N-linked glycosylation of flavivirus E protein contributes to viral particle formation

PLoS Pathog. 2023 Oct 11;19(10):e1011681. doi: 10.1371/journal.ppat.1011681. eCollection 2023 Oct.

Abstract

In the case of the Japanese encephalitis virus (JEV), the envelope protein (E), a major component of viral particles, contains a highly conserved N-linked glycosylation site (E: N154). Glycosylation of the E protein is thought to play an important role in the ability of the virus to attach to target cells during transmission; however, its role in viral particle formation and release remains poorly understood. In this study, we investigated the role of N-glycosylation of flaviviral structural proteins in viral particle formation and secretion by introducing mutations in viral structural proteins or cellular factors involved in glycoprotein transport and processing. The number of secreted subviral particles (SVPs) was significantly reduced in N154A, a glycosylation-null mutant, but increased in D67N, a mutant containing additional glycosylation sites, indicating that the amount of E glycosylation regulates the release of SVPs. SVP secretion was reduced in cells deficient in galactose, sialic acid, and N-acetylglucosamine modifications in the Golgi apparatus; however, these reductions were not significant, suggesting that glycosylation mainly plays a role in pre-Golgi transport. Fluorescent labeling of SVPs using a split green fluorescent protein (GFP) system and time-lapse imaging by retention using selective hooks (RUSH) system revealed that the glycosylation-deficient mutant was arrested before endoplasmic reticulum (ER)- Golgi transport. However, the absence of ERGIC-53 and ERGIC-L, ER-Golgi transport cargo receptors that recognize sugar chains on cargo proteins, does not impair SVP secretion. In contrast, the solubility of the N154A mutant of E or the N15A/T17A mutant of prM in cells was markedly lower than that of the wild type, and proteasome-mediated rapid degradation of these mutants was observed, indicating the significance of glycosylation of both prM and E in proper protein folding and assembly of viral particles in the ER.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Encephalitis Virus, Japanese* / metabolism
  • Flavivirus* / metabolism
  • Glycosylation
  • Viral Envelope Proteins / metabolism
  • Virion / metabolism

Substances

  • Viral Envelope Proteins

Grants and funding

This research was supported by JSPS KAKENHI [grant numbers 21H02625 and JP17H06414 (to H.Y.) and 22H00553, 22H02873, 22K18378, 20H05305, 20K21874, 17K08849, and 17H06413 (to E.M.)], JST CREST, Japan [grant number JPMJCR17H4] (to E.M.), AMED, Japan [grant number JP20fk0108521, 22fk0108527 (to E.M.)], and the Takeda Science Foundation (to E.M.). This research was also supported by Research Support Project for Life Science and Drug Discovery (Basis for Supporting Innovative Drug Discovery and Life Science Research [BINDS]) from AMED under Grant Number JP22ama121008 (to Y.K.).The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. None of the authors received a salary from the funders.