Force-induced conformational changes in PIEZO1.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
09 2019
Historique:
received: 14 11 2018
accepted: 25 07 2019
pubmed: 23 8 2019
medline: 27 3 2020
entrez: 23 8 2019
Statut: ppublish

Résumé

PIEZO1 is a mechanosensitive channel that converts applied force into electrical signals. Partial molecular structures show that PIEZO1 is a bowl-shaped trimer with extended arms. Here we use cryo-electron microscopy to show that PIEZO1 adopts different degrees of curvature in lipid vesicles of different sizes. We also use high-speed atomic force microscopy to analyse the deformability of PIEZO1 under force in membranes on a mica surface, and show that PIEZO1 can be flattened reversibly into the membrane plane. By approximating the absolute force applied, we estimate a range of values for the mechanical spring constant of PIEZO1. Both methods of microscopy demonstrate that PIEZO1 can deform its shape towards a planar structure. This deformation could explain how lateral membrane tension can be converted into a conformation-dependent change in free energy to gate the PIEZO1 channel in response to mechanical perturbations.

Identifiants

pubmed: 31435018
doi: 10.1038/s41586-019-1499-2
pii: 10.1038/s41586-019-1499-2
pmc: PMC7258172
mid: NIHMS1585185
doi:

Substances chimiques

Aluminum Silicates 0
Ion Channels 0
Liposomes 0
Piezo1 protein, mouse 0
mica V8A1AW0880

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

230-234

Subventions

Organisme : NCCIH NIH HHS
ID : DP1 AT010874
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States

