N-glycosylation of viral glycoprotein is a novel determinant for the tropism and virulence of highly pathogenic tick-borne bunyaviruses

PLoS Pathog. 2024 Jul 15;20(7):e1012348. doi: 10.1371/journal.ppat.1012348. eCollection 2024 Jul.

Abstract

Severe fever with thrombocytopenia syndrome (SFTS) virus, a tick-borne bunyavirus, causes a severe/fatal disease termed SFTS; however, the viral virulence is not fully understood. The viral non-structural protein, NSs, is the sole known virulence factor. NSs disturbs host innate immune responses and an NSs-mutant SFTS virus causes no disease in an SFTS animal model. The present study reports a novel determinant of viral tropism as well as virulence in animal models, within the glycoprotein (GP) of SFTS virus and an SFTS-related tick-borne bunyavirus. Infection with mutant SFTS viruses lacking the N-linked glycosylation of GP resulted in negligible usage of calcium-dependent lectins in cells, less efficient infection, high susceptibility to a neutralizing antibody, low cytokine production in macrophage-like cells, and reduced virulence in Ifnar-/- mice, when compared with wildtype virus. Three SFTS virus-related bunyaviruses had N-glycosylation motifs at similar positions within their GP and a glycan-deficient mutant of Heartland virus showed in vitro and in vivo phenotypes like those of the SFTS virus. Thus, N-linked glycosylation of viral GP is a novel determinant for the tropism and virulence of SFTS virus and of a related virus. These findings will help us understand the process of severe/fatal diseases caused by tick-borne bunyaviruses.

MeSH terms

  • Animals
  • Bunyaviridae Infections / metabolism
  • Bunyaviridae Infections / virology
  • Glycoproteins* / genetics
  • Glycoproteins* / metabolism
  • Glycosylation
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Orthobunyavirus / genetics
  • Orthobunyavirus / metabolism
  • Orthobunyavirus / pathogenicity
  • Phlebovirus* / genetics
  • Phlebovirus* / pathogenicity
  • Severe Fever with Thrombocytopenia Syndrome / virology
  • Ticks / virology
  • Viral Tropism*
  • Virulence

Substances

  • Glycoproteins

Grants and funding

This work was funded by the Application Procedures for Fund for the Promotion of Joint International Research (Fostering Joint International Research [B]) to M.S. and by the Japan Agency for Medical Research and Development (AMED; JP21fk0108080, JP21fk0108081, JP22fk0108614, and JP22fk0108624) to M.S. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.