Blue light regenerates functional visual pigments in mammals through a retinyl-phospholipid intermediate

Joanna J Kaylor,Tongzhou Xu,Gabriel H Travis,Gordon L Fain,Hayk Hakobyan,Avian Tsan,Norianne T Ingram

doi:10.1038/s41467-017-00018-4

Joanna J Kaylor, Tongzhou Xu + Show 5 more

Open Access

https://doi.org/10.1038/s41467-017-00018-4

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Abstract

The light absorbing chromophore in opsin visual pigments is the protonated Schiff base of 11-cis-retinaldehyde (11cRAL). Absorption of a photon isomerizes 11cRAL to all-trans-retinaldehyde (atRAL), briefly activating the pigment before it dissociates. Light sensitivity is restored when apo-opsin combines with another 11cRAL to form a new visual pigment. Conversion of atRAL to 11cRAL is carried out by enzyme pathways in neighboring cells. Here we show that blue (450-nm) light converts atRAL specifically to 11cRAL through a retinyl-phospholipid intermediate in photoreceptor membranes. The quantum efficiency of this photoconversion is similar to rhodopsin. Photoreceptor membranes synthesize 11cRAL chromophore faster under blue light than in darkness. Live mice regenerate rhodopsin more rapidly in blue light. Finally, whole retinas and isolated cone cells show increased photosensitivity following exposure to blue light. These results indicate that light contributes to visual-pigment renewal in mammalian rods and cones through a non-enzymatic process involving retinyl-phospholipids.

Highlights

The light absorbing chromophore in opsin visual pigments is the protonated Schiff base of 11-cis-retinaldehyde (11cRAL)
Rhodopsin and the cone opsin pigments require a continuous supply of visual chromophore to maintain photosensitivity in bright light
Estimates of the maximum turnover rates suggest that the visual cycles cannot keep up with the high rates of rhodopsin and cone-opsin photoisomerization occurring in daylight[36]

Summary

Introduction

The light absorbing chromophore in opsin visual pigments is the protonated Schiff base of 11-cis-retinaldehyde (11cRAL). Light perception in metazoans is mediated by two types of photosensitive cells, rhabdomeric and ciliary photoreceptors Both contain membranous structures filled with opsin pigments. Absorption of a second photon flips the atRAL back to 11cRAL, restoring light sensitivity through photoregeneration[1] For this reason, rhabdomeric opsins are called bistable pigments. Following photon absorption by a ciliary opsin, the resulting metarhodopsin I may absorb a second photon, converting the atRAL back to 11cRAL, and the pigment to its light sensitive state[3, 4]. We show that mammalian photoreceptors possess a mechanism for light-driven regeneration of opsin pigments, employing N-ret-PE as a light-sensitive intermediate This mechanism is distinct from both photoregeneration of bistable opsins in rhabdomeric photoreceptors and the enzymatic visual cycles in RPE and Müller cells of vertebrates

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