TRIM72 restricts lyssavirus infection by inducing K48-linked ubiquitination and proteasome degradation of the matrix protein

PLoS Pathog. 2024 Feb 26;20(2):e1011718. doi: 10.1371/journal.ppat.1011718. eCollection 2024 Feb.

Abstract

The tripartite motif (TRIM) protein family is the largest subfamily of E3 ubiquitin ligases, playing a crucial role in the antiviral process. In this study, we found that TRIM72, a member of the TRIM protein family, was increased in neuronal cells and mouse brains following rabies lyssavirus (RABV) infection. Over-expression of TRIM72 significantly reduced the viral titer of RABV in neuronal cells and mitigated the pathogenicity of RABV in mice. Furthermore, we found that TRIM72 over-expression effectively prevents the assembly and/or release of RABV. In terms of the mechanism, TRIM72 promotes the K48-linked ubiquitination of RABV Matrix protein (M), leading to the degradation of M through the proteasome pathway. TRIM72 directly interacts with M and the interaction sites were identified and confirmed through TRIM72-M interaction model construction and mutation analysis. Further investigation revealed that the degradation of M induced by TRIM72 was attributed to TRIM72's promotion of ubiquitination at site K195 in M. Importantly, the K195 site was found to be partially conserved among lyssavirus's M proteins, and TRIM72 over-expression induced the degradation of these lyssavirus M proteins. In summary, our study has uncovered a TRIM family protein, TRIM72, that can restrict lyssavirus replication by degrading M, and we have identified a novel ubiquitination site (K195) in lyssavirus M.

MeSH terms

  • Animals
  • Lyssavirus* / genetics
  • Mice
  • Proteasome Endopeptidase Complex* / metabolism
  • Proteins / metabolism
  • Tripartite Motif Proteins / genetics
  • Tripartite Motif Proteins / metabolism
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination

Substances

  • Proteasome Endopeptidase Complex
  • Proteins
  • Ubiquitin-Protein Ligases
  • Tripartite Motif Proteins

Grants and funding

This study was supported by the National Natural Science Foundation of China (grant number 32102648 to B.K.S.), the Fundamental Research Funds for the Central Universities (grant number 2662023PY005 to L.Z.), the National Key Research and Development Program of China (grant number 2022YFD1800100 to M.Z.), the China Postdoctoral Science Foundation (grant number BX2021109 to B.K.S., grant number 2021M691170 to B.K.S.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.