The Predicted Splicing Variant c.11+5G>A in RPE65 Leads to a Reduction in mRNA Expression in a Cell-Specific Manner

Cells. 2022 Nov 17;11(22):3640. doi: 10.3390/cells11223640.

Abstract

Pathogenic variants in RPE65 lead to retinal diseases, causing a vision impairment. In this work, we investigated the pathomechanism behind the frequent RPE65 variant, c.11+5G>A. Previous in silico predictions classified this change as a splice variant. Our prediction using novel software's suggested a 124-nt exon elongation containing a premature stop codon. This elongation was validated using midigenes-based approaches. Similar results were observed in patient-derived induced pluripotent stem cells (iPSC) and photoreceptor precursor cells. However, the splicing defect in all cases was detected at low levels and thereby does not fully explain the recessive condition of the resulting disease. Long-read sequencing discarded other rearrangements or variants that could explain the diseases. Subsequently, a more relevant model was employed: iPSC-derived retinal pigment epithelium (RPE) cells. In patient-derived iPSC-RPE cells, the expression of RPE65 was strongly reduced even after inhibiting a nonsense-mediated decay, contradicting the predicted splicing defect. Additional experiments demonstrated a cell-specific gene expression reduction due to the presence of the c.11+5G>A variant. This decrease also leads to the lack of the RPE65 protein, and differences in size and pigmentation between the patient and control iPSC-RPE. Altogether, our data suggest that the c.11+5G>A variant causes a cell-specific defect in the expression of RPE65 rather than the anticipated splicing defect which was predicted in silico.

Keywords: Leber congenital amaurosis; RPE65 gene; cell-specific defects; iPSC-derived models; induced pluripotent stem cells (iPSCs); inherited retinal diseases; retinal pigment epithelium (RPE).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Exons / genetics
  • Humans
  • Induced Pluripotent Stem Cells* / metabolism
  • RNA Splicing* / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Retinal Pigment Epithelium / metabolism

Substances

  • RNA, Messenger

Grants and funding

This research was funded by the Foundation Fighting Blindness USA Project Program Award, grant no. PPA-0517–0717-RAD (to F.P.M.C., R.W.J.C., S.R. and A.G.). Proteomic studies were supported the NWO ZonMw medium investment grant no. 9118025. The funding organizations provided unrestricted grants and had no role in the design or conduct of this research.