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The Molecular Basis of Mechanosensory Transduction

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Sensing in Nature

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 739))

Abstract

Multiple senses, including hearing, touch and osmotic regulation, require the ability to convert force into an electrical signal: A process called mechanotransduction. Mechanotransduction occurs through specialized proteins that open an ion channel pore in response to a mechanical stimulus. Many of these proteins remain unidentified in vertebrates, but known mechanotransduction channels in lower organisms provide clues into their identity and mechanism. Bacteria, fruit flies and nematodes have all been used to elucidate the molecules necessary for force transduction. This chapter discusses many different mechanical senses and takes an evolutionary approach to review the proteins responsible for mechanotransduction in various biological kingdoms.

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References

  1. Martinac B. Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci 2004; 117(Pt 12): 2449–2460.

    Article  PubMed  CAS  Google Scholar 

  2. Corey DP, Hudspeth AJ. Kinetics of the receptor current in bullfrog saccular hair cells. J Neurosci 1983; 3(5):962–976.

    PubMed  CAS  Google Scholar 

  3. Kung C. A possible unifying principle for mechanosensation. Nature 2005; 436(7051):647–654.

    Article  PubMed  CAS  Google Scholar 

  4. Berrier C, Besnard M, Ajouz B et al. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J Membr Biol 1996; 151(2):175–187.

    Article  PubMed  CAS  Google Scholar 

  5. Martinac B, Buechner M, Delcour AH et al. Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci USA 1987; 84(8):2297–2301.

    Article  PubMed  CAS  Google Scholar 

  6. Perozo E, Cortes DM, Sompornpisut P et al. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 2002; 418(6901):942–948.

    Article  PubMed  CAS  Google Scholar 

  7. Perozo E, Kloda A, Cortes DM et al. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 2002; 9(9):696–703.

    Article  PubMed  CAS  Google Scholar 

  8. Levina N, Totemeyer S, Stokes NR et al. 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 1999; 18(7):1730–1737.

    Article  PubMed  CAS  Google Scholar 

  9. Kloda A, Martinac B. Mechanosensitive channels in archaea. Cell Biochem Biophys 2001; 34(3):349–381.

    Article  PubMed  CAS  Google Scholar 

  10. Haswell ES, Peyronnet R, Barbier-Brygoo H et al. Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr Biol 2008; 18(10):730–734.

    Article  PubMed  CAS  Google Scholar 

  11. Braam J. In touch: plant responses to mechanical stimuli. New Phytol 2005; 165(2):373–389.

    Article  PubMed  Google Scholar 

  12. Haswell ES, Meyerowitz EM. MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr Biol 2006; 16(1):1–11.

    Article  Google Scholar 

  13. Xiao R, Xu XZ. Function and regulation of TRP family channels in C. elegans. Pflugers Arch 2009; 458(5):851–860.

    Article  PubMed  CAS  Google Scholar 

  14. Tobin D, Madsen D, Kahn-Kirby A et al. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 2002; 35(2):307–318.

    Article  PubMed  CAS  Google Scholar 

  15. Su Z, Zhou X, Loukin SH et al. The use of yeast to understand TRP-channel mechanosensitivity. Pflugers Arch 2009; 458(5):861–867.

    Article  PubMed  CAS  Google Scholar 

  16. Tavernarakis N, Driscoll M. Mechanotransduction in Caenorhabditis elegans: the role of DEG/ENaC ion channels. Cell Biochem Biophys 2001; 35(1):1–18.

    Article  PubMed  CAS  Google Scholar 

  17. Chalfie M, Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 1981; 82(2):358–370.

    Article  PubMed  CAS  Google Scholar 

  18. Chalfie M, Au M. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 1989; 243(4894 Pt 1):1027–1033.

    Article  PubMed  CAS  Google Scholar 

  19. Brown AL, Liao Z, Goodman MB. MEC-2 and MEC-6 in the Caenorhabditis elegans sensory mechanotransduction complex: auxiliary subunits that enable channel activity. J Gen Physiol 2008; 131(6):605–616.

    Article  PubMed  CAS  Google Scholar 

  20. Goodman MB. Mechanosensation. WormBook 2006; 6:1–14

    Google Scholar 

  21. Drew LJ, Wood JN. Worm sensation! Mol Pain 2005; 1:8.

    Article  PubMed  Google Scholar 

  22. Tavernarakis N, Shreffler W, Wang S et al. unc-8, a DEG/ENaC family member, encodes a subunit of a candidate mechanically gated channel that modulates C. elegans locomotion. Neuron 1997; 18(1):107–119.

