A lever-like transduction pathway for long-distance chemical- and mechano-gating of the mechanosensitive Piezo1 channel

Nature Communications, Journal Year: 2018, Volume and Issue: 9(1)

Published: April 3, 2018

Abstract Piezo1 represents a prototype of eukaryotic mechanotransduction channels. The full-length 2547-residue mouse possesses unique 38-transmembrane-helix (TM) topology and is organized into three-bladed, propeller-shaped architecture, comprising central ion-conducting pore, three peripheral blade-like structures, 90-Å-long intracellular beam-resembling structures that bridge the blades to pore. However, how mechanical force chemicals activate gigantic machinery remains elusive. Here we identify novel set chemical activators, termed Jedi, which activates through extracellular side blade instead C-terminal domain indicating long-range allosteric gating. Remarkably, Jedi-induced activation requires key components, including two loops in distal leucine residues proximal end beam. Thus, employs blade-beam-constituted lever-like apparatus as designated transduction pathway for long-distance mechano- chemical-gating

Language: Английский

---

How cells channel their stress: Interplay between Piezo1 and the cytoskeleton

Seminars in Cell and Developmental Biology, Journal Year: 2017, Volume and Issue: 71, P. 3 - 12

Published: July 1, 2017

Language: Английский

---

Roles of the cytoskeleton, cell adhesion and rho signalling in mechanosensing and mechanotransduction

The Journal of Biochemistry, Journal Year: 2017, Volume and Issue: unknown, P. mvw082 - mvw082

Published: Jan. 12, 2017

All cells sense and respond to various mechanical forces in properties of their environment. To appropriately, must be able the location, direction, strength duration these forces. Recent progress mechanobiology has provided a better understanding mechanisms mechanoresponses underlying many cellular developmental processes. Various roles development tissue homeostasis have been elucidated, molecules involved mechanotransduction identified. However, whole picture functions molecular remains understood. Recently, novel for sensing transducing stresses via cytoskeleton, cell–substrate cell–cell adhesions related proteins In this review, we outline adhesions, mechanosensing mechanotransduction. We also describe regulation Rho-family GTPases mechanoresponses.

