Inborn errors of TLR3- or MDA5-dependent type I IFN immunity in children with enterovirus rhombencephalitis

J Exp Med. 2021 Dec 6;218(12):e20211349. doi: 10.1084/jem.20211349. Epub 2021 Nov 2.

Abstract

Enterovirus (EV) infection rarely results in life-threatening infection of the central nervous system. We report two unrelated children with EV30 and EV71 rhombencephalitis. One patient carries compound heterozygous TLR3 variants (loss-of-function F322fs2* and hypomorphic D280N), and the other is homozygous for an IFIH1 variant (loss-of-function c.1641+1G>C). Their fibroblasts respond poorly to extracellular (TLR3) or intracellular (MDA5) poly(I:C) stimulation. The baseline (TLR3) and EV-responsive (MDA5) levels of IFN-β in the patients' fibroblasts are low. EV growth is enhanced at early and late time points of infection in TLR3- and MDA5-deficient fibroblasts, respectively. Treatment with exogenous IFN-α2b before infection renders both cell lines resistant to EV30 and EV71, whereas post-infection treatment with IFN-α2b rescues viral susceptibility fully only in MDA5-deficient fibroblasts. Finally, the poly(I:C) and viral phenotypes of fibroblasts are rescued by the expression of WT TLR3 or MDA5. Human TLR3 and MDA5 are critical for cell-intrinsic immunity to EV, via the control of baseline and virus-induced type I IFN production, respectively.

Publication types

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

MeSH terms

  • Cells, Cultured
  • Child, Preschool
  • Encephalitis, Viral / genetics
  • Encephalitis, Viral / immunology*
  • Enterovirus / drug effects
  • Enterovirus / physiology
  • Enterovirus Infections / genetics
  • Enterovirus Infections / immunology*
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / immunology
  • Fibroblasts / virology
  • Humans
  • Infant
  • Interferon alpha-2 / pharmacology
  • Interferon-Induced Helicase, IFIH1 / genetics*
  • Interferon-Induced Helicase, IFIH1 / immunology
  • Interferon-beta / immunology
  • Interferon-beta / metabolism
  • Loss of Function Mutation
  • Male
  • Metabolism, Inborn Errors / genetics
  • Metabolism, Inborn Errors / immunology
  • Poly I-C / pharmacology
  • Rhombencephalon / virology
  • Toll-Like Receptor 3 / genetics*
  • Toll-Like Receptor 3 / immunology
  • Virus Replication / drug effects

Substances

  • Interferon alpha-2
  • Interferon-alpha2b
  • TLR3 protein, human
  • Toll-Like Receptor 3
  • Interferon-beta
  • IFIH1 protein, human
  • Interferon-Induced Helicase, IFIH1
  • Poly I-C