Life-Threatening Enterovirus 71 Encephalitis in Unrelated Children with Autosomal Dominant TLR3 Deficiency

J Clin Immunol. 2022 Apr;42(3):606-617. doi: 10.1007/s10875-021-01170-9. Epub 2022 Jan 18.

Abstract

Purpose: Enterovirus A71 (EV71) causes a broad spectrum of childhood diseases, ranging from asymptomatic infection or self-limited hand-foot-and-mouth disease (HFMD) to life-threatening encephalitis. The molecular mechanisms underlying these different clinical presentations remain unknown. We hypothesized that EV71 encephalitis in children might reflect an intrinsic host single-gene defect of antiviral immunity. We searched for mutations in the toll-like receptor 3 (TLR3) gene. Such mutations have already been identified in children with herpes simplex virus encephalitis (HSE).

Methods: We sequenced TLR3 and assessed the impact of the mutations identified. We tested dermal fibroblasts from a patient with EV71 encephalitis and a TLR3 mutation and other patients with known genetic defects of TLR3 or related genes, assessing the response of these cells to TLR3 agonist poly(I:C) stimulation and EV71 infection.

Results: Three children with EV71 encephalitis were heterozygous for rare mutations-TLR3 W769X, E211K, and R867Q-all of which were shown to affect TLR3 function. Furthermore, fibroblasts from the patient heterozygous for the W769X mutation displayed an impaired, but not abolished, response to poly(I:C). We found that TLR3-deficient and TLR3-heterozygous W769X fibroblasts were highly susceptible to EV71 infection.

Conclusions: Autosomal dominant TLR3 deficiency may underlie severe EV71 infection with encephalitis. Human TLR3 immunity is essential to protect the central nervous system against HSV-1 and EV71. Children with severe EV71 infections, such as encephalitis in particular, should be tested for inborn errors of TLR3 immunity.

Keywords: Encephalitis; Enterovirus 71; Inborn error of immunity; Toll-like receptor 3.

MeSH terms

  • Cells, Cultured
  • Child
  • Encephalitis, Herpes Simplex* / diagnosis
  • Encephalitis, Herpes Simplex* / genetics
  • Encephalitis, Viral* / diagnosis
  • Encephalitis, Viral* / genetics
  • Enterovirus A, Human* / genetics
  • Enterovirus Infections* / diagnosis
  • Enterovirus Infections* / genetics
  • Enterovirus*
  • Humans
  • Poly I-C
  • Toll-Like Receptor 3 / genetics

Substances

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