Mechanosensitive channels: Feeling tension in a world under pressure

Frontiers in Plant Science

Volumn 5, Issue OCT, 2014, Pages

  Peyronnet, Rémi ^a   Tran, Daniel ^b   Girault, Tiffanie ^b   Frachisse, Jean Marie ^b  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b CNRS   (France)

Author keywords

Cytoskeleton; Mechanobiology; Mechanotransduction; Membrane tension; MscS; MSL; Plant; Stretch activated channels

Indexed keywords

EID: 84908237457     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00558     Document Type: Review

References (132)

1. Akitake, B., Anishkin, A., Liu, N., and Sukharev, S. (2007). Straightening and sequential buckling of the pore-lining helices define the gating cycle of MscS. Nat. Struct. Mol. Biol. 14, 1141-1149. doi: 10.1038/nsmb1341
2. Alexandre, J., and Lassalles, J. P. (1991). Hydrostatic and osmotic pressure activated channel in plant vacuole. Biophys. J. 60, 1326-1336. doi: 10.1016/S0006-3495(91)82170-1
3. Al-Rekabi, Z., Haase, K., and Pelling, A. E. (2014). Microtubules mediate changes in membrane cortical elasticity during contractile activation. Exp. Cell Res. 322, 21-29. doi: 10.1016/j.yexcr.2013.12.027
4. Alloui, A., Zimmermann, K., Mamet, J., Duprat, F., Noel, J., Chemin, J.,et al. (2006). TREK-1, a K+-channel involved in polymodal pain perception. EMBO J. 25, 2368-2376. doi: 10.1038/sj.emboj.7601116
5. Ambrose, J. C., Shoji, T., Kotzer, A. M., Pighin, J. A., and Wasteneys, G. O. (2007). The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19, 2763-2775. doi: 10.1105/tpc.107.053777
6. Arnadottir, J., and Chalfie, M. (2010). Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39, 111-137. doi: 10.1146/annurev.biophys.37.032807.125836
7. Badot, P. M., Ding, J. P., and Pickard, B. G. (1992). Mechanically activated ion channels occur in vacuoles of onion bulb scale parenchyma. C. R. Acad. Sci. Gen. 315, 437-443.
8. Bae, C., Gottlieb, P. A., and Sachs, F. (2013). Human PIEZO1: removing inactivation. Biophys. J. 105, 880-886. doi: 10.1016/j.bpj.2013.07.019
9. Bae, C., Sachs, F., and Gottlieb, P. A. (2011). The mechanosensitive ion channel piezo1 is inhibited by the peptide GsMTx4. Biochemistry 50, 6295-6300. doi: 10.1021/bi200770q
10. Bang, H., Kim, Y., and Kim, D. (2000). TREK-2, a new member of the mechanosensitive tandem-pore K1 channel family. J. Biol. Chem. 275, 17412-17419. doi: 10.1074/jbc.M000445200
11. Bass, R. B., Strop, P., Barclay, M., and Rees, D. C. (2002). Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298, 1582-1587. doi: 10.1126/science.1077945
12. Bastien, R., Bohr, T., Moulia, B., and Douady, S. (2013). Unifying model of shoot gravitropism reveals proprioception as a central feature of posture control in plants. Proc. Natl. Acad. Sci. U.S.A. 110, 755-760. doi: 10.1073/pnas.1214301109
13. Belyy, V., Kamaraju, K., Akitake, B., Anishkin, A., and Sukharev, S. (2010). Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics. J. Gen. Physiol. 135, 641-652. doi: 10.1085/jgp.200910371
14. Boer, M., Anishkin, A., and Sukharev, S. (2011). Adaptive MscS gating in the osmotic permeability response in E. coli: the question of time. Biochemistry 50, 4087-4096. doi: 10.1021/bi1019435
15. Brandizzi, F., and Wasteneys, G. O. (2013). Cytoskeleton-dependent endomembrane organization in plant cells: an emerging role for microtubules. Plant J. 75, 339-349. doi: 10.1111/tpj.12227
16. Brohawn, S. G., Campbell, E. B., and Mackinnon, R. (2013). Domain-swapped chain connectivity and gated membrane access in a Fab-mediated crystal of the human TRAAK K+-channel. Proc. Natl. Acad. Sci. U.S.A. 110, 2129-2134. doi: 10.1073/pnas.1218950110
17. Brohawn, S. G., Del Marmol, J., and Mackinnon, R. (2012). Crystal structure of the human K2P-TRAAK, a lipid- and mechano-sensitive K+-ion channel. Science 335, 436-441. doi: 10.1126/science.1213808
18. Brohawn, S. G., 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: 10.1073/pnas.1320768111
19. Campás, O., Mammoto, T., Hasso, S., Sperling, R. A., O'connell, D., Bischof, A. G.,et al. (2014). Quantifying cell-generated mechanical forces within living embryonic tissues. Nat. Methods 11, 183-189. doi: 10.1038/nmeth.2761