Language: Английский

---

Biophysical Principles of Ion-Channel-Mediated Mechanosensory Transduction

Cell Reports, Journal Year: 2019, Volume and Issue: 29(1), P. 1 - 12

Published: Oct. 1, 2019

Recent rapid progress in the field of mechanobiology has been driven by novel emerging tools and methodologies growing interest from different scientific disciplines. Specific made toward understanding how cell mechanics is linked to intracellular signaling regulation gene expression response a variety mechanical stimuli. There direct link between mechanoreceptors at surface biochemical signaling, which turn controls downstream effector molecules. Among membrane, mechanosensitive (MS) ion channels are essential for ultra-rapid (millisecond) transduction stimuli into biologically relevant signals. The three decades research on resulted formulation two basic principles channel gating: force-from-lipids force-from-filament. In this review, we revisit biophysical that underlie innate force-sensing ability as contributors force-dependent evolution life forms. Mechanobiology an exciting, rapidly multidisciplinary area intersection biology, physics, engineering, medicine. It studies role forces play physiology pathology biological systems combining large array complementary (Roca-Cusachs et al., 2017Roca-Cusachs P. Conte V. Trepat X. Quantifying biology.Nat. Cell Biol. 2017; 19: 742-751Crossref PubMed Scopus (73) Google Scholar, Lele 2007Lele T.P. Sero J.E. Matthews B.D. Kumar S. Xia Montoya-Zavala M. Polte T. Overby D. Wang N. Ingber D.E. Tools study mechanotransduction.Methods 2007; 83: 443-472PubMed Sinha 2018Sinha B. Biswas A. Soni G.V. Cellular Nuclear Forces: An Overview.Methods Mol. 2018; 1805: 1-29Crossref (1) Scholar). Thanks new available recent biophysics, molecular genetics, computational modeling, engineering research, greatly contributed our environmental cues influence cytoplasmic nuclear events. Major cellular behavior fate (Discher 2005Discher Janmey Y.L. Tissue cells feel respond stiffness their substrate.Science. 2005; 310: 1139-1143Crossref (3754) Iskratsch 2014Iskratsch Wolfenson H. Sheetz M.P. Appreciating force shape—the rise mechanotransduction Rev. 2014; 15: 825-833Crossref (330) Paluch Discher, 2015Paluch E.K. Discher motion mechanobiology.Mol. Cell. 2015; 26: 1011Crossref (3) Given manifests itself many forms, including omnipresent gravitational osmotic well contact-based sound, shear stress, stretching, bending, twisting, compressing, it seems obvious throughout evolution, forms have developed multitude ways counteract adapt challenges they continuously experience corresponding niches. receptors channels, G protein-coupled (GPCRs), integrins. These indirectly or directly interact with cytosolic elements, such microtubules actin filaments. This way, can sense transmit may regulate transcription level (Sinha primary mechanosensory membrane proteins origin cascades, quite unique, most converting electrochemical signals (e.g., millisecond timescale) (Martinac Cox, 2017Martinac Cox C.D. Mechanosensory transduction: focus channels.in: Comprehensive Biophysics. Elsevier, 2017https://doi.org/10.1016/B978-0-12-809633-8.08094-8Google studied >30 years widely expressed both specialized sensory non-specialized types. They cloned all domains encompassing prokaryotic eukaryotic organisms, red blood (Hamill, 1983Hamill O.P. Potassium chloride current cells.in: Sakmann Neher E. Single-Channel Recording. Springer, 1983: 451-471Crossref Scholar), chick skeletal (Guharay Sachs, 1984Guharay F. Sachs Stretch-activated single currents tissue-cultured embryonic muscle.J. Physiol. 1984; 352: 685-701Crossref Scholar) frog muscle (Brehm 1984Brehm Kullberg R. Moody-Corbett Properties non-junctional acetylcholine receptor innervated Xenopus laevis.J. 350: 631-648Crossref (0) bacteria 1987Martinac Buechner Delcour A.H. Adler J. Kung C. Pressure-sensitive Escherichia coli.Proc. Natl. Acad. Sci. USA. 1987; 84: 2297-2301Crossref (454) fungi (Gustin 1988Gustin M.C. Zhou X.L. Martinac A yeast plasma membrane.Science. 