Literature DB >> 28636944

Transduction of Repetitive Mechanical Stimuli by Piezo1 and Piezo2 Ion Channels.

Amanda H Lewis1, Alisa F Cui1, Malcolm F McDonald1, Jörg Grandl2.   

Abstract

Several cell types experience repetitive mechanical stimuli, including vein endothelial cells during pulsating blood flow, inner ear hair cells upon sound exposure, and skin cells and their innervating dorsal root ganglion (DRG) neurons when sweeping across a textured surface or touching a vibrating object. While mechanosensitive Piezo ion channels have been clearly implicated in sensing static touch, their roles in transducing repetitive stimulations are less clear. Here, we perform electrophysiological recordings of heterologously expressed mouse Piezo1 and Piezo2 responding to repetitive mechanical stimulations. We find that both channels function as pronounced frequency filters whose transduction efficiencies vary with stimulus frequency, waveform, and duration. We then use numerical simulations and human disease-related point mutations to demonstrate that channel inactivation is the molecular mechanism underlying frequency filtering and further show that frequency filtering is conserved in rapidly adapting mouse DRG neurons. Our results give insight into the potential contributions of Piezos in transducing repetitive mechanical stimuli.
Copyright © 2017 The Author(s). Published by Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Piezo1; Piezo2; dorsal root ganglia neurons; four-state gating mechanism; frequency filtering; inactivation; mechanosensitive ion channel; mechanotransduction; repetitive stimulation

Mesh:

Substances:

Year:  2017        PMID: 28636944      PMCID: PMC5646378          DOI: 10.1016/j.celrep.2017.05.079

Source DB:  PubMed          Journal:  Cell Rep            Impact factor:   9.423


  54 in total

1.  Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release.

Authors:  ShengPeng Wang; Ramesh Chennupati; Harmandeep Kaur; Andras Iring; Nina Wettschureck; Stefan Offermanns
Journal:  J Clin Invest       Date:  2016-10-31       Impact factor: 14.808

2.  Piezo1, a mechanically activated ion channel, is required for vascular development in mice.

Authors:  Sanjeev S Ranade; Zhaozhu Qiu; Seung-Hyun Woo; Sung Sik Hur; Swetha E Murthy; Stuart M Cahalan; Jie Xu; Jayanti Mathur; Michael Bandell; Bertrand Coste; Yi-Shuan J Li; Shu Chien; Ardem Patapoutian
Journal:  Proc Natl Acad Sci U S A       Date:  2014-06-23       Impact factor: 11.205

3.  Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels.

Authors:  Bertrand Coste; Jayanti Mathur; Manuela Schmidt; Taryn J Earley; Sanjeev Ranade; Matt J Petrus; Adrienne E Dubin; Ardem Patapoutian
Journal:  Science       Date:  2010-09-02       Impact factor: 47.728

4.  Mechanical transmission in a Pacinian corpuscle. An analysis and a theory.

Authors:  W R Loewenstein; R Skalak
Journal:  J Physiol       Date:  1966-01       Impact factor: 5.182

5.  Value of the duplex waveform at the common femoral artery for diagnosing obstructive aortoiliac disease.

Authors:  Sandra Spronk; Pieter T den Hoed; Leenoud C W de Jonge; Lukas C van Dijk; Peter M T Pattynama
Journal:  J Vasc Surg       Date:  2005-08       Impact factor: 4.268

6.  Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1.

Authors:  Chilman Bae; Radhakrishnan Gnanasambandam; Chris Nicolai; Frederick Sachs; Philip A Gottlieb
Journal:  Proc Natl Acad Sci U S A       Date:  2013-03-04       Impact factor: 11.205

7.  The Role of PIEZO2 in Human Mechanosensation.

Authors:  Alexander T Chesler; Marcin Szczot; Diana Bharucha-Goebel; Marta Čeko; Sandra Donkervoort; Claire Laubacher; Leslie H Hayes; Katharine Alter; Cristiane Zampieri; Christopher Stanley; A Micheil Innes; Jean K Mah; Carla M Grosmann; Nathaniel Bradley; David Nguyen; A Reghan Foley; Claire E Le Pichon; Carsten G Bönnemann
Journal:  N Engl J Med       Date:  2016-09-21       Impact factor: 91.245

8.  Piezo1 ion channel pore properties are dictated by C-terminal region.

Authors:  Bertrand Coste; Swetha E Murthy; Jayanti Mathur; Manuela Schmidt; Yasmine Mechioukhi; Patrick Delmas; Ardem Patapoutian
Journal:  Nat Commun       Date:  2015-05-26       Impact factor: 14.919

