Nature, Journal Year: 2021, Volume and Issue: 590(7846), P. 509 - 514
Published: Feb. 10, 2021
Language: Английский
Annual Review of Neuroscience, Journal Year: 2020, Volume and Issue: 43(1), P. 207 - 229
Published: Feb. 22, 2020
Activation of mechanosensitive ion channels underlies a variety fundamental physiological processes that require sensation mechanical force. Different adapt distinctive structures and mechanotransduction mechanisms to fit their biological roles. How work, especially in animals, has been extensively studied the past decade. Here we review key findings functional structural characterizations these highlight features relevant mechanism each specific channel.
Language: Английский
Citations
211
Nature Communications, Journal Year: 2019, Volume and Issue: 10(1)
Published: Oct. 3, 2019
Mechanosensitive Piezo1 and Piezo2 channels transduce various forms of mechanical forces into cellular signals that play vital roles in many important biological processes vertebrate organisms. Besides forces, is selectively activated by micromolar concentrations the small molecule Yoda1 through an unknown mechanism. Here, using a combination all-atom molecular dynamics simulations, calcium imaging electrophysiology, we identify allosteric binding pocket located putative mechanosensory domain, approximately 40 Å away from central pore. Our simulations further indicate presence agonist correlates with increased tension-induced motions Yoda1-bound subunit. results suggest model wherein acts as wedge, facilitating force-induced conformational changes, effectively lowering channel's threshold for activation. The identification site will pave way rational design future Piezo modulators clinical value.
Language: Английский
Citations
208
Arteriosclerosis Thrombosis and Vascular Biology, Journal Year: 2019, Volume and Issue: 39(11), P. 2228 - 2239
Published: Sept. 19, 2019
Mechanical forces are fundamental in cardiovascular biology, and deciphering the mechanisms by which they act remains a testing frontier research. Here, we raise awareness of 2 recently discovered proteins, Piezo1 Piezo2, assemble as transmembrane triskelions to combine exquisite force sensing with regulated calcium influx. There is emerging evidence for their importance endothelial shear stress secretion, NO generation, vascular tone, angiogenesis, atherosclerosis, permeability remodeling, blood pressure regulation, insulin sensitivity, exercise performance, baroreceptor reflex, there early suggestions relevance cardiac fibroblasts myocytes. Human genetic analysis points significance lymphatic disease, anemia, varicose veins, potentially heart failure, hypertension, aneurysms, stroke. These channels appear be versatile sensors, used creatively inform various force-sensing situations. We discuss emergent concepts controversies suggest that potential new important understanding substantial.
Language: Английский
Citations
200
Protein Science, Journal Year: 2021, Volume and Issue: 31(1), P. 209 - 220
Published: Oct. 30, 2021
Cellular protrusions, invaginations, and many intracellular organelles have strongly curved membrane regions. Transmembrane peripheral proteins that induce, sense, or stabilize such regions cannot be properly fitted into a single flat bilayer. To treat proteins, we developed new method web tool, PPM 3.0, for positioning in planar, multiple membranes. This determines the energetically optimal spatial position, hydrophobic thickness, radius of intrinsic curvature membrane-deforming protein structure by arranging it several sphere-shaped planar sections. In addition, can define lipid-embedded simultaneously spans membranes determine position peptide spherical micelle. The 3.0 server operates with 17 types biological 4 artificial bilayers. It is publicly available at https://opm.phar.umich.edu/ppm_server3. was applied to identify characterize arrangements 128 significant curvature, as BAR domains, annexins, Piezo, MscS mechanosensitive channels, cation-chloride cotransporters, well mitochondrial ATP synthases, calcium uniporters, TOM complexes. These form large complexes are mainly localized mitochondria, plasma membranes, endosomes. Structures bacterial drug efflux pumps, AcrAB-TolC, MexAB-OrpM, MacAB-TolC, were positioned both cell envelop, while structures multimeric gap-junction channels arranged two opposed cellular
Language: Английский
Citations
198
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
Citations
197
Nature Communications, Journal Year: 2018, Volume and Issue: 9(1)
Published: April 24, 2018
Merely touching the pancreas can lead to premature zymogen activation and pancreatitis but mechanism is not completely understood. Here we demonstrate that pancreatic acinar cells express mechanoreceptor Piezo1 application of pressure within gland produces pancreatitis. To determine if this effect through activation, induce by intrapancreatic duct instillation agonist Yoda1. Pancreatitis induced prevented a antagonist. In cells, Yoda1 stimulates calcium influx induces calcium-dependent injury. Finally, selective cell-specific genetic deletion protects mice against pressure-induced Thus, in for may explain why develops following on as abdominal trauma, obstruction, pancreatography, or surgery. blockade prevent when manipulation anticipated.
Language: Английский
Citations
196
Communications Biology, Journal Year: 2019, Volume and Issue: 2(1)
Published: Aug. 7, 2019
Piezo channels transduce mechanical stimuli into electrical and chemical signals to powerfully influence development, tissue homeostasis, regeneration. Studies on Piezo1 have largely focused transduction of "outside-in" forces, its response internal, cell-generated forces remains poorly understood. Here, using measurements endogenous activity traction in native cellular conditions, we show that generate spatially-restricted Piezo1-mediated Ca
Language: Английский
Citations
182
Cell, Journal Year: 2019, Volume and Issue: 179(2), P. 340 - 354
Published: Oct. 1, 2019
Language: Английский
Citations
171
Nature, Journal Year: 2022, Volume and Issue: 604(7905), P. 377 - 383
Published: April 6, 2022
Language: Английский
Citations
166
Nature Communications, Journal Year: 2018, Volume and Issue: 9(1)
Published: March 9, 2018
Mechanosensitive PIEZO ion channels are evolutionarily conserved proteins whose presence is critical for normal physiology in multicellular organisms. Here we show that, addition to mechanical stimuli, also powerfully modulated by voltage and can even switch a purely voltage-gated mode. Mutations that cause human diseases, such as xerocytosis, profoundly shift sensitivity of PIEZO1 toward the resting membrane potential strongly promote gating. Voltage modulation may be explained an inactivation gate pore, opening which promoted outward permeation. Older invertebrate (fly) vertebrate (fish) sensitive, but gating much more prominent feature these older channels. We propose deep property co-opted add regulatory mechanism activation widely different cellular contexts.
Language: Английский
Citations
165