BOR-syndrome-associated Eya1 mutations lead to enhanced proteasomal degradation of Eya1 protein

PLoS One. 2014 Jan 29;9(1):e87407. doi: 10.1371/journal.pone.0087407. eCollection 2014.

Abstract

Mutations in the human EYA1 gene have been associated with several human diseases including branchio-oto (BO) and branchio-oto-renal (BOR) syndrome, as well as congenital cataracts and ocular anterior segment anomalies. BOR patients suffer from severe malformations of the ears, branchial arches and kidneys. The phenotype of Eya1-heterozygous mice resembles the symptoms of human patients suffering from BOR syndrome. The Eya1 gene encodes a multifunctional protein that acts as a protein tyrosine phosphatase and a transcriptional coactivator. It has been shown that Eya1 interacts with Six transcription factors, which are also required for nuclear translocation of the Eya1 protein. We investigated the effects of seven disease-causing Eya1 missense mutations on Eya1 protein function, in particular cellular localization, ability to interact with Six proteins, and protein stability. We show here that the BOR-associated Eya1 missense mutations S454P, L472R, and L550P lead to enhanced proteasomal degradation of the Eya1 protein in mammalian cells. Moreover, Six proteins lead to a significant stabilization of Eya1, which is caused by Six-mediated protection from proteasomal degradation. In case of the mutant L550P, loss of interaction with Six proteins leads to rapid protein degradation. Our observations suggest that protein destabilization constitutes a novel disease causing mechanism for Eya1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Branchio-Oto-Renal Syndrome / genetics*
  • COS Cells
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Chlorocebus aethiops
  • Homeodomain Proteins / metabolism
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Mice
  • Mutation, Missense
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Proteasome Endopeptidase Complex / metabolism*
  • Protein Binding
  • Protein Stability
  • Protein Transport
  • Protein Tyrosine Phosphatases / genetics*
  • Protein Tyrosine Phosphatases / metabolism
  • Proteolysis
  • Ubiquitination

Substances

  • Homeodomain Proteins
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • Eya1 protein, mouse
  • Protein Tyrosine Phosphatases
  • Proteasome Endopeptidase Complex

Grants and funding

This work was supported by a grant from the Deutsche Forschungsgemeinschaft [SFB604, project C7 to C.E.]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.