20. Chan, J., Eder, M., Crowell, E. F., Hampson, J., Calder, G., and Lloyd, C. (2011). Microtubules and CESA tracks at the inner epidermal wall align independently of those on the outer wall of light-grown Arabidopsis hypocotyls. J. Cell Sci. 124, 1088-1094. doi: 10.1242/jcs.086702
21. Chang, G., Spencer, R. H., Lee, A. T., Barclay, M. T., and Rees, D. C. (1998). Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282, 2220-2226. doi: 10.1126/science.282.5397.2220
22. Cosgrove, D. J. (1993). Water uptake by growing cells: an assessment of the controlling roles of wall relaxation, solute uptake, and hydraulic conductance. Int. J. Plant Sci. 154, 10-21. doi: 10.1086/297087
23. Cosgrove, D. J. (1996). Plant cell enlargement and the action of expansins. Bioessays 18, 533-540. doi: 10.1002/bies.950180704
24. Cosgrove, D. J., and Jarvis, M. C. (2012). Comparative structure and biomechanics of plant primary and secondary cell walls. Front. Plant Sci. 3:204. doi: 10.3389/fpls.2012.00204
25. Coste, B., Mathur, J., Schmidt, M., Earley, T. J., Ranade, S., Petrus, M. J.,et al. (2010). Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60. doi: 10.1126/science.1193270
26. Coste, B., Xiao, B., Santos, J. S., Syeda, R., Grandl, J., Spencer, K. S.,et al. (2012). Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483, 176-181. doi: 10.1038/nature10812
27. Coutand, C. (2010). Mechanosensing and thigmomorphogenesis, a physiological and biomechanical point of view. Plant Sci. 179, 168-182. doi: 10.1016/j.plantsci.2010.05.001
28. Cox, C. D., Nakayama, Y., Nomura, T., and Martinac, B. (2014). The evolutionary 'tinkering' of MscS-like channels: generation of structural and functional diversity. Pflugers Arch. doi: 10.1007/s00424-014-1522-2
29. Dai, J., Sheetz, M. P., Wan, X., and Morris, C. E. (1998). Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci. 18, 6681-6692.
30. Dedman, A., Sharif-Naeini, R., Folgering, J. H., Duprat, F., Patel, A., and Honore, E. (2009). The mechano-gated K(2P) channel TREK-1. Eur. Biophys. J. 38, 293-303. doi: 10.1007/s00249-008-0318-8
31. Eijkelkamp, N., Quick, K., and Wood, J. N. (2013). Transient receptor potential channels and mechanosensation. Annu. Rev. Neurosci. 36, 519-546. doi: 10.1146/annurev-neuro-062012-170412
32. Ellis, R. J. (2001). Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 26, 597-604. doi: 10.1016/S0968-0004(01)01938-7
33. Evans, E., and Ludwig, F. (2000). Dynamic strengths of molecular anchoring and material cohesion in fluid biomembranes. J. Phys. Condens. Matter 12:A315. doi: 10.1088/0953-8984/12/8A/341
34. Falke, L. C., Edwards, K. L., Pickard, B. G., and Misler, S. (1988). A stretch-activated anion channel in tobacco protoplasts. FEBS Lett. 237, 141-144. doi: 10.1016/0014-5793(88)80188-1
35. Franks, P. J., Buckley, T. N., Shope, J. C., and Mott, K. A. (2001). Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe. Plant Physiol. 125, 1577-1584. doi: 10.1104/pp.125.4.1577
36. Furuichi, T., Iida, H., Sokabe, M., and Tatsumi, H. (2012). Expression of Arabidopsis MCA1 enhanced mechanosensitive channel activity in the Xenopus laevis oocyte plasma membrane. Plant Signal. Behav. 7, 1022-1026. doi: 10.4161/psb.20783
37. Gardiner, J. (2013). The evolution and diversification of plant microtubule-associated proteins. Plant J. 75, 219-229. doi: 10.1111/tpj.12189
38. Gauthier, N. C., Masters, T. A., and Sheetz, M. P. (2012). Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 22, 527-535. doi: 10.1016/j.tcb.2012.07.005
39. Gottlieb, P. A., Bae, C., and Sachs, F. (2012). Gating the mechanical channel Piezo1. A comparison between whole-cell and patch recording. Channels 6, 282-289. doi: 10.4161/Chan.21064
40. Gottlieb, P. A., and Sachs, F. (2012). Piezo1: properties of a cation selective mechanical channel. Channels 6, 214-219. doi: 10.4161/chan.21050
41. Grashoff, C., Hoffman, B. D., Brenner, M. D., Zhou, R., Parsons, M., Yang, M. T.,et al. (2010). Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266. doi: 10.1038/nature09198
