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Elife 2023 Jul 14;12. doi: 10.7554/eLife.89160.
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Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure.

Lewis TR , Phan S , Castillo CM , Kim KY , Coppenrath K , Thomas W , Hao Y , Skiba NP , Horb ME , Ellisman MH , Arshavsky VY .

The first steps of vision take place within a stack of tightly packed disc-shaped membranes, or 'discs', located in the outer segment compartment of photoreceptor cells. In rod photoreceptors, discs are enclosed inside the outer segment and contain deep indentations in their rims called 'incisures'. The presence of incisures has been documented in a variety of species, yet their role remains elusive. In this study, we combined traditional electron microscopy with three-dimensional electron tomography to demonstrate that incisures are formed only after discs become completely enclosed. We also observed that, at the earliest stage of their formation, discs are not round as typically depicted but rather are highly irregular in shape and resemble expanding lamellipodia. Using genetically manipulated mice and frogs and measuring outer segment protein abundances by quantitative mass spectrometry, we further found that incisure size is determined by the molar ratio between peripherin-2, a disc rim protein critical for the process of disc enclosure, and rhodopsin, the major structural component of disc membranes. While a high perpherin-2 to rhodopsin ratio causes an increase in incisure size and structural complexity, a low ratio precludes incisure formation. Based on these data, we propose a model whereby normal rods express a modest excess of peripherin-2 over the amount required for complete disc enclosure in order to ensure that this important step of disc formation is accomplished. Once the disc is enclosed, the excess peripherin-2 incorporates into the rim to form an incisure.

PubMed ID: 37449984
PMC ID: PMC10361718
Article link: Elife
Grant support: [+]

Species referenced: Xenopus tropicalis Xenopus laevis
Genes referenced: prph prph2 prph2l rho rom1
GO keywords: photoreceptor cell development [+]
gRNAs referenced: prph2 gRNA6 prph2 gRNA7

Article Images: [+] show captions