The nanophthalmos protein TMEM98 inhibits MYRF self-cleavage and is required for eye size specification

PLoS Genet. 2020 Apr 1;16(4):e1008583. doi: 10.1371/journal.pgen.1008583. eCollection 2020 Apr.

Abstract

The precise control of eye size is essential for normal vision. TMEM98 is a highly conserved and widely expressed gene which appears to be involved in eye size regulation. Mutations in human TMEM98 are found in patients with nanophthalmos (very small eyes) and variants near the gene are associated in population studies with myopia and increased eye size. As complete loss of function mutations in mouse Tmem98 result in perinatal lethality, we produced mice deficient for Tmem98 in the retinal pigment epithelium (RPE), where Tmem98 is highly expressed. These mice have greatly enlarged eyes that are very fragile with very thin retinas, compressed choroid and thin sclera. To gain insight into the mechanism of action we used a proximity labelling approach to discover interacting proteins and identified MYRF as an interacting partner. Mutations of MYRF are also associated with nanophthalmos. The protein is an endoplasmic reticulum-tethered transcription factor which undergoes autoproteolytic cleavage to liberate the N-terminal part which then translocates to the nucleus where it acts as a transcription factor. We find that TMEM98 inhibits the self-cleavage of MYRF, in a novel regulatory mechanism. In RPE lacking TMEM98, MYRF is ectopically activated and abnormally localised to the nuclei. Our findings highlight the importance of the interplay between TMEM98 and MYRF in determining the size of the eye.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Electroretinography
  • Eye / anatomy & histology*
  • Eye / metabolism*
  • Eye Abnormalities / genetics
  • Female
  • Gene Deletion
  • Loss of Function Mutation
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Knockout
  • Organ Size / genetics
  • Protein Binding
  • Protein Transport
  • Retinal Pigment Epithelium / abnormalities
  • Retinal Pigment Epithelium / metabolism
  • Retinaldehyde / metabolism
  • Transcription Factors / antagonists & inhibitors*
  • Transcription Factors / chemistry
  • Transcription Factors / metabolism

Substances

  • Membrane Proteins
  • Tmem98 protein, mouse
  • Transcription Factors
  • myelin gene regulatory factor, mouse
  • Retinaldehyde