    Article  PubMed  CAS  Google Scholar 

  23. Walker RG, Willingham AT, Zuker CS. A Drosophila mechanosensory transduction channel. Science 2000; 287(5461):2229–2234.

    Article  PubMed  CAS  Google Scholar 

  24. Kernan MJ. Mechanotransduction and auditory transduction in Drosophila. Pflugers Arch 2007; 454(5):703–720.

    Article  PubMed  CAS  Google Scholar 

  25. Eberl DF, Hardy RW, Kernan MJ. Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 2000; 20(16):5981–5988.

    PubMed  CAS  Google Scholar 

  26. Li W, Feng Z, Sternberg PW et al. A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 2006; 440(7084):684–687.

    Article  PubMed  CAS  Google Scholar 

  27. Howard J, Bechstedt S. Hypothesis: a helix of ankyrin repeats of the NOMPC-TR P ion channel is the gating spring of mechanoreceptors. Curr Biol 2004; 14(6):R224–R226.

    Article  PubMed  CAS  Google Scholar 

  28. Sidi S, Friedrich RW, Nicolson T. NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 2003; 301(5629):96–99.

    Article  PubMed  CAS  Google Scholar 

  29. Gong Z, Son W, Chung YD et al. Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 2004; 24(41):9059–9066.

    Article  PubMed  CAS  Google Scholar 

  30. Kim J, Chung YD, Park DY et al. A TRPV family ion channel required for hearing in Drosophila. Nature 2003; 424(6944):81–84.

    Article  PubMed  CAS  Google Scholar 

  31. Boekhoff-Falk G. Hearing in Drosophila: development of Johnston’s organ and emerging parallels to vertebrate ear development. Dev Dyn 2005; 232(3):550–558.

    Article  PubMed  CAS  Google Scholar 

  32. Bermingham NA, Hassan BA, Price SD et al. Math1: an essential gene for the generation of inner ear hair cells. Science 1999; 284(5421):1837–1841.

    Article  PubMed  CAS  Google Scholar 

  33. Lumpkin EA, Collisson T, Parab P et al. Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expr Patterns 2003; 3(4):389–395.

    Article  PubMed  CAS  Google Scholar 

  34. Gopfert MC, Robert D. Motion generation by Drosophila mechanosensory neurons. Proc Natl Acad Sci USA 2003; 100(9):5514–5519.

    Article  PubMed  CAS  Google Scholar 

  35. Yorozu S, Wong A, Fischer BJ et al. Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 2009; 458(7235):201–205.

    Article  PubMed  CAS  Google Scholar 

  36. Kamikouchi A, Inagaki HK, Effertz T et al. The neural basis of Drosophila gravity-sensing and hearing. Nature 2009; 458(7235):165–171.

    Article  PubMed  CAS  Google Scholar 

  37. Tracey WD Jr, Wilson RI, Laurent G et al. Painless, a Drosophila gene essential for nociception. Cell 2003; 113(2):261–273.

    Article  PubMed  CAS  Google Scholar 

  38. Xu SY, Cang CL, Liu XF et al. Thermal nociception in adult Drosophila: behavioral characterization and the role of the painless gene. Genes Brain Behav 2006; 5(8):602–613.

    Article  PubMed  CAS  Google Scholar 

  39. Wetzel C, Hu J, Riethmacher D et al. A stomatin-domain protein essential for touch sensation in the mouse. Nature 2007; 445(7124):206–209.

    Article  PubMed  CAS  Google Scholar 

  40. Drew LJ, Rohrer DK, Price MP et al. Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J Physiol 2004; 556(Pt 3):691–710.

    Article  PubMed  CAS  Google Scholar 

  41. Price MP, Lewin GR, McIlwrath SL et al. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 2000; 407(6807):1007–1011.

    Article  PubMed  CAS  Google Scholar 

  42. Price MP, McIlwrath SL, Xie J et al. The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 2001; 32(6):1071–1083.

    Article  PubMed  CAS  Google Scholar 

  43. Mogil JS, Breese NM, Witty MF et al. Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci 2005; 25(43):9893–9901.

    Article  PubMed  CAS  Google Scholar 

  44. Bhattacharya MR, Bautista DM, Wu K et al. Radial stretch reveals distinct populations of mechanosensitive mammalian somatosensory neurons. Proc Natl Acad Sci USA 2008; 105(50):20015–20020.