42. Guharay, F., and Sachs, F. (1984). Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J. Physiol. 352, 685-701.
43. Guo, J., Sachs, F., and Meng, F. (2013). Fluorescence-based force/tension sensors: a novel tool to visualize mechanical forces in structural proteins in live cells. Antioxid. Redox Signal. 20, 986-999. doi: 10.1089/ars.2013.5708
44. Gustin, M. C., Zhou, X. L., Martinac, B., and Kung, C. (1988). A mechanosensitive ion channel in the yeast plasma membrane. Science 242, 762-765. doi: 10.1126/science.2460920
45. Hamill, O. P., and Martinac, B. (2001). Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81, 685-740.
46. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85-100. doi: 10.1007/BF00656997
47. Haswell, E. S. (2007). "MscS-like proteins in plants,"in Mechanosensitive Ion Channels, Part A, ed. O. P. Hamill (San Diego, CA: Elsevier and Academic Press), 329-359. doi: 10.1016/S1063-5823(06)58013-5
48. Haswell, E. S., and Meyerowitz, E. M. (2006). MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr. Biol. 16, 1-11. doi: 10.1016/j.cub.2005.11.044
49. Haswell, E. S., Peyronnet, R., Barbier-Brygoo, H., Meyerowitz, E. M., and Frachisse, J. M. (2008). Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr. Biol. 18, 730-734. doi: 10.1016/j.cub.2008.04.039
50. Hayakawa, K., Tatsumi, H., and Sokabe, M. (2012). Mechano-sensing by actin filaments and focal adhesion proteins. Commun. Integr. Biol. 5, 572-577. doi: 10.4161/cib.21891
51. Heurteaux, C., Guy, N., Laigle, C., Blondeau, N., Duprat, F., Mazzuca, M.,et al. (2004). TREK-1, a K+-channel involved in neuroprotection and general anesthesia. EMBO J. 23, 2684-2695. doi: 10.1038/sj.emboj.7600234
52. Heurteaux, C., Lucas, G., Guy, N., El Yacoubi, M., Thummler, S., Peng, X. D.,et al. (2006). Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nat. Neurosci. 9, 1134-1141. doi: 10.1038/nn1749
53. Honore, E., Patel, A. J., Chemin, J., Suchyna, T., and Sachs, F. (2006). Desensitization of mechano-gated K2Pchannels. Proc. Natl. Acad. Sci. U.S.A. 103, 6859-6864. doi: 10.1073/pnas.0600463103
54. Hurwitz, C. G., and Segal, A. S. (2001). Application of pressure steps to mechanosensitive channels in membrane patches: a simple, economical, and fast system. Pflugers Arch. 442, 150-156. doi: 10.1007/s004240100541
55. Jaqaman, K., and Grinstein, S. (2012). Regulation from within: the cytoskeleton in transmembrane signaling. Trends Cell Biol. 22, 515-526. doi: 10.1016/j.tcb.2012.07.006
56. Kamaraju, K., Belyy, V., Rowe, I., Anishkin, A., and Sukharev, S. (2011). The pathway and spatial scale for MscS inactivation. J. Gen. Physiol. 138, 49-57. doi: 10.1085/jgp.201110606
57. Kamkin, A., and Kiseleva, I. (2008). "Mechanically gated channels and mechanosensitive channels," in Mechanosensitivity in Cells and Tissues: Mechanosensitive Ion Channels, eds A. Kamkin and I. Kiseleva, (Berlin: Springer), xiii-xviii. doi: 10.1007/978-1-4020-6426-5
58. Kim, S. E., Coste, B., Chadha, A., Cook, B., and Patapoutian, A. (2012). The role of Drosophila Piezo in mechanical nociception. Nature 483, 209-212. doi: 10.1038/nature10801
59. Knepper, C., Savory, E. A., and Day, B. (2011). Arabidopsis NDR1 is an integrin-like protein with a role in fluid loss and plasma membrane-cell wall adhesion. Plant Physiol. 156, 286-300. doi: 10.1104/pp.110.169656
