Publication Date

5-21-2024

Journal

Nature Communications

DOI

10.1038/s41467-024-48639-w

PMID

38773095

PMCID

PMC11109262

PubMedCentral® Posted Date

5-21-2024

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

Animals, Actins, Mice, Retinitis Pigmentosa, Eye Proteins, Cilia, Humans, Retinal Photoreceptor Cell Outer Segment, Mice, Knockout, Mice, Inbred C57BL, Cell Membrane, Hereditary eye disease, Retinal diseases, Mechanisms of disease, Actin, Disease genetics

Abstract

As signalling organelles, cilia regulate their G protein-coupled receptor content by ectocytosis, a process requiring localised actin dynamics to alter membrane shape. Photoreceptor outer segments comprise an expanse of folded membranes (discs) at the tip of highly-specialised connecting cilia, into which photosensitive GPCRs are concentrated. Discs are shed and remade daily. Defects in this process, due to mutations, cause retinitis pigmentosa (RP). Whilst fundamental for vision, the mechanism of photoreceptor disc generation is poorly understood. Here, we show membrane deformation required for disc genesis is driven by dynamic actin changes in a process akin to ectocytosis. We show RPGR, a leading RP gene, regulates actin-binding protein activity central to this process. Actin dynamics, required for disc formation, are perturbed in Rpgr mouse models, leading to aborted membrane shedding as ectosome-like vesicles, photoreceptor death and visual loss. Actin manipulation partially rescues this, suggesting the pathway could be targeted therapeutically. These findings help define how actin-mediated dynamics control outer segment turnover.

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