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Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas

Ciliary neurotrophic factor (CNTF) acts as a potent neuroprotective cytokine in multiple models of retinal degeneration. To understand mechanisms underlying its broad neuroprotective effects, we have investigated the influence of CNTF on metabolism in a mouse model of photoreceptor degeneration. CNT...

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Autores principales: Do Rhee, Kun, Wang, Yanjie, ten Hoeve, Johanna, Stiles, Linsey, Nguyen, Thao Thi Thu, Zhang, Xiangmei, Vergnes, Laurent, Reue, Karen, Shirihai, Orian, Bok, Dean, Yang, Xian-Jie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9672129/
https://www.ncbi.nlm.nih.gov/pubmed/36396639
http://dx.doi.org/10.1038/s41467-022-34443-x
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author Do Rhee, Kun
Wang, Yanjie
ten Hoeve, Johanna
Stiles, Linsey
Nguyen, Thao Thi Thu
Zhang, Xiangmei
Vergnes, Laurent
Reue, Karen
Shirihai, Orian
Bok, Dean
Yang, Xian-Jie
author_facet Do Rhee, Kun
Wang, Yanjie
ten Hoeve, Johanna
Stiles, Linsey
Nguyen, Thao Thi Thu
Zhang, Xiangmei
Vergnes, Laurent
Reue, Karen
Shirihai, Orian
Bok, Dean
Yang, Xian-Jie
author_sort Do Rhee, Kun
collection PubMed
description Ciliary neurotrophic factor (CNTF) acts as a potent neuroprotective cytokine in multiple models of retinal degeneration. To understand mechanisms underlying its broad neuroprotective effects, we have investigated the influence of CNTF on metabolism in a mouse model of photoreceptor degeneration. CNTF treatment improves the morphology of photoreceptor mitochondria, but also leads to reduced oxygen consumption and suppressed respiratory chain activities. Molecular analyses show elevated glycolytic pathway gene transcripts and active enzymes. Metabolomics analyses detect significantly higher levels of ATP and the energy currency phosphocreatine, elevated glycolytic pathway metabolites, increased TCA cycle metabolites, lipid biosynthetic pathway intermediates, nucleotides, and amino acids. Moreover, CNTF treatment restores the key antioxidant glutathione to the wild type level. Therefore, CNTF significantly impacts the metabolic status of degenerating retinas by promoting aerobic glycolysis and augmenting anabolic activities. These findings reveal cellular mechanisms underlying enhanced neuronal viability and suggest potential therapies for treating retinal degeneration.
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spelling pubmed-96721292022-11-19 Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas Do Rhee, Kun Wang, Yanjie ten Hoeve, Johanna Stiles, Linsey Nguyen, Thao Thi Thu Zhang, Xiangmei Vergnes, Laurent Reue, Karen Shirihai, Orian Bok, Dean Yang, Xian-Jie Nat Commun Article Ciliary neurotrophic factor (CNTF) acts as a potent neuroprotective cytokine in multiple models of retinal degeneration. To understand mechanisms underlying its broad neuroprotective effects, we have investigated the influence of CNTF on metabolism in a mouse model of photoreceptor degeneration. CNTF treatment improves the morphology of photoreceptor mitochondria, but also leads to reduced oxygen consumption and suppressed respiratory chain activities. Molecular analyses show elevated glycolytic pathway gene transcripts and active enzymes. Metabolomics analyses detect significantly higher levels of ATP and the energy currency phosphocreatine, elevated glycolytic pathway metabolites, increased TCA cycle metabolites, lipid biosynthetic pathway intermediates, nucleotides, and amino acids. Moreover, CNTF treatment restores the key antioxidant glutathione to the wild type level. Therefore, CNTF significantly impacts the metabolic status of degenerating retinas by promoting aerobic glycolysis and augmenting anabolic activities. These findings reveal cellular mechanisms underlying enhanced neuronal viability and suggest potential therapies for treating retinal degeneration. Nature Publishing Group UK 2022-11-17 /pmc/articles/PMC9672129/ /pubmed/36396639 http://dx.doi.org/10.1038/s41467-022-34443-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Do Rhee, Kun
Wang, Yanjie
ten Hoeve, Johanna
Stiles, Linsey
Nguyen, Thao Thi Thu
Zhang, Xiangmei
Vergnes, Laurent
Reue, Karen
Shirihai, Orian
Bok, Dean
Yang, Xian-Jie
Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas
title Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas
title_full Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas
title_fullStr Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas
title_full_unstemmed Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas
title_short Ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas
title_sort ciliary neurotrophic factor-mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9672129/
https://www.ncbi.nlm.nih.gov/pubmed/36396639
http://dx.doi.org/10.1038/s41467-022-34443-x
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