60. Kung, C., Martinac, B., and Sukharev, S. (2010). Mechanosensitive channels in microbes. Annu. Rev. Microbiol. 64, 313-329. doi: 10.1146/annurev.micro.112408.134106
61. Kurusu, T., Kuchitsu, K., Nakano, M., Nakayama, Y., and Iida, H. (2013). Plant mechanosensing and Ca2+-transport. Trends Plant Sci. 18, 227-233. doi: 10.1016/j.tplants.2012.12.002
62. Kwok, R., and Evans, E. (1981). Thermoelasticity of large lecithin bilayer vesicles. Biophys. J. 35, 637-652. doi: 10.1016/S0006-3495(81)84817-5
63. Lauritzen, I., Chemin, J., Honore, E., Jodar, M., Guy, N., Lazdunski, M.,et al. (2005). Cross-talk between the mechano-gated K2P-channel TREK-1 and the actin cytoskeleton. EMBO Rep. 6, 642-648. doi: 10.1038/sj.embor.7400449
64. Le Guennec, J. Y., Peineau, N., Argibay, J. A., Mongo, K. G., and Garnier, D. (1990). A new method of attachment of isolated mammalian ventricular myocytes for tension recording: length dependence of passive and active tension. J. Mol. Cell Cardiol. 22, 1083-1093. doi: 10.1016/0022-2828(90)90072-A
65. Levina, N., Totemeyer, S., Stokes, N. R., Louis, P., Jones, M. A., and Booth, I. R. (1999). Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J. 18, 1730-1737. doi: 10.1093/emboj/18.7.1730
66. Maathuis, F. J. (2011). Vacuolar two-pore K+-channels act as vacuolar osmosensors. New Phytol. 191, 84-91. doi: 10.1111/j.1469-8137.2011.03664.x
67. Maingret, F., Patel, A. J., Lesage, F., Lazdunski, M., and Honore, E. (2000). Lysophospholipids open the two-pore domain mechano-gated K+-channels TREK-1 and TRAAK. J. Biol. Chem. 275, 10128-10133. doi: 10.1074/jbc.275.14.10128
68. Maksaev, G., and Haswell, E. S. (2012). MscS-Like10 is a stretch-activated ion channel from Arabidopsis thaliana with a preference for anions. Proc. Natl. Acad. Sci. U.S.A. 109, 19015-19020. doi: 10.1073/pnas.1213931109
69. Martinac, B. (2011). Bacterial mechanosensitive channels as a paradigm for mechanosensory transduction. Cell Physiol. Biochem. 28, 1051-1060. doi: 10.1159/000335842
70. Martinac, B., Adler, J., and Kung, C. (1990). Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348, 261-263. doi: 10.1038/348261a0
71. Martinac, B., Buechner, M., Delcour, A. H., Adler, J., and Kung, C. (1987). Pressure-sensitive ion channel in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 84, 2297-2301. doi: 10.1073/pnas.84.8.2297
72. Martinac, B., Saimi, Y., and Kung, C. (2008). Ion channels in microbes. Physiol. Rev. 88, 1449-1490. doi: 10.1152/physrev.00005.2008
73. McBride, D. W. Jr., and Hamill, O. P. (1992). Pressure-clamp: a method for rapid step perturbation of mechanosensitive channels. Pflugers Arch. 421, 606-612. doi: 10.1007/BF00375058
74. Meckel, T., Hurst, A. C., Thiel, G., and Homann, U. (2004). Endocytosis against high turgor: intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-tagged K-channel KAT1. Plant J. 39, 182-193. doi: 10.1111/j.1365-313X.2004.02119.x
75. Meng, F., and Sachs, F. (2011). Visualizing dynamic cytoplasmic forces with a compliance-matched FRET sensor. J. Cell Sci. 124, 261-269. doi: 10.1242/jcs.071928
76. Miedema, H., Demidchik, V., Very, A. A., Bothwell, J. H., Brownlee, C., and Davies, J. M. (2008). Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytol. 179, 378-385. doi: 10.1111/j.1469-8137.2008.02465.x
