1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Neuroscience
  4. Volume 43, 2020
  5. Article

Annual Review of Neuroscience

Volume 43, 2020

Mechanosensitive Ion Channels: Structural Features Relevant to Mechanotransduction Mechanisms

Abstract

Activation of mechanosensitive ion channels underlies a variety of fundamental physiological processes that require sensation of mechanical force. Different mechanosensitive channels adapt distinctive structures and mechanotransduction mechanisms to fit their biological roles. How mechanosensitive channels work, especially in animals, has been extensively studied in the past decade. Here we review key findings in the functional and structural characterizations of these channels and highlight the structural features relevant to the mechanotransduction mechanism of each specific channel.

Keyword(s): ENaC/DEG, K2P, mechanosensitive channel, NompC, PIEZO, TMEM16 superfamily
Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-070918-050509
2020-07-08
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/neuro/43/1/annurev-neuro-070918-050509.html?itemId=/content/journals/10.1146/annurev-neuro-070918-050509&mimeType=html&fmt=ahah

Literature Cited

  1. Alloui A, Zimmermann K, Mamet J, Duprat F, Noël J et al. 2006. TREK-1, a K+ channel involved in polymodal pain perception. EMBO J 25:112368–76
     [Google Scholar]
  2. Alvadia C, Lim NK, Mosina VC, Oostergetel GT, Dutzler R, Paulino C 2019. Cryo-EM structures and functional characterization of the murine lipid scramblase TMEM16F. eLife 8:e44365
     [Google Scholar]
  3. Anderson EO, Schneider ER, Matson JD, Gracheva EO, Bagriantsev SN 2018. TMEM150C/Tentonin3 is a regulator of mechano-gated ion channels. Cell Rep 23:3701–8
     [Google Scholar]
  4. Argudo D, Capponi S, Bethel NP, Grabe M 2019. A multiscale model of mechanotransduction by the ankyrin chains of the NOMPC channel. J. Gen. Physiol. 151:3316–27
     [Google Scholar]
  5. Árnadóttir J, Chalfie M. 2010. Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39:111–37
     [Google Scholar]
  6. Árnadóttir 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]
  7. Aryal P, Jarerattanachat V, Clausen MV, Schewe M, McClenaghan C et al. 2017. Bilayer-mediated structural transitions control mechanosensitivity of the TREK-2 K2P channel. Structure 25:5708–18.e2
     [Google Scholar]
  8. Autzen HE, Julius D, Cheng Y 2019. Membrane mimetic systems in cryoEM: keeping membrane proteins in their native environment. Curr. Opin. Struct. Biol. 58:259–68
     [Google Scholar]
  9. Baconguis I, Bohlen CJ, Goehring A, Julius D, Gouaux E 2014. X-ray structure of acid-sensing ion channel 1-snake toxin complex reveals open state of a Na+-selective channel. Cell 156:4717–29
     [Google Scholar]
  10. Baconguis I, Gouaux E. 2012. Structural plasticity and dynamic selectivity of acid-sensing ion channel–spider toxin complexes. Nature 489:7416400–5
     [Google Scholar]
  11. Bae C, Gnanasambandam R, Nicolai C, Sachs F, Gottlieb PA 2013a. Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1. PNAS 110:12E1162–68
     [Google Scholar]
  12. Bae C, Gottlieb PA, Sachs F 2013b. Human PIEZO1: removing inactivation. Biophys. J. 105:4880–86
     [Google Scholar]
  13. Ballesteros A, Fenollar-Ferrer C, Swartz KJ 2018. Structural relationship between the putative hair cell mechanotransduction channel TMC1 and TMEM16 proteins. eLife 7:e38433
     [Google Scholar]
  14. Bang H, Kim Y, Kim D 2000. TREK-2, a new member of the mechanosensitive tandem-pore K+ channel family. J. Biol. Chem. 275:2317412–19
     [Google Scholar]
