Heterozygous Truncating Variants in POMP Escape Nonsense-Mediated Decay and Cause a Unique Immune Dysregulatory Syndrome

Am J Hum Genet. 2018 Jun 7;102(6):1126-1142. doi: 10.1016/j.ajhg.2018.04.010. Epub 2018 May 24.

Abstract

The proteasome processes proteins to facilitate immune recognition and host defense. When inherently defective, it can lead to aberrant immunity resulting in a dysregulated response that can cause autoimmunity and/or autoinflammation. Biallelic or digenic loss-of-function variants in some of the proteasome subunits have been described as causing a primary immunodeficiency disease that manifests as a severe dysregulatory syndrome: chronic atypical neutrophilic dermatosis with lipodystrophy and elevated temperature (CANDLE). Proteasome maturation protein (POMP) is a chaperone for proteasome assembly and is critical for the incorporation of catalytic subunits into the proteasome. Here, we characterize and describe POMP-related autoinflammation and immune dysregulation disease (PRAID) discovered in two unrelated individuals with a unique constellation of early-onset combined immunodeficiency, inflammatory neutrophilic dermatosis, and autoimmunity. We also begin to delineate a complex genetic mechanism whereby de novo heterozygous frameshift variants in the penultimate exon of POMP escape nonsense-mediated mRNA decay (NMD) and result in a truncated protein that perturbs proteasome assembly by a dominant-negative mechanism. To our knowledge, this mechanism has not been reported in any primary immunodeficiencies, autoinflammatory syndromes, or autoimmune diseases. Here, we define a unique hypo- and hyper-immune phenotype and report an immune dysregulation syndrome caused by frameshift mutations that escape NMD.

Keywords: PID; POMP; POMP-related autoinflammation and immune dysregulation disease; PRAID; autoinflammatory syndrome; core particle proteasome 20S; dominant negative; interferonopathy; nonsense-mediated decay; primary immune deficiency.

Publication types

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

MeSH terms

  • Base Sequence
  • Cell Line
  • Endoplasmic Reticulum Stress
  • Exons / genetics
  • Family
  • Frameshift Mutation / genetics
  • Genetic Predisposition to Disease*
  • Heterozygote
  • Humans
  • Immunologic Deficiency Syndromes / genetics
  • Immunophenotyping
  • Infant, Newborn
  • Inflammation / pathology
  • Interferon Type I / metabolism
  • Male
  • Molecular Chaperones / genetics*
  • Mutant Proteins / metabolism
  • Mutation / genetics*
  • Nonsense Mediated mRNA Decay / genetics*
  • Phenotype
  • Proteasome Endopeptidase Complex / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Syndrome
  • Unfolded Protein Response

Substances

  • Interferon Type I
  • Molecular Chaperones
  • Mutant Proteins
  • RNA, Messenger
  • proteasome maturation protein
  • Proteasome Endopeptidase Complex