77. Monshausen, G. B., Bibikova, T. N., Weisenseel, M. H., and Gilroy, S. (2009). Ca2+-regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21, 2341-2356. doi: 10.1105/tpc.109.068395
78. Monshausen, G. B., and Gilroy, S. (2009). Feeling green: mechanosensing in plants. Trends Cell Biol. 19, 228-235. doi: 10.1016/j.tcb.2009.02.005
79. Monshausen, G. B., and Haswell, E. S. (2013). A force of nature: molecular mechanisms of mechanoperception in plants. J. Exp. Bot. 64, 4663-4680. doi: 10.1093/jxb/ert204
80. Morris, C. E., and Homann, U. (2001). Cell surface area regulation and membrane tension. J. Membr. Biol. 179, 79-102. doi: 10.1007/s002320010040
81. Mukherjee, N., Jose, M. D., Birkner, J. P., Walko, M., Ingolfsson, H. I., Dimitrova, A.,et al. (2014). The activation mode of the mechanosensitive ion channel, MscL, by lysophosphatidylcholine differs from tension-induced gating.FASEB J. 28, 4292-4302. doi: 10.1096/fj.14-251579
82. Nakagawa, Y., Katagiri, T., Shinozaki, K., Qi, Z., Tatsumi, H., Furuichi, T.,et al. (2007). Arabidopsis plasma membrane protein crucial for Ca2+-influx and touch sensing in roots. Proc. Natl. Acad. Sci. U.S.A. 104, 3639-3644. doi: 10.1073/pnas.0607703104
83. Nakayama, Y., Yoshimura, K., and Iida, H. (2013). Electrophysiological characterization of the mechanosensitive channel MscCG in Corynebacterium glutamicum. Biophys. J. 105, 1366-1375. doi: 10.1016/j.bpj.2013.06.054
84. Nichol, J. A., and Hutter, O. F. (1996). Tensile strength and dilatational elasticity of giant sarcolemmal vesicles shed from rabbit muscle. J. Physiol. 493(Pt 1), 187-198.
85. Nick, P. (2013). Microtubules, signalling and abiotic stress. Plant J. 75, 309-323. doi: 10.1111/tpj.12102
86. Nilius, B., and Honore, E. (2012). Sensing pressure with ion channels. Trends Neurosci. 35, 477-486. doi: 10.1016/j.tins.2012.04.002
87. Noel, J., Sandoz, G., and Lesage, F. (2011). Molecular regulations governing TREK and TRAAK channel functions. Channels 5, 402-409. doi: 10.4161/chan.5.5.16469
88. Nomura, T., Cranfield, C. G., Deplazes, E., Owen, D. M., Macmillan, A., Battle, A. R.,et al. (2012). Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc. Natl. Acad. Sci. U.S.A. 109, 8770-8775. doi: 10.1073/pnas.1200051109
89. Ofer, N., Mogilner, A., and Keren, K. (2011). Actin disassembly clock determines shape and speed of lamellipodial fragments. Proc. Natl. Acad. Sci. U.S.A. 108, 20394-20399. doi: 10.1073/pnas.1105333108
90. Paredez, A. R., Somerville, C. R., and Ehrhardt, D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495. doi: 10.1126/science.1126551
91. Patel, A. J., Honore, E., Maingret, F., Lesage, F., Fink, M., Duprat, F.,et al. (1998). A mammalian two pore domain mechano-gated S-like K+-channel. EMBO J. 17, 4283-4290. doi: 10.1093/emboj/17.15.4283
92. Perozo, E., Kloda, A., Cortes, D. M., and Martinac, B. (2002). Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9, 696-703. doi: 10.1038/nsb827
93. Perozo, E., and Rees, D. C. (2003). Structure and mechanism in prokaryotic mechanosensitive channels. Curr. Opin. Struct. Biol. 13, 432-442. doi: 10.1016/S0959-440X(03)00106-4
94. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J., Evans, P. R.,et al. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499. doi: 10.1126/science.1092586