  15. Beurg M, Xiong W, Zhao B, Müller U, Fettiplace R 2015. Subunit determination of the conductance of hair-cell mechanotransducer channels. PNAS 112:51589–94
     [Google Scholar]
  16. Bounoutas A, Kratz J, Emtage L, Ma C, Nguyen KC, Chalfie M 2011. Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway. PNAS 108:103982–87
     [Google Scholar]
  17. Brohawn SG. 2015. How ion channels sense mechanical force: insights from mechanosensitive K2P channels TRAAK, TREK1, and TREK2. Ann. N. Y. Acad. Sci. 1352:120–32
     [Google Scholar]
  18. Brohawn SG, Campbell EB, MacKinnon R 2014a. Physical mechanism for gating and mechanosensitivity of the human TRAAK K+ channel. Nature 516:729126–30
     [Google Scholar]
  19. Brohawn SG, del Mármol J, MacKinnon R 2012. Crystal structure of the human K2P TRAAK, a lipid- and mechano-sensitive K+ ion channel. Science 335:6067436–41
     [Google Scholar]
  20. Brohawn SG, Su Z, MacKinnon R 2014b. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. PNAS 111:93614–19
     [Google Scholar]
  21. Canessa CM, Schild L, Buell G, Thorens B, Gautschi I et al. 1994. Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 367:463–67
     [Google Scholar]
  22. Cao E, Liao M, Cheng Y, Julius D 2013. TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504:7478113–18
     [Google Scholar]
  23. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C et al. 2008. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322:590–94
     [Google Scholar]
  24. Chalfie M. 2009. Neurosensory mechanotransduction. Nat. Rev. Mol. Cell Biol. 10:144–52
     [Google Scholar]
  25. Chalfie M, Au M. 1989. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243:291027–33
     [Google Scholar]
  26. 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]
  27. Chen X, Wanggou S, Bodalia A, Zhu M, Dong W et al. 2018. A feedforward mechanism mediated by mechanosensitive ion channel PIEZO1 and tissue mechanics promotes glioma aggression. Neuron 100:4799–815.e7
     [Google Scholar]
  28. Chen Y, Bharill S, Isacoff EY, Chalfie M 2015. Subunit composition of a DEG/ENaC mechanosensory channel of Caenorhabditis elegans. . PNAS 112:3711690–95
     [Google Scholar]
  29. 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]
  30. Cheng Y. 2015. Single-particle cryo-EM at crystallographic resolution. Cell 161:3450–57
     [Google Scholar]
  31. Cheng Y, Grigorieff N, Penczek PA, Walz T 2015. A primer to single-particle cryo-electron microscopy. Cell 161:3438–49
     [Google Scholar]
  32. Cheng Y-R, Jiang B-Y, Chen C-C 2018. Acid-sensing ion channels: dual function proteins for chemo-sensing and mechano-sensing. J. Biomed. Sci. 25:4646
     [Google Scholar]
  33. Christensen AP, Corey DP. 2007. TRP channels in mechanosensation: direct or indirect activation. ? Nat. Rev. Neurosci. 8:7510–21
     [Google Scholar]
  34. Chung YD, Zhu J, Han YG, Kernan MJ 2001. nompA encodes a PNS-specific, ZP domain protein required to connect mechanosensory dendrites to sensory structures. Neuron 29:2415–28
     [Google Scholar]
  35. Clapham DE. 2003. TRP channels as cellular sensors. Nature 426:6966517–24
     [Google Scholar]
  36. Corey D, Hudspeth J. 1979. Ionic basis of the receptor potential in a vertebrate hair cell. Nature 281:5733675–77
     [Google Scholar]
  37. Corey DP, Holt JR. 2016. Are TMCs the mechanotransduction channels of vertebrate hair cells. ? J. Neurosci. 36:4310921–26
     [Google Scholar]
  38. Corns LF, Johnson SL, Kros CJ, Marcotti W 2016. Tmc1 point mutation affects Ca2+ sensitivity and block by dihydrostreptomycin of the mechanoelectrical transducer current of mouse outer hair cells. J. Neurosci. 36:2336–49
     [Google Scholar]
