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Structure deformation and curvature sensing of PIEZO1 in lipid membranes

Author

Listed:
  • Xuzhong Yang

    (Tsinghua University)

  • Chao Lin

    (Tsinghua University)

  • Xudong Chen

    (Tsinghua University)

  • Shouqin Li

    (Tsinghua University
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xueming Li

    (Tsinghua University)

  • Bailong Xiao

    (Tsinghua University)

Abstract

PIEZO channels respond to piconewton-scale forces to mediate critical physiological and pathophysiological processes1–5. Detergent-solubilized PIEZO channels form bowl-shaped trimers comprising a central ion-conducting pore with an extracellular cap and three curved and non-planar blades with intracellular beams6–10, which may undergo force-induced deformation within lipid membranes11. However, the structures and mechanisms underlying the gating dynamics of PIEZO channels in lipid membranes remain unresolved. Here we determine the curved and flattened structures of PIEZO1 reconstituted in liposome vesicles, directly visualizing the substantial deformability of the PIEZO1–lipid bilayer system and an in-plane areal expansion of approximately 300 nm2 in the flattened structure. The curved structure of PIEZO1 resembles the structure determined from detergent micelles, but has numerous bound phospholipids. By contrast, the flattened structure exhibits membrane tension-induced flattening of the blade, bending of the beam and detaching and rotating of the cap, which could collectively lead to gating of the ion-conducting pathway. On the basis of the measured in-plane membrane area expansion and stiffness constant of PIEZO1 (ref. 11), we calculate a half maximal activation tension of about 1.9 pN nm−1, matching experimentally measured values. Thus, our studies provide a fundamental understanding of how the notable deformability and structural rearrangement of PIEZO1 achieve exquisite mechanosensitivity and unique curvature-based gating in lipid membranes.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:604:y:2022:i:7905:d:10.1038_s41586-022-04574-8
    DOI: 10.1038/s41586-022-04574-8
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    Cited by:

    1. Jingying Zhang & Grigory Maksaev & Peng Yuan, 2023. "Open structure and gating of the Arabidopsis mechanosensitive ion channel MSL10," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    2. 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.
    3. Haoqing Jerry Wang & Yao Wang & Seyed Sajad Mirjavadi & Tomas Andersen & Laura Moldovan & Parham Vatankhah & Blake Russell & Jasmine Jin & Zijing Zhou & Qing Li & Charles D. Cox & Qian Peter Su & Lini, 2024. "Microscale geometrical modulation of PIEZO1 mediated mechanosensing through cytoskeletal redistribution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Yuanyue Shan & Mengmeng Zhang & Meiyu Chen & Xinyi Guo & Ying Li & Mingfeng Zhang & Duanqing Pei, 2024. "Activation mechanisms of dimeric mechanosensitive OSCA/TMEM63 channels," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Luis O. Romero & Rebeca Caires & A. Kaitlyn Victor & Juanma Ramirez & Francisco J. Sierra-Valdez & Patrick Walsh & Vincent Truong & Jungsoo Lee & Ugo Mayor & Lawrence T. Reiter & Valeria Vásquez & Jul, 2023. "Linoleic acid improves PIEZO2 dysfunction in a mouse model of Angelman Syndrome," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Jonathan Mount & Grigory Maksaev & Brock T. Summers & James A. J. Fitzpatrick & Peng Yuan, 2022. "Structural basis for mechanotransduction in a potassium-dependent mechanosensitive ion channel," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. Francisco Andrés Peralta & Mélaine Balcon & Adeline Martz & Deniza Biljali & Federico Cevoli & Benoit Arnould & Antoine Taly & Thierry Chataigneau & Thomas Grutter, 2023. "Optical control of PIEZO1 channels," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Matthias Pöhnl & Marius F. W. Trollmann & Rainer A. Böckmann, 2023. "Nonuniversal impact of cholesterol on membranes mobility, curvature sensing and elasticity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Jeong Han Lee & Maria C. Perez-Flores & Seojin Park & Hyo Jeong Kim & Yingying Chen & Mincheol Kang & Jennifer Kersigo & Jinsil Choi & Phung N. Thai & Ryan L. Woltz & Dolores Columba Perez-Flores & Gu, 2024. "The Piezo channel is a mechano-sensitive complex component in the mammalian inner ear hair cell," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. Sara Baratchi & Habiba Danish & Chanly Chheang & Ying Zhou & Angela Huang & Austin Lai & Manijeh Khanmohammadi & Kylie M. Quinn & Khashayar Khoshmanesh & Karlheinz Peter, 2024. "Piezo1 expression in neutrophils regulates shear-induced NETosis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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