Distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecups

Abstract Age-related macular degeneration (AMD) is associated with chronic inflammation of the retinal pigment epithelium (RPE) and elevated cytokines including TNFα, TGF-β, IL-6, and IL-1β. As a metabolic intermediary supporting aerobic glycolysis in the adjacent photoreceptors, the RPE’s metabolic...

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Main Authors: David S. Hansman, Kelly Lim, Daniel Thomas, Robert J. Casson, Daniel J. Peet
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-93882-w
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author David S. Hansman
Kelly Lim
Daniel Thomas
Robert J. Casson
Daniel J. Peet
author_facet David S. Hansman
Kelly Lim
Daniel Thomas
Robert J. Casson
Daniel J. Peet
author_sort David S. Hansman
collection DOAJ
description Abstract Age-related macular degeneration (AMD) is associated with chronic inflammation of the retinal pigment epithelium (RPE) and elevated cytokines including TNFα, TGF-β, IL-6, and IL-1β. As a metabolic intermediary supporting aerobic glycolysis in the adjacent photoreceptors, the RPE’s metabolic responses to inflammation and the optimal methods to study cytokine-driven metabolic programming remain unclear. We performed a rigorous comparison of ARPE-19 cells and rat eyecup metabolomes, revealing key distinctions. Rat eyecups exhibit higher levels of lactate and palmitate but depleted glutathione and high-energy nucleotides. Conversely, ARPE-19 cells are enriched with high-energy currency metabolites and the membrane phospholipid precursors phosphocholine and inositol. Both models showed contrasting responses to individual cytokines: ARPE-19 cells were more sensitive to TNFα, while eyecups responded more strongly to TGF-β2. Notably, a combined cytokine cocktail elicited stronger metabolic effects on ARPE-19 cells, more potently impacting both metabolite abundance (41 vs. 29) and glucose carbon flux (29 vs. 5), and influencing key RPE metabolites such as alanine, glycine, aspartate, proline, citrate, α-ketoglutarate, and palmitate. Overall, these findings position ARPE-19 cells as a more responsive platform for studying inflammatory cytokine effects on RPE metabolism and reveal critical RPE metabolites which may be linked with AMD pathogenesis.
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spelling doaj-art-e55c2c4dfd9d478b888dc57db59fb8d62025-08-20T02:17:54ZengNature PortfolioScientific Reports2045-23222025-04-0115111710.1038/s41598-025-93882-wDistinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecupsDavid S. Hansman0Kelly Lim1Daniel Thomas2Robert J. Casson3Daniel J. Peet4School of Biological Sciences, University of AdelaideSouth Australian Health and Medical Research Institute, Adelaide Medical School, University of AdelaideSouth Australian Health and Medical Research Institute, Adelaide Medical School, University of AdelaideDiscipline of Ophthalmology and Visual Science, Adelaide Medical School, University of AdelaideSchool of Biological Sciences, University of AdelaideAbstract Age-related macular degeneration (AMD) is associated with chronic inflammation of the retinal pigment epithelium (RPE) and elevated cytokines including TNFα, TGF-β, IL-6, and IL-1β. As a metabolic intermediary supporting aerobic glycolysis in the adjacent photoreceptors, the RPE’s metabolic responses to inflammation and the optimal methods to study cytokine-driven metabolic programming remain unclear. We performed a rigorous comparison of ARPE-19 cells and rat eyecup metabolomes, revealing key distinctions. Rat eyecups exhibit higher levels of lactate and palmitate but depleted glutathione and high-energy nucleotides. Conversely, ARPE-19 cells are enriched with high-energy currency metabolites and the membrane phospholipid precursors phosphocholine and inositol. Both models showed contrasting responses to individual cytokines: ARPE-19 cells were more sensitive to TNFα, while eyecups responded more strongly to TGF-β2. Notably, a combined cytokine cocktail elicited stronger metabolic effects on ARPE-19 cells, more potently impacting both metabolite abundance (41 vs. 29) and glucose carbon flux (29 vs. 5), and influencing key RPE metabolites such as alanine, glycine, aspartate, proline, citrate, α-ketoglutarate, and palmitate. Overall, these findings position ARPE-19 cells as a more responsive platform for studying inflammatory cytokine effects on RPE metabolism and reveal critical RPE metabolites which may be linked with AMD pathogenesis.https://doi.org/10.1038/s41598-025-93882-wAge-related macular degenerationRetinal pigment epitheliumMetabolismRetina inflammationCytokinesMetabolic ecosystem
spellingShingle David S. Hansman
Kelly Lim
Daniel Thomas
Robert J. Casson
Daniel J. Peet
Distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecups
Scientific Reports
Age-related macular degeneration
Retinal pigment epithelium
Metabolism
Retina inflammation
Cytokines
Metabolic ecosystem
title Distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecups
title_full Distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecups
title_fullStr Distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecups
title_full_unstemmed Distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecups
title_short Distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age-related macular degeneration: comparison of ARPE-19 cells and eyecups
title_sort distinct metabolome and flux responses in the retinal pigment epithelium to cytokines associated with age related macular degeneration comparison of arpe 19 cells and eyecups
topic Age-related macular degeneration
Retinal pigment epithelium
Metabolism
Retina inflammation
Cytokines
Metabolic ecosystem
url https://doi.org/10.1038/s41598-025-93882-w
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