  39. 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]
  40. Coste B, Murthy SE, Mathur J, Schmidt M, Mechioukhi Y et al. 2015. Piezo1 ion channel pore properties are dictated by C-terminal region. Nat. Commun. 6:7223
     [Google Scholar]
  41. 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]
  42. Cox CD, Bae C, Ziegler L, Hartley S, Nikolova-Krstevski V et al. 2016. Removal of the mechanoprotective influence of the cytoskeleton reveals PIEZO1 is gated by bilayer tension. Nat. Commun. 7:10366
     [Google Scholar]
  43. Cox CD, Bavi N, Martinac B 2018. Bacterial mechanosensors. Annu. Rev. Physiol. 80:71–93
     [Google Scholar]
  44. 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]
  45. Dang S, Feng S, Tien J, Peters CJ, Bulkley D et al. 2017. Cryo-EM structures of the TMEM16A calcium-activated chloride channel. Nature 552:7685426–29
     [Google Scholar]
  46. Dietrich A, Kalwa H, Storch U, Mederos y Schnitzler M, Salanova B et al. 2007. Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Arch 455:3465–77
     [Google Scholar]
  47. Dietrich A, Mederos y Schnitzler M, Gollasch M, Gross V, Storch U et al. 2005. Increased vascular smooth muscle contractility in TRPC6−/− mice. Mol. Cell. Biol. 25:166980–89
     [Google Scholar]
  48. Dong YY, Pike ACW, Mackenzie A, McClenaghan C, Aryal P et al. 2015. K2P channel gating mechanisms revealed by structures of TREK-2 and a complex with Prozac. Science 347:62271256–59
     [Google Scholar]
  49. Du H, Gu G, William CM, Chalfie M 1996. Extracellular proteins needed for C. elegans mechanosensation. Neuron 16:1183–94
     [Google Scholar]
  50. Eastwood AL, Goodman MB. 2012. Insight into DEG/ENaC channel gating from genetics and structure. Physiology 27:5282–90
     [Google Scholar]
  51. Effertz T, Nadrowski B, Piepenbrock D, Albert JT, Göpfert MC 2012. Direct gating and mechanical integrity of Drosophila auditory transducers require TRPN1. Nat. Neurosci. 15:91198–200
     [Google Scholar]
  52. Effertz T, Wiek R, Göpfert MC 2011. NompC TRP channel is essential for Drosophila sound receptor function. Curr. Biol. 21:7592–97
     [Google Scholar]
  53. Eijkelkamp N, Quick K, Wood JN 2013. Transient receptor potential channels and mechanosensation. Annu. Rev. Neurosci. 36:519–46
     [Google Scholar]
  54. Ellefsen KL, Holt JR, Chang AC, Nourse JL, Arulmoli J et al. 2019. Myosin-II mediated traction forces evoke localized Piezo1-dependent Ca2+ flickers. Commun. Biol. 2:298
     [Google Scholar]
  55. Emtage L, Gu G, Hartwieg E, Chalfie M 2004. The mechanosensory channel complex in C. elegans touch receptor neurons. Neuron 44:5795–807
     [Google Scholar]
  56. Enyedi P, Czirják G. 2010. Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol. Rev. 90:2559–605
     [Google Scholar]
  57. Falleroni F, Torre V, Cojoc D 2018. Cell mechanotransduction with piconewton forces applied by optical tweezers. Front. Cell. Neurosci. 12:130
     [Google Scholar]
  58. Faucherre A, Nargeot J, Mangoni ME, Jopling C 2013. piezo2b regulates vertebrate light touch response. J. Neurosci. 33:4317089–94
     [Google Scholar]
  59. Falzone ME, Rheinberger J, Lee BC, Peyear T, Sasset L et al. 2019. Structural basis of Ca2+-dependent activation and lipid transport by a TMEM16 scramblase. eLife 8:e43229
     [Google Scholar]
  60. Feng S, Dang S, Han TW, Jan YN, Jan LY et al. 2019. Cryo-EM studies of TMEM16F calcium-activated ion channel suggest features important for lipid article cryo-EM studies of TMEM16F calcium-activated ion channel suggest features important for lipid scrambling. Cell Rep 28:2567–79.e4
     [Google Scholar]
