(Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial Cells

Docosahexaenoate is a cytoprotective ω-3 polyunsaturated lipid that is abundant in the retina and is essential for its function. Due to its six unsaturated double bonds, docosahexaenoate is highly susceptible to oxidation and the formation of products with photosensitizing properties. This study aim...

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Main Authors: Linda M. Bakker, Michael E. Boulton, Małgorzata B. Różanowska
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Antioxidants
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Online Access:https://www.mdpi.com/2076-3921/13/11/1428
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author Linda M. Bakker
Michael E. Boulton
Małgorzata B. Różanowska
author_facet Linda M. Bakker
Michael E. Boulton
Małgorzata B. Różanowska
author_sort Linda M. Bakker
collection DOAJ
description Docosahexaenoate is a cytoprotective ω-3 polyunsaturated lipid that is abundant in the retina and is essential for its function. Due to its six unsaturated double bonds, docosahexaenoate is highly susceptible to oxidation and the formation of products with photosensitizing properties. This study aimed to test on cultured human retinal pigment epithelial cells ARPE-19 the (photo)cytotoxic potential of partly oxidized docosahexaenoate and its effect on the formation of lipofuscin from phagocytosed photoreceptor outer segments (POSs). The results demonstrate that the cytoprotective effects of docosahexaenoate do not counteract the deleterious effects of its oxidation products, leading to the concentration-dependent loss of cell metabolic activity, which is exacerbated by concomitant exposure to visible light. Partly oxidized docosahexaenoate does not cause permeability of the cell plasma membrane but does cause apoptosis. While vitamin E can provide partial protection from the (photo)toxicity of partly oxidized docosahexaenoate, zeaxanthin undergoes rapid photodegradation and can exacerbate the (photo)toxicity. Feeding cells with POSs enriched in partly oxidized docosahexaenoate results in a greater accumulation of intracellular fluorescent lipofuscin than in cells fed POSs without the addition. In conclusion, partly oxidized docosahexaenoate increases the accumulation of lipofuscin-like intracellular deposits, is cytotoxic, and its toxicity increases during exposure to light. These effects may contribute to the increased progression of geographic atrophy observed after long-term supplementation with docosahexaenoate in age-related macular degeneration patients.
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spelling doaj-art-b1add18a592346dbbf84b9ec491182b02024-11-26T17:47:23ZengMDPI AGAntioxidants2076-39212024-11-011311142810.3390/antiox13111428(Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial CellsLinda M. Bakker0Michael E. Boulton1Małgorzata B. Różanowska2School of Optometry and Vision Sciences, Cardiff University, Cardiff CF24 4HQ, Wales, UKDepartment of Ophthalmology and Visual Sciences, University of Alabama at Birmingham, Birmingham, AL 35294, USASchool of Optometry and Vision Sciences, Cardiff University, Cardiff CF24 4HQ, Wales, UKDocosahexaenoate is a cytoprotective ω-3 polyunsaturated lipid that is abundant in the retina and is essential for its function. Due to its six unsaturated double bonds, docosahexaenoate is highly susceptible to oxidation and the formation of products with photosensitizing properties. This study aimed to test on cultured human retinal pigment epithelial cells ARPE-19 the (photo)cytotoxic potential of partly oxidized docosahexaenoate and its effect on the formation of lipofuscin from phagocytosed photoreceptor outer segments (POSs). The results demonstrate that the cytoprotective effects of docosahexaenoate do not counteract the deleterious effects of its oxidation products, leading to the concentration-dependent loss of cell metabolic activity, which is exacerbated by concomitant exposure to visible light. Partly oxidized docosahexaenoate does not cause permeability of the cell plasma membrane but does cause apoptosis. While vitamin E can provide partial protection from the (photo)toxicity of partly oxidized docosahexaenoate, zeaxanthin undergoes rapid photodegradation and can exacerbate the (photo)toxicity. Feeding cells with POSs enriched in partly oxidized docosahexaenoate results in a greater accumulation of intracellular fluorescent lipofuscin than in cells fed POSs without the addition. In conclusion, partly oxidized docosahexaenoate increases the accumulation of lipofuscin-like intracellular deposits, is cytotoxic, and its toxicity increases during exposure to light. These effects may contribute to the increased progression of geographic atrophy observed after long-term supplementation with docosahexaenoate in age-related macular degeneration patients.https://www.mdpi.com/2076-3921/13/11/1428docosahexaenoic acidomega-3 fatty acidretinalipid peroxidationretinal pigment epitheliumphotoreceptor outer segments
spellingShingle Linda M. Bakker
Michael E. Boulton
Małgorzata B. Różanowska
(Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial Cells
Antioxidants
docosahexaenoic acid
omega-3 fatty acid
retina
lipid peroxidation
retinal pigment epithelium
photoreceptor outer segments
title (Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial Cells
title_full (Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial Cells
title_fullStr (Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial Cells
title_full_unstemmed (Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial Cells
title_short (Photo)toxicity of Partially Oxidized Docosahexaenoate and Its Effect on the Formation of Lipofuscin in Cultured Human Retinal Pigment Epithelial Cells
title_sort photo toxicity of partially oxidized docosahexaenoate and its effect on the formation of lipofuscin in cultured human retinal pigment epithelial cells
topic docosahexaenoic acid
omega-3 fatty acid
retina
lipid peroxidation
retinal pigment epithelium
photoreceptor outer segments
url https://www.mdpi.com/2076-3921/13/11/1428
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