A novel Dutch mutation in UNC13D reveals an essential role of the C2B domain in munc13-4 function

Pediatr Blood Cancer. 2012 Apr;58(4):598-605. doi: 10.1002/pbc.23253. Epub 2011 Jul 13.

Abstract

Background: UNC13D, encoding the protein munc13-4, is essential in intracellular trafficking and exocytosis of lytic granules. Mutations in this gene are associated with familial hemophagocytic lymphohistiocytosis type 3 (FHL3), a genetically heterogeneous, rare autosomal recessive immune disorder. How mutations affect function of munc13-4 is poorly understood. Since 2006 we genetically identified seven FHL patients with mutations in UNC13D.

Procedures: Here, we report for the first time a c.2695C>T (p.Arg899X) mutation in exon 28 of UNC13D in three young unrelated Dutch patients. The mutation causes a premature stop codon and encodes munc13-4(1-899), which lacks the C-terminal C2 domain. Genealogical research and haplotyping of the patient families demonstrated that a single ancestral founder introduced the mutation in the Netherlands. We then characterized the mutant protein phenotypically in cell biological and immunological assays.

Results: Munc13-4(1-899) was correctly targeted to CD63-positive secretory lysosomes, although its stability was reduced and dynamic turnover on the granule membrane became uncoupled from receptor signaling. In accord, and in contrast to wild-type munc13-4, ectopically expressed mutant failed to rescue degranulation in cells with silenced endogenous munc13-4.

Conclusions: The functional and clinical data showed that this novel Dutch founder mutation leads to severe early onset of FHL3 due to misfolding and degradation of munc13-4(1-899).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Degranulation / genetics
  • Cell Line, Tumor
  • Codon, Terminator*
  • Humans
  • Lymphohistiocytosis, Hemophagocytic* / genetics
  • Lymphohistiocytosis, Hemophagocytic* / metabolism
  • Lysosomes / genetics
  • Lysosomes / metabolism
  • Membrane Proteins* / genetics
  • Membrane Proteins* / metabolism
  • Netherlands
  • Point Mutation*
  • Protein Folding*
  • Protein Structure, Tertiary
  • Proteins* / genetics
  • Proteins* / metabolism
  • Proteolysis*
  • Rats
  • Tetraspanin 30 / genetics
  • Tetraspanin 30 / metabolism

Substances

  • CD63 protein, human
  • Cd63 protein, rat
  • Codon, Terminator
  • Membrane Proteins
  • Proteins
  • Tetraspanin 30
  • UNC13D protein, human
  • Unc13d protein, rat