  61. Fettiplace R. 2016. Is TMC1 the hair cell mechanotransducer channel?. Biophys. J. 111:13–9
     [Google Scholar]
  62. Fukushige T, Siddiqui ZK, Chou M, Culotti JG, Gogonea CB et al. 1999. MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J. Cell Sci 112:395–403
     [Google Scholar]
  63. Gao X, Tao Y, Lamas V, Huang M, Yeh WH et al. 2018. Treatment of autosomal dominant hearing loss by in vivo delivery of genome editing agents. Nature 553:7687217–21
     [Google Scholar]
  64. Ge J, Li W, Zhao Q, Li N, Chen M et al. 2015. Architecture of the mammalian mechanosensitive Piezo1 channel. Nature 527:757664–69
     [Google Scholar]
  65. Geffeney SL, Cueva JG, Glauser DA, Doll JC, Lee THC 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]
  66. Gonzales EB, Kawate T, Gouaux E 2009. Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 460:7255599–604
     [Google Scholar]
  67. 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]
  68. Göpfert MC, Robert D. 2003. Motion generation by Drosophila mechanosensory neurons. PNAS 100:95514–19
     [Google Scholar]
  69. Gottlieb P, Folgering J, Maroto R, Raso A, Wood TG et al. 2008. Revisiting TRPC1 and TRPC6 mechanosensitivity. Pflugers Arch 455:61097–103
     [Google Scholar]
  70. Gottlieb PA, Bae C, Sachs F 2012. Gating the mechanical channel Piezo1: a comparison between whole-cell and patch recording. Channels 6:4282–89
     [Google Scholar]
  71. Guo Y, Wang Y, Zhang W, Meltzer S, Zanini D et al. 2016. Transmembrane channel-like (tmc) gene regulates Drosophila larval locomotion. PNAS 113:267243–48
     [Google Scholar]
  72. Guo YR, MacKinnon R. 2017. Structure-based membrane dome mechanism for Piezo mechanosensitivity. eLife 6:e33660
     [Google Scholar]
  73. György B, Nist-Lund C, Pan B, Asai Y, Karavitaki KD et al. 2019. Allele-specific gene editing prevents deafness in a model of dominant progressive hearing loss. Nat. Med. 25:71123–30
     [Google Scholar]
  74. Hamilton ES, Schlegel AM, Haswell ES 2014. United in diversity: mechanosensitive ion channels in plants. Annu. Rev. Plant Biol. 66:113–37
     [Google Scholar]
  75. Hanukoglu I, Hanukoglu A. 2016. Epithelial sodium channel (ENaC) family: phylogeny, structure-function, tissue distribution, and associated inherited diseases. Gene 579:295–132
     [Google Scholar]
  76. Harkcom WT, Papanikolaou M, Kanda V, Crump SM, Abbott GW 2019. KCNQ1 rescues TMC1 plasma membrane expression but not mechanosensitive channel activity. J. Cell. Physiol. 234:813361–69
     [Google Scholar]
  77. Haselwandter CA, MacKinnon R. 2018. Piezo's membrane footprint and its contribution to mechanosensitivity. eLife 7:e41968
     [Google Scholar]
  78. He L, Gulyanon S, Mihovilovic Skanata M, Karagyozov D, Heckscher ES et al. 2019. Direction selectivity in Drosophila proprioceptors requires the mechanosensory channel Tmc. Curr. Biol. 29:6945–956.e3
     [Google Scholar]
  79. He L, Si G, Huang J, Samuel ADT, Perrimon N 2018. Mechanical regulation of stem-cell differentiation by the stretch-activated Piezo channel. Nature 555:7694103–6
     [Google Scholar]
  80. Hong GS, Lee B, Wee J, Chun H, Kim H et al. 2016. Tentonin 3/TMEM150c confers distinct mechanosensitive currents in dorsal-root ganglion neurons with proprioceptive function. Neuron 91:1107–18
     [Google Scholar]
  81. Hou C, Tian W, Kleist T, He K, Garcia V et al. 2014. DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Res 24:5632–35
     [Google Scholar]
  82. Howard J, Bechstedt S. 2004. Hypothesis: A helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr. Biol. 14:6R224–26
     [Google Scholar]
  83. Huang M, Chalfie M. 1994. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. . Nature 367:6462467–70
