Corneal fibrosis abrogation by a localized AAV-mediated inhibitor of differentiation 3 (Id3) gene therapy in rabbit eyes in vivo

Mol Ther. 2022 Oct 5;30(10):3257-3269. doi: 10.1016/j.ymthe.2022.06.018. Epub 2022 Jul 2.

Abstract

Previously we found that inhibitor of differentiation 3 (Id3) gene, a transcriptional repressor, efficiently inhibits corneal keratocyte differentiation to myofibroblasts in vitro. This study evaluated the potential of adeno-associated virus 5 (AAV5)-mediated Id3 gene therapy to treat corneal scarring using an established rabbit in vivo disease model. Corneal scarring/fibrosis in rabbit eyes was induced by alkali trauma, and 24 h thereafter corneas were administered with either balanced salt solution AAV5-naked vector, or AAV5-Id3 vector (n = 6/group) via an optimized reported method. Therapeutic effects of AAV5-Id3 gene therapy on corneal pathology and ocular health were evaluated with clinical, histological, and molecular techniques. Localized AAV5-Id3 gene therapy significantly inhibited corneal fibrosis/haze clinically from 2.7 to 0.7 on the Fantes scale in live animals (AAV5-naked versus AAV5-Id3; p < 0.001). Furthermore, AAV5-Id3 treatment significantly reduced profibrotic gene mRNA levels: α-smooth muscle actin (α-SMA) (2.8-fold; p < 0.001), fibronectin (3.2-fold; p < 0.001), collagen I (0.8-fold; p < 0.001), and collagen III (1.4-fold; p < 0.001), as well as protein levels of α-SMA (23.8%; p < 0.001) and collagens (1.8-fold; p < 0.001). The anti-fibrotic activity of AAV5-Id3 is attributed to reduced myofibroblast formation by disrupting the binding of E-box proteins to the promoter of α-SMA, a transforming growth factor-β signaling downstream target gene. In conclusion, these results indicate that localized AAV5-Id3 delivery in stroma caused no clinically relevant ocular symptoms or corneal cellular toxicity in the rabbit eyes.

Keywords: AAV5; Id3; alkali injury; corneal fibrosis; gene therapy; helix-loop-helix; inhibitor of differentiation 3.

Publication types

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

MeSH terms

  • Actins / genetics
  • Alkalies
  • Animals
  • Cicatrix / pathology
  • Cicatrix / therapy
  • Cornea
  • Corneal Diseases* / genetics
  • Corneal Diseases* / therapy
  • Corneal Injuries* / pathology
  • Corneal Injuries* / therapy
  • Corneal Opacity* / pathology
  • Corneal Opacity* / therapy
  • Dependovirus
  • Fibronectins / genetics
  • Fibrosis
  • Genetic Therapy / methods
  • RNA, Messenger
  • Rabbits
  • Transforming Growth Factors / genetics

Substances

  • Actins
  • Alkalies
  • Fibronectins
  • RNA, Messenger
  • Transforming Growth Factors

Supplementary concepts

  • Adeno-associated virus-5