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Membrane curvature governs the distribution of Piezo1 in live cells

Author

Listed:
  • Shilong Yang

    (Rutgers University)

  • Xinwen Miao

    (Nanyang Technological University)

  • Steven Arnold

    (Rutgers University)

  • Boxuan Li

    (Rutgers University)

  • Alan T. Ly

    (UC Irvine
    UC Irvine)

  • Huan Wang

    (Rutgers University)

  • Matthew Wang

    (Rutgers University)

  • Xiangfu Guo

    (Nanyang Technological University)

  • Medha M. Pathak

    (UC Irvine
    UC Irvine)

  • Wenting Zhao

    (Nanyang Technological University)

  • Charles D. Cox

    (Victor Chang Cardiac Research Institute)

  • Zheng Shi

    (Rutgers University
    Rutgers University)

Abstract

Piezo1 is a bona fide mechanosensitive ion channel ubiquitously expressed in mammalian cells. The distribution of Piezo1 within a cell is essential for various biological processes including cytokinesis, cell migration, and wound healing. However, the underlying principles that guide the subcellular distribution of Piezo1 remain largely unexplored. Here, we demonstrate that membrane curvature serves as a key regulator of the spatial distribution of Piezo1 in the plasma membrane of living cells. Piezo1 depletes from highly curved membrane protrusions such as filopodia and enriches to nanoscale membrane invaginations. Quantification of the curvature-dependent sorting of Piezo1 directly reveals the in situ nano-geometry of the Piezo1-membrane complex. Piezo1 density on filopodia increases upon activation, independent of calcium, suggesting flattening of the channel upon opening. Consequently, the expression of Piezo1 inhibits filopodia formation, an effect that diminishes with channel activation.

Suggested Citation

  • Shilong Yang & Xinwen Miao & Steven Arnold & Boxuan Li & Alan T. Ly & Huan Wang & Matthew Wang & Xiangfu Guo & Medha M. Pathak & Wenting Zhao & Charles D. Cox & Zheng Shi, 2022. "Membrane curvature governs the distribution of Piezo1 in live cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35034-6
    DOI: 10.1038/s41467-022-35034-6
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    1. Bertrand Coste & Bailong Xiao & Jose S. Santos & Ruhma Syeda & Jörg Grandl & Kathryn S. Spencer & Sung Eun Kim & Manuela Schmidt & Jayanti Mathur & Adrienne E. Dubin & Mauricio Montal & Ardem Patapout, 2012. "Piezo proteins are pore-forming subunits of mechanically activated channels," Nature, Nature, vol. 483(7388), pages 176-181, March.
    2. Qiancheng Zhao & Heng Zhou & Shaopeng Chi & Yanfeng Wang & Jianhua Wang & Jie Geng & Kun Wu & Wenhao Liu & Tingxin Zhang & Meng-Qiu Dong & Jiawei Wang & Xueming Li & Bailong Xiao, 2018. "Structure and mechanogating mechanism of the Piezo1 channel," Nature, Nature, vol. 554(7693), pages 487-492, February.
    3. Kei Saotome & Swetha E. Murthy & Jennifer M. Kefauver & Tess Whitwam & Ardem Patapoutian & Andrew B. Ward, 2018. "Structure of the mechanically activated ion channel Piezo1," Nature, Nature, vol. 554(7693), pages 481-486, February.
    4. Charles D. Cox & Chilman Bae & Lynn Ziegler & Silas Hartley & Vesna Nikolova-Krstevski & Paul R. Rohde & Chai-Ann Ng & Frederick Sachs & Philip A. Gottlieb & Boris Martinac, 2016. "Removal of the mechanoprotective influence of the cytoskeleton reveals PIEZO1 is gated by bilayer tension," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    5. Luis O. Romero & Rebeca Caires & Alec R. Nickolls & Alexander T. Chesler & Julio F. Cordero-Morales & Valeria Vásquez, 2020. "A dietary fatty acid counteracts neuronal mechanical sensitization," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    6. Jingpeng Ge & Wanqiu Li & Qiancheng Zhao & Ningning Li & Maofei Chen & Peng Zhi & Ruochong Li & Ning Gao & Bailong Xiao & Maojun Yang, 2015. "Architecture of the mammalian mechanosensitive Piezo1 channel," Nature, Nature, vol. 527(7576), pages 64-69, November.
    7. J. M. Kefauver & A. B. Ward & A. Patapoutian, 2020. "Discoveries in structure and physiology of mechanically activated ion channels," Nature, Nature, vol. 587(7835), pages 567-576, November.
    8. Qiancheng Zhao & Heng Zhou & Shaopeng Chi & Yanfeng Wang & Jianhua Wang & Jie Geng & Kun Wu & Wenhao Liu & Tingxin Zhang & Meng-Qiu Dong & Jiawei Wang & Xueming Li & Bailong Xiao, 2018. "Author Correction: Structure and mechanogating mechanism of the Piezo1 channel," Nature, Nature, vol. 563(7730), pages 19-19, November.
    9. Clement Verkest & Irina Schaefer & Timo A. Nees & Na Wang & Juri M. Jegelka & Francisco J. Taberner & Stefan G. Lechner, 2022. "Intrinsically disordered intracellular domains control key features of the mechanically-gated ion channel PIEZO2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Zheng Shi & Tobias Baumgart, 2015. "Membrane tension and peripheral protein density mediate membrane shape transitions," Nature Communications, Nature, vol. 6(1), pages 1-8, May.
    11. Guillaume T. Charras & Justin C. Yarrow & Mike A. Horton & L. Mahadevan & T. J. Mitchison, 2005. "Non-equilibration of hydrostatic pressure in blebbing cells," Nature, Nature, vol. 435(7040), pages 365-369, May.
    12. Fan Jiang & Kunlun Yin & Kun Wu & Mingmin Zhang & Shiqiang Wang & Heping Cheng & Zhou Zhou & Bailong Xiao, 2021. "The mechanosensitive Piezo1 channel mediates heart mechano-chemo transduction," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    13. Xuzhong Yang & Chao Lin & Xudong Chen & Shouqin Li & Xueming Li & Bailong Xiao, 2022. "Structure deformation and curvature sensing of PIEZO1 in lipid membranes," Nature, Nature, vol. 604(7905), pages 377-383, April.
    14. Luis O. Romero & Rebeca Caires & Alec R. Nickolls & Alexander T. Chesler & Julio F. Cordero-Morales & Valeria Vásquez, 2020. "Publisher Correction: A dietary fatty acid counteracts neuronal mechanical sensitization," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
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