     [Google Scholar]
  84. Ibsen S, Tong A, Schutt C, Esener S, Chalasani SH 2015. Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans. Nat. Commun 6:8264
     [Google Scholar]
  85. Imtiaz A, Maqsood A, Rehman AU, Morell RJ, Holt JR et al. 2016. Recessive mutations of TMC1 associated with moderate to severe hearing loss. Neurogenetics 17:2115–23
     [Google Scholar]
  86. Jaggers OB, Ridone P, Martinac B, Baker MAB 2019. Fluorescence microscopy of Piezo1 in droplet hydrogel bilayers. Channels 13:1102–9
     [Google Scholar]
  87. Jaramillo F, Hudspeth AJ. 1991. Localization of the hair cell's transduction channels at the hair bundle's top by iontophoretic application of a channel blocker. Neuron 7:3409–20
     [Google Scholar]
  88. Jasti J, Furukawa H, Gonzales EB, Gouaux E 2007. Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 449:7160316–23
     [Google Scholar]
  89. Jia Y, Zhao Y, Kusakizako T, Wang Y, Pan C et al. 2020. TMC1 and TMC2 proteins are pore-forming subunits of mechanosensitive ion channels. Neuron 105:310–21.e3
     [Google Scholar]
  90. Jin P, Bulkley D, Guo Y, Zhang W, Guo Z et al. 2017. Electron cryo-microscopy structure of the mechanotransduction channel NOMPC. Nature 547:7661118–22
     [Google Scholar]
  91. Jojoa-Cruz S, Saotome K, Murthy SE, Tsui CCA, Sansom MS et al. 2018. Cryo-EM structure of the mechanically activated ion channel OSCA1.2. eLife 7:e41845
     [Google Scholar]
  92. 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]
  93. 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]
  94. Kernan M, Cowan D, Zuker C 1994. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. . Neuron 12:61195–206
     [Google Scholar]
  95. 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]
  96. Kleyman TR, Kashlan OB, Hughey RP 2018. Epithelial Na+ channel regulation by extracellular and intracellular factors. Annu. Rev. Physiol. 80:263–81
     [Google Scholar]
  97. Koser DE, Thompson AJ, Foster SK, Dwivedy A, Pillai EK et al. 2016. Mechanosensing is critical for axon growth in the developing brain. Nat. Neurosci. 19:121592–98
     [Google Scholar]
  98. Kung C. 2005. A possible unifying principle for mechanosensation. Nature 436:7051647–54
     [Google Scholar]
  99. Kurima K, Ebrahim S, Pan B, Sedlacek M, Sengupta P et al. 2015. TMC1 and TMC2 localize at the site of mechanotransduction in mammalian inner ear hair cell stereocilia. Cell Rep 12:101606–17
     [Google Scholar]
  100. Labay V, Weichert RM, Makishima T, Griffith AJ 2010. Topology of transmembrane channel–like gene 1 protein. Biochemistry 49:398592–98
     [Google Scholar]
  101. Lee G, Abdi K, Jiang Y, Michaely P, Bennett V, Marszalek PE 2006. Nanospring behaviour of ankyrin repeats. Nature 440:7081246–49
     [Google Scholar]
  102. Lehnert BP, Baker AE, Gaudry Q, Chiang AS, Wilson RI 2013. Distinct roles of TRP channels in auditory transduction and amplification in Drosophila. . Neuron 77:1115–28
     [Google Scholar]
  103. Lewis AH, Grandl J. 2015. Mechanical sensitivity of Piezo1 ion channels can be tuned by cellular membrane tension. eLife 4:e12088
     [Google Scholar]
  104. Li C, Rezania S, Kammerer S, Sokolowski A, Devaney T et al. 2015. Piezo1 forms mechanosensitive ion channels in the human MCF-7 breast cancer cell line. Sci. Rep. 5:8364
     [Google Scholar]
  105. Li J, Hou B, Tumova S, Muraki K, Bruns A et al. 2014. Piezo1 integration of vascular architecture with physiological force. Nature 515:7526279–82
     [Google Scholar]
  106. Li W, Feng Z, Sternberg PW, Xu XZS 2006. A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:7084684–87
