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http://dx.doi.org/10.5483/BMBRep.2018.51.12.237

Cellular machinery for sensing mechanical force  

Lim, Chul-Gyun (Department of Life Sciences, Korea University)
Jang, Jiyoung (Department of Life Sciences, Korea University)
Kim, Chungho (Department of Life Sciences, Korea University)
Publication Information
BMB Reports / v.51, no.12, 2018 , pp. 623-629 More about this Journal
Abstract
For mechanical force to induce changes in cellular behaviors, two main processes are inevitable; perception of the force and response to it. Perception of mechanical force by cells, or mechanosensing, requires mechanical force-induced conformational changes in mechanosensors. For this, at least one end of the mechanosensors should be anchored to relatively fixed structures, such as extracellular matrices or the cytoskeletons, while the other end should be pulled along the direction of the mechanical force. Alternatively, mechanosensors may be positioned in lipid bilayers, so that conformational changes in the embedded sensors can be induced by mechanical force-driven tension in the lipid bilayer. Responses to mechanical force by cells, or mechanotransduction, require translation of such mechanical force-induced conformational changes into biochemical signaling. For this, protein-protein interactions or enzymatic activities of mechanosensors should be modulated in response to force-induced structural changes. In the last decade, several molecules that met the required criteria of mechanosensors have been identified and proven to directly sense mechanical force. The present review introduces examples of such mechanosensors and summarizes their mechanisms of action.
Keywords
Lipid bilayer model; Mechanical force; Mechanosensors; Tethered model;
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1 Luu YK, Capilla E, Rosen CJ et al (2009) Mechanical stimulation of mesenchymal stem cell proliferation and differentiation promotes osteogenesis while preventing dietary-induced obesity. J Bone Miner Res 24, 50-61   DOI
2 Song G, Ju Y, Shen X, Luo Q, Shi Y and Qin J (2007) Mechanical stretch promotes proliferation of rat bone marrow mesenchymal stem cells. Colloids Surf B Biointerfaces 58, 271-277   DOI
3 Baratchi S, Khoshmanesh K, Woodman OL, Potocnik S, Peter K and McIntyre P (2017) Molecular Sensors of Blood Flow in Endothelial Cells. Trends Mol Med 23, 850-868   DOI
4 Hajra L, Evans AI, Chen M, Hyduk SJ, Collins T and Cybulsky MI (2000) The NF-kappa B signal transduction pathway in aortic endothelial cells is primed for activation in regions predisposed to atherosclerotic lesion formation. Proc Natl Acad Sci U S A 97, 9052-9057   DOI
5 Nesbitt WS, Westein E, Tovar-Lopez FJ et al (2009) A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 15, 665-673   DOI
6 Engler AJ, Sen S, Sweeney HL and Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689   DOI
7 Beck FX, Burger-Kentischer A and Muller E (1998) Cellular response to osmotic stress in the renal medulla. Pflugers Arch 436, 814-827   DOI
8 DuFort CC, Paszek MJ and Weaver VM (2011) Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 12, 308-319
9 van Helvert S, Storm C and Friedl P (2018) Mechanoreciprocity in cell migration. Nat Cell Biol 20, 8-20   DOI
10 Hamill OP and Martinac B (2001) Molecular basis of mechanotransduction in living cells. Physiol Rev 81, 685-740   DOI
11 Hu X, Margadant FM, Yao M and Sheetz MP (2017) Molecular stretching modulates mechanosensing pathways. Protein Sci 26, 1337-1351   DOI
12 Gillespie PG and Walker RG (2001) Molecular basis of mechanosensory transduction. Nature 413, 194-202   DOI
13 Nyholm TK, Ozdirekcan S and Killian JA (2007) How protein transmembrane segments sense the lipid environment. Biochemistry (Mosc) 46, 1457-1465   DOI
14 Anishkin A, Loukin SH, Teng J and Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci U S A 111, 7898-7905   DOI
15 Haswell ES, Phillips R and Rees DC (2011) Mechanosensitive Channels: What Can They Do and How Do They Do It? Structure 19, 1356-1369   DOI
16 Janmey PA and McCulloch CA (2007) Cell mechanics: integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng 9, 1-34   DOI
17 Conway DE, Breckenridge MT, Hinde E, Gratton E, Chen CS and Schwartz MA (2013) Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr Biol 23, 1024-1030   DOI
18 del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM and Sheetz MP (2009) Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641   DOI
19 Horwitz A, Duggan K, Buck C, Beckerle MC and Burridge K (1986) Interaction of plasma membrane fibronectin receptor with talin--a transmembrane linkage. Nature 320, 531-533   DOI
20 Yao M, Qiu W, Liu R et al (2014) Force-dependent conformational switch of alpha-catenin controls vinculin binding. Nat Commun 5, 4525   DOI
21 Coon BG, Baeyens N, Han J et al (2015) Intramembrane binding of VE-cadherin to VEGFR2 and VEGFR3 assembles the endothelial mechanosensory complex. J Cell Biol 208, 975-986   DOI
22 Tzima E, Irani-Tehrani M, Kiosses WB et al (2005) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431   DOI
