IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39688-8.html
   My bibliography  Save this article

A mechanical-coupling mechanism in OSCA/TMEM63 channel mechanosensitivity

Author

Listed:
  • Mingfeng Zhang

    (Fudan University
    Westlake University)

  • Yuanyue Shan

    (Fudan University
    Westlake University)

  • Charles D. Cox

    (Victor Chang Cardiac Research Institute
    Faculty of Medicine & Health, UNSW Sydney)

  • Duanqing Pei

    (Westlake University)

Abstract

Mechanosensitive (MS) ion channels are a ubiquitous type of molecular force sensor sensing forces from the surrounding bilayer. The profound structural diversity in these channels suggests that the molecular mechanisms of force sensing follow unique structural blueprints. Here we determine the structures of plant and mammalian OSCA/TMEM63 proteins, allowing us to identify essential elements for mechanotransduction and propose roles for putative bound lipids in OSCA/TMEM63 mechanosensation. Briefly, the central cavity created by the dimer interface couples each subunit and modulates dimeric OSCA/TMEM63 channel mechanosensitivity through the modulating lipids while the cytosolic side of the pore is gated by a plug lipid that prevents the ion permeation. Our results suggest that the gating mechanism of OSCA/TMEM63 channels may combine structural aspects of the ‘lipid-gated’ mechanism of MscS and TRAAK channels and the calcium-induced gating mechanism of the TMEM16 family, which may provide insights into the structural rearrangements of TMEM16/TMC superfamilies.