Commentaires et corrections

Type : CommentIn

Références

Coste, B. et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55–60 (2010).
doi: 10.1126/science.1193270
Coste, B. et al. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483, 176–181 (2012).
doi: 10.1038/nature10812
Wu, J., Lewis, A. H. & Grandl, J. Touch, tension, and transduction – the function and regulation of Piezo ion channels. Trends Biochem. Sci. 42, 57–71 (2017).
doi: 10.1016/j.tibs.2016.09.004
Li, J. et al. Piezo1 integration of vascular architecture with physiological force. Nature 515, 279–282 (2014).
doi: 10.1038/nature13701
Ranade, S. S. et al. Piezo1, a mechanically activated ion channel, is required for vascular development in mice. Proc. Natl Acad. Sci. USA 111, 10347–10352 (2014).
doi: 10.1073/pnas.1409233111
Retailleau, K. et al. Piezo1 in smooth muscle cells is involved in hypertension-dependent arterial remodeling. Cell Reports 13, 1161–1171 (2015).
doi: 10.1016/j.celrep.2015.09.072
Cahalan, S. M. et al. Piezo1 links mechanical forces to red blood cell volume. eLife 4, (2015).
Wang, S. et al. Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release. J. Clin. Invest. 126, 4527–4536 (2016).
doi: 10.1172/JCI87343
Rode, B. et al. Piezo1 channels sense whole body physical activity to reset cardiovascular homeostasis and enhance performance. Nat. Commun. 8, 350 (2017).
doi: 10.1038/s41467-017-00429-3
Ranade, S. S. et al. Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 516, 121–125 (2014).
doi: 10.1038/nature13980
Woo, S. H. et al. Piezo2 is the principal mechanotransduction channel for proprioception. Nat. Neurosci. 18, 1756–1762 (2015).
doi: 10.1038/nn.4162
Demolombe, S., Duprat, F., Honoré, E. & Patel, A. Slower Piezo1 inactivation in dehydrated hereditary stomatocytosis (xerocytosis). Biophys. J. 105, 833–834 (2013).
doi: 10.1016/j.bpj.2013.07.018
Andolfo, I. et al. Novel Gardos channel mutations linked to dehydrated hereditary stomatocytosis (xerocytosis). Am. J. Hematol. 90, 921–926 (2015).
doi: 10.1002/ajh.24117
Fotiou, E. et al. Novel mutations in PIEZO1 cause an autosomal recessive generalized lymphatic dysplasia with non-immune hydrops fetalis. Nat. Commun. 6, 8085 (2015).
doi: 10.1038/ncomms9085
Coste, B. et al. Gain-of-function mutations in the mechanically activated ion channel PIEZO2 cause a subtype of distal arthrogryposis. Proc. Natl Acad. Sci. USA 110, 4667–4672 (2013).
doi: 10.1073/pnas.1221400110
Guo, Y. R. & MacKinnon, R. Structure-based membrane dome mechanism for Piezo mechanosensitivity. eLife 6, e33660 (2017).
doi: 10.7554/eLife.33660
Saotome, K. et al. Structure of the mechanically activated ion channel Piezo1. Nature 554, 481–486 (2018).
doi: 10.1038/nature25453
Zhao, Q. et al. Structure and mechanogating mechanism of the Piezo1 channel. Nature 554, 487–492 (2018).
doi: 10.1038/nature25743
Wu, J., Goyal, R. & Grandl, J. Localized force application reveals mechanically sensitive domains of Piezo1. Nat. Commun. 7, 12939 (2016).
doi: 10.1038/ncomms12939
Wang, Y. et al. A lever-like transduction pathway for long-distance chemical- and mechano-gating of the mechanosensitive Piezo1 channel. Nat. Commun. 9, 1300 (2018).
doi: 10.1038/s41467-018-03570-9
Lewis, A. H. & Grandl, J. Mechanical sensitivity of Piezo1 ion channels can be tuned by cellular membrane tension. eLife 4, e12088 (2015
doi: 10.7554/eLife.12088
Cox, C. D. et al. Removal of the mechanoprotective influence of the cytoskeleton reveals PIEZO1 is gated by bilayer tension. Nat. Commun. 7, 10366 (2016).
doi: 10.1038/ncomms10366
Árnadóttir, J. & Chalfie, M. Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39, 111–137 (2010).
doi: 10.1146/annurev.biophys.37.032807.125836
Brohawn, S. G., Su, Z. & MacKinnon, R. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K
doi: 10.1073/pnas.1320768111
Brohawn, S. G., Campbell, E. B. & MacKinnon, R. Physical mechanism for gating and mechanosensitivity of the human TRAAK K
doi: 10.1038/nature14013
Moe, P. & Blount, P. Assessment of potential stimuli for mechano-dependent gating of MscL: effects of pressure, tension, and lipid headgroups. Biochemistry 44, 12239–12244 (2005).
doi: 10.1021/bi0509649
Zhang, W. et al. Ankyrin repeats convey force to gate the NOMPC mechanotransduction channel. Cell 162, 1391–1403 (2015).
doi: 10.1016/j.cell.2015.08.024
Jin, P. et al. Electron cryo-microscopy structure of the mechanotransduction channel NOMPC. Nature 547, 118–122 (2017).
doi: 10.1038/nature22981
Gaub, B. M. & Müller, D. J. Mechanical stimulation of Piezo1 receptors depends on extracellular matrix proteins and directionality of force. Nano Lett. 17, 2064–2072 (2017).
doi: 10.1021/acs.nanolett.7b00177
Hamill, O. P. & McBride, D. W., Jr. Induced membrane hypo/hyper-mechanosensitivity: a limitation of patch-clamp recording. Annu. Rev. Physiol. 59, 621–631 (1997).
doi: 10.1146/annurev.physiol.59.1.621
Suchyna, T. M., Markin, V. S. & Sachs, F. Biophysics and structure of the patch and the gigaseal. Biophys. J. 97, 738–747 (2009).
doi: 10.1016/j.bpj.2009.05.018
Moroni, M., Servin-Vences, M. R., Fleischer, R., Sánchez-Carranza, O. & Lewin, G. R. Voltage gating of mechanosensitive PIEZO channels. Nat. Commun. 9, 1096 (2018).
doi: 10.1038/s41467-018-03502-7
Lacroix, J. J., Botello-Smith, W. M. & Luo, Y. Probing the gating mechanism of the mechanosensitive channel Piezo1 with the small molecule Yoda1. Nat. Commun. 9, 2029 (2018).
doi: 10.1038/s41467-018-04405-3
Ando, T., Uchihashi, T. & Scheuring, S. Filming biomolecular processes by high-speed atomic force microscopy. Chem. Rev. 114, 3120–3188 (2014).
doi: 10.1021/cr4003837
Miyagi, A. & Scheuring, S. Automated force controller for amplitude modulation atomic force microscopy. Rev. Sci. Instrum. 87, 053705 (2016).
doi: 10.1063/1.4950777
Helfrich, W. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. C 28, 693–703 (1973).
doi: 10.1515/znc-1973-11-1209
Legleiter, J., Park, M., Cusick, B. & Kowalewski, T. Scanning probe acceleration microscopy (SPAM) in fluids: mapping mechanical properties of surfaces at the nanoscale. Proc. Natl Acad. Sci. USA 103, 4813–4818 (2006).
doi: 10.1073/pnas.0505628103
Kiracofe, D. et al. VEDA: Virtual Environment for Dynamic AFM, https://nanohub.org/resources/veda (2012).
Guzman, H. V., Garcia, P. D. & Garcia, R. Dynamic force microscopy simulator (dForce): A tool for planning and understanding tapping and bimodal AFM experiments. Beilstein J. Nanotechnol. 6, 369–379 (2015).
doi: 10.3762/bjnano.6.36
García, R. & San Paulo, A. Attractive and repulsive tip-sample interaction regimes in tapping-mode atomic force microscopy. Phys. Rev. B 60, 4961–4967 (1999).
doi: 10.1103/PhysRevB.60.4961
Weisstein, E. W. Spherical Cap, from MathWorld–a Wolfram web resource. http://mathworld.wolfram.com/SphericalCap.html .
Haselwandter, C. A. & MacKinnon, R. Piezo’s membrane footprint and its contribution to mechanosensitivity. eLife 7, e41968 (2018).
doi: 10.7554/eLife.41968
Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
doi: 10.1016/j.jsb.2005.07.007
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
doi: 10.1038/nmeth.4193
Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
doi: 10.1016/j.jsb.2015.08.008
Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
doi: 10.1016/j.jsb.2012.09.006
Kimanius, D., Forsberg, B. O., Scheres, S. H. & Lindahl, E. Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. eLife 5, e18722 (2016).
doi: 10.7554/eLife.18722

Auteurs

Yi-Chih Lin (YC)

Department of Anesthesiology, Weill Cornell Medicine, New York, NY, USA.
Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA.

Yusong R Guo (YR)

Laboratory of Molecular Neurobiology and Biophysics, Howard Hughes Medical Institute, TheRockefeller University, New York, NY, USA.

Atsushi Miyagi (A)

Department of Anesthesiology, Weill Cornell Medicine, New York, NY, USA.
Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA.

Jesper Levring (J)

Laboratory of Molecular Neurobiology and Biophysics, Howard Hughes Medical Institute, TheRockefeller University, New York, NY, USA.

Roderick MacKinnon (R)

Laboratory of Molecular Neurobiology and Biophysics, Howard Hughes Medical Institute, TheRockefeller University, New York, NY, USA. mackinn@mail.rockefeller.edu.

Simon Scheuring (S)

Department of Anesthesiology, Weill Cornell Medicine, New York, NY, USA. sis2019@med.cornell.edu.
Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA. sis2019@med.cornell.edu.

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