1932

Abstract

Organisms as diverse as microbes, roundworms, insects, and mammals detect and respond to applied force. In animals, this ability depends on ionotropic force receptors, known as mechanoelectrical transduction (MeT) channels, that are expressed by specialized mechanoreceptor cells embedded in diverse tissues and distributed throughout the body. These cells mediate hearing, touch, and proprioception and play a crucial role in regulating organ function. Here, we attempt to integrate knowledge about the architecture of mechanoreceptor cells and their sensory organs with principles of cell mechanics, and we consider how engulfing tissues contribute to mechanical filtering. We address progress in the quest to identify the proteins that form MeT channels and to understand how these channels are gated. For clarity and convenience, we focus on sensory mechanobiology in nematodes, fruit flies, and mice. These themes are emphasized: asymmetric responses to applied forces, which may reflect anisotropy of the structure and mechanics of sensory mechanoreceptor cells, and proteins that function as MeT channels, which appear to have emerged many times through evolution.

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2015-11-13
2024-04-30
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Literature Cited

  1. Anishkin A, Kung C. 2013. Stiffened lipid platforms at molecular force foci. PNAS 110:134886–92 [Google Scholar]
  2. Anishkin A, Loukin SH, Teng J, Kung C. 2014. Feeling the hidden mechanical forces in lipid bilayer is an original sense. PNAS 111:227898–905 [Google Scholar]
  3. Arnadóttir J, Chalfie M. 2010. Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39:1111–37 [Google Scholar]
  4. Arnadóttir J, O'Hagan R, Chen Y, Goodman MB, Chalfie M. 2011. The DEG/ENaC protein MEC-10 regulates the transduction channel complex in Caenorhabditis elegans touch receptor neurons. J. Neurosci. 31:3512695–704 [Google Scholar]
  5. Bagriantsev SN, Gracheva EO, Gallagher PG. 2014. Piezo proteins: regulators of mechanosensation and other cellular processes. J. Biol. Chem. 289:4631673–81 [Google Scholar]
  6. Beurg M, Fettiplace R, Nam J-H, Ricci AJ. 2009. Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging. Nat. Neurosci. 12:5553–58 [Google Scholar]
  7. Biswas A, Manivannan M, Srinivasan MA. 2015. Multiscale layered biomechanical model of the Pacinian corpuscle. IEEE Trans. Haptics 8:131–42 [Google Scholar]
  8. Bitan A, Guild GM, Bar-Dubin D, Abdu U. 2010. Asymmetric microtubule function is an essential requirement for polarized organization of the Drosophila bristle. Mol. Cell. Biol. 30:2496–507 [Google Scholar]
  9. Boal D. 2013. The cell's biological rods and ropes. MRS Bull. 24:1027–31 [Google Scholar]
  10. Bohlen CJ, Chesler AT, Sharif-Naeini R, Medzihradszky KF, Zhou S. et al. 2012. A heteromeric Texas coral snake toxin targets acid-sensing ion channels to produce pain. Nature 479:7373410–14 [Google Scholar]
  11. Bounoutas A, Hagan RO, Chalfie M. 2009. The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation. Curr. Biol. 19:161362–67 [Google Scholar]
  12. Brangwynne CP, MacKintosh FC, Kumar S, Geisse NA, Talbot J. et al. 2006. Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J. Cell Biol. 173:5733–41 [Google Scholar]
  13. Brohawn SG, Su Z, MacKinnon R. 2014. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. PNAS 111:93614–19 [Google Scholar]
  14. Brown AG, Iggo A. 1967. A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit. J. Physiol. 193:3707–33 [Google Scholar]