Suggested Citation

  • Mingfeng Zhang & Yuanyue Shan & Charles D. Cox & Duanqing Pei, 2023. "A mechanical-coupling mechanism in OSCA/TMEM63 channel mechanosensitivity," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39688-8
    DOI: 10.1038/s41467-023-39688-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39688-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39688-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Fang Yuan & Huimin Yang & Yan Xue & Dongdong Kong & Rui Ye & Chijun Li & Jingyuan Zhang & Lynn Theprungsirikul & Tayler Shrift & Bryan Krichilsky & Douglas M. Johnson & Gary B. Swift & Yikun He & Jame, 2014. "OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis," Nature, Nature, vol. 514(7522), pages 367-371, October.
    2. Shangyu Dang & Shengjie Feng & Jason Tien & Christian J. Peters & David Bulkley & Marco Lolicato & Jianhua Zhao & Kathrin Zuberbühler & Wenlei Ye & Lijun Qi & Tingxu Chen & Charles S. Craik & Yuh Nung, 2017. "Cryo-EM structures of the TMEM16A calcium-activated chloride channel," Nature, Nature, vol. 552(7685), pages 426-429, December.
    3. 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.
    4. Janice L. Robertson & Ludmila Kolmakova-Partensky & Christopher Miller, 2010. "Design, function and structure of a monomeric ClC transporter," Nature, Nature, vol. 468(7325), pages 844-847, December.
    5. 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.
    6. Hanbin Jeong & Sarah Clark & April Goehring & Sepehr Dehghani-Ghahnaviyeh & Ali Rasouli & Emad Tajkhorshid & Eric Gouaux, 2022. "Structures of the TMC-1 complex illuminate mechanosensory transduction," Nature, Nature, vol. 610(7933), pages 796-803, October.
    7. Cristina Paulino & Valeria Kalienkova & Andy K. M. Lam & Yvonne Neldner & Raimund Dutzler, 2017. "Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM," Nature, Nature, vol. 552(7685), pages 421-425, December.
    8. Raimund Dutzler & Ernest B. Campbell & Martine Cadene & Brian T. Chait & Roderick MacKinnon, 2002. "X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity," Nature, Nature, vol. 415(6869), pages 287-294, January.
    9. Navid Bavi & Michael David Clark & Gustavo F. Contreras & Rong Shen & Bharat G. Reddy & Wieslawa Milewski & Eduardo Perozo, 2021. "The conformational cycle of prestin underlies outer-hair cell electromotility," Nature, Nature, vol. 600(7889), pages 553-558, December.
    10. Simon R. Bushell & Ashley C. W. Pike & Maria E. Falzone & Nils J. G. Rorsman & Chau M. Ta & Robin A. Corey & Thomas D. Newport & John C. Christianson & Lara F. Scofano & Chitra A. Shintre & Annamaria , 2019. "The structural basis of lipid scrambling and inactivation in the endoplasmic reticulum scramblase TMEM16K," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    11. Stephen G. Brohawn & Ernest B. Campbell & Roderick MacKinnon, 2014. "Physical mechanism for gating and mechanosensitivity of the human TRAAK K+ channel," Nature, Nature, vol. 516(7529), pages 126-130, December.
    12. Yixiao Zhang & Csaba Daday & Ruo-Xu Gu & Charles D. Cox & Boris Martinac & Bert L. Groot & Thomas Walz, 2021. "Visualization of the mechanosensitive ion channel MscS under membrane tension," Nature, Nature, vol. 590(7846), pages 509-514, February.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.
    2. Yuqi Qin & Daqi Yu & Dan Wu & Jiangqing Dong & William Thomas Li & Chang Ye & Kai Chit Cheung & Yingyi Zhang & Yun Xu & YongQiang Wang & Yun Stone Shi & Shangyu Dang, 2023. "Cryo-EM structure of TMEM63C suggests it functions as a monomer," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. Han Niu & Masahiro Maruoka & Yuki Noguchi & Hidetaka Kosako & Jun Suzuki, 2024. "Phospholipid scrambling induced by an ion channel/metabolite transporter complex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Yuqi Qin & Daqi Yu & Dan Wu & Jiangqing Dong & William Thomas Li & Chang Ye & Kai Chit Cheung & Yingyi Zhang & Yun Xu & YongQiang Wang & Yun Stone Shi & Shangyu Dang, 2023. "Cryo-EM structure of TMEM63C suggests it functions as a monomer," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. Shengjie Feng & Cristina Puchades & Juyeon Ko & Hao Wu & Yifei Chen & Eric E. Figueroa & Shuo Gu & Tina W. Han & Brandon Ho & Tong Cheng & Junrui Li & Brian Shoichet & Yuh Nung Jan & Yifan Cheng & Lil, 2023. "Identification of a drug binding pocket in TMEM16F calcium-activated ion channel and lipid scramblase," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Zhongjie Ye & Nicola Galvanetto & Leonardo Puppulin & Simone Pifferi & Holger Flechsig & Melanie Arndt & Cesar Adolfo Sánchez Triviño & Michael Palma & Shifeng Guo & Horst Vogel & Anna Menini & Clemen, 2024. "Structural heterogeneity of the ion and lipid channel TMEM16F," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. 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.
    6. Baobin Li & Christopher M. Hoel & Stephen G. Brohawn, 2021. "Structures of tweety homolog proteins TTYH2 and TTYH3 reveal a Ca2+-dependent switch from intra- to intermembrane dimerization," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    7. 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.
    8. Yangzhuoqun Wan & Shuangshuang Guo & Wenxuan Zhen & Lizhen Xu & Xiaoying Chen & Fangyue Liu & Yi Shen & Shuangshuang Liu & Lidan Hu & Xinyan Wang & Fengcan Ye & Qinrui Wang & Han Wen & Fan Yang, 2024. "Structural basis of adenine nucleotides regulation and neurodegenerative pathology in ClC-3 exchanger," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    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. Melanie Arndt & Carolina Alvadia & Monique S. Straub & Vanessa Clerico Mosina & Cristina Paulino & Raimund Dutzler, 2022. "Structural basis for the activation of the lipid scramblase TMEM16F," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Philipp A. M. Schmidpeter & John T. Petroff & Leila Khajoueinejad & Aboubacar Wague & Cheryl Frankfater & Wayland W. L. Cheng & Crina M. Nimigean & Paul M. Riegelhaupt, 2023. "Membrane phospholipids control gating of the mechanosensitive potassium leak channel TREK1," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Martina Nicoletti & Letizia Chiodo & Alessandro Loppini, 2021. "Biophysics and Modeling of Mechanotransduction in Neurons: A Review," Mathematics, MDPI, vol. 9(4), pages 1-32, February.
    13. Weijia Sun & Shuai Guo & Yuheng Li & JianWei Li & Caizhi Liu & Yafei Chen & Xuzhao Wang & Yingjun Tan & Hua Tian & Cheng Wang & Ruikai Du & Guohui Zhong & Sai Shi & Biao Ma & Chang Qu & Jingxuan Fu & , 2022. "Anoctamin 1 controls bone resorption by coupling Cl− channel activation with RANKL-RANK signaling transduction," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Maria E. Falzone & Zhang Feng & Omar E. Alvarenga & Yangang Pan & ByoungCheol Lee & Xiaolu Cheng & Eva Fortea & Simon Scheuring & Alessio Accardi, 2022. "TMEM16 scramblases thin the membrane to enable lipid scrambling," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    15. 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.
    16. Andy K. M. Lam & Sonja Rutz & Raimund Dutzler, 2022. "Inhibition mechanism of the chloride channel TMEM16A by the pore blocker 1PBC," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    17. Keri A McKiernan & Anna K Koster & Merritt Maduke & Vijay S Pande, 2020. "Dynamical model of the CLC-2 ion channel reveals conformational changes associated with selectivity-filter gating," PLOS Computational Biology, Public Library of Science, vol. 16(3), pages 1-24, March.
    18. Xiaofen Liu & Weiwei Wang, 2023. "Asymmetric gating of a human hetero-pentameric glycine receptor," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    19. Samuel Hume & Claudia P. Grou & Pauline Lascaux & Vincenzo D’Angiolella & Arnaud J. Legrand & Kristijan Ramadan & Grigory L. Dianov, 2021. "The NUCKS1-SKP2-p21/p27 axis controls S phase entry," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    20. Qianying Liu & Xiang Zhang & Hui Huang & Yuxin Chen & Fang Wang & Aihua Hao & Wuqiang Zhan & Qiyu Mao & Yuxia Hu & Lin Han & Yifang Sun & Meng Zhang & Zhimin Liu & Geng-Lin Li & Weijia Zhang & Yilai S, 2023. "Asymmetric pendrin homodimer reveals its molecular mechanism as anion exchanger," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39688-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.