Single amino acid charge switch defines clinically distinct proline-serine-threonine phosphatase-interacting protein 1 (PSTPIP1)-associated inflammatory diseases

J Allergy Clin Immunol. 2015 Nov;136(5):1337-45. doi: 10.1016/j.jaci.2015.04.016. Epub 2015 May 27.

Abstract

Background: Hyperzincemia and hypercalprotectinemia (Hz/Hc) is a distinct autoinflammatory entity involving extremely high serum concentrations of the proinflammatory alarmin myeloid-related protein (MRP) 8/14 (S100A8/S100A9 and calprotectin).

Objective: We sought to characterize the genetic cause and clinical spectrum of Hz/Hc.

Methods: Proline-serine-threonine phosphatase-interacting protein 1 (PSTPIP1) gene sequencing was performed in 14 patients with Hz/Hc, and their clinical phenotype was compared with that of 11 patients with pyogenic arthritis, pyoderma gangrenosum, and acne (PAPA) syndrome. PSTPIP1-pyrin interactions were analyzed by means of immunoprecipitation and Western blotting. A structural model of the PSTPIP1 dimer was generated. Cytokine profiles were analyzed by using the multiplex immunoassay, and MRP8/14 serum concentrations were analyzed by using an ELISA.

Results: Thirteen patients were heterozygous for a missense mutation in the PSTPIP1 gene, resulting in a p.E250K mutation, and 1 carried a mutation resulting in p.E257K. Both mutations substantially alter the electrostatic potential of the PSTPIP1 dimer model in a region critical for protein-protein interaction. Patients with Hz/Hc have extremely high MRP8/14 concentrations (2045 ± 1300 μg/mL) compared with those with PAPA syndrome (116 ± 74 μg/mL) and have a distinct clinical phenotype. A specific cytokine profile is associated with Hz/Hc. Hz/Hc mutations altered protein binding of PSTPIP1, increasing interaction with pyrin through phosphorylation of PSTPIP1.

Conclusion: Mutations resulting in charge reversal in the y-domain of PSTPIP1 (E→K) and increased interaction with pyrin cause a distinct autoinflammatory disorder defined by clinical and biochemical features not found in patients with PAPA syndrome, indicating a unique genotype-phenotype correlation for mutations in the PSTPIP1 gene. This is the first inborn autoinflammatory syndrome in which inflammation is driven by uncontrolled release of members of the alarmin family.

Keywords: Hyperzincemia and hypercalprotectinemia; S100 proteins; autoinflammation; calprotectin; genotype; myeloid-related protein 8/14; phenotype; proline-serine-threonine phosphatase-interacting protein 1; pyogenic arthritis, pyoderma gangrenosum, and acne syndrome; zinc.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Adolescent
  • Alarmins / genetics
  • Alarmins / metabolism
  • Calgranulin A / genetics
  • Calgranulin A / metabolism
  • Child
  • Cytokines / metabolism
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • Female
  • Genotype
  • Humans
  • Leukocyte L1 Antigen Complex / genetics
  • Leukocyte L1 Antigen Complex / metabolism*
  • Male
  • Metal Metabolism, Inborn Errors / genetics
  • Metal Metabolism, Inborn Errors / immunology*
  • Mutation, Missense / genetics
  • Phenotype
  • Phosphorylation
  • Protein Binding / genetics
  • Protein Interaction Maps / genetics
  • Protein Multimerization
  • Pyrin
  • Young Adult

Substances

  • Adaptor Proteins, Signal Transducing
  • Alarmins
  • Calgranulin A
  • Cytokines
  • Cytoskeletal Proteins
  • Leukocyte L1 Antigen Complex
  • MEFV protein, human
  • PSTPIP1 protein, human
  • Pyrin

Supplementary concepts

  • Hyperzincemia and Hypercalprotectinemia