Dual ABCA4-AAV Vector Treatment Reduces Pathogenic Retinal A2E Accumulation in a Mouse Model of Autosomal Recessive Stargardt Disease

Hum Gene Ther. 2019 Nov;30(11):1361-1370. doi: 10.1089/hum.2019.132. Epub 2019 Sep 30.

Abstract

Autosomal recessive Stargardt disease is the most common inherited macular degeneration in humans. It is caused by mutations in the retina-specific ATP binding cassette transporter A4 (ABCA4) that is essential for the clearance of all-trans-retinal from photoreceptor cells. Loss of this function results in the accumulation of toxic bisretinoids in the outer segment disk membranes and their subsequent transfer into adjacent retinal pigment epithelium (RPE) cells. This ultimately leads to the Stargardt disease phenotype of increased retinal autofluorescence and progressive RPE and photoreceptor cell loss. Adeno-associated virus (AAV) vectors have been widely used in gene therapeutic applications, but their limited cDNA packaging capacity of ∼4.5 kb has impeded their use for transgenes exceeding this limit. AAV dual vectors were developed to overcome this size restriction. In this study, we have evaluated the in vitro expression of ABCA4 using three options: overlap, transplicing, and hybrid ABCA4 dual vector systems. The hybrid system was the most efficient of these dual vector alternatives and used to express the full-length ABCA4 in Abca4-/- mice. The full-length ABCA4 protein correctly localized to photoreceptor outer segments. Moreover, treatment of Abca4-/- mice with this ABCA4 hybrid dual vector system resulted in a reduced accumulation of the lipofuscin/N-retinylidene-N-retinylethanolamine (A2E) autofluorescence in vivo, and retinal A2E quantification supported these findings. These results show that the hybrid AAV dual vector option is both safe and therapeutic in mice, and the delivered ABCA4 transgene is functional and has a significant effect on reducing A2E accumulation in the Abca4-/- mouse model of Stargardt disease.

Keywords: AAV dual vectors; AAV hybrid vectors; Stargardt disease.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • ATP-Binding Cassette Transporters / genetics*
  • ATP-Binding Cassette Transporters / therapeutic use*
  • Animals
  • Dependovirus / genetics*
  • Disease Models, Animal
  • Fluorescence
  • Fundus Oculi
  • Genes, Recessive*
  • Genetic Vectors / metabolism*
  • HEK293 Cells
  • Humans
  • Mice, Inbred C57BL
  • Retina / metabolism
  • Retina / pathology*
  • Retinoids / metabolism
  • Stargardt Disease / genetics*
  • Stargardt Disease / therapy*

Substances

  • A2-E (N-retinylidene-N-retinylethanolamine)
  • ATP-Binding Cassette Transporters
  • Abca4 protein, mouse
  • Retinoids