A large-scale CRISPR screen reveals context-specific genetic regulation of retinal ganglion cell regeneration

Development. 2024 Aug 1;151(15):dev202754. doi: 10.1242/dev.202754. Epub 2024 Aug 12.

Abstract

Many genes are known to regulate retinal regeneration after widespread tissue damage. Conversely, genes controlling regeneration after limited cell loss, as per degenerative diseases, are undefined. As stem/progenitor cell responses scale to injury levels, understanding how the extent and specificity of cell loss impact regenerative processes is important. Here, transgenic zebrafish enabling selective retinal ganglion cell (RGC) ablation were used to identify genes that regulate RGC regeneration. A single cell multiomics-informed screen of 100 genes identified seven knockouts that inhibited and 11 that promoted RGC regeneration. Surprisingly, 35 out of 36 genes known and/or implicated as being required for regeneration after widespread retinal damage were not required for RGC regeneration. The loss of seven even enhanced regeneration kinetics, including the proneural factors neurog1, olig2 and ascl1a. Mechanistic analyses revealed that ascl1a disruption increased the propensity of progenitor cells to produce RGCs, i.e. increased 'fate bias'. These data demonstrate plasticity in the mechanism through which Müller glia convert to a stem-like state and context specificity in how genes function during regeneration. Increased understanding of how the regeneration of disease-relevant cell types is specifically controlled will support the development of disease-tailored regenerative therapeutics.

Keywords: Ascl1; CRISPR screen; Neural stem cell; Regeneration; Retina.

MeSH terms

  • Animals
  • Animals, Genetically Modified*
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • CRISPR-Cas Systems / genetics
  • Nerve Regeneration / genetics
  • Nerve Regeneration / physiology
  • Regeneration / genetics
  • Regeneration / physiology
  • Retina / cytology
  • Retina / metabolism
  • Retinal Ganglion Cells* / cytology
  • Retinal Ganglion Cells* / metabolism
  • Retinal Ganglion Cells* / physiology
  • Stem Cells / cytology
  • Stem Cells / metabolism
  • Transcription Factors
  • Zebrafish Proteins* / genetics
  • Zebrafish Proteins* / metabolism
  • Zebrafish* / genetics

Substances

  • Zebrafish Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • Ascl1a protein, zebrafish
  • Transcription Factors