1988; 242: 762-765Crossref plants (Falke 1988Falke L.C. Edwards K.L. Pickard B.G. Misler stretch-activated anion tobacco protoplasts.FEBS Lett. 237: 141-144Crossref Functional pivotal numerous processes ranging osmoregulation bacteria, fungi, highly senses hearing touch. As result, present "specialized" dedicated detecting exogenous cells. Examples include those found cutaneous nerve formations, example, Meissner's corpuscle (rapidly adapting mechanoreceptors) Merkel (slowly mechanoreceptors), harbor Piezo2 fine touch (García-Mesa 2017García-Mesa Y. García-Piqueras García Feito Cabo Cobo Vega J.A. García-Suárez O. corpuscles human digital skin display immunoreactivity.J. Anat. 231: 978-989Crossref Ranade 2014Ranade S.S. Woo S.H. Dubin A.E. Moshourab R.A. Wetzel Petrus Mathur Bégay Coste Mainquist al.Piezo2 major transducer sensation mice.Nature. 516: 121-125Crossref (212) 2014Woo Weyer A.D. Baba Qiu Z. Miyamoto Reddy K. Lumpkin E.A. required Merkel-cell mechanotransduction.Nature. 509: 622-626Crossref (231) Maksimovic 2014Maksimovic Nakatani Nelson A.M. Marshall Wellnitz S.A. Firozi Patapoutian Epidermal tune mammalian receptors.Nature. 617-621Crossref (189) Auditory hair cells, site final transformer underlies hearing, rely functional transmembrane channel-like 1 (TMC1) TMC2 proteins, whose genetic deletion renders knockout mouse mechanically insensitive (Corey Holt, 2016Corey D.P. Holt J.R. Are TMCs Mechanotransduction Channels Vertebrate Hair Cells?.J. Neurosci. 2016; 36: 10921-10926Crossref (15) TMC1 seem be part larger complex, but alone combination, line pore (Pan 2018Pan Akyuz Liu X.P. Asai Nist-Lund Kurima Derfler B.H. Gyorgy Limapichat W. Walujkar al.TMC1 Forms Pore Transduction Inner Ear Cells.Neuron. 99: 736-753.e6Abstract Full Text PDF Both members Piezo family also important determinants mechanosensing baroreceptive neurons innervate regions aortic arch (Zeng 2018Zeng W.Z. Min Daou I. Chapleau M.W. Abboud F.M. Liberles S.D. PIEZOs mediate neuronal sensing pressure baroreceptor reflex.Science. 362: 464-467Crossref (7) Furthermore, global Piezo1 was shown lethal mice, indicating importance mammals (Li 2014Li Hou Tumova Muraki Bruns Ludlow M.J. Sedo Hyman A.J. McKeown L. Young R.S. al.Piezo1 integration vascular architecture physiological force.Nature. 515: 279-282Crossref (225) Moreover, mutations cause plethora hereditary diseases contribute pathophysiology complex chronic conditions (Bae 2013Bae Gnanasambandam Nicolai Gottlieb P.A. Xerocytosis caused alter kinetics PIEZO1.Proc. 2013; 110: E1162-E1168Crossref (129) Fotiou 2015Fotiou Martin-Almedina Simpson M.A. Lin Gordon Brice G. Atton Jeffery Rees D.C. Mignot al.Novel PIEZO1 autosomal recessive generalized lymphatic dysplasia non-immune hydrops fetalis.Nat. Commun. 6: 8085Crossref (83) Alper, 2017Alper S.L. Genetic Diseases PIEZO2 Dysfunction.Curr. Top. Membr. 79: 97-134Crossref (13) (For comprehensive review roles readers directed 2015Ranade Syeda Mechanically Activated Ion Channels.Neuron. 87: 1162-1179Abstract (141) Scholar; Hamilton 2015bHamilton E.S. Schlegel Haswell United diversity: plants.Annu. Plant 66: 113-137Crossref (47) Scholar.) addition mentioned above, almost every system contains endogenous likely involved general functions migration rigidity sense, mechanosensitive. makes heterologous characterization types difficult (Dubin 2017Dubin Murthy Lewis Brosse Cahalan S.M. Grandl Endogenous Can Confound Channel Identification Characterization.Neuron. 94: 266-270.e3Abstract (22) systems, tissue tends scarce structural environment equally identity channel. application experimental not readily controlled ligand concentration, temperature, voltage. Despite difficulties identification, exciting think organisms remains unsolved. Central these change conformation deformation. some earliest reports activity, immediately recognized gating had stretch (Sachs, 1988Sachs Mechanical systems.Crit. Biomed. Eng. 16: 141-169PubMed When assessed whether (stress normal plane membrane) tension gated could demonstrated whole-cell "excised patch" experiments (Sokabe 1991Sokabe Jing Z.Q. Quantitative video microscopy patch clamped membranes strain, capacitance, activation.Biophys. 