The mechanobiology of brain function

Nature Reviews Neuroscience

Volumn 13, Issue 12, 2012, Pages 867-878

  Tyler, William J ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COLLAGEN; FIBRONECTIN; LAMININ; SPECTRIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ACTIN FILAMENT; ACTIN POLYMERIZATION; BRAIN CELL; BRAIN FUNCTION; BRAIN NERVE CELL; CELL MEMBRANE; DENDRITIC SPINE; ELASTOGRAPHY; EXTRACELLULAR MATRIX; HUMAN; MECHANICS; MICROTUBULE; NERVE CELL PLASTICITY; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; TRAUMATIC BRAIN INJURY; YOUNG MODULUS;

ANIMALS; BIOMECHANICS; BRAIN; CELL PHYSIOLOGICAL PHENOMENA; HUMANS; ION CHANNELS; MECHANOTRANSDUCTION, CELLULAR; NEURONS;

EID: 84872019086     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3383     Document Type: Review

References (134)

1. Hamill, O. P. & Martinac, B. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81, 685-740 (2001).
2. Kim, D. H., Wong, P. K., Park, J., Levchenko, A. & Sun, Y. Microengineered platforms for cell mechanobiology. Annu. Rev. Biomed. Eng. 11, 203-233 (2009).
3. Eyckmans, J., Boudou, T., Yu, X. & Chen, C. S. A hitchhiker's guide to mechanobiology. Dev. Cell 21, 35-47 (2011).
4. Hill, D. K. The volume change resulting from stimulation of a giant nerve fibre. J. Physiol. 111, 304-327 (1950).
5. Tasaki, I., Kusano, K. & Byrne, P. M. Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse. Biophys. J. 55, 1033-1040 (1989).
6. Kim, G. H., Kosterin, P., Obaid, A. L. & Salzberg, B. M. A mechanical spike accompanies the action potential in Mammalian nerve terminals. Biophys. J. 92, 3122-3129 (2007).
7. Crick, F. Do dendritic spines twitch? Trends Neurosci. 5, 44-46 (1982).
8. Star, E. N., Kwiatkowski, D. J. & Murthy, V. N. Rapid turnover of actin in dendritic spines and its regulation by activity. Nature Neurosci. 5, 239-246 (2002).
9. Elkin, B. S., Azeloglu, E. U., Costa, K. D. & Morrison, B. Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. J. Neurotrauma 24, 812-822 (2007).
10. Gefen, A., Gefen, N., Zhu, Q., Raghupathi, R. & Margulies, S. S. Age-dependent changes in material properties of the brain and braincase of the rat. J. Neurotrauma 20, 1163-1177 (2003).
11. Kruse, S. A. et al. Magnetic resonance elastography of the brain. Neuroimage 39, 231-237 (2008).
12. Moore, S. W. & Sheetz, M. P. Biophysics of substrate interaction: influence on neural motility, differentiation, and repair. Dev. Neurobiol. 71, 1090-1101 (2011).
13. Moore, S. W., Roca-Cusachs, P. & Sheetz, M. P. Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev. Cell 19, 194-206 (2010).
14. McCracken, P. J., Manduca, A., Felmlee, J. & Ehman, R. L. Mechanical transient-based magnetic resonance elastography. Magn. Reson. Med. 53, 628-639 (2005).
15. Zhang, J., Green, M. A., Sinkus, R. & Bilston, L. E. Viscoelastic properties of human cerebellum using magnetic resonance elastography. J. Biomech. 44, 1909-1913 (2011).
16. Sack, I., Streitberger, K. J., Krefting, D., Paul, F. & Braun, J. The influence of physiological aging and atrophy on brain viscoelastic properties in humans. PLoS ONE 6, e23451 (2011).
17. Wuerfel, J. et al. MRelastography reveals degradation of tissue integrity in multiple sclerosis. Neuroimage 49, 2520-2525 (2010).
18. Murphy, M. C. et al. Decreased brain stiffness in Alzheimer's disease determined by magnetic resonance elastography. J. Magn. Reson. Imaging 34, 494-498 (2011).