  15. Brown JW, Bullitt E, Sriswasdi S, Harper S, Speicher DW, McKnight CJ. 2015. The physiological molecular shape of spectrin: a compact supercoil resembling a Chinese finger trap. PLOS Comp. Biol. 11:e1004302 [Google Scholar]
  16. Burnette DT, Ji L, Schaefer AW, Medeiros NA, Danuser G, Forscher P. 2008. Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. Dev. Cell 15:1163–69 [Google Scholar]
  17. Chalfie M, Au M. 1989. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243:48941027–33 [Google Scholar]
  18. Chalfie M, Sulston JE. 1981. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev. Biol. 82:2358–70 [Google Scholar]
  19. Chang H, Nathans J. 2013. Responses of hair follicle-associated structures to loss of planar cell polarity signaling. PNAS 110:10E908–17 [Google Scholar]
  20. Chatzigeorgiou M, Bang S, Hwang SW, Schafer WR. 2013. tmc-1 encodes a sodium-sensitive channel required for salt chemosensation in C. elegans. Nature 494:743595–99 [Google Scholar]
  21. Chelur DS, Ernstrom GG, Goodman MB, Yao CA, Chen L. et al. 2002. The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel. Nature 420:6916669–73 [Google Scholar]
  22. Cheng LE, Song W, Looger LL, Jan LY, Jan YN. 2010. The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron 67:3373–80 [Google Scholar]
  23. Chesterton LJ, McIntyre CW. 2005. The assessment of baroreflex sensitivity in patients with chronic kidney disease: implications for vasomotor instability. Curr. Opin. Nephrol. Hypertens. 14:6586–91 [Google Scholar]
  24. Colbert HA, Smith TL, Bargmann CI. 1997. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 17:218259–69 [Google Scholar]
  25. Coste B, Houge G, Murray MF, Stitziel N, Bandell M. et al. 2013. Gain-of-function mutations in the mechanically activated ion channel PIEZO2 cause a subtype of distal arthrogryposis. PNAS 110:124667–72 [Google Scholar]
  26. Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S. et al. 2010. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330:600055–60 [Google Scholar]
  27. Coste B, Xiao B, Santos JS, Syeda R, Grandl J. et al. 2012. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483:7388176–81 [Google Scholar]
  28. Cueva JG, Mulholland A, Goodman MB. 2007. Nanoscale organization of the MEC-4 DEG/ENaC sensory mechanotransduction channel in Caenorhabditis elegans touch receptor neurons. J. Neurosci. 27:5114089–98 [Google Scholar]
  29. De R, Zemel A, Safran SA. 2008. Do cells sense stress or strain? Measurement of cellular orientation can provide a clue. Biophys. J. 94:5L29–31 [Google Scholar]
  30. Delmas P, Hao J, Rodat-Despoix L. 2011. Molecular mechanisms of mechanotransduction in mammalian sensory neurons. Nat. Rev. Neurosci. 12:3139–53 [Google Scholar]
  31. Dickinson M. 2006. Insect flight. Curr. Biol. 16:9R309–14 [Google Scholar]
  32. Diochot S, Baron A, Salinas M, Douguet D, Scarzello S. et al. 2013. Black mamba venom peptides target acid-sensing ion channels to abolish pain. Nature 490:7421552–55 [Google Scholar]
  33. Du H, Gu G, William CM, Chalfie M. 1996. Extracellular proteins needed for C. elegans mechanosensation. Neuron 16:1183–94 [Google Scholar]
  34. Dubin AE, Schmidt M, Mathur J, Petrus MJ, Xiao B. et al. 2012. Inflammatory signals enhance Piezo2-mediated mechanosensitive currents. Cell Rep. 2:3511–17 [Google Scholar]
  35. Dykes RW. 1975. Afferent fibers from mystacial vibrissae of cats and seals. J. Neurophysiol. 38:3650–62 [Google Scholar]
  36. Effertz T, Scharr AL, Ricci AJ. 2015. The how and why of identifying the hair cell mechano-electrical transduction channel. Pflügers Arch. 467:173–84 [Google Scholar]
