Collagen and actin network mediate antiviral immunity against Orsay virus in C. elegans intestinal cells

PLoS Pathog. 2024 Jan 8;20(1):e1011366. doi: 10.1371/journal.ppat.1011366. eCollection 2024 Jan.

Abstract

C. elegans is a free-living nematode that is widely used as a small animal model for studying fundamental biological processes and disease mechanisms. Since the discovery of the Orsay virus in 2011, C. elegans also holds the promise of dissecting virus-host interaction networks and innate antiviral immunity pathways in an intact animal. Orsay virus primarily targets the worm intestine, causing enlarged intestinal lumen as well as visible changes to infected cells such as liquefaction of cytoplasm and convoluted apical border. Previous studies of Orsay virus identified that C. elegans is able to mount antiviral responses by DRH-1/RIG-I mediated RNA interference and Intracellular Pathogen Response, a uridylyltransferase that destabilizes viral RNAs by 3' end uridylation, and ubiquitin protein modifications and turnover. To comprehensively search for novel antiviral pathways in C. elegans, we performed genome-wide RNAi screens by bacterial feeding using existing bacterial RNAi libraries covering 94% of the entire genome. Out of the 106 potential antiviral gene hits identified, we investigated those in three new pathways: collagens, actin remodelers, and epigenetic regulators. By characterizing Orsay virus infection in RNAi and mutant worms, our results indicate that collagens likely form a physical barrier in intestine cells to inhibit viral infection by preventing Orsay virus entry. Furthermore, evidence suggests that actin remodeling proteins (unc-34, wve-1 and wsp-1) and chromatin remodelers (nurf-1 and isw-1) exert their antiviral activities by regulating the intestinal actin (act-5), a critical component of the terminal web which likely function as another physical barrier to prevent Orsay infection.

MeSH terms

  • Actins / metabolism
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Collagen / genetics
  • Collagen / metabolism
  • Host-Pathogen Interactions
  • Nerve Tissue Proteins / metabolism
  • RNA Interference
  • Virus Diseases* / genetics

Substances

  • Caenorhabditis elegans Proteins
  • Actins
  • Collagen
  • unc-34 protein, C elegans
  • Nerve Tissue Proteins