Severe influenza pneumonitis in children with inherited TLR3 deficiency

Hye Kyung Lim, Sarah X.L. Huang, Jie Chen, Gaspard Kerner, Olivier Gilliaux, Paul Bastard, Kerry Dobbs, Nicholas Hernandez, Nicolas Goudin, Mary L. Hasek, Eduardo Javier García Reino, Fabien G. Lafaille, Lazaro Lorenzo, Priya Luthra, Tatiana Kochetkov, Benedetta Bigio, Soraya Boucherit, Flore Rozenberg, Catherine Vedrinne, Michael D. KellerYuval Itan, Adolfo García-Sastre, Marie Celard, Jordan S. Orange, Michael J. Ciancanelli, Isabelle Meyts, Qian Zhang, Laurent Abel, Luigi D. Notarangelo, Hans Willem Snoeck, Jean Laurent Casanova, Shen Ying Zhang

Research output: Contribution to journalArticlepeer-review

141 Scopus citations

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 IFNα2b 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.

Original languageEnglish
Pages (from-to)2038-2056
Number of pages19
JournalJournal of Experimental Medicine
Volume216
Issue number9
DOIs
StatePublished - 1 Sep 2019

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