  37. Effertz T, Wiek R, Göpfert MC. 2011. NompC TRP channel is essential for Drosophila sound receptor function. Curr. Biol. 21:7592–97 [Google Scholar]
  38. Eijkelkamp N, Linley JE, Torres JM, Bee L, Dickenson AH. et al. 2013. A role for Piezo2 in EPAC1-dependent mechanical allodynia. Nat. Commun. 4:1682 [Google Scholar]
  39. Emtage L, Gu G, Hartwieg E, Chalfie M. 2004. Extracellular proteins organize the mechanosensory channel complex in C. elegans touch receptor neurons. Neuron 44:5795–807 [Google Scholar]
  40. Ernstrom GG, Chalfie M. 2002. Genetics of sensory mechanotransduction. Annu. Rev. Genet. 36:1411–53 [Google Scholar]
  41. Escoubas P, De Weille JR, Lecoq A, Diochot S, Waldmann R. et al. 2000. Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J. Biol. Chem. 275:3325116–21 [Google Scholar]
  42. Ezan J, Montcouquiol M. 2013. Revisiting planar cell polarity in the inner ear. Semin. Cell Dev. Biol. 24:5499–506 [Google Scholar]
  43. Fabre CCG, Casal JE, Lawrence PA. 2008. The abdomen of Drosophila: Does planar cell polarity orient the neurons of mechanosensory bristles?. Neural Dev. 3:12 [Google Scholar]
  44. Faust U, Hampe N, Rubner W, Kirchgeßner N, Safran S. et al. 2011. Cyclic stress at mHz frequencies aligns fibroblasts in direction of zero strain. PLOS ONE 6:12e28963 [Google Scholar]
  45. Fettiplace R. 2006. Active hair bundle movements in auditory hair cells. J. Physiol. 576:129–36 [Google Scholar]
  46. Fettiplace R, Fuchs PA. 1999. Mechanisms of hair cell tuning. Annu. Rev. Physiol. 61:1809–34 [Google Scholar]
  47. Fettiplace R, Kim KX. 2014. The physiology of mechanoelectrical transduction channels in hearing. Physiol. Rev. 94:3951–86 [Google Scholar]
  48. Field LH, Matheson T. 1998. Chordotonal organs of insects. Advances in Insect Physiology 27 PD Evans 1–228 New York: Academic [Google Scholar]
  49. Fletcher DA, Mullins RD. 2010. Cell mechanics and the cytoskeleton. Nature 463:7280485–92 [Google Scholar]
  50. Foelix RF. 1985. Mechano- and chemoreceptive sensilla. Neurobiology of Arachnids FG Barth 118–37 New York: Springer [Google Scholar]
  51. Geffeney SL, Cueva JG, Glauser DA, Doll JC, Lee TH-C. et al. 2011. DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron 71:5845–57 [Google Scholar]
  52. Geffeney SL, Goodman MB. 2012. How we feel: ion channel partnerships that detect mechanical inputs and give rise to touch and pain perception. Neuron 74:4609–19 [Google Scholar]
  53. Geurten B, Spalthoff C, Göpfert MC. 2013. Insect hearing: active amplification in tympanal ears. Curr. Biol. 23:21R950–52 [Google Scholar]
  54. Gillespie PG, Müller U. 2009. Mechanotransduction by hair cells: models, molecules, and mechanisms. Cell 139:133–44 [Google Scholar]
  55. Gong J, Wang Q, Wang Z. 2013. NOMPC is likely a key component of Drosophila mechanotransduction channels. Eur. J. Neurosci. 38:12057–64 [Google Scholar]
  56. Goodman MB. 2006. Mechanosensation. WormBook. http://www.wormbook.org/chapters/www_mechanosensation/mechanosensation.html
  57. Goodman MB, Ernstrom GG, Chelur DS, O'Hagan R, Yao CA, Chalfie M. 2002. MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature 415:68751039–42 [Google Scholar]
  58. Goodman MB, Schwarz EM. 2003. Transducing touch in Caenorhabditis elegans. Annu. Rev. Physiol. 65:429–52 [Google Scholar]
  59. Göpfert MC, Robert D. 2002. The mechanical basis of Drosophila audition. J. Exp. Biol. 205:91199–208 [Google Scholar]
  60. Gorczyca DA, Younger S, Meltzer S, Kim SE, Cheng L. et al. 2014. Identification of Ppk26, a DEG/ENaC channel functioning with Ppk1 in a mutually dependent manner to guide locomotion behavior in Drosophila. Cell Rep. 9:41446–58 [Google Scholar]
