The ubiquitin-like protein PLIC-1 or ubiquilin 1 inhibits TLR3-Trif signaling

PLoS One. 2011;6(6):e21153. doi: 10.1371/journal.pone.0021153. Epub 2011 Jun 17.

Abstract

Background: The innate immune responses to virus infection are initiated by either Toll-like receptors (TLR3/7/8/9) or cytoplasmic double-stranded RNA (dsRNA)-recognizing RNA helicases RIG-I and MDA5. To avoid causing injury to the host, these signaling pathways must be switched off in time by negative regulators.

Methodology/principal findings: Through yeast-two hybrid screening, we found that an ubiquitin-like protein named protein linking integrin-associated protein to cytoskeleton 1(PLIC-1 or Ubiquilin 1) interacted with the Toll/interleukin-1 receptor (TIR) domain of TLR4. Interestingly, PLIC-1 had modest effect on TLR4-mediated signaling, but strongly suppressed the transcriptional activation of IFN-β promoter through the TLR3-Trif-dependent pathway. Concomitantly, reduction of endogenous PLIC-1 by short-hairpin interfering RNA (shRNA) enhanced TLR3 activation both in luciferase reporter assays as well as in new castle disease virus (NDV) infected cells. An interaction between PLIC-1 and Trif was confirmed in co-immunoprecipitation (Co-IP) and GST-pull-down assays. Subsequent confocal microscopic analysis revealed that PLIC-1 and Trif colocalized with the autophagosome marker LC3 in punctate subcellular structures. Finally, overexpression of PLIC-1 decreased Trif protein abundance in a Nocodazole-sensitive manner.

Conclusions: Our results suggest that PLIC-1 is a novel inhibitor of the TLR3-Trif antiviral pathway by reducing the abundance of Trif.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Adaptor Proteins, Vesicular Transport / metabolism*
  • Autophagy-Related Proteins
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Line, Tumor
  • Down-Regulation / drug effects
  • Gene Knockdown Techniques
  • Genes, Reporter / genetics
  • HEK293 Cells
  • Humans
  • Interferon-beta / genetics
  • Luciferases / genetics
  • NF-kappa B / metabolism
  • Newcastle disease virus / drug effects
  • Newcastle disease virus / physiology
  • Poly I-C / pharmacology
  • Promoter Regions, Genetic / genetics
  • Protein Transport / drug effects
  • RNA, Small Interfering / genetics
  • Signal Transduction* / drug effects
  • Signal Transduction* / genetics
  • Toll-Like Receptor 3 / metabolism*
  • Two-Hybrid System Techniques

Substances

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport
  • Autophagy-Related Proteins
  • Carrier Proteins
  • Cell Cycle Proteins
  • MAVS protein, human
  • NF-kappa B
  • RNA, Small Interfering
  • TICAM1 protein, human
  • TLR3 protein, human
  • Toll-Like Receptor 3
  • UBQLN1 protein, human
  • Interferon-beta
  • Luciferases
  • Poly I-C