95. Petrov, E., Palanivelu, D., Constantine, M., Rohde, P. R., Cox, C. D., Nomura, T.,et al. (2013). Patch-clamp characterization of the MscS-like mechanosensitive channel from Silicibacter pomeroyi. Biophys. J. 104, 1426-1434. doi: 10.1016/j.bpj.2013.01.055
96. Peyronnet R., Haswell, E. S., Barbier-Brygoo H., and Frachisse, J. M. (2008). AtMSL9 and AtMSL10: Sensors of plasma membrane tension in Arabidopsis roots. Plant Signal. Behav. 3, 726-729. doi: 10.4161/psb.3.9.6487
97. Peyronnet, R., Sharif-Naeini, R., Folgering, J. H., Arhatte, M., Jodar, M., El Boustany, C.,et al. (2012). Mechanoprotection by polycystins against apoptosis is mediated through the opening of stretch-activated K2Pchannels. Cell Rep. 1, 241-250. doi: 10.1016/j.celrep.2012.01.006
98. Pranke, I. M., Morello, V., Bigay, J., Gibson, K., Verbavatz, J. M., Antonny, B.,et al. (2011). alpha-Synuclein and ALPS motifs are membrane curvature sensors whose contrasting chemistry mediates selective vesicle binding. J. Cell Biol. 194, 89-103. doi: 10.1083/jcb.201011118
99. Pritchard, J., Barlow, P. W., Adam, J. S., and Tomos, A. D. (1990). Biophysics of the inhibition of the growth of maize roots by lowered temperature. Plant Physiol. 93, 222-230. doi: 10.1104/pp.93.1.222
100. Ren, G., Vajjhala, P., Lee, J. S., Winsor, B., and Munn, A. L. (2006). The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 70, 37-120. doi: 10.1128/MMBR.70.1.37-120.2006
101. Rowe, I., Anishkin, A., Kamaraju, K., Yoshimura, K., and Sukharev, S. (2014). The cytoplasmic cage domain of the mechanosensitive channel MscS is a sensor of macromolecular crowding. J. Gen. Physiol. 143, 543-557. doi: 10.1085/jgp.201311114
102. Sachs, F. (2010). Stretch-activated ion channels: what are they? Physiology (Bethesda) 25, 50-56. doi: 10.1152/physiol.00042.2009
103. Sachs, F., and Morris, C. E. (1998). Mechanosensitive ion channels in nonspecialized cells. Rev. Physiol. Biochem. Pharmacol. 132, 1-77. doi: 10.1007/BFb0004985
104. Saravanan, S., Meghana, C., and Narasimha, M. (2013). Local, cell-nonautonomous feedback regulation of myosin dynamics patterns transitions in cell behavior: a role for tension and geometry? Mol. Biol. Cell 24, 2350-2361. doi: 10.1091/mbc.E12-12-0868
105. Shabala, S. N., and Lew, R. R. (2002). Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol. 129, 290-299. doi: 10.1104/pp.020005
106. Sheetz, M. P., and Singer, S. J. (1974). Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. U.S.A. 71, 4457-4461. doi: 10.1073/pnas.71.11.4457
107. Solsona, C., Innocenti, B., and Fernandez, J. M. (1998). Regulation of exocytotic fusion by cell inflation. Biophys. J. 74, 1061-1073. doi: 10.1016/S0006-3495(98)74030-5
108. Sotomayor, M., Vasquez, V., Perozo, E., and Schulten, K. (2007). Ion conduction through MscS as determined by electrophysiology and simulation. Biophys. J. 92, 886-902. doi: 10.1529/biophysj.106.095232
109. Suchyna, T. M., Tape, S. E., Koeppe, R. E. II, Andersen, O. S., Sachs, F., and Gottlieb, P. A. (2004). Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature 430, 235-240. doi: 10.1038/nature02743
110. Sukharev, S. (1999). Mechanosensitive channels in bacteria as membrane tension reporters. FASEB J. 13 (Suppl.), S55-S61.