23 Robertson IB and Rifkin DB (2016) Regulation of the Bioavailability of TGF-beta and TGF-beta-Related Proteins. Cold Spring Harb Perspect Biol 8, a021907   DOI
24 Hinz B (2015) The extracellular matrix and transforming growth factor-beta1: Tale of a strained relationship. Matrix Biol 47, 54-65   DOI
25 Buscemi L, Ramonet D, Klingberg F et al (2011) The single-molecule mechanics of the latent TGF-beta1 complex. Curr Biol 21, 2046-2054   DOI
26 Dong X, Zhao B, Iacob RE et al (2017) Force interacts with macromolecular structure in activation of TGF-beta. Nature 542, 55-59   DOI
27 Jin P, Bulkley D, Guo Y et al (2017) Electron cryomicroscopy structure of the mechanotransduction channel NOMPC. Nature 547, 118-122   DOI
28 Lenting PJ, Christophe OD and Denis CV (2015) von Willebrand factor biosynthesis, secretion, and clearance: connecting the far ends. Blood 125, 2019-2028   DOI
29 Springer TA (2014) von Willebrand factor, Jedi knight of the bloodstream. Blood 124, 1412-1425   DOI
30 Walker RG, Willingham AT and Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287, 2229-2234   DOI
31 Tuthill JC and Wilson RI (2016) Parallel Transformation of Tactile Signals in Central Circuits of Drosophila. Cell 164, 1046-1059   DOI
32 Zhang W, Cheng LE, Kittelmann M et al (2015) Ankyrin Repeats Convey Force to Gate the NOMPC Mechanotransduction Channel. Cell 162, 1391-1403   DOI
33 Brohawn SG, Campbell EB and MacKinnon R (2014) Physical mechanism for gating and mechanosensitivity of the human TRAAK K+ channel. Nature 516, 126-130   DOI
34 Brohawn SG (2015) How ion channels sense mechanical force: insights from mechanosensitive K2P channels TRAAK, TREK1, and TREK2. Ann N Y Acad Sci 1352, 20-32   DOI
35 Arnadottir J and Chalfie M (2010) Eukaryotic mechanosensitive channels. Annu Rev Biophys 39, 111-137   DOI
36 Sukharev SI, Blount P, Martinac B, Blattner FR and Kung C (1994) A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368, 265-268   DOI
37 Maingret F, Patel AJ, Lesage F, Lazdunski M and Honore E (1999) Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel. J Biol Chem 274, 26691-26696   DOI
38 Denisov IG, Grinkova YV, Lazarides AA and Sligar SG (2004) Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J Am Chem Soc 126, 3477-3487   DOI
39 Rawson S, Davies S, Lippiat JD and Muench SP (2016) The changing landscape of membrane protein structural biology through developments in electron microscopy. Mol Membr Biol 33, 12-22   DOI
40 Patel AJ, Honore E, Maingret F et al (1998) A mammalian two pore domain mechano-gated S-like K+ channel. EMBO J 17, 4283-4290   DOI
41 Maingret F, Fosset M, Lesage F, Lazdunski M and Honore E (1999) TRAAK is a mammalian neuronal mechano-gated K+ channel. J Biol Chem 274, 1381-1387   DOI
42 Lesage F, Terrenoire C, Romey G and Lazdunski M (2000) Human TREK2, a 2P domain mechano-sensitive K+ channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq proteincoupled receptors. J Biol Chem 275, 28398-28405   DOI
43 Brohawn SG, Su Z and MacKinnon R (2014) Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. Proc Natl Acad Sci U S A 111, 3614-3619   DOI
44 Dong YY, Pike AC, Mackenzie A et al (2015) K2P channel gating mechanisms revealed by structures of TREK-2 and a complex with Prozac. Science 347, 1256-1259   DOI
45 Nonomura K, Woo SH, Chang RB et al (2017) Piezo2 senses airway stretch and mediates lung inflation-induced apnoea. Nature 541, 176-181   DOI
46 Coste B, Mathur J, Schmidt M et al (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60   DOI
47 Ranade SS, Qiu Z, Woo SH et al (2014) Piezo1, a mechanically activated ion channel, is required for vascular development in mice. Proc Natl Acad Sci U S A 111, 10347-10352   DOI
48 Li J, Hou B, Tumova S et al (2014) Piezo1 integration of vascular architecture with physiological force. Nature 515, 279-282   DOI
49 Ranade SS, Woo SH, Dubin AE et al (2014) Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 516, 121-125   DOI
50 Woo SH, Ranade S, Weyer AD et al (2014) Piezo2 is required for Merkel-cell mechanotransduction. Nature 509, 622-626   DOI
51 Syeda R, Florendo MN, Cox CD et al (2016) Piezo1 Channels Are Inherently Mechanosensitive. Cell Rep 17, 1739-1746   DOI
52 Zhao Q, Zhou H, Chi S et al (2018) Structure and mechanogating mechanism of the Piezo1 channel. Nature 554, 487-492   DOI
53 Saotome K, Murthy SE, Kefauver JM, Whitwam T, Patapoutian A and Ward AB (2018) Structure of the mechanically activated ion channel Piezo1. Nature 554, 481-486   DOI
54 Liang X and Howard J (2018) Structural Biology: Piezo Senses Tension through Curvature. Curr Biol 28, R357-R359   DOI
55 Guo YR and MacKinnon R (2017) Structure-based membrane dome mechanism for Piezo mechanosensitivity. Elife 6, e33660   DOI
56 Elosegui-Artola A, Andreu I, Beedle AEM et al (2017) Force Triggers YAP Nuclear Entry by Regulating Transport across Nuclear Pores. Cell 171, 1397-1410 e1314   DOI
57 Chesler AT and Szczot M (2018) Portraits of a pressure sensor. Elife 7, e34396   DOI
58 Shiu JY, Aires L, Lin Z and Vogel V (2018) Nanopillar force measurements reveal actin-cap-mediated YAP mechanotransduction. Nat Cell Biol 20, 262-271   DOI