19. Crawford, G. E. & Earnshaw, J. C. Viscoelastic relaxation of bilayer lipid membranes. Frequency-dependent tension and membrane viscosity. Biophys. J. 52, 87-94 (1987).
20. Pastor, R. W. & Feller, S. E. Time scales of lipid dynamics and molecular dynamics. Biol. Membr. 1, 4-29 (1996).
21. Almeida, P. F. F. & Vaz, W. L. C. in Structure and Dynamics of Membranes: From Cells to Vesicles Vol. 1 (eds Lipowsky, R. & Sackmann, E.) 305-357 (Elsevier, 1995).
22. Evans, E. A. & Hochmuth, R. M. in Current Topics in Membranes and Transport Vol. 10 (eds Bronner, F. & Kleinzeller, A.) 1-64 (Academic Press, 1978).
23. Seifriz, W. An elastic value of protoplasm, with further observations on the viscosity of protoplasm. J. Exp. Biol. 2, 1-11 (1924).
24. Kueh, H. Y. & Mitchison, T. J. Structural plasticity in actin and tubulin polymer dynamics. Science 325, 960-963 (2009).
25. Galkin, V. E., Orlova, A. & Egelman, E. H. Actin filaments as tension sensors. Curr. Biol. 22, R96-R101 (2012).
26. Hill, T. L. & Kirschner, M. W. Bioenergetics and kinetics of microtubule and actin filament assembly-disassembly. Int. Rev. Cytol. 78, 1-125 (1982).
27. Theriot, J. A. The polymerization motor. Traffic 1, 19-28 (2000).
28. Feynman, R. P., Leighton, R. B. & Sands, M. in The Feynman Lectures on Physics Vol. 1, Ch. 46, 46-49 (Addison-Wessley, 1963).
29. Peskin, C. S., Odell, G. M. & Oster, G. F. Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys. J. 65, 316-324 (1993).
30. Hill, T. L. & Kirschner, M. W. Subunit treadmilling of microtubules or actin in the presence of cellular barriers: possible conversion of chemical free energy into mechanical work. Proc. Natl Acad. Sci. USA 79, 490-494 (1982).
31. Footer, M. J., Kerssemakers, J. W., Theriot, J. A. & Dogterom, M. Direct measurement of force generation by actin filament polymerization using an optical trap. Proc. Natl Acad. Sci. USA 104, 2181-2186 (2007).
32. Parekh, S. H., Chaudhuri, O., Theriot, J. A. & Fletcher, D. A. Loading history determines the velocity of actin-network growth. Nature Cell Biol. 7, 1219-1223 (2005).
33. Kosztin, I., Bruinsma, R., O'Lague, P. & Schulten, K. Mechanical force generation by G proteins. Proc. Natl Acad. Sci. USA 99, 3575-3580 (2002).
34. Schliwa, M. & Woehlke, G. Molecular motors. Nature 422, 759-765 (2003).
35. Smith, S. J. Neuronal cytomechanics: the actin-based motility of growth cones. Science 242, 708-715 (1988).
36. Betz, T., Koch, D., Lu, Y. B., Franze, K. & Kas, J. A. Growth cones as soft and weak force generators. Proc. Natl Acad. Sci. USA 108, 13420-13425 (2011).
37. Chan, C. E. & Odde, D. J. Traction dynamics of filopodia on compliant substrates. Science 322, 1687-1691 (2008).
38. Matus, A. Actin-based plasticity in dendritic spines. Science 290, 754-758 (2000).
39. Gao, Y. et al. β-III spectrin is critical for development of Purkinje cell dendritic tree and spine morphogenesis. J. Neurosci. 31, 16581-16590 (2011).
40. Nestor, M. W., Cai, X., Stone, M. R., Bloch, R. J. & Thompson, S. M. The actin binding domain of βI-spectrin regulates the morphological and functional dynamics of dendritic spines. PLoS ONE 6, e16197 (2011).
41. Komada, M. & Soriano, P. βIVspectrin regulates sodium channel clustering through ankyrinG at axon initial segments and nodes of Ranvier. J. Cell Biol. 156, 337-348 (2002).
42. Devaux, J. J. The Cterminal domain of ssIV-spectrin is crucial for KCNQ2 aggregation and excitability at nodes of Ranvier. J. Physiol. 588, 4719-4730 (2010).
