Severe influenza pneumonitis in children with inherited TLR3 deficiency

J Exp Med. 2019 Sep 2;216(9):2038-2056. doi: 10.1084/jem.20181621. Epub 2019 Jun 19.

Abstract

Autosomal recessive IRF7 and IRF9 deficiencies impair type I and III IFN immunity and underlie severe influenza pneumonitis. We report three unrelated children with influenza A virus (IAV) infection manifesting as acute respiratory distress syndrome (IAV-ARDS), heterozygous for rare TLR3 variants (P554S in two patients and P680L in the third) causing autosomal dominant (AD) TLR3 deficiency. AD TLR3 deficiency can underlie herpes simplex virus-1 (HSV-1) encephalitis (HSE) by impairing cortical neuron-intrinsic type I IFN immunity to HSV-1. TLR3-mutated leukocytes produce normal levels of IFNs in response to IAV. In contrast, TLR3-mutated fibroblasts produce lower levels of IFN-β and -λ, and display enhanced viral susceptibility, upon IAV infection. Moreover, the patients' iPSC-derived pulmonary epithelial cells (PECs) are susceptible to IAV. Treatment with IFN-α2b or IFN-λ1 rescues this phenotype. AD TLR3 deficiency may thus underlie IAV-ARDS by impairing TLR3-dependent, type I and/or III IFN-mediated, PEC-intrinsic immunity. Its clinical penetrance is incomplete for both IAV-ARDS and HSE, consistent with their typically sporadic nature.

Publication types

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

MeSH terms

  • Alleles
  • Child
  • Child, Preschool
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Fatal Outcome
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / pathology
  • Heterozygote
  • Humans
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism
  • Infant
  • Infant, Newborn
  • Influenza A virus / drug effects
  • Influenza A virus / physiology
  • Influenza, Human / genetics*
  • Inheritance Patterns / genetics*
  • Interferons / metabolism
  • Loss of Function Mutation / genetics
  • Lung / pathology
  • Male
  • Mutation, Missense / genetics
  • Pneumonia / genetics*
  • Poly I-C / pharmacology
  • Protein Transport
  • Toll-Like Receptor 3 / deficiency*

Substances

  • TLR3 protein, human
  • Toll-Like Receptor 3
  • Interferons
  • Poly I-C