     [Google Scholar]
  107. Liang X, Madrid J, Gärtner R, Verbavatz JM, 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]
  108. Liang X, Madrid J, Saleh HS, Howard J 2011. 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]
  109. Liao M, Cao E, Julius D, Cheng Y 2013. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:7478107–12
     [Google Scholar]
  110. Lin Y-C, Guo YR, Miyagi A, Levring J, MacKinnon R, Scheuring S 2019. Force-induced conformational changes in PIEZO1. Nature 573:230–34
     [Google Scholar]
  111. Liu C, Montell C. 2015. Forcing open TRP channels: mechanical gating as a unifying activation mechanism. Biochem. Biophys. Res. Commun. 460:122–25
     [Google Scholar]
  112. Liu X, Wang J, Sun L 2018. Structure of the hyperosmolality-gated calcium-permeable channel OSCA1.2. Nat. Commun. 9:5060
     [Google Scholar]
  113. Lolicato M, Arrigoni C, Mori T, Sekioka Y, Bryant C et al. 2017. K2P2.1 (TREK-1)-activator complexes reveal a cryptic selectivity filter binding site. Nature 547:7663364–68
     [Google Scholar]
  114. Lolicato M, Riegelhaupt PM, Arrigoni C, Clark KA, Minor DL 2014. Transmembrane helix straightening and buckling underlies activation of mechanosensitive and thermosensitive K2P channels. Neuron 84:61198–212
     [Google Scholar]
  115. Maingret F, Fosset M, Lesage F, Lazdunski M, Honoré E 1999. TRAAK is a mammalian neuronal mechano-gated K+ channel. J. Biol. Chem. 274:31381–87
     [Google Scholar]
  116. Maity K, Heumann JM, McGrath AP, Kopcho NJ, Hsu P-K et al. 2019. Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating. PNAS 116:2814309–18
     [Google Scholar]
  117. Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP 2005. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat. Cell Biol. 7:2179–85
     [Google Scholar]
  118. Martino F, Perestrelo AR, Vinarský V, Pagliari S, Forte G 2018. Cellular mechanotransduction: from tension to function. Front. Physiol. 9:824
     [Google Scholar]
  119. Medrano-Soto A, Moreno-Hagelsieb G, McLaughlin D, Ye ZS, Hendargo KJ, Saier MH 2018. Bioinformatic characterization of the Anoctamin Superfamily of Ca2+-activated ion channels and lipid scramblases. PLOS ONE 13:3e0192851
     [Google Scholar]
  120. Montell C. 2001. Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Sci. STKE 2001:90re1
     [Google Scholar]
  121. Murthy SE, Dubin AE, Patapoutian A 2017. Piezos thrive under pressure: mechanically activated ion channels in health and disease. Nat. Rev. Mol. Cell Biol. 18:12771–83
     [Google Scholar]
  122. Murthy SE, Dubin AE, Whitwam T, Jojoa-Cruz S, Cahalan SM et al. 2018. OSCA/TMEM63 are an evolutionarily conserved family of mechanically activated ion channels. eLife 7:e41844
     [Google Scholar]
  123. Noël J, Zimmermann K, Busserolles J, Deval E, Alloui A et al. 2009. The mechano-activated K+ channels TRAAK and TREK-1 control both warm and cold perception. EMBO J 28:91308–18
     [Google Scholar]
  124. Noreng S, Bharadwaj A, Posert R, Yoshioka C, Baconguis I 2018. Structure of the human epithelial sodium channel by cryo-electron microscopy. eLife 7:e39340
     [Google Scholar]
  125. 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]
  126. Pacentine IV, Nicolson T. 2019. Subunits of the mechano-electrical transduction channel, Tmc1/2b, require Tmie to localize in zebrafish sensory hair cells. PLOS Genet 15:2e1007635
     [Google Scholar]
  127. Pan B, Akyuz N, Liu XP, Asai Y, Nist-Lund C et al. 2018. TMC1 forms the pore of mechanosensory transduction channels in vertebrate inner ear hair cells. Neuron 99:4736–53.e6
     [Google Scholar]
  128. 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]
