Involvement of the same TNFR1 residue in mendelian and multifactorial inflammatory disorders

PLoS One. 2013 Jul 24;8(7):e69757. doi: 10.1371/journal.pone.0069757. Print 2013.

Abstract

Objectives: TNFRSF1A is involved in an autosomal dominant autoinflammatory disorder called TNFR-associated periodic syndrome (TRAPS). Most TNFRSF1A mutations are missense changes and, apart from those affecting conserved cysteines, their deleterious effect remains often questionable. This is especially true for the frequent R92Q mutation, which might not be responsible for TRAPS per se but represents a susceptibility factor to multifactorial inflammatory disorders. This study investigates TRAPS pathophysiology in a family exceptional by its size (13 members) and compares the consequences of several mutations affecting arginine 92.

Methods: TNFRSF1A screening was performed by PCR-sequencing. Comparison of the 3-dimensional structure and electrostatic properties of wild-type and mutated TNFR1 proteins was performed by in silico homology modeling. TNFR1 expression was assessed by FACS analysis, western blotting and ELISA in lysates and supernatants of HEK293T cells transiently expressing wild-type and mutated TNFR1.

Results: A TNFRSF1A heterozygous missense mutation, R92W (c.361C>T), was shown to perfectly segregate with typical TRAPS manifestations within the family investigated (p<5.10(-4)). It was associated with very high disease penetrance (0.9). Prediction of its impact on the protein structure revealed local conformational changes and alterations of the receptor electrostatic properties. R92W also impairs the TNFR1 expression at the cell surface and the levels of soluble receptor. Similar results were obtained with R92P, another mutation previously identified in a very small familial form with incomplete penetrance and variable expressivity. In contrast, TNFR1-R92Q behaves like the wild-type receptor.

Conclusions: These data demonstrate the pathogenicity of a mutation affecting arginine 92, a residue whose involvement in inflammatory disorders is deeply debated. Combined with previous reports on arginine 92 mutations, this study discloses an unusual situation in which different amino acid substitutions at the same position in the protein are associated with a clinical spectrum bridging Mendelian to multifactorial conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Arginine / chemistry
  • Arginine / genetics
  • Blotting, Western
  • Child
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Flow Cytometry
  • Genotype
  • Hereditary Autoinflammatory Diseases / genetics
  • Hereditary Autoinflammatory Diseases / metabolism*
  • Humans
  • Male
  • Mutation, Missense / genetics
  • Pedigree
  • Polymerase Chain Reaction
  • Protein Transport
  • Receptors, Tumor Necrosis Factor, Type I / chemistry
  • Receptors, Tumor Necrosis Factor, Type I / genetics
  • Receptors, Tumor Necrosis Factor, Type I / metabolism*
  • Static Electricity
  • Young Adult

Substances

  • Receptors, Tumor Necrosis Factor, Type I
  • Arginine

Grants and funding

This work was supported by grants from the Institut national de la santé et de la recherche médicale (INSERM); and the Université Pierre et Marie Curie - Paris 6. The funders had no rule in study design, data collection and analysis, decision to publish, or preparation of the manuscript.