  61. Gottschaldt K, Vahle-Hinz C. 1981. Merkel cell receptors: structure and transducer function. Science 214:4517183–86 [Google Scholar]
  62. Guo C-L, Ouyang M, Yu J-Y, Maslov J, Price A, Shen C-Y. 2012. Long-range mechanical force enables self-assembly of epithelial tubular patterns. PNAS 109:155576–82 [Google Scholar]
  63. Guo Y, Wang Y, Wang Q, Wang Z. 2014. The role of PPK26 in Drosophila larval mechanical nociception. Cell Rep. 9:41183–90 [Google Scholar]
  64. Guzmán C, Jeney S, Kreplak L, Kasas S, Kulik AJ. et al. 2006. Exploring the mechanical properties of single vimentin intermediate filaments by atomic force microscopy. J. Mol. Biol. 360:623–30 [Google Scholar]
  65. Haswell ES, Phillips R, Rees DC. 2011. Mechanosensitive channels: What can they do and how do they do it?. Structure 19:101356–69 [Google Scholar]
  66. Hayakawa K, Tatsumi H, Sokabe M. 2008. Actin stress fibers transmit and focus force to activate mechanosensitive channels. J. Cell. Sci. 121:4496–503 [Google Scholar]
  67. Herrmann H, Bär H, Kreplak L, Strelkov SV, Aebi U. 2007. Intermediate filaments: from cell architecture to nanomechanics. Nat. Rev. Mol. Cell Biol. 8:562–73 [Google Scholar]
  68. Hilliard MA, Bergamasco C, Arbucci S, Plasterk RHA, Bazzicalupo P. 2004. Worms taste bitter: ASH neurons, QUI-1, GPA-3 and ODR-3 mediate quinine avoidance in Caenorhabditis elegans. EMBO J. 23:51101–11 [Google Scholar]
  69. Hires SA, Pammer L, Svoboda K, Golomb D, Tsodyks M. 2013. Tapered whiskers are required for active tactile sensation. eLife 2:e01350 [Google Scholar]
  70. Hochmuth RM. 2000. Micropipette aspiration of living cells. J. Biomech. 33:15–22 [Google Scholar]
  71. Hoffman BD, Grashoff C, Schwartz MA. 2011. Dynamic molecular processes mediate cellular mechanotransduction. Nature 475:7356316–23 [Google Scholar]
  72. Hudspeth AJ. 1982. Extracellular current flow and the site of transduction by vertebrate hair cells. J. Neurosci. 2:11–10 [Google Scholar]
  73. Hudspeth AJ. 2014. Integrating the active process of hair cells with cochlear function. Nat. Rev. Neurosci. 15:9600–14 [Google Scholar]
  74. Hudspeth AJ, Corey DP. 1977. Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. PNAS 74:62407–11 [Google Scholar]
  75. Husson SJ, Costa WS, Wabnig S, Stirman JN, Watson JD. et al. 2012. Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors. Curr. Biol. 22:9743–52 [Google Scholar]
  76. Hwang RY, Zhong L, Xu Y, Johnson T, Zhang F. et al. 2007. Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 17:242105–16 [Google Scholar]
  77. Iggo A, Muir AR. 1969. The structure and function of a slowly adapting touch corpuscle in hairy skin. J. Physiol. 200:3763–96 [Google Scholar]
  78. Ikeda R, Cha M, Ling J, Jia Z, Coyle D, Gu JG. 2014. Merkel cells transduce and encode tactile stimuli to drive Aβ-afferent impulses. Cell 157:3664–75 [Google Scholar]
  79. Ingber DE. 1993. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell. Sci. 104:Pt. 3613–27 [Google Scholar]
  80. Ingber DE, Wang N, Stamenovic D. 2014. Tensegrity, cellular biophysics, and the mechanics of living systems. Rep. Prog. Phys. 77:446603 [Google Scholar]
  81. Iskratsch T, Wolfenson H, Sheetz MP. 2014. Appreciating force and shape—the rise of mechanotransduction in cell biology. Nat. Rev. Mol. Cell Biol. 15:12825–33 [Google Scholar]
  82. Kachar B, Parakkal M, Kurc M, Zhao Y, Gillespie PG. 2000. High-resolution structure of hair-cell tip links. PNAS 97:2413336–41 [Google Scholar]
