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Photooxidation mediated by 11-cis and all-trans retinal in single isolated mouse rod photoreceptors

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Abstract

Retinal, the vitamin A aldehyde, is a potent photosensitizer that plays a major role in light-induced damage to vertebrate photoreceptors. 11-Cis retinal is the light-sensitive chromophore of rhodopsin, the photopigment of vertebrate rod photoreceptors. It is isomerized by light to all-trans, activating rhodopsin and beginning the process of light detection. All-trans retinal is released by activated rhodopsin, allowing its regeneration by fresh 11-cis retinal continually supplied to photoreceptors. The released all-trans retinal is reduced to all-trans retinol in a reaction using NADPH. We have examined the photooxidation mediated by 11-cis and all-trans retinal in single living rod photoreceptors isolated from mouse retinas. Photooxidation was measured with fluorescence imaging from the oxidation of internalized BODIPY C11, a fluorescent dye whose fluorescence changes upon oxidation. We found that photooxidation increased with the concentration of exogenously added 11-cis or all-trans retinal to metabolically compromised rod outer segments that lacked NADPH supply. In dark-adapted metabolically intact rod outer segments with access to NADPH, there was no significant increase in photooxidation following exposure of the cell to light, but there was significant increase following addition of exogenous 11-cis retinal. The results indicate that both 11-cis and all-trans retinal can mediate light-induced damage in rod photoreceptors. In metabolically intact cells, the removal of the all-trans retinal generated by light through its reduction to retinol minimizes all-trans retinal-mediated photooxidation. However, because the enzymatic machinery of the rod outer segment cannot remove 11-cis retinal, 11-cis-retinal-mediated photooxidation may play a significant role in light-induced damage to photoreceptor cells.

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Abbreviations

BSA:

Bovine serum albumin

bROS:

Broken off rod outer segment(s)

BODIPY C11:

BODIPY 581/591 undecanoic acid

MDA:

Malondialdehyde

TBA:

Thiobarbituric acid

TBARS:

Thiobarbituric acid reactive species

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Authors and Affiliations

  1. Department of Ophthalmology, Medical University of South Carolina, 167 Ashley Avenue, Charleston, SC, 29425, USA

    Chunhe Chen, Masahiro Kono & Yiannis Koutalos

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  1. Chunhe Chen
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  2. Masahiro Kono
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Correspondence to Yiannis Koutalos.

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Chen, C., Kono, M. & Koutalos, Y. Photooxidation mediated by 11-cis and all-trans retinal in single isolated mouse rod photoreceptors. Photochem Photobiol Sci 19, 1300–1307 (2020). https://doi.org/10.1039/d0pp00060d

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