111. Sukharev, S. (2002). Purification of the small mechanosensitive channel of Escherichia coli (MscS): the subunit structure, conduction, and gating characteristics in liposomes. Biophys. J. 83, 290-298. doi: 10.1016/S0006-3495(02)75169-2
112. Sukharev, S., Betanzos, M., Chiang, C. S., and Guy, H. R. (2001). The gating mechanism of the large mechanosensitive channel MscL. Nature 409, 720-724. doi: 10.1038/35055559
113. Sukharev, S., and Sachs, F. (2012). Molecular force transduction by ion channels: diversity and unifying principles. J. Cell Sci. 125, 3075-3083. doi: 10.1242/jcs.092353
114. Sukharev, S. I., Blount, P., Martinac, B., Blattner, F. R., and Kung, C. (1994a). A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368, 265-268. doi: 10.1038/368265a0
115. Sukharev, S. I., Martinac, B., Blount, P., and Kung, C. (1994b). Functional reconstitution as an assay for biochemical isolation of channel proteins: application to the molecular identification of a bacterial mechanosensitive channel. Methods 6, 51-59. doi: 10.1006/meth.1994.1007
116. Sukharev, S. I., Blount, P., Martinac, B., and Kung, C. (1997). Mechanosensitive channels of Escherichia coli: the MscL gene, protein, and activities. Annu. Rev. Physiol. 59, 633-657. doi: 10.1146/annurev.physiol.59.1.633
117. Sukharev, S. I., Sigurdson, W. J., Kung, C., and Sachs, F. (1999). Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J. Gen. Physiol. 113, 525-540. doi: 10.1085/jgp.113.4.525
118. Szymanski, D. B., and Cosgrove, D. J. (2009). Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr. Biol. 19, R800-R811. doi: 10.1016/j.cub.2009.07.056
119. Teng, J., Loukin, S., Anishkin, A., and Kung, C. (2014). The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflugers Arch. doi: 10.1007/s00424-014-1530-2 [Epub ahead of Print].
120. Vasquez, V., Sotomayor, M., Cordero-Morales, J., Schulten, K., and Perozo, E. (2008). A structural mechanism for MscS gating in lipid bilayers. Science 321, 1210-1214. doi: 10.1126/science.1159674
121. Wang, Y., Liu, Y., Deberg, H. A., Nomura, T., Hoffman, M. T., Rohde, P. R.,et al. (2014). Single molecule FRET reveals pore size and opening mechanism of a mechano-sensitive ion channel. Elife 3:e01834. doi: 10.7554/eLife.01834
122. Wilson, M. E., Jensen, G. S., and Haswell, E. S. (2011). Two mechanosensitive channel homologs influence division ring placement in Arabidopsis chloroplasts. Plant Cell 23, 2939-2949. doi: 10.1105/tpc.111.088112
123. Wilson, M. E., Maksaev, G., and Haswell, E. S. (2013). MscS-like mechanosensitive channels in plants and microbes. Biochemistry 52, 5708-5722. doi: 10.1021/bi400804z
124. Wolf, S., Hematy, K., and Hofte, H. (2012). Growth control and cell wall signaling in plants. Annu. Rev. Plant Biol. 63, 381-407. doi: 10.1146/annurev-arplant-042811-105449
125. Wolfe, J., Dowgert, M. F., and Steponkus, P. L. (1985). Dynamics of membrane exchange of the plasma membrane and the lysis of isolated protoplasts during rapid expansion in area. J. Membr. Biol. 86, 127-138. doi: 10.1007/BF01870779
126. Woo, S. H., Ranade, S., Weyer, A. D., Dubin, A. E., Baba, Y., Qiu, Z.,et al. (2014). Piezo2 is required for Merkel-cell mechanotransduction. Nature 509, 622-626. doi: 10.1038/nature13251
127. Wood, J. M. (1999). Osmosensing by bacteria: signals and membrane-based sensors. Microbiol. Mol. Biol. Rev. 63, 230-262.
128. Yoo, J., and Cui, Q. (2009). Curvature generation and pressure profile modulation in membrane by lysolipids: insights from coarse-grained simulations. Biophys. J. 97, 2267-2276. doi: 10.1016/j.bpj.2009.07.051
129. Zarychanski, R., Schulz, V. P., Houston, B. L., Maksimova, Y., Houston, D. S., Smith, B.,et al. (2012). Mutations in the mechanotransduction protein PIEZO1 are associated with hereditary xerocytosis. Blood 120, 1908-1915. doi: 10.1182/blood-2012-04-422253
130. Zhang, W., Fan, L. M., and Wu, W. H. (2007). Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiol. 143, 1140-1151. doi: 10.1104/pp.106.091405
131. Zhou, X. L., Batiza, A. F., Loukin, S. H., Palmer, C. P., Kung, C., and Saimi, Y. (2003). The transient receptor potential channel on the yeast vacuole is mechanosensitive. Proc. Natl. Acad. Sci. U.S.A. 100, 7105-7110. doi: 10.1073/pnas.1230540100
132. Zhuang, X., and Jiang, L. (2014). Autophagosome biogenesis in plants: roles of SH3P2. Autophagy 10, 704-705. doi: 10.4161/auto.28060