  83. Kamikouchi A, Albert JT, Göpfert MC. 2010. Mechanical feedback amplification in Drosophila hearing is independent of synaptic transmission. Eur. J. Neurosci. 31:4697–703 [Google Scholar]
  84. Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A. et al. 2009. The neural basis of Drosophila gravity-sensing and hearing. Nature 457:7235165–71 [Google Scholar]
  85. Kang L, Gao J, Schafer WR, Xie Z, Xu XZS. 2010. C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron 67:3381–91 [Google Scholar]
  86. Kawashima Y, Géléoc GSG, Kurima K, Labay V, Lelli A. et al. 2011. Mechanotransduction in mouse inner ear hair cells requires transmembrane channel-like genes. J. Clin. Investig. 121:124796–809 [Google Scholar]
  87. Kernan MJ. 2007. Mechanotransduction and auditory transduction in Drosophila. Pflügers Arch. 454:5703–20 [Google Scholar]
  88. Kernan MJ, Cowan D, Zuker C. 1994. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12:61195–206 [Google Scholar]
  89. Kim KX, Beurg M, Hackney CM, Furness DN, Mahendrasingam S, Fettiplace R. 2013. The role of transmembrane channel-like proteins in the operation of hair cell mechanotransducer channels. J. Gen. Physiol. 142:5493–505 [Google Scholar]
  90. Kim SE, Coste B, Chadha A, Cook B, Patapoutian A. 2012. The role of Drosophila Piezo in mechanical nociception. Nature 483:7388209–12 [Google Scholar]
  91. Kloda A, Martinac B. 2002. Mechanosensitive channels of bacteria and archaea share a common ancestral origin. Eur. Biophys. J. 31:114–25 [Google Scholar]
  92. Kreplak L, Fudge D. 2007. Biomechanical properties of intermediate filaments: from tissues to single filaments and back. BioEssays 29:26–35 [Google Scholar]
  93. Krieg M, Arboleda-Estudillo Y, Puech PH, Käfer J, Graner F. et al. 2008. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10:4429–36 [Google Scholar]
  94. Krieg M, Dunn AR, Goodman MB. 2014. Mechanical control of the sense of touch by β-spectrin. Nat. Cell Biol. 16:3224–33 [Google Scholar]
  95. Kumar S, Maxwell IZ, Heisterkamp A, Polte TR, Lele TP. et al. 2006. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys. J. 90:103762–73 [Google Scholar]
  96. Kung C. 2005. A possible unifying principle for mechanosensation. Nat. Cell Biol. 436:7051647–54 [Google Scholar]
  97. Kung C, Martinac B, Sukharev S. 2010. Mechanosensitive channels in microbes. Annu. Rev. Microbiol. 64:1313–29 [Google Scholar]
  98. Kurusu T, Kuchitsu K, Nakano M, Nakayama Y, Iida H. 2013. Plant mechanosensing and Ca2+ transport. Trends Plant Sci. 18:4227–33 [Google Scholar]
  99. Kwegyir-Afful EE, Marella S, Simons DJ. 2008. Response properties of mouse trigeminal ganglion neurons. Somatosens. Mot. Res. 25:4209–21 [Google Scholar]
  100. Lechner SG, Lewin GR. 2013. Hairy sensation. Physiology 28:3142–50 [Google Scholar]
  101. Lesniak DR, Marshall KL, Wellnitz SA, Jenkins BA, Baba Y. et al. 2014. Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors. eLife 3:0e01488 [Google Scholar]
  102. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L. et al. 2011. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147:71615–27 [Google Scholar]
  103. Liang X, Madrid J, Gärtner R, Verbavatz J-M, Schiklenk C. et al. 2013. A NOMPC-dependent membrane-microtubule connector is a candidate for the gating spring in fly mechanoreceptors. Curr. Biol. 23:9755–63 [Google Scholar]
  104. Liang X, Madrid J, Howard J. 2014. The microtubule-based cytoskeleton is a component of a mechanical signaling pathway in fly campaniform receptors. Biophys. J. 107:122767–74 [Google Scholar]
