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

Author

Listed:
  • Elizabeth Haythorne

    (University of Oxford, Parks Road)

  • Matthew Lloyd

    (University of Oxford, Parks Road)

  • John Walsby-Tickle

    (University of Oxford)

  • Andrei I. Tarasov

    (Ulster University)

  • Jonas Sandbrink

    (University of Oxford, Parks Road)

  • Idoia Portillo

    (University of Oxford, Parks Road)

  • Raul Terron Exposito

    (University of Oxford, Parks Road
    Institute for Diabetes and Cancer (IDC), Helmholtz Center)

  • Gregor Sachse

    (University of Oxford, Parks Road
    ZTM-BB)

  • Malgorzata Cyranka

    (University of Oxford, Parks Road)

  • Maria Rohm

    (University of Oxford, Parks Road
    Institute for Diabetes and Cancer (IDC), Helmholtz Center)

  • Patrik Rorsman

    (University of Oxford, Churchill Hospital)

  • James McCullagh

    (University of Oxford)

  • Frances M. Ashcroft

    (University of Oxford, Parks Road)

Abstract

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.

Suggested Citation

  • Elizabeth Haythorne & Matthew Lloyd & John Walsby-Tickle & Andrei I. Tarasov & Jonas Sandbrink & Idoia Portillo & Raul Terron Exposito & Gregor Sachse & Malgorzata Cyranka & Maria Rohm & Patrik Rorsma, 2022. "Altered glycolysis triggers impaired mitochondrial metabolism and mTORC1 activation in diabetic β-cells," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34095-x
    DOI: 10.1038/s41467-022-34095-x
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    References listed on IDEAS

    as
    1. Elizabeth Haythorne & Maria Rohm & Martijn Bunt & Melissa F. Brereton & Andrei I. Tarasov & Thomas S. Blacker & Gregor Sachse & Mariana Silva dos Santos & Raul Terron Exposito & Simon Davis & Otto Bab, 2019. "Diabetes causes marked inhibition of mitochondrial metabolism in pancreatic β-cells," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    2. Chen-Song Zhang & Simon A. Hawley & Yue Zong & Mengqi Li & Zhichao Wang & Alexander Gray & Teng Ma & Jiwen Cui & Jin-Wei Feng & Mingjiang Zhu & Yu-Qing Wu & Terytty Yang Li & Zhiyun Ye & Shu-Yong Lin , 2017. "Fructose-1,6-bisphosphate and aldolase mediate glucose sensing by AMPK," Nature, Nature, vol. 548(7665), pages 112-116, August.
    3. Pierre Maechler & Claes B. Wollheim, 2001. "Mitochondrial function in normal and diabetic β-cells," Nature, Nature, vol. 414(6865), pages 807-812, December.
    4. Melissa F. Brereton & Michaela Iberl & Kenju Shimomura & Quan Zhang & Alice E. Adriaenssens & Peter Proks & Ioannis I. Spiliotis & William Dace & Katia K. Mattis & Reshma Ramracheya & Fiona M. Gribble, 2014. "Reversible changes in pancreatic islet structure and function produced by elevated blood glucose," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
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