The bestrophin mutation A243V, linked to adult-onset vitelliform macular dystrophy, impairs its chloride channel function

Invest Ophthalmol Vis Sci. 2006 Nov;47(11):4956-61. doi: 10.1167/iovs.06-0524.

Abstract

Purpose: It has been proposed that Best vitelliform macular dystrophy (BVMD) is caused by dysfunction in the Cl(-) channel function of human bestrophin-1 (hBest1), but some patients with BVMD who have the hBest1 A243V mutation have normal electro-oculograms, suggesting that this mutation may not affect Cl(-) channel function. The purpose of this study was to determine whether the A243V mutation affects the Cl(-) channel function of hBest1.

Methods: Wild-type alanine at position 243 was changed to valine by PCR-based mutagenesis. Wild-type (WT) and A243V hBest1 were transfected into HEK-293 cells, and Cl(-) currents were measured with the whole-cell patch-clamp technique. The trafficking of proteins to the plasma membrane was tested by cell-surface biotinylation.

Results: WT hBest1 induced Ca(2+)-activated Cl(-) currents in HEK cells that were >1 nA in amplitude. The currents produced by the A243V mutant, however, were only approximately 10% as large as WT. This was not due to the inability of the A243V mutant to reach the plasma membrane, as shown by cell-surface biotinylation. The A243V mutation changed channel anion selectivity. The WT current exhibited a relative permeability P(X)/P(Cl) order of SCN(-) > or = I(-) > or = NO(3)(-) > Br(-) > Cl(-) > HCO(3)(-) and a relative conductance G(X)/G(Cl) order of NO(3)(-) > SCN(-) > I(-) > or = Br(-) > or = Cl(-) > HCO(3)(-). However, the A243V current exhibited different sequences: P(X)/P(Cl) was SCN(-) > NO(3)(-) > I(-) > Br(-) > Cl(-) > HCO(3)(-) and G(X)/G(Cl) was SCN(-) > NO(3)(-) > or = I(-) > or = Br(-) > Cl(-) > HCO(3)(-). Unlike several other hBest1 mutations that have dominant-negative effects on wild-type channels, the A243V-mutation did not influence the wild-type current when A243V and WT hBest1 were transfected together.

Conclusions: The disease-causing A243V mutation is associated with altered hBest1 Cl(-) channel activity. The absence of a dominant negative effect of A243V is consistent with the more mild symptoms associated with this mutation. These results are interpreted in terms of the hypotheses that bestrophins are Cl(-) channels and regulators of Ca signaling.

Publication types

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

MeSH terms

  • Bestrophins
  • Biotinylation
  • Cell Membrane
  • Chloride Channels / metabolism*
  • Eye Proteins / genetics*
  • Gene Expression
  • Humans
  • Kidney / embryology
  • Macular Degeneration / genetics*
  • Macular Degeneration / metabolism
  • Membrane Proteins / metabolism
  • Mutagenesis, Site-Directed
  • Patch-Clamp Techniques
  • Point Mutation*
  • Transfection

Substances

  • BEST1 protein, human
  • Bestrophins
  • CLCA1 protein, human
  • Chloride Channels
  • Eye Proteins
  • Membrane Proteins