  105. Liang X, Madrid J, Saleh HS, Howard J. 2010. NOMPC, a member of the TRP channel family, localizes to the tubular body and distal cilium of Drosophila campaniform and chordotonal receptor cells. Cytoskeleton 68:11–7 [Google Scholar]
  106. Lichtenstein SH, Carvell GE, Simons DJ. 1990. Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. Somatosens. Mot. Res. 7:147–65 [Google Scholar]
  107. Lin S-H, Sun W-H, Chen C-C. 2015. Genetic exploration of the role of acid-sensing ion channels. Neuropharmacology 94:99–118 [Google Scholar]
  108. Liu L, Tüzel E, Ross JL. 2011. Loop formation of microtubules during gliding at high density. J. Phys. Condens. Matter 23:37374104 [Google Scholar]
  109. Liu SC, Derick LH, Palek J. 1987. Visualization of the hexagonal lattice in the erythrocyte membrane skeleton. J. Cell Biol. 104:3527–36 [Google Scholar]
  110. Loewenstein WR, Mendelson M. 1965. Components of receptor adaptation in a Pacinian corpuscle. J. Physiol. 177:377–97 [Google Scholar]
  111. Loewenstein WR, Skalak R. 1966. Mechanical transmission in a Pacinian corpuscle. An analysis and a theory. J. Physiol. 182:2346–78 [Google Scholar]
  112. Lumpkin EA, Marshall KL, Nelson AM. 2010. Probing mammalian touch transduction. J. Cell Biol. 191:2237–48 [Google Scholar]
  113. Maoiléidigh , Nicola EM, Hudspeth AJ. 2012. The diverse effects of mechanical loading on active hair bundles. PNAS 109:61943–48 [Google Scholar]
  114. Maksimovic S, Nakatani M, Baba Y, Nelson AM, Marshall KL. et al. 2014. Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509:7502617–21 [Google Scholar]
  115. Mani NLM, Menon C. 2010. Effect of orientation of fibers and holes on the radial strain amplification of campaniform sensilla. J. Bionic Eng. 7:4314–20 [Google Scholar]
  116. Martinac B, Kloda A. 2003. Evolutionary origins of mechanosensitive ion channels. Prog. Biophys. Mol. Biol. 82:1–311–24 [Google Scholar]
  117. Maruhashi J, Mizuguchi K, Tasaki I. 1952. Action currents in single afferent nerve fibres elicited by stimulation of the skin of the toad and the cat. J. Physiol. 117:2129–51 [Google Scholar]
  118. Mauthner SE, Hwang RY, Lewis AH, Xiao Q, Tsubouchi A. et al. 2014. Balboa binds to Pickpocket in vivo and is required for mechanical nociception in Drosophila larvae. Curr. Biol. 24:242920–25 [Google Scholar]
  119. Meaud J, Grosh K. 2010. The effect of tectorial membrane and basilar membrane longitudinal coupling in cochlear mechanics. J. Acoust. Soc. Am. 127:31411–21 [Google Scholar]
  120. Mendelson M, Loewenstein WR. 1964. Mechanisms of receptor adaptation. Science 144:3618554–55 [Google Scholar]
  121. Meng F, Sachs F. 2012. Orientation-based FRET sensor for real-time imaging of cellular forces. J. Cell. Sci. 125:3743–50 [Google Scholar]
  122. Mitchison TJ, Charras GT, Mahadevan L. 2008. Implications of a poroelastic cytoplasm for the dynamics of animal cell shape. Semin. Cell Dev. Biol. 19:3215–23 [Google Scholar]
  123. Moeendarbary E, Harris AR. 2014. Cell mechanics: principles, practices, and prospects. Wiley Interdiscip. Rev. Syst. Biol. Med. 6:5371–88 [Google Scholar]
  124. Moeendarbary E, Valon L, Fritzsche M, Harris AR, Moulding DA. et al. 2013. The cytoplasm of living cells behaves as a poroelastic material. Nat. Mater. 12:3253–61 [Google Scholar]
  125. Nadrowski B, Albert JT, Göpfert MC. 2008. Transducer-based force generation explains active process in Drosophila hearing. Curr. Biol 18:181365–72 [Google Scholar]
  126. O'Hagan R, Chalfie M, Goodman MB. 2005. The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat. Neurosci. 8:143–50 [Google Scholar]
