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A critical role of the mechanosensor PIEZO1 in glucose-induced insulin secretion in pancreatic β-cells

Author

Listed:
  • Yingying Ye

    (Lund University)

  • Mohammad Barghouth

    (Lund University)

  • Haiqiang Dou

    (University of Göteborg)

  • Cheng Luan

    (Lund University)

  • Yongzhi Wang

    (Lund University)

  • Alexandros Karagiannopoulos

    (Lund University)

  • Xiaoping Jiang

    (Lund University
    Southwest University)

  • Ulrika Krus

    (Lund University)

  • Malin Fex

    (Lund University)

  • Quan Zhang

    (University of Oxford)

  • Lena Eliasson

    (Lund University)

  • Patrik Rorsman

    (University of Göteborg
    University of Oxford)

  • Enming Zhang

    (Lund University)

  • Erik Renström

    (Lund University)

Abstract

Glucose-induced insulin secretion depends on β-cell electrical activity. Inhibition of ATP-regulated potassium (KATP) channels is a key event in this process. However, KATP channel closure alone is not sufficient to induce β-cell electrical activity; activation of a depolarizing membrane current is also required. Here we examine the role of the mechanosensor ion channel PIEZO1 in this process. Yoda1, a specific PIEZO1 agonist, activates a small membrane current and thereby triggers β-cell electrical activity with resultant stimulation of Ca2+-influx and insulin secretion. Conversely, the PIEZO1 antagonist GsMTx4 reduces glucose-induced Ca2+-signaling, electrical activity and insulin secretion. Yet, PIEZO1 expression is elevated in islets from human donors with type-2 diabetes (T2D) and a rodent T2D model (db/db mouse), in which insulin secretion is reduced. This paradox is resolved by our finding that PIEZO1 translocates from the plasmalemma into the nucleus (where it cannot influence the membrane potential of the β-cell) under experimental conditions emulating T2D (high glucose culture). β-cell-specific Piezo1-knockout mice show impaired glucose tolerance in vivo and reduced glucose-induced insulin secretion, β-cell electrical activity and Ca2+ elevation in vitro. These results implicate mechanotransduction and activation of PIEZO1, via intracellular accumulation of glucose metabolites, as an important physiological regulator of insulin secretion.

Suggested Citation

  • Yingying Ye & Mohammad Barghouth & Haiqiang Dou & Cheng Luan & Yongzhi Wang & Alexandros Karagiannopoulos & Xiaoping Jiang & Ulrika Krus & Malin Fex & Quan Zhang & Lena Eliasson & Patrik Rorsman & Enm, 2022. "A critical role of the mechanosensor PIEZO1 in glucose-induced insulin secretion in pancreatic β-cells," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31103-y
    DOI: 10.1038/s41467-022-31103-y
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