Hypomorphic nuclear factor-kappaB essential modulator mutation database and reconstitution system identifies phenotypic and immunologic diversity

J Allergy Clin Immunol. 2008 Dec;122(6):1169-1177.e16. doi: 10.1016/j.jaci.2008.08.018. Epub 2008 Oct 11.

Abstract

Background: Human hypomorphic nuclear factor-kappaB essential modulator (NEMO) mutations cause diverse clinical and immunologic phenotypes, but understanding of their scope and mechanistic links to immune function and genotype is incomplete.

Objective: We created and analyzed a database of hypomorphic NEMO mutations to determine the spectrum of phenotypes and their associated genotypes and sought to establish a standardized NEMO reconstitution system to obtain mechanistic insights.

Methods: Phenotypes of 72 individuals with NEMO mutations were compiled. NEMO L153R and C417R were investigated further in a reconstitution system. TNF-alpha or Toll-like receptor (TLR)-5 signals were evaluated for nuclear factor-kappaB activation, programmed cell death, and A20 gene expression.

Results: Thirty-two different mutations were identified; 53% affect the zinc finger domain. Seventy-seven percent were associated with ectodermal dysplasia, 86% with serious pyogenic infection, 39% with mycobacterial infection, 19% with serious viral infection, and 23% with inflammatory diseases. Thirty-six percent of individuals died at a mean age of 6.4 years. CD40, IL-1, TNF-alpha, TLR, and T-cell receptor signals were impaired in 15 of 16 (94%), 6 of 7 (86%), 9 of 11 (82%), 9 of 14 (64%), and 7 of 18 (39%), respectively. Hypomorphism-reconstituted NEMO-deficient cells demonstrated partial restoration of NEMO functions. Although both L153R and C417R impaired TLR and TNF-alpha-induced NF-kappaB activation, L153R also increased TNF-alpha-induced programmed cell death with decreased A20 expression.

Conclusion: Distinct NEMO hypomorphs define specific disease and genetic characteristics. A reconstitution system can identify attributes of hypomorphisms independent of an individual's genetic background. Apoptosis susceptibility in L153R reconstituted cells defines a specific phenotype of this mutation that likely contributes to the excessive inflammation with which it is clinically associated.

Publication types

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

MeSH terms

  • Amino Acid Substitution
  • Apoptosis / genetics
  • CD40 Antigens / metabolism
  • DNA-Binding Proteins
  • Databases, Genetic*
  • Gene Expression Regulation / genetics
  • Genetic Complementation Test / methods
  • Genotype
  • Humans
  • I-kappa B Kinase / genetics*
  • I-kappa B Kinase / metabolism*
  • Immunologic Deficiency Syndromes / genetics*
  • Immunologic Deficiency Syndromes / metabolism*
  • Intracellular Signaling Peptides and Proteins
  • Jurkat Cells
  • Mutation, Missense*
  • NF-kappa B / metabolism
  • Nuclear Proteins / biosynthesis
  • Phenotype
  • Protein Structure, Tertiary / genetics
  • Receptors, Antigen, T-Cell / metabolism
  • Signal Transduction / genetics
  • Toll-Like Receptor 5 / metabolism
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • CD40 Antigens
  • DNA-Binding Proteins
  • IKBKG protein, human
  • Intracellular Signaling Peptides and Proteins
  • NF-kappa B
  • Nuclear Proteins
  • Receptors, Antigen, T-Cell
  • TLR5 protein, human
  • Toll-Like Receptor 5
  • Tumor Necrosis Factor-alpha
  • I-kappa B Kinase
  • TNFAIP3 protein, human
  • Tumor Necrosis Factor alpha-Induced Protein 3