  127. Odde DJ, Ma L, Briggs AH, DeMarco A, Kirschner MW. 1999. Microtubule bending and breaking in living fibroblast cells. J. Cell. Sci. 112:Pt. 193283–88 [Google Scholar]
  128. Pampaloni F, Florin E-L. 2008. Microtubule architecture: inspiration for novel carbon nanotube-based biomimetic materials. Trends Biotechnol. 26:6302–10 [Google Scholar]
  129. Pan B, Géléoc GS, Asai Y, Horwitz GC, Kurima K. et al. 2013. TMC1 and TMC2 are components of the mechanotransduction channel in hair cells of the mammalian inner ear. Neuron 79:3504–15 [Google Scholar]
  130. Phillips R, Ursell T, Wiggins P, Sens P. 2009. Emerging roles for lipids in shaping membrane-protein function. Nature 459:7245379–85 [Google Scholar]
  131. Pivetti CD, Yen MR, Miller S, Busch W, Tseng YH. et al. 2003. Two families of mechanosensitive channel proteins. Microbiol. Mol. Biol. Rev. 67:166–85 [Google Scholar]
  132. Prole DL, Taylor CW. 2012. Identification and analysis of cation channel homologues in human pathogenic fungi. PLOS ONE 7:8e42404 [Google Scholar]
  133. Prole DL, Taylor CW. 2013. Identification and analysis of putative homologues of mechanosensitive channels in pathogenic protozoa. PLOS ONE 8:6e66068 [Google Scholar]
  134. Proske U, Gandevia SC. 2012. The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol. Rev. 92:41651–97 [Google Scholar]
  135. Qin Z, Kreplak L, Buehler MJ. 2009. Hierarchical structure controls nanomechanical properties of vimentin intermediate filaments. PLOS ONE 4:10e7294 [Google Scholar]
  136. Radmacher M, Fritz M, Kacher CM, Cleveland JP, Hansma PK. 1996. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys. J. 70:1556–67 [Google Scholar]
  137. Ranade SS, Woo S-H, Dubin AE, Moshourab RA, Wetzel C. et al. 2014. Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 516:7529121–25 [Google Scholar]
  138. Richardson GP, Lukashkin AN, Russell IJ. 2008. The tectorial membrane: one slice of a complex cochlear sandwich. Curr. Opin. Otolaryngol. Head Neck Surg. 16:5458–64 [Google Scholar]
  139. Robinson DR, Gebhart GF. 2008. Inside information: the unique features of visceral sensation. Mol. Interv. 8:5242–53 [Google Scholar]
  140. Rutlin M, Ho C-Y, Abraira VE, Cassidy C, Woodbury CJ, Ginty DD. 2014. The cellular and molecular basis of direction selectivity of Aδ-LTMRs. Cell 159:71640–51 [Google Scholar]
  141. Sato M. 1961. Response of Pacinian corpuscles to sinusoidal vibration. J. Physiol. 159:391–409 [Google Scholar]
  142. Schafer WR. 2014. Mechanosensory molecules and circuits in C. elegans. Pflügers Arch. 467:139–48 [Google Scholar]
  143. Sienknecht UJ, Köppl C, Fritzsch B. 2014. Evolution and development of hair cell polarity and efferent function in the inner ear. Brain Behav. Evol. 83:2150–61 [Google Scholar]
  144. Sukharev S, Corey DP. 2004. Mechanosensitive channels: multiplicity of families and gating paradigms. Sci. Signal. 2004:219re4 [Google Scholar]
  145. Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S-I. et al. 2003. Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160:3409–21 [Google Scholar]
  146. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PC. et al. 2013. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341:61491240104 [Google Scholar]
  147. Tanner K, Boudreau A, Bissell MJ, Kumar S. 2010. Dissecting regional variations in stress fiber mechanics in living cells with laser nanosurgery. Biophys. J. 99:92775–83 [Google Scholar]
  148. Thomas WE, Vogel V, Sokurenko E. 2008. Biophysics of catch bonds. Annu. Rev. Biophys. 37:1399–416 [Google Scholar]