1991; 59: 722-728Abstract regulated activity. justified use Laplace's law thin-walled sphere equilibrium, links T P radius r through = Pr/2 1986Sachs Biophysics mechanoreception.Membr. Biochem. 1986; 173-195Crossref issue, however, reconciling fact tensions generated orders magnitude lower (0.01–0.1 mN/m) than experimentally measured gate patch-clamp (0.5–10 (Lewis Grandl, 2015Lewis sensitivity tuned tension.eLife. 4: e12088Crossref (70) Maksaev 2011Maksaev Milac Anishkin Guy H.R. Sukharev Analyses thermodynamics effects deletions TREK-1: comparisons models.Channels (Austin). 2011; 5: 34-42Crossref Apart relative simplicity assumptions theoretical modeling properties (Bavi 2014aBavi Nakayama Bavi Qin Q.H. Biophysical implications lipid bilayer rheometry channels.Proc. 111: 13864-13869Crossref (18) Rawicz 2000Rawicz Olbrich K.C. McIntosh Needham Evans Effect chain length unsaturation elasticity bilayers.Biophys. 2000; 328-339Abstract Rodowicz 2010Rodowicz K.A. Francisco Layton Determination DOPC:DOPS liposomes using image procession algorithm micropipette-aspiration techniques.Chem. Phys. Lipids. 2010; 163: 787-793Crossref (11) discrepancy rooted vitro clamp) often very distinct way native environment. Two famous cases point asymmetry due its intrinsic profile asymmetric insertion amphipaths) local curvature energetically shift equilibrium state MS 1990Martinac Mechanosensitive coli activated amphipaths.Nature. 1990; 348: 261-263Crossref (322) Guo MacKinnon, 2017Guo Y.R.A.M. MacKinnon Structure-based dome mechanism mechanosensitivity.eLife. e33660Crossref (39) 2016bBavi Vossoughi Naghdabadi Jamali Influence Global Local Membrane Curvature Channels: Finite Element Approach.Membranes (Basel). E14Crossref aim perspective article update concepts used describe mechanotransduction. We discuss possible unifying principle narrows various physical affecting tissues distilled down. Our reduce discussions "spherical cows," propose lowest common denominator acting interface. addition, address "force sharing" explain vagaries mechanosensitive-channel-mediated transduction. hope provocative discussion will help lead better evolutionary mechanotransduction, anchored universal laws physics chemistry guided act ways, shearing, rupturing wall, and/or cytoskeletal integrins, cadherins), depending direction intensity. To protect integrity, belonging phyla tree strategies potentially negative impact physiologically acceptable level. Cell-walled prokaryotes (Bacteria Archaea) plants, protected sudden changes osmolarity thick walls. Without support would destroy fragile water uptake upon hypo-osmotic shock. Although structure components wall vary among cell-walled (Hamill Martinac, 2001Hamill Molecular basis living cells.Physiol. 2001; 81: 685-740Crossref average resist pressures up 30 atm Kloda, 2003Martinac Kloda Evolutionary origins channels.Prog. Biophys. 2003; 82: 11-24Crossref Peyronnet 2014Peyronnet Tran Girault Frachisse J.M. channels: feeling world under pressure.Front. 558Crossref (31) 2018aCox Bacterial Mechanosensors.Annu. 80: 71-93Crossref thickness Young's elastic modulus (a property indicative solid material) differ envelopes Gram-negative Gram-positive bacteria. apparent reported 50 150 MPa, while estimated 100 200 MPa Bacillus subtilis (i.e., stiffer) (Tuson 2012Tuson H.H. Auer G.K. Renner L.D. Hasebe Tropini Salick Crone W.C. Gopinathan Huang Weibel D.B. Measuring bacterial growth rates hydrogels tunable elasticity.Mol. Microbiol. 