More broadly, we showed that SAMD9L restricts primate lentiviruses, but not a gammaretrovirus (MLV), nor 2 RNA viruses (arenavirus MOPV and rhabdovirus VSV). Using structural modeling and mutagenesis of SAMD9L, we identified a conserved Schlafen-like active site necessary for HIV-1 restriction by human and a rodent SAMD9L. By testing a gain-of-function constitutively active variant from patients with SAMD9L-associated autoinflammatory disease, we determined that SAMD9L pathogenic functions also depend on the Schlafen-like active site. Finally, we found that the constitutively active SAMD9L strongly inhibited HIV, MLV, and, to a lesser extent, MOPV. This suggests that the virus-specific effect of SAMD9L may involve its differential activation/sensing and the virus ability to evade from SAMD9L restriction. Overall, our study identifies SAMD9L as an HIV-1 antiviral factor from the cell autonomous immunity and deciphers host determinants underlying the translational repression. This provides novel links and therapeutic avenues against viral infections and genetic diseases.

MeSH terms

  • Animals
  • Antiviral Restriction Factors
  • HEK293 Cells
  • HIV Infections / drug therapy
  • HIV Infections / virology
  • HIV-1* / genetics
  • HIV-1* / physiology
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Lentiviruses, Primate* / genetics
  • Lentiviruses, Primate* / metabolism
  • Protein Biosynthesis
  • Tumor Suppressor Proteins
  • Virus Replication*

Substances

  • SAMD9L protein, human
  • SAMD9 protein, human
  • Antiviral Restriction Factors
  • Intracellular Signaling Peptides and Proteins
  • Tumor Suppressor Proteins

Grants and funding

This work was funded by grants from the French Research Agency on HIV and Emerging Infectious Diseases ANRS/MIE (#ECTZ19143 and #ECTZ118944 to LE, #ECTZ245897 to LE and FF, #ECTZ243795 to CBT, #ECTZ3306 to EPR), as well as from the ANR LABEX ECOFECT (ANR-11-LABX-0048 of Université de Lyon, within the program "Investissements d'Avenir" (ANR-11-IDEX-0007) operated by the French National Research Agency, to LE and LG), the amfAR (Mathilde Krim Phase II Fellowship #109140-58-RKHF, to LE), the “Fondation pour la Recherche Médicale” (FRM “Projet Innovant” #ING20160435028 to LE), the FINOVI (“recently settled scientist” grant to LE), and the Sidaction (to LE #23-1-AEQ-13601, and to AC). LE and AC are supported by the CNRS. LG is supported by the Université Claude Bernard Lyon 1 and Swedish Center of Advanced Study. AL is supported by PhD fellowships from Sidaction (2020 - n°12673, 2023 - n°13574). The funders play no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.