Multisystem inflammation and susceptibility to viral infections in human ZNFX1 deficiency

J Allergy Clin Immunol. 2021 Aug;148(2):381-393. doi: 10.1016/j.jaci.2021.03.045. Epub 2021 Apr 17.

Abstract

Background: Recognition of viral nucleic acids is one of the primary triggers for a type I interferon-mediated antiviral immune response. Inborn errors of type I interferon immunity can be associated with increased inflammation and/or increased susceptibility to viral infections as a result of dysbalanced interferon production. NFX1-type zinc finger-containing 1 (ZNFX1) is an interferon-stimulated double-stranded RNA sensor that restricts the replication of RNA viruses in mice. The role of ZNFX1 in the human immune response is not known.

Objective: We studied 15 patients from 8 families with an autosomal recessive immunodeficiency characterized by severe infections by both RNA and DNA viruses and virally triggered inflammatory episodes with hemophagocytic lymphohistiocytosis-like disease, early-onset seizures, and renal and lung disease.

Methods: Whole exome sequencing was performed on 13 patients from 8 families. We investigated the transcriptome, posttranscriptional regulation of interferon-stimulated genes (ISGs) and predisposition to viral infections in primary cells from patients and controls stimulated with synthetic double-stranded nucleic acids.

Results: Deleterious homozygous and compound heterozygous ZNFX1 variants were identified in all 13 patients. Stimulation of patient-derived primary cells with synthetic double-stranded nucleic acids was associated with a deregulated pattern of expression of ISGs and alterations in the half-life of the mRNA of ISGs and also associated with poorer clearance of viral infections by monocytes.

Conclusion: ZNFX1 is an important regulator of the response to double-stranded nucleic acids stimuli following viral infections. ZNFX1 deficiency predisposes to severe viral infections and a multisystem inflammatory disease.

Keywords: HLH-like disease; ZNFX1; brain calcification; interstitial lung disease; leukoencephalopathy; susceptibility to viral infections; thrombotic microangiopathy; type I interferon; virally induced hepatitis.

Publication types

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

MeSH terms

  • Antigens, Neoplasm / genetics*
  • Antigens, Neoplasm / immunology
  • Child
  • Child, Preschool
  • Exome Sequencing*
  • Female
  • Genetic Predisposition to Disease*
  • Humans
  • Infant
  • Inflammation / diagnostic imaging
  • Inflammation / genetics
  • Inflammation / immunology
  • Male
  • Primary Immunodeficiency Diseases / diagnostic imaging
  • Primary Immunodeficiency Diseases / genetics
  • Primary Immunodeficiency Diseases / immunology*
  • Virus Diseases / diagnostic imaging
  • Virus Diseases / genetics*
  • Virus Diseases / immunology

Substances

  • Antigens, Neoplasm
  • ZNFX1 protein, human