2012; 874-891Crossref (84) relatively thicker well. Considering properties, ∼90% turgor pressure, whereas remaining 10% sustained (Cox supported only rudimentary cytoskeleton (Mayer, 2003Mayer Cytoskeletons prokaryotes.Cell Int. 27: 429-438Crossref component must share during shocks. correspond ∼18 mN/m, approximates lytic pure (∼20 (Nomura 2012Nomura Cranfield C.G. Deplazes Owen D.M. Macmillan Battle A.R. Constantine Sokabe Differential lipids lyso-lipids mechanosensitivity MscL MscS.Proc. 109: 8770-8775Crossref (88) discussed briefly here further text, sufficient fully activate MscS, function nanovalves (Levina 1999Levina Tötemeyer Stokes N.R. Louis Jones Booth I.R. Protection against extreme activation MscS identification genes activity.EMBO 1999; 18: 1730-1737Crossref Consequently, peptidoglycan protects excessive taking majority (Shaikh 2014Shaikh Nomura Energetics azolectin giant spheroplasts.Channels. 8: 321-326Crossref (17) exhibits increased liposome patches compared spheroplasts, contain other proteins; them seemingly contact remnants spheroplasts. form separate subfamilies channels. subfamily largely confined archaeal diverse terms function, spread origins, algae, yeast, parasites Plasmodium Trypanosoma (Malcolm Maurer, 2012Malcolm Maurer small conductance (MscS) superfamily: just anymore.ChemBioChem. 13: 2037-2043Crossref 2015Cox 'tinkering' MscS-like generation diversity.Pflugers Arch. 467: 3-13Crossref Haswell, 2007Haswell plants.Curr. 58: 329-359Crossref Yoshimura, 1998Yoshimura body Chlamydomonas.J. 1998; 166: 149-155Crossref Kung, 1992Zhou Schizosaccharomyces pombe.EMBO 1992; 11: 2869-2875Crossref Pivetti 2003Pivetti Yen M.R. Miller Busch Tseng Y.H. Saier Jr., M.H. families proteins.Microbiol. 67: 66-85Crossref (151) 2014Martinac Chi Petrov Rohde P.R. Foo Rothnagel Carne al.Bacterial models studying transduction.Antioxid. Redox Signal. 20: 952-969Crossref high 15–20 (Haswell, resting plant protoplasts ∼0.12 mN/m (Morris Homann, 2001Morris C.E. Homann U. tension.J. 179: 79-102Crossref enough However, given protoplast were lyse ∼5 (Wolfe Steponkus, 1983Wolfe Steponkus P.L. isolated protoplasts: hyperosmotic extracellular freezing injury.Plant 1983; 71: 276-285Crossref temporary ≤5 possible. thus similar prokaryotes. more processes, plastid morphology (Haswell Meyerowitz, 2006Haswell Meyerowitz E.M. control size shape Arabidopsis thaliana.Curr. 2006; 1-11Abstract (179) pollen germination (Hamilton 2015aHamilton Jensen G.S. Katims Sherp MSL8 regulates hydration germination.Science. 438-441Crossref (49) Compared animal usually fluctuations possess matrix, preserving deformability growth, differentiation, movement (Figure 1A). matrix meshed soft structures, allowing modify deformation (Elson, 1988Elson E.L. indicator function.Annu. Chem. 17: 397-430Crossref Due differences components, varies hundreds Pascals several megapascals, type (Qi 2015Qi Andolfi Frattini Mayer Lazzarino Hu stiffening STOML3 facilita

Language: Английский

---

An Ultrasensitive, Visco‐Poroelastic Artificial Mechanotransducer Skin Inspired by Piezo2 Protein in Mammalian Merkel Cells

Advanced Materials, Journal Year: 2017, Volume and Issue: 29(13)

Published: Feb. 10, 2017

An artificial ionic mechanotransducer skin with an unprecedented sensitivity over a wide spectrum of pressure by fabricating visco-poroelastic nanochannels and microstructured features, directly mimicking the physiological tactile sensing mechanism Piezo2 protein is demonstrated. This capability enables voice identification, health monitoring, daily measurements, even measurements heavy weight beyond capabilities human skin. As service to our authors readers, this journal provides supporting information supplied authors. Such materials are peer reviewed may be re-organized for online delivery, but not copy-edited or typeset. Technical support issues arising from (other than missing files) should addressed Please note: The publisher responsible content functionality any Any queries content) directed corresponding author article.

Language: Английский

---