Peli1 facilitates virus replication and promotes neuroinflammation during West Nile virus infection

J Clin Invest. 2018 Nov 1;128(11):4980-4991. doi: 10.1172/JCI99902. Epub 2018 Sep 24.

Abstract

The E3 ubiquitin ligase Pellino 1 (Peli1) is a microglia-specific mediator of autoimmune encephalomyelitis. Its role in neurotropic flavivirus infection is largely unknown. Here, we report that mice deficient in Peli1 (Peli1-/-) were more resistant to lethal West Nile virus (WNV) infection and exhibited reduced viral loads in tissues and attenuated brain inflammation. Peli1 mediates chemokine and proinflammatory cytokine production in microglia and promotes T cell and macrophage infiltration into the CNS. Unexpectedly, Peli1 was required for WNV entry and replication in mouse macrophages and mouse and human neurons and microglia. It was also highly expressed on WNV-infected neurons and adjacent inflammatory cells from postmortem patients who died of acute WNV encephalitis. WNV passaged in Peli1-/- macrophages or neurons induced a lower viral load and impaired activation in WT microglia and thereby reduced lethality in mice. Smaducin-6, which blocks interactions between Peli1 and IRAK1, RIP1, and IKKε, did not inhibit WNV-triggered microglia activation. Collectively, our findings suggest a nonimmune regulatory role for Peli1 in promoting microglia activation during WNV infection and identify a potentially novel host factor for flavivirus cell entry and replication.

Keywords: Inflammation; Innate immunity; Neurological disorders; Virology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chemokines / genetics
  • Chemokines / metabolism
  • Chlorocebus aethiops
  • Humans
  • Inflammation / genetics
  • Inflammation / metabolism
  • Inflammation / pathology
  • Inflammation / virology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Macrophages / virology
  • Mice
  • Mice, Knockout
  • Microglia / metabolism
  • Microglia / pathology
  • Microglia / virology
  • Neurons / metabolism*
  • Neurons / pathology
  • Neurons / virology
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*
  • Vero Cells
  • Viral Load
  • Virus Replication / physiology*
  • West Nile Fever / genetics
  • West Nile Fever / metabolism*
  • West Nile Fever / pathology
  • West Nile virus / physiology*

Substances

  • Chemokines
  • Nuclear Proteins
  • PELI1 protein, human
  • Ubiquitin-Protein Ligases