43. Desai, A. & Mitchison, T. J. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117 (1997).
44. Odde, D. J., Ma, L., Briggs, A. H., DeMarco, A. & Kirschner, M. W. Microtubule bending and breaking in living fibroblast cells. J. Cell Sci. 112, 3283-3288 (1999).
45. Dogterom, M. & Yurke, B. Measurement of the force-velocity relation for growing microtubules. Science 278, 856-860 (1997).
46. Svoboda, K. & Block, S. M. Force and velocity measured for single kinesin molecules. Cell 77, 773-784 (1994).
47. Visscher, K., Schnitzer, M. J. & Block, S. M. Single kinesin molecules studied with a molecular force clamp. Nature 400, 184-189 (1999).
48. Brangwynne, C. P. et al. Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J. Cell Biol. 173, 733-741 (2006).
49. Hu, X., Viesselmann, C., Nam, S., Merriam, E. & Dent, E. W. Activity-dependent dynamic microtubule invasion of dendritic spines. J. Neurosci. 28, 13094-13105 (2008).
50. Jaworski, J. et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61, 85-100 (2009).
51. Lee, M. K. & Cleveland, D. W. Neuronal intermediate filaments. Annu. Rev. Neurosci. 19, 187-217 (1996).
52. Mukhopadhyay, R., Kumar, S. & Hoh, J. H. Molecular mechanisms for organizing the neuronal cytoskeleton. Bioessays 26, 1017-1025 (2004).
53. Geisler, N. & Weber, K. Self-assembly in vitro of the 68,000 molecular weight component of the mammalian neurofilament triplet proteins into intermediate-sized filaments. J. Mol. Biol. 151, 565-571 (1981).
54. Brown, H. G. & Hoh, J. H. Entropic exclusion by neurofilament sidearms: a mechanism for maintaining interfilament spacing. Biochemistry 36, 15035-15040 (1997).
55. Pekny, M. & Lane, E. B. Intermediate filaments and stress. Exp. Cell Res. 313, 2244-2254 (2007).
56. Cleveland, D. W. et al. Involvement of neurofilaments in the radial growth of axons. J. Cell Sci. Suppl. 15, 85-95 (1991).
57. Kumar, S., Yin, X., Trapp, B. D., Paulaitis, M. E. & Hoh, J. H. Role of long-range repulsive forces in organizing axonal neurofilament distributions: evidence from mice deficient in myelin-associated glycoprotein. J. Neurosci. Res. 68, 681-690 (2002).
58. Leterrier, J. F., Kas, J., Hartwig, J., Vegners, R. & Janmey, P. A. Mechanical effects of neurofilament cross-bridges. Modulation by phosphorylation, lipids, and interactions with Factin. J. Biol. Chem. 271, 15687-15694 (1996).
59. Dityatev, A., Schachner, M. & Sonderegger, P. The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nature Rev. Neurosci. 11, 735-746 (2010).
60. Dityatev, A. & Fellin, T. Extracellular matrix in plasticity and epileptogenesis. Neuron Glia Biol. 4, 235-247 (2008).
61. Pantazopoulos, H., Woo, T. U., Lim, M. P., Lange, N. & Berretta, S. Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch. Gen. Psychiatry 67, 155-166 (2010).
62. Thoumine, O., Kocian, P., Kottelat, A. & Meister, J. J. Short-term binding of fibroblasts to fibronectin: optical tweezers experiments and probabilistic analysis. Eur. Biophys. J. 29, 398-408 (2000).
63. Chavis, P. & Westbrook, G. Integrins mediate functional pre-and postsynaptic maturation at a hippocampal synapse. Nature 411, 317-321 (2001).
64. Baumgartner, W., Golenhofen, N., Grundhofer, N., Wiegand, J. & Drenckhahn, D. Ca2+ dependency of Ncadherin function probed by laser tweezer and atomic force microscopy. J. Neurosci. 23, 11008-11014 (2003).
65. Mendez, P., De Roo, M., Poglia, L., Klauser, P. & Muller, D. Ncadherin mediates plasticity-induced long-term spine stabilization. J. Cell Biol. 189, 589-600 (2010).