    Article  PubMed  CAS  Google Scholar 

  45. Viana F, de la Pena E, Pecson B et al. Swelling-activated calcium signalling in cultured mouse primary sensory neurons. Eur J Neurosci 2001; 13(4):722–734.

    Article  PubMed  CAS  Google Scholar 

  46. Takahashi A, Gotoh H. Mechanosensitive whole-cell currents in cultured rat somatosensory neurons. Brain Res 2000; 869(1–2):225–230.

    Article  PubMed  CAS  Google Scholar 

  47. McCarter GC, Levine JD. Ionic basis of a mechanotransduction current in adult rat dorsal root ganglion neurons. Mol Pain 2006; 2:28.

    Article  PubMed  Google Scholar 

  48. Hu J, Chiang LY, Koch M et al. Evidence for a protein tether involved in somatic touch. EMBO J 29(4): 855–867.

    Google Scholar 

  49. Maricich SM, Wellnitz SA, Nelson AM et al. Merkel cells are essential for light-touch responses. Science 2009; 324(5934):1580–1582.

    Article  CAS  Google Scholar 

  50. Haeberle H, Bryan LA, Vadakkan TJ et al. Swelling-activated Ca2+ channels trigger Ca2+ signals in Merkel cells. PLoS One 2008; 3(3):e1750.

    Article  Google Scholar 

  51. Haeberle H, Lumpkin EA. Merkel cells in somatosensation. Chemosens Percept 2008; 1(2):110–118.

    Article  PubMed  Google Scholar 

  52. Haeberle H, Fujiwara M, Chuang J et al. Molecular profiling reveals synaptic release machinery in Merkel cells. Proc Natl Acad Sci USA 2004; 101(40):14503–14508.

    Article  PubMed  CAS  Google Scholar 

  53. Kazmierczak P, Sakaguchi H, Tokita J et al. Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 2007; 449(7158):87–91.

    Article  PubMed  CAS  Google Scholar 

  54. Blount P, Sukharev SI, Schroeder MJ et al. Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli. Proc Natl Acad Sci USA 1996; 93(21):11652–11657.

    Article  PubMed  CAS  Google Scholar 

  55. Hase CC, Le Dain AC, Martinac B. Molecular dissection of the large mechanosensitive ion channel (MscL) of E. coli: mutants with altered channel gating and pressure sensitivity. J Membr Biol 1997; 157(1):17–25.

    Article  PubMed  CAS  Google Scholar 

  56. Dedman A, Sharif-Naeini R, Folgering JH et al. The mechano-gated K(2P) channel TREK-1. Eur Biophys J 2009; 38(3):293–303.

    Article  PubMed  CAS  Google Scholar 

  57. Alloui A, Zimmermann K, Mamet J et al. TREK-1, a K+ channel involved in polymodal pain perception. EMBO J 2006; 25(11):2368–2376.

    Article  PubMed  CAS  Google Scholar 

  58. Patel AJ, Lazdunski M, Honore E. Lipid and mechano-gated 2P domain K(+) channels. Curr Opin Cell Biol 2001; 13(4):422–428.

    Article  PubMed  CAS  Google Scholar 

  59. Liedtke W, Friedman JM. Abnormal osmotic regulation in trpv4−/− mice. Proc Natl Acad Sci USA 2003; 100(23):13698–13703.

    Article  PubMed  CAS  Google Scholar 

  60. Brierley SM, Page AJ, Hughes PA et al. Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology 2008; 134(7):2059–2069.

    Article  PubMed  CAS  Google Scholar 

  61. Hartmannsgruber V, Heyken WT, Kacik M et al. Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLoS One 2007; 2(9):e827.

    Article  Google Scholar 

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Author information

Authors and Affiliations

  1. Integrated Graduate Program in Cellular, Molecular and Biomedical, Columbia University College of Physicians and Surgeons, New York, New York, USA

    Kara L. Marshall

  2. Departments of Dermatology and Physiology and Cellular Biophysics, Columbia University College of Physicians and Surgeons, New York, New York, USA

    Ellen A. Lumpkin

Authors
  1. Kara L. Marshall
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  2. Ellen A. Lumpkin
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Correspondence to Ellen A. Lumpkin .

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Editors and Affiliations

  1. Department of Immunology, Hospital Universitario Central de Asturias, Oviedo, Spain

    Carlos López-Larrea PhD

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Marshall, K.L., Lumpkin, E.A. (2012). The Molecular Basis of Mechanosensory Transduction. In: López-Larrea, C. (eds) Sensing in Nature. Advances in Experimental Medicine and Biology, vol 739. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-1704-0_9

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