  149. Thrasher TN. 2004. Baroreceptors, baroreceptor unloading, and the long-term control of blood pressure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:4R819–27 [Google Scholar]
  150. Thurm U. 1965. An insect mechanoreceptor. I. Fine structure and adequate stimulus. Cold Spring Harb. Symp. Quant. Biol. 30:75–82 [Google Scholar]
  151. Tilney LG, DeRosier DJ. 2005. How to make a curved Drosophila bristle using straight actin bundles. PNAS 102:5218785–92 [Google Scholar]
  152. Tobin DM, Madsen DM, Kahn-Kirby A, Peckol EL, Moulder G. et al. 2002. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:2307–18 [Google Scholar]
  153. Tracey WD, Wilson RI, Laurent G, Benzer S. 2003. painless, a Drosophila gene essential for nociception. Cell 113:2261–73 [Google Scholar]
  154. Tsubouchi A, Caldwell JC, Tracey WD. 2012. Dendritic filopodia, Ripped Pocket, NOMPC, and NMDARs contribute to the sense of touch in Drosophila larvae. Curr. Biol. 22:222124–34 [Google Scholar]
  155. Tuszyński JA, Luchko T, Portet S, Dixon JM. 2005. Anisotropic elastic properties of microtubules. Eur. Phys. J. E 17:129–35 [Google Scholar]
  156. Tuckett RP. 1978. Response of cutaneous hair and field mechanoreceptors in cat to paired mechanical stimuli. J. Neurophysiol. 41:1150–56 [Google Scholar]
  157. Vásquez V, Krieg M, Lockhead D, Goodman MB. 2014. Phospholipids that contain polyunsaturated fatty acids enhance neuronal cell mechanics and touch sensation. Cell Rep. 6:170–80 [Google Scholar]
  158. Walker RG, Willingham AT, Zuker CS. 2000. A Drosophila mechanosensory transduction channel. Science 287:54612229–34 [Google Scholar]
  159. Wang N, Tytell JD, Ingber DE. 2009. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10:175–82 [Google Scholar]
  160. Wang Y, Marshall KL, Baba Y, Gerling GJ, Lumpkin EA. 2013. Hyperelastic material properties of mouse skin under compression. PLOS ONE 8:6e67439 [Google Scholar]
  161. Warren B, Lukashkin AN, Russell IJ. 2010. The dynein-tubulin motor powers active oscillations and amplification in the hearing organ of the mosquito. Proc. R. Soc. B 277:16881761–69 [Google Scholar]
  162. Williams CM, Kramer EM. 2010. The advantages of a tapered whisker. PLOS ONE 5:1e8806 [Google Scholar]
  163. Windmill JFC, Sueur J, Robert D. 2009. The next step in cicada audition: measuring pico-mechanics in the cicada's ear. J. Exp. Biol. 212:Pt. 244079–83 [Google Scholar]
  164. Wolstenholme AJ, Williamson SM, Reaves BJ. 2010. TRP channels in parasites. Adv. Exp. Med. Biol. 704:359–71 [Google Scholar]
  165. Woo S-H, Ranade S, Weyer AD, Dubin AE, Baba Y. et al. 2014. Piezo2 is required for Merkel-cell mechanotransduction. Nature 509:7502622–26 [Google Scholar]
  166. Xu K, Zhong G, Zhuang X. 2013. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339:6118452–56 [Google Scholar]
  167. Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y. et al. 2013. Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493:7431221–25 [Google Scholar]
  168. Zelle KM, Lu B, Pyfrom SC, Ben-Shahar Y. 2013. The genetic architecture of degenerin/epithelial sodium channels in Drosophila. G3 3:3441–50 [Google Scholar]
  169. Zhang W, Yan Z, Jan LY, Jan YN. 2013. Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae. PNAS 110:3313612–17 [Google Scholar]
  170. Zhou EH, Martinez FD, Fredberg JJ. 2013. Cell rheology: mush rather than machine. Nat. Mater. 12:3184–85 [Google Scholar]
  171. Zimmerman A, Bai L, Ginty DD. 2014. The gentle touch receptors of mammalian skin. Science 346:6212950–54 [Google Scholar]
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