66. Arikkath, J. & Reichardt, L. F. Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci. 31, 487-494 (2008).
67. Arnadottir, J. & Chalfie, M. Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39, 111-137 (2010).
68. Reeves, D., Ursell, T., Sens, P., Kondev, J. & Phillips, R. Membrane mechanics as a probe of ion-channel gating mechanisms. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 78, 041901 (2008).
69. Sukharev, S. & Corey, D. P. Mechanosensitive channels: multiplicity of families and gating paradigms. Sci. STKE 2004, re4 (2004).
70. Morris, C. E. Voltage-gated channel mechanosensitivity: fact or friction? Front. Physiol. 2, 25 (2011).
71. Cantor, R. S. The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry 36, 2339-2344 (1997).
72. Jerabek, H., Pabst, G., Rappolt, M. & Stockner, T. Membrane-mediated effect on ion channels induced by the anesthetic drug ketamine. J. Am. Chem. Soc. 132, 7990-7997 (2010).
73. Schikorski, T. & Stevens, C. F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17, 5858-5867 (1997).
74. Murthy, V. N., Schikorski, T., Stevens, C. F. & Zhu, Y. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32, 673-682 (2001).
75. Siechen, S., Yang, S., Chiba, A. & Saif, T. Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals. Proc. Natl Acad. Sci. USA 106, 12611-12616 (2009).
76. Umeda, T., Ebihara, T. & Okabe, S. Simultaneous observation of stably associated presynaptic varicosities and postsynaptic spines: morphological alterations of CA3CA1 synapses in hippocampal slice cultures. Mol. Cell. Neurosci. 28, 264-274 (2005).
77. Chen, B. M. & Grinnell, A. D. Integrins and modulation of transmitter release from motor nerve terminals by stretch. Science 269, 1578-1580 (1995).
78. Fatt, P. & Katz, B. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. 117, 109-128 (1952).
79. Balice-Gordon, R. J. & Lichtman, J. W. In vivo visualization of the growth of pre-and postsynaptic elements of neuromuscular junctions in the mouse. J. Neurosci. 10, 894-908 (1990).
80. Yasuda, R. & Murakoshi, H. The mechanisms underlying the spatial spreading of signaling activity. Curr. Opin. Neurobiol. 21, 313-321 (2011).
81. Murakoshi, H., Wang, H. & Yasuda, R. Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472, 100-104 (2011).
82. Kostic, A., Sap, J. & Sheetz, M. P. RPTPα is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons. J. Cell Sci. 120, 3895-3904 (2007).
83. Flanagan, L. A., Ju, Y. E., Marg, B., Osterfield, M. & Janmey, P. A. Neurite branching on deformable substrates. Neuroreport 13, 2411-2415 (2002).
84. Pfister, B. J., Iwata, A., Meaney, D. F. & Smith, D. H. Extreme stretch growth of integrated axons. J. Neurosci. 24, 7978-7983 (2004).
85. Fass, J. N. & Odde, D. J. Tensile force-dependent neurite elicitation via antiβ1 integrin antibody-coated magnetic beads. Biophys. J. 85, 623-636 (2003).
86. Zheng, J. et al. Tensile regulation of axonal elongation and initiation. J. Neurosci. 11, 1117-1125 (1991).
87. Koch, D., Rosoff, W. J., Jiang, J., Geller, H. M. & Urbach, J. S. Strength in the periphery: growth cone biomechanics and substrate rigidity response in peripheral and central nervous system neurons. Biophys. J. 102, 452-460 (2012).
88. Bridgman, P. C., Dave, S., Asnes, C. F., Tullio, A. N. & Adelstein, R. S. Myosin IIB is required for growth cone motility. J. Neurosci. 21, 6159-6169 (2001).
89. Bray, D. Axonal growth in response to experimentally applied mechanical tension. Dev. Biol. 102, 379-389 (1984).
90. Hoge, C. W. et al. Mild traumatic brain injury in U.S. soldiers returning from Iraq. N. Engl. J. Med. 358, 453-463 (2008).