9.  Gigaseal mechanics: creep of the gigaseal under the action of pressure, adhesion, and voltage.

Authors:  Radomir I Slavchov; Takeshi Nomura; Boris Martinac; Masahiro Sokabe; Frederick Sachs
Journal:  J Phys Chem B       Date:  2014-10-22       Impact factor: 2.991

10.  Localized force application reveals mechanically sensitive domains of Piezo1.

Authors:  Jason Wu; Raman Goyal; Jörg Grandl
Journal:  Nat Commun       Date:  2016-10-03       Impact factor: 14.919

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  32 in total

1.  Cellular transduction of mechanical oscillations in plants by the plasma-membrane mechanosensitive channel MSL10.

Authors:  Daniel Tran; Tiffanie Girault; Marjorie Guichard; Sébastien Thomine; Nathalie Leblanc-Fournier; Bruno Moulia; Emmanuel de Langre; Jean-Marc Allain; Jean-Marie Frachisse
Journal:  Proc Natl Acad Sci U S A       Date:  2021-01-05       Impact factor: 11.205

Review 2.  Piezos thrive under pressure: mechanically activated ion channels in health and disease.

Authors:  Swetha E Murthy; Adrienne E Dubin; Ardem Patapoutian
Journal:  Nat Rev Mol Cell Biol       Date:  2017-10-04       Impact factor: 94.444

3.  Molecular basis of tactile specialization in the duck bill.

Authors:  Eve R Schneider; Evan O Anderson; Marco Mastrotto; Jon D Matson; Vincent P Schulz; Patrick G Gallagher; Robert H LaMotte; Elena O Gracheva; Sviatoslav N Bagriantsev
Journal:  Proc Natl Acad Sci U S A       Date:  2017-11-06       Impact factor: 11.205

Review 4.  Mechanotransduction and Uterine Blood Flow in Preeclampsia: The Role of Mechanosensing Piezo 1 Ion Channels.

Authors:  Olufunke O Arishe; Anthony B Ebeigbe; R Clinton Webb
Journal:  Am J Hypertens       Date:  2020-01-01       Impact factor: 2.689

5.  Roles of TRPV4 and piezo channels in stretch-evoked Ca2+ response in chondrocytes.

Authors:  Genlai Du; Li Li; Xinwang Zhang; Jianbing Liu; Jianqing Hao; Jianjun Zhu; Hao Wu; Weiyi Chen; Quanyou Zhang
Journal:  Exp Biol Med (Maywood)       Date:  2019-12-02

6.  Cell-Type-Specific Splicing of Piezo2 Regulates Mechanotransduction.

Authors:  Marcin Szczot; Leah A Pogorzala; Hans Jürgen Solinski; Lynn Young; Philina Yee; Claire E Le Pichon; Alexander T Chesler; Mark A Hoon
Journal:  Cell Rep       Date:  2017-12-05       Impact factor: 9.423

7.  Mechanically activated piezo channels modulate outflow tract valve development through the Yap1 and Klf2-Notch signaling axis.

Authors:  Anne-Laure Duchemin; Hélène Vignes; Julien Vermot
Journal:  Elife       Date:  2019-09-16       Impact factor: 8.140

8.  TRPV4 channel opening mediates pressure-induced pancreatitis initiated by Piezo1 activation.

Authors:  Sandip M Swain; Joelle M-J Romac; Rafiq A Shahid; Stephen J Pandol; Wolfgang Liedtke; Steven R Vigna; Rodger A Liddle
Journal:  J Clin Invest       Date:  2020-05-01       Impact factor: 14.808

Review 9.  The Form and Function of PIEZO2.

Authors:  Marcin Szczot; Alec R Nickolls; Ruby M Lam; Alexander T Chesler
Journal:  Annu Rev Biochem       Date:  2021-06-20       Impact factor: 23.643

10.  Piezo1 channels mediate trabecular meshwork mechanotransduction and promote aqueous fluid outflow.

Authors:  Oleg Yarishkin; Tam T T Phuong; Jackson M Baumann; Michael L De Ieso; Felix Vazquez-Chona; Christopher N Rudzitis; Chad Sundberg; Monika Lakk; W Daniel Stamer; David Križaj
Journal:  J Physiol       Date:  2020-12-12       Impact factor: 5.182

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