Abstract
We have studied dark-adaptation at three levels in the eyes of the crustacean Mysis relicta over 2–3 weeks after exposing initially dark-adapted animals to strong white light: regeneration of 11-cis retinal through the retinoid cycle (by HPLC), restoration of native rhodopsin in photoreceptor membranes (by MSP), and recovery of eye photosensitivity (by ERG). We compare two model populations (“Sea”, Sp, and “Lake”, Lp) inhabiting, respectively, a low light and an extremely dark environment. 11-cis retinal reached 60–70% of the pre-exposure levels after 2 weeks in darkness in both populations. The only significant Lp/Sp difference in the retinoid cycle was that Lp had much higher levels of retinol, both basal and light-released. In Sp, rhodopsin restoration and eye photoresponse recovery parallelled 11-cis retinal regeneration. In Lp, however, even after 3 weeks only ca. 25% of the rhabdoms studied had incorporated new rhodopsin, and eye photosensitivity showed only incipient recovery from severe depression. The absorbance spectra of the majority of the Lp rhabdoms stayed constant around 490–500 nm, consistent with metarhodopsin II dominance. We conclude that sensitivity recovery of Sp eyes was rate-limited by the regeneration of 11-cis retinal, whilst that of Lp eyes was limited by inertia in photoreceptor membrane turnover.
Highlights
All visual pigments consist of a G-proteincoupled receptor protein covalently binding a lightsensitive cofactor, which is some form of retinal
The first event in vision is photoisomerization of the retinal from the 11-cis to the all-trans configuration, which triggers a sequence of very fast conformational changes of the opsin leading to the reasonably long-lived, G-proteinactivating form metarhodopsin II (MII) (Fain et al 2010)
In the c-opsins of the vertebrate ciliary photoreceptors, all-trans retinal soon detaches from MII, is reduced to retinol in the photoreceptor outer segment, and transported to the retinal pigment epithelium (RPE)
Summary
All visual pigments (rhodopsins) consist of a G-proteincoupled receptor protein (opsin) covalently binding a lightsensitive cofactor (the chromophore), which is some form of retinal. A necessary condition for complete recovery of photoreceptor light sensitivity in darkness is restoration of the full complement of native rhodopsin (R) with 11-cis retinal In both vertebrates and arthropods, this involves enzymatic conversion of all-trans to 11-cis retinoid through several steps, partly in cells other than the photoreceptors (e.g., Wang et al 2010; Kiser et al 2012). There, alltrans retinol is converted to 11-cis retinol in an enzymatic reaction chain, whereupon the 11-cis retinol is oxidized to retinal and delivered over the interphotoreceptor matrix to free opsins in the photoreceptor cells This visual cycle (or parts of it) may occur in Müller cells, or in the photoreceptors themselves, instead of the RPE (Wang and Kefalov 2011). It has been shown that visual-pigment renewal in mammalian photoreceptor membranes may occur through a non-enzymatic, light-driven process involving retinyl phospholipids (Kaylor et al 2017)
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