91. Meaney, D. F. & Smith, D. H. Biomechanics of concussion. Clin. Sports Med. 30, 19-31 (2011).
92. Farkas, O. & Povlishock, J. T. Cellular and subcellular change evoked by diffuse traumatic brain injury: a complex web of change extending far beyond focal damage. Prog. Brain Res. 161, 43-59 (2007).
93. Wolf, J. A., Stys, P. K., Lusardi, T., Meaney, D. & Smith, D. H. Traumatic axonal injury induces calcium influx modulated by tetrodotoxin- sensitive sodium channels. J. Neurosci. 21, 1923-1930 (2001).
94. Hemphill, M. A. et al. A possible role for integrin signaling in diffuse axonal injury. PLoS ONE 6, e22899 (2011).
95. Farkas, O., Lifshitz, J. & Povlishock, J. T. Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury? J. Neurosci. 26, 3130-3140 (2006).
96. Kilinc, D., Gallo, G. & Barbee, K. A. Mechanically-induced membrane poration causes axonal beading and localized cytoskeletal damage. Exp. Neurol. 212, 422-430 (2008).
97. Lo, E. H., Wang, X. & Cuzner, M. L. Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J. Neurosci. Res. 69, 1-9 (2002).
98. Rajagopalan, J. & Saif, M. T. MEMS sensors and microsystems for cell mechanobiology. J. Micromech. Microeng. 21, 54002-54012 (2011).
99. McBride, D. W. Jr & Hamill, O. P. Pressure-clamp technique for measurement of the relaxation kinetics of mechanosensitive channels. Trends Neurosci. 16, 341-345 (1993).
100. Gullapalli, R. R., Tabouillot, T., Mathura, R., Dangaria, J. H. & Butler, P. J. Integrated multimodal microscopy, time-resolved fluorescence, and optical-trap rheometry: toward single molecule mechanobiology. J. Biomed. Opt. 12, 014012 (2007).
101. Wang, Y. & Wang, N. FRET and mechanobiology. Integr. Biol. 1, 565-573 (2009).
102. Meng, F., Suchyna, T. M., Lazakovitch, E., Gronostajski, R. M. & Sachs, F. Real time FRET based detection of mechanical stress in cytoskeletal and extracellular matrix proteins. Cell. Mol. Bioeng. 4, 148-159 (2011).
103. Azeloglu, E. U. & Costa, K. D. Atomic force microscopy in mechanobiology: measuring microelastic heterogeneity of living cells. Methods Mol. Biol. 736, 303-329 (2011).
104. Yang, M. T., Fu, J., Wang, Y. K., Desai, R. A. & Chen, C. S. Assaying stem cell mechanobiology on microfabricated elastomeric substrates with geometrically modulated rigidity. Nature Protoc. 6, 187-213 (2011).
105. Simmons, C. S. et al. Integrated strain array for cellular mechanobiology studies. J. Micromech. Microeng. 21, 54016-54025 (2011).
106. Taylor, A. M., Dieterich, D. C., Ito, H. T., Kim, S. A. & Schuman, E. M. Microfluidic local perfusion chambers for the visualization and manipulation of synapses. Neuron 66, 57-68 (2010).
107. Taylor, A. M. et al. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nature Methods 2, 599-605 (2005).
108. Cheng, C. M. et al. Probing localized neural mechanotransduction through surface-modified elastomeric matrices and electrophysiology. Nature Protoc. 5, 714-724 (2010).
109. Dalecki, D. Mechanical bioeffects of ultrasound. Annu. Rev. Biomed. Eng. 6, 229-248 (2004).
110. Tufail, Y., Yoshihiro, A., Pati, S., Tauchmann, M. L. & Tyler, W. J. Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound. Nature Protoc. 6, 1453-1470 (2011).
111. Kucewicz, J. C. et al. Functional tissue pulsatility imaging of the brain during visual stimulation. Ultrasound Med. Biol. 33, 681-690 (2007).
112. Berg, D. Hyperechogenicity of the substantia nigra: pitfalls in assessment and specificity for Parkinson's disease. J. Neural Transm. 118, 453-461 (2011).
113. Mariappan, Y. K., Glaser, K. J. & Ehman, R. L. Magnetic resonance elastography: a review. Clin. Anat. 23, 497-511 (2010).
