Small Molecules Restore Bestrophin 1 Expression and Function of Both Dominant and Recessive Bestrophinopathies in Patient-Derived Retinal Pigment Epithelium

Invest Ophthalmol Vis Sci. 2020 May 11;61(5):28. doi: 10.1167/iovs.61.5.28.

Abstract

Purpose: Bestrophinopathies are a group of untreatable inherited retinal dystrophies caused by mutations in the retinal pigment epithelium (RPE) Cl- channel bestrophin 1. We tested whether sodium phenylbutyrate (4PBA) could rescue the function of mutant bestrophin 1 associated with autosomal dominant and recessive disease. We then sought analogues of 4PBA with increased potency and determined the mode of action for 4PBA and a lead compound 2-naphthoxyacetic acid (2-NOAA). Lastly, we tested if 4PBA and 2-NOAA could functionally rescue bestrophin 1 function in RPE generated from induced pluripotent stem cells (iPSC-RPEs) derived from patients with a dominant or recessive bestrophinopathy.

Methods: Global and plasma membrane expression was determined by Western blot and immunofluorescent microscopy, respectively. The effect of 4PBA and 2-NOAA on transcription was measured by quantitative RT-PCR and the rate of protein turnover by cycloheximide chase and Western blot. Channel function was measured by whole-cell patch clamp.

Results: 4PBA and 2-NOAA can rescue the global and membrane expression of mutant bestrophin 1 associated with autosomal dominant disease (Best vitelliform macular dystrophy [BVMD]) and autosome recessive bestrophinopathy (ARB), and these small molecules have different modes of action. Both 4PBA and 2-NOAA significantly increased the channel function of mutant BVMD and ARB bestrophin 1 in HEK293T and iPSC-RPE cells derived from patients with BVMD and ARB. For 4PBA, the increased mutant channel function in BVMD and ARB iPSC-RPE was equal to that of wild-type iPSC-RPE bestrophin 1.

Conclusions: The restoration of bestrophin 1 function in patient-derived RPE confirms the US Food and Drug Administration-approved drug 4PBA as a promising therapeutic treatment for bestrophinopathies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Bestrophins / genetics*
  • Blotting, Western
  • Cell Membrane / metabolism
  • Chloride Channels / metabolism
  • Cycloheximide / pharmacology
  • Electrophoresis, Polyacrylamide Gel
  • Eye Diseases, Hereditary / drug therapy*
  • Eye Diseases, Hereditary / genetics
  • Eye Diseases, Hereditary / metabolism
  • Gene Expression Regulation / physiology*
  • Genes, Recessive
  • Glycolates / pharmacology*
  • HEK293 Cells / drug effects
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Microscopy, Fluorescence
  • Patch-Clamp Techniques
  • Phenylbutyrates / pharmacology*
  • Real-Time Polymerase Chain Reaction
  • Retinal Diseases / drug therapy*
  • Retinal Diseases / genetics
  • Retinal Diseases / metabolism
  • Retinal Pigment Epithelium / drug effects*
  • Retinal Pigment Epithelium / metabolism
  • Transfection

Substances

  • Antineoplastic Agents
  • BEST1 protein, human
  • Bestrophins
  • Chloride Channels
  • Glycolates
  • Phenylbutyrates
  • 2-naphthoxyacetic acid
  • 4-phenylbutyric acid
  • Cycloheximide

Supplementary concepts

  • Bestrophinopathy