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The Piezo channel is a mechano-sensitive complex component in the mammalian inner ear hair cell

Author

Listed:
  • Jeong Han Lee

    (University of Nevada)

  • Maria C. Perez-Flores

    (University of Nevada)

  • Seojin Park

    (University of Nevada
    Prestige Biopharma)

  • Hyo Jeong Kim

    (University of Nevada)

  • Yingying Chen

    (University of Nevada)

  • Mincheol Kang

    (University of Nevada
    Prestige Biopharma)

  • Jennifer Kersigo

    (University of Iowa)

  • Jinsil Choi

    (University of Nevada)

  • Phung N. Thai

    (University of California)

  • Ryan L. Woltz

    (University of California)

  • Dolores Columba Perez-Flores

    (University of Nevada)

  • Guy Perkins

    (University of California San Diego)

  • Choong-Ryoul Sihn

    (University of Nevada)

  • Pauline Trinh

    (University of California)

  • Xiao-Dong Zhang

    (University of California)

  • Padmini Sirish

    (University of California)

  • Yao Dong

    (University of California)

  • Wayne Wei Feng

    (University of California)

  • Isaac N. Pessah

    (University of California)

  • Rose E. Dixon

    (Tupper Hall)

  • Bernd Sokolowski

    (University of South Florida)

  • Bernd Fritzsch

    (University of Iowa)

  • Nipavan Chiamvimonvat

    (University of California
    VA Northern California Healthcare System)

  • Ebenezer N. Yamoah

    (University of Nevada)

Abstract

The inner ear is the hub where hair cells (HCs) transduce sound, gravity, and head acceleration stimuli to the brain. Hearing and balance rely on mechanosensation, the fastest sensory signals transmitted to the brain. The mechanoelectrical transducer (MET) channel is the entryway for the sound-balance-brain interface, but the channel-complex composition is not entirely known. Here, we report that the mouse utilizes Piezo1 (Pz1) and Piezo2 (Pz2) isoforms as MET-complex components. The Pz channels, expressed in HC stereocilia, and cell lines are co-localized and co-assembled with MET complex partners. Mice expressing non-functional Pz1 and Pz2 at the ROSA26 locus have impaired auditory and vestibular traits that can only be explained if the Pzs are integral to the MET complex. We suggest that Pz subunits constitute part of the MET complex and that interactions with other MET complex components yield functional MET units to generate HC MET currents.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44230-x
    DOI: 10.1038/s41467-023-44230-x
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    References listed on IDEAS

    as
    1. 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.
    2. Piotr Kazmierczak & Hirofumi Sakaguchi & Joshua Tokita & Elizabeth M. Wilson-Kubalek & Ronald A. Milligan & Ulrich Müller & Bechara Kachar, 2007. "Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells," Nature, Nature, vol. 449(7158), pages 87-91, September.
    3. 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.
    4. Seung-Hyun Woo & Sanjeev Ranade & Andy D. Weyer & Adrienne E. Dubin & Yoshichika Baba & Zhaozhu Qiu & Matt Petrus & Takashi Miyamoto & Kritika Reddy & Ellen A. Lumpkin & Cheryl L. Stucky & Ardem Patap, 2014. "Piezo2 is required for Merkel-cell mechanotransduction," Nature, Nature, vol. 509(7502), pages 622-626, May.
    5. 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.
    6. Beth A. McNally & Agila Somasundaram & Megumi Yamashita & Murali Prakriya, 2012. "Gated regulation of CRAC channel ion selectivity by STIM1," Nature, Nature, vol. 482(7384), pages 241-245, February.
    7. Jan Siemens & Concepcion Lillo & Rachel A. Dumont & Anna Reynolds & David S. Williams & Peter G. Gillespie & Ulrich Müller, 2004. "Cadherin 23 is a component of the tip link in hair-cell stereocilia," Nature, Nature, vol. 428(6986), pages 950-955, April.
    8. Anthony W. Peng & Felipe T. Salles & Bifeng Pan & Anthony J. Ricci, 2011. "Integrating the biophysical and molecular mechanisms of auditory hair cell mechanotransduction," Nature Communications, Nature, vol. 2(1), pages 1-14, September.
    9. Christian Söllner & Gerd-Jörg Rauch & Jan Siemens & Robert Geisler & Stephan C. Schuster & Ulrich Müller & Teresa Nicolson, 2004. "Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells," Nature, Nature, vol. 428(6986), pages 955-959, April.
    10. 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.
    11. Maryline Beurg & Runjia Cui & Adam C. Goldring & Seham Ebrahim & Robert Fettiplace & Bechara Kachar, 2018. "Variable number of TMC1-dependent mechanotransducer channels underlie tonotopic conductance gradients in the cochlea," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
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