114. Boulet, T., Kelso, M. L. & Othman, S. F. Microscopic magnetic resonance elastography of traumatic brain injury model. J. Neurosci. Methods 201, 296-306 (2011).
115. Engelhardt, H., Gaub, H. & Sackmann, E. Viscoelastic properties of erythrocyte membranes in high-frequency electric fields. Nature 307, 378-380 (1984).
116. Katnik, C. & Waugh, R. Electric fields induce reversible changes in the surface to volume ratio of micropipette-aspirated erythrocytes. Biophys. J. 57, 865-875 (1990).
117. MacQueen, L. A., Buschmann, M. D. & Wertheimer, M. R. Mechanical properties of mammalian cells in suspension measured by electro-deformation. J. Micromech. Microeng. 20, 065007 (2010).
118. Tabarean, I. V. & Morris, C. E. Membrane stretch accelerates activation and slow inactivation in Shaker channels with S3S4 linker deletions. Biophys. J. 82, 2982-2994 (2002).
119. Maingret, F., Fosset, M., Lesage, F., Lazdunski, M. & Honore, E. TRAAK is a mammalian neuronal mechano-gated K+ channel. J. Biol. Chem. 274, 1381-1387 (1999).
120. Brohawn, S. G., del Marmol, J. & MacKinnon, R. Crystal structure of the human K2P TRAAK, a lipid-and mechano-sensitive K+ ion channel. Science 335, 436-441 (2012).
121. Maingret, F., Patel, A. J., Lesage, F., Lazdunski, M. & Honore, E. Mechano-or acid stimulation, two interactive modes of activation of the TREK1 potassium channel. J. Biol. Chem. 274, 26691-26696 (1999).
122. Lin, W., Laitko, U., Juranka, P. F. & Morris, C. E. Dual stretch responses of mHCN2 pacemaker channels: accelerated activation, accelerated deactivation. Biophys. J. 92, 1559-1572 (2007).
123. Niu, X., Qian, X. & Magleby, K. L. Linker-gating ring complex as passive spring and Ca2+-dependent machine for a voltage-and Ca2+-activated potassium channel. Neuron 42, 745-756 (2004).
124. Morris, C. E. & Juranka, P. F. Nav channel mechanosensitivity: activation and inactivation accelerate reversibly with stretch. Biophys. J. 93, 822-833 (2007).
125. Beyder, A. et al. Mechanosensitivity of Nav1.5, a voltage-sensitive sodium channel. J. Physiol. 588, 4969-4985 (2010).
126. Calabrese, B., Tabarean, I. V., Juranka, P. & Morris, C. E. Mechanosensitivity of Ntype calcium channel currents. Biophys. J. 83, 2560-2574 (2002).
127. Etzion, Y. & Grossman, Y. Pressure-induced depression of synaptic transmission in the cerebellar parallel fibre synapse involves suppression of presynaptic Ntype Ca2+ channels. Eur. J. Neurosci. 12, 4007-4016 (2000).
128. Paoletti, P. & Ascher, P. Mechanosensitivity of NMDA receptors in cultured mouse central neurons. Neuron 13, 645-655 (1994).
129. Singh, P. et al. Nmethyl-daspartate receptor mechanosensitivity is governed by C terminus of NR2B subunit. J. Biol. Chem. 287, 4348-4359 (2012).
130. Maroto, R. et al. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nature Cell Biol. 7, 179-185 (2005).
131. Liedtke, W. Handbook of Experimental Pharmacology Vol. 179 (eds Flockerzi, V. & Nilius, B.) 473-487 (Springer, 2007).
132. Grimm, C., Kraft, R., Sauerbruch, S., Schultz, G. & Harteneck, C. Molecular and functional characterization of the melastatin-related cation channel TRPM3. J. Biol. Chem. 278, 21493-21501 (2003).
133. Thomas, D., Plant, L. D., Wilkens, C. M., McCrossan, Z. A. & Goldstein, S. A. Alternative translation initiation in rat brain yields K2P2.1 potassium channels permeable to sodium. Neuron 58, 859-870 (2008).
134. Zhang, W. K. et al. Mechanosensitive gating of CFTR. Nature Cell Biol. 12, 507-512 (2010).