IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28511-5.html
   My bibliography  Save this article

Structural insights into the Venus flytrap mechanosensitive ion channel Flycatcher1

Author

Listed:
  • Sebastian Jojoa-Cruz

    (Department of Integrative Structural and Computational Biology, Scripps Research)

  • Kei Saotome

    (Department of Integrative Structural and Computational Biology, Scripps Research
    Howard Hughes Medical Institute, Department of Neuroscience, Dorris Neuroscience Center, Scripps Research
    Regeneron Pharmaceuticals)

  • Che Chun Alex Tsui

    (Department of Integrative Structural and Computational Biology, Scripps Research
    University of Oxford)

  • Wen-Hsin Lee

    (Department of Integrative Structural and Computational Biology, Scripps Research)

  • Mark S. P. Sansom

    (University of Oxford)

  • Swetha E. Murthy

    (Howard Hughes Medical Institute, Department of Neuroscience, Dorris Neuroscience Center, Scripps Research
    Oregon Health and Science University)

  • Ardem Patapoutian

    (Howard Hughes Medical Institute, Department of Neuroscience, Dorris Neuroscience Center, Scripps Research)

  • Andrew B. Ward

    (Department of Integrative Structural and Computational Biology, Scripps Research)

Abstract

Flycatcher1 (FLYC1), a MscS homolog, has recently been identified as a candidate mechanosensitive (MS) ion channel involved in Venus flytrap prey recognition. FLYC1 is a larger protein and its sequence diverges from previously studied MscS homologs, suggesting it has unique structural features that contribute to its function. Here, we characterize FLYC1 by cryo-electron microscopy, molecular dynamics simulations, and electrophysiology. Akin to bacterial MscS and plant MSL1 channels, we find that FLYC1 central core includes side portals in the cytoplasmic cage that regulate ion preference and conduction, by identifying critical residues that modulate channel conductance. Topologically unique cytoplasmic flanking regions can adopt ‘up’ or ‘down’ conformations, making the channel asymmetric. Disruption of an up conformation-specific interaction severely delays channel deactivation by 40-fold likely due to stabilization of the channel open state. Our results illustrate novel structural features and likely conformational transitions that regulate mechano-gating of FLYC1.

Suggested Citation

  • Sebastian Jojoa-Cruz & Kei Saotome & Che Chun Alex Tsui & Wen-Hsin Lee & Mark S. P. Sansom & Swetha E. Murthy & Ardem Patapoutian & Andrew B. Ward, 2022. "Structural insights into the Venus flytrap mechanosensitive ion channel Flycatcher1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28511-5
    DOI: 10.1038/s41467-022-28511-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28511-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28511-5?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. C. D. Cox & T. Nomura & C. S. Ziegler & A. K. Campbell & K. T. Wann & B. Martinac, 2013. "Selectivity mechanism of the mechanosensitive channel MscS revealed by probing channel subconducting states," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    2. Zengqin Deng & Grigory Maksaev & Angela M. Schlegel & Jingying Zhang & Michael Rau & James A. J. Fitzpatrick & Elizabeth S. Haswell & Peng Yuan, 2020. "Structural mechanism for gating of a eukaryotic mechanosensitive channel of small conductance," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. Viktor Lukacs & Jayanti Mathur & Rong Mao & Pinar Bayrak-Toydemir & Melinda Procter & Stuart M. Cahalan & Helen J. Kim & Michael Bandell & Nicola Longo & Ronald W. Day & David A. Stevenson & Ardem Pat, 2015. "Impaired PIEZO1 function in patients with a novel autosomal recessive congenital lymphatic dysplasia," Nature Communications, Nature, vol. 6(1), pages 1-7, November.
    4. 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)

    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. 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.
    2. 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.
    3. Sine Yaganoglu & Konstantinos Kalyviotis & Christina Vagena-Pantoula & Dörthe Jülich & Benjamin M. Gaub & Maaike Welling & Tatiana Lopes & Dariusz Lachowski & See Swee Tang & Armando Del Rio Hernandez, 2023. "Highly specific and non-invasive imaging of Piezo1-dependent activity across scales using GenEPi," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Nathalia G. Amado & Elena D. Nosyreva & David Thompson & Thomas J. Egeland & Osita W. Ogujiofor & Michelle Yang & Alexandria N. Fusco & Niccolo Passoni & Jeremy Mathews & Brandi Cantarel & Linda A. Ba, 2024. "PIEZO1 loss-of-function compound heterozygous mutations in the rare congenital human disorder Prune Belly Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Waheed-Ul-Rahman Ahmed & Sam Kleeman & Michael Ng & Wei Wang & Adam Auton & Regent Lee & Ashok Handa & Krina T. Zondervan & Akira Wiberg & Dominic Furniss, 2022. "Genome-wide association analysis and replication in 810,625 individuals with varicose veins," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    6. Zhihui He & Yonghui Zhao & Michael J. Rau & James A. J. Fitzpatrick & Rajan Sah & Hongzhen Hu & Peng Yuan, 2023. "Structural and functional analysis of human pannexin 2 channel," Nature Communications, Nature, vol. 14(1), pages 1-10, 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. 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.
    9. 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.
    10. Ruo-Xu Gu & Bert L. Groot, 2023. "Central cavity dehydration as a gating mechanism of potassium channels," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    11. 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.

    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:13:y:2022:i:1:d:10.1038_s41467-022-28511-5. 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.