Long-term rescue of cone photoreceptor degeneration in retinitis pigmentosa 2 (RP2)-knockout mice by gene replacement therapy

Hum Mol Genet. 2015 Nov 15;24(22):6446-58. doi: 10.1093/hmg/ddv354. Epub 2015 Sep 10.

Abstract

Retinal neurodegenerative diseases are especially attractive targets for gene replacement therapy, which appears to be clinically effective for several monogenic diseases. X-linked forms of retinitis pigmentosa (XLRP) are relatively severe blinding disorders, resulting from progressive photoreceptor dysfunction primarily caused by mutations in RPGR or RP2 gene. With a goal to develop gene therapy for the XLRP-RP2 disease, we first performed detailed characterization of the Rp2-knockout (Rp2-KO) mice and observed early-onset cone dysfunction, which was followed by progressive cone degeneration, mimicking cone vision impairment in XLRP patients. The mice also exhibited distinct and significantly delayed falling phase of photopic b-wave of electroretinogram (ERG). Concurrently, we generated a self-complementary adeno-associated viral (AAV) vector carrying human RP2-coding sequence and demonstrated its ability to mediate stable RP2 protein expression in mouse photoreceptors. A long-term efficacy study was then conducted in Rp2-KO mice following AAV-RP2 vector administration. Preservation of cone function was achieved with a wide dose range over 18-month duration, as evidenced by photopic ERG and optomotor tests. The slower b-wave kinetics was also completely restored. Morphologically, the treatment preserved cone viability, corrected mis-trafficking of M-cone opsin and restored cone PDE6 expression. The therapeutic effect was achieved even in mice that received treatment at an advanced disease stage. The highest AAV-RP2 dose group demonstrated retinal toxicity, highlighting the importance of careful vector dosing in designing future human trials. The wide range of effective dose, a broad treatment window and long-lasting therapeutic effects should make the RP2 gene therapy attractive for clinical development.

Publication types

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

MeSH terms

  • Animals
  • Electroretinography
  • Eye Proteins / biosynthesis
  • Eye Proteins / genetics*
  • GTP-Binding Proteins
  • Genetic Diseases, X-Linked / genetics
  • Genetic Therapy / methods*
  • Genetic Vectors
  • HEK293 Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / biosynthesis
  • Intracellular Signaling Peptides and Proteins / genetics*
  • Membrane Proteins / biosynthesis
  • Membrane Proteins / genetics*
  • Mice
  • Mice, Knockout
  • Mutation
  • Pyrophosphatases / deficiency
  • Pyrophosphatases / genetics
  • Retinal Cone Photoreceptor Cells / metabolism
  • Retinal Cone Photoreceptor Cells / pathology
  • Retinal Cone Photoreceptor Cells / physiology*
  • Retinal Degeneration / genetics
  • Retinitis Pigmentosa / genetics*
  • Retinitis Pigmentosa / metabolism
  • Retinitis Pigmentosa / therapy*

Substances

  • Eye Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • RP2 protein, human
  • RP2 protein, mouse
  • GTP-Binding Proteins
  • Pyrophosphatases

Supplementary concepts

  • Retinal Cone Dystrophy 1
  • Retinitis Pigmentosa 2