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Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells

Chronic hyperglycaemia causes a dramatic decrease in mitochondrial metabolism and insulin content in pancreatic β-cells. This underlies the progressive decline in β-cell function in diabetes. However, the molecular mechanisms by which hyperglycaemia produces these effects remain unresolved. Using is...

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Autores principales: Haythorne, Elizabeth, Lloyd, Matthew, Walsby-Tickle, John, Tarasov, Andrei I., Sandbrink, Jonas, Portillo, Idoia, Exposito, Raul Terron, Sachse, Gregor, Cyranka, Malgorzata, Rohm, Maria, Rorsman, Patrik, McCullagh, James, Ashcroft, Frances M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9663558/
https://www.ncbi.nlm.nih.gov/pubmed/36376280
http://dx.doi.org/10.1038/s41467-022-34095-x
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author Haythorne, Elizabeth
Lloyd, Matthew
Walsby-Tickle, John
Tarasov, Andrei I.
Sandbrink, Jonas
Portillo, Idoia
Exposito, Raul Terron
Sachse, Gregor
Cyranka, Malgorzata
Rohm, Maria
Rorsman, Patrik
McCullagh, James
Ashcroft, Frances M.
author_facet Haythorne, Elizabeth
Lloyd, Matthew
Walsby-Tickle, John
Tarasov, Andrei I.
Sandbrink, Jonas
Portillo, Idoia
Exposito, Raul Terron
Sachse, Gregor
Cyranka, Malgorzata
Rohm, Maria
Rorsman, Patrik
McCullagh, James
Ashcroft, Frances M.
author_sort Haythorne, Elizabeth
collection PubMed
description Chronic hyperglycaemia causes a dramatic decrease in mitochondrial metabolism and insulin content in pancreatic β-cells. This underlies the progressive decline in β-cell function in diabetes. However, the molecular mechanisms by which hyperglycaemia produces these effects remain unresolved. Using isolated islets and INS-1 cells, we show here that one or more glycolytic metabolites downstream of phosphofructokinase and upstream of GAPDH mediates the effects of chronic hyperglycemia. This metabolite stimulates marked upregulation of mTORC1 and concomitant downregulation of AMPK. Increased mTORC1 activity causes inhibition of pyruvate dehydrogenase which reduces pyruvate entry into the tricarboxylic acid cycle and partially accounts for the hyperglycaemia-induced reduction in oxidative phosphorylation and insulin secretion. In addition, hyperglycaemia (or diabetes) dramatically inhibits GAPDH activity, thereby impairing glucose metabolism. Our data also reveal that restricting glucose metabolism during hyperglycaemia prevents these changes and thus may be of therapeutic benefit. In summary, we have identified a pathway by which chronic hyperglycaemia reduces β-cell function.
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spelling pubmed-96635582022-11-15 Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells Haythorne, Elizabeth Lloyd, Matthew Walsby-Tickle, John Tarasov, Andrei I. Sandbrink, Jonas Portillo, Idoia Exposito, Raul Terron Sachse, Gregor Cyranka, Malgorzata Rohm, Maria Rorsman, Patrik McCullagh, James Ashcroft, Frances M. Nat Commun Article Chronic hyperglycaemia causes a dramatic decrease in mitochondrial metabolism and insulin content in pancreatic β-cells. This underlies the progressive decline in β-cell function in diabetes. However, the molecular mechanisms by which hyperglycaemia produces these effects remain unresolved. Using isolated islets and INS-1 cells, we show here that one or more glycolytic metabolites downstream of phosphofructokinase and upstream of GAPDH mediates the effects of chronic hyperglycemia. This metabolite stimulates marked upregulation of mTORC1 and concomitant downregulation of AMPK. Increased mTORC1 activity causes inhibition of pyruvate dehydrogenase which reduces pyruvate entry into the tricarboxylic acid cycle and partially accounts for the hyperglycaemia-induced reduction in oxidative phosphorylation and insulin secretion. In addition, hyperglycaemia (or diabetes) dramatically inhibits GAPDH activity, thereby impairing glucose metabolism. Our data also reveal that restricting glucose metabolism during hyperglycaemia prevents these changes and thus may be of therapeutic benefit. In summary, we have identified a pathway by which chronic hyperglycaemia reduces β-cell function. Nature Publishing Group UK 2022-11-14 /pmc/articles/PMC9663558/ /pubmed/36376280 http://dx.doi.org/10.1038/s41467-022-34095-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
Haythorne, Elizabeth
Lloyd, Matthew
Walsby-Tickle, John
Tarasov, Andrei I.
Sandbrink, Jonas
Portillo, Idoia
Exposito, Raul Terron
Sachse, Gregor
Cyranka, Malgorzata
Rohm, Maria
Rorsman, Patrik
McCullagh, James
Ashcroft, Frances M.
Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells
title Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells
title_full Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells
title_fullStr Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells
title_full_unstemmed Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells
title_short Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells
title_sort altered glycolysis triggers impaired mitochondrial metabolism and mtorc1 activation in diabetic β-cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9663558/
https://www.ncbi.nlm.nih.gov/pubmed/36376280
http://dx.doi.org/10.1038/s41467-022-34095-x
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