  129. Patel AJ, Honoré E, Maingret F, Lesage F, Fink M et al. 1998. A mammalian two pore domain mechano-gated S-like K+ channel. EMBO J 17:154283–90
     [Google Scholar]
  130. Pathak MM, Nourse JL, Tran T, Hwe J, Arulmoli J et al. 2014. Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. PNAS 111:4516148–53
     [Google Scholar]
  131. Paulino C, Kalienkova V, Lam AKM, Neldner Y, Dutzler R 2017a. Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM. Nature 552:7685421–25
     [Google Scholar]
  132. Paulino C, Neldner Y, Lam AKM, Kalienkova V, Brunner JD et al. 2017b. Structural basis for anion conduction in the calcium-activated chloride channel TMEM16A. eLife 6:e26232
     [Google Scholar]
  133. Pereira V, Busserolles J, Christin M, Devilliers M, Poupon L et al. 2014. Role of the TREK2 potassium channel in cold and warm thermosensation and in pain perception. Pain 155:122534–44
     [Google Scholar]
  134. Poole K, Herget R, Lapatsina L, Ngo HD, Lewin GR 2014. Tuning Piezo ion channels to detect molecular-scale movements relevant for fine touch. Nat. Commun. 5:3520
     [Google Scholar]
  135. Qi Y, Andolfi L, Frattini F, Mayer F, Lazzarino M, Hu J 2015. Membrane stiffening by STOML3 facilitates mechanosensation in sensory neurons. Nat. Commun. 6:8512
     [Google Scholar]
  136. Qiu X, Müller U. 2018. Mechanically gated ion channels in mammalian hair cells. Front. Cell. Neurosci. 12:100
     [Google Scholar]
  137. Ramdya P, Lichocki P, Cruchet S, Frisch L, Tse W et al. 2015. Mechanosensory interactions drive collective behaviour in Drosophila. . Nature 519:7542233–36
     [Google Scholar]
  138. Retailleau K, Duprat F, Arhatte M, Ranade SS, Peyronnet R et al. 2015. Piezo1 in smooth muscle cells is involved in hypertension-dependent arterial remodeling. Cell Rep 13:61161–71
     [Google Scholar]
  139. Saotome K, Murthy SE, Kefauver JM, Whitwam T, Patapoutian A, Ward AB 2018. Structure of the mechanically activated ion channel Piezo1. Nature 554:7693481–86
     [Google Scholar]
  140. Saotome K, Singh AK, Yelshanskaya MV, Sobolevsky AI 2016. Crystal structure of the epithelial calcium channel TRPV6. Nature 534:7608506–11
     [Google Scholar]
  141. Savage C, Hamelin M, Culotti JG, Coulson A, Albertson DG, Chalfie M 1989. mec-7 is a β-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 3:6870–81
     [Google Scholar]
  142. Scholz N, Monk KR, Kittel RJ, Langenhan T 2016. Adhesion GPCRs as a putative class of metabotropic mechanosensors. Handbook of Experimental Pharmacology, Vol. 234: Adhesion G Protein–Coupled Receptors T Langenhan, T Schöneburg 221–47 Cham, Switz.: Springer
     [Google Scholar]
  143. Schroeder BC, Cheng T, Jan YN, Jan LY 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:61019–29
     [Google Scholar]
  144. Schüler A, Schmitz G, Reft A, Özbek S, Thurm U, Bornberg-Bauer E 2015. The rise and fall of TRP-N, an ancient family of mechanogated ion channels, in metazoa. Genome Biol. Evol. 7:61713–27
     [Google Scholar]
  145. Segel M, Neumann B, Hill MFE, Weber IP, Viscomi C et al. 2019. Niche stiffness underlies the ageing of central nervous system progenitor cells. Nature 573:130–34
     [Google Scholar]
  146. Shi S, Luke CJ, Miedel MT, Silverman GA, Kleyman TR 2016. Activation of the Caenorhabditis elegans degenerin channel by shear stress requires the MEC-10 subunit. J. Biol. Chem. 291:2714012–22
     [Google Scholar]
  147. Shin J-B, Adams D, Paukert M, Siba M, Sidi S et al. 2005. Xenopus TRPN1 (NOMPC) localizes to microtubule-based cilia in epithelial cells, including inner-ear hair cells. PNAS 102:3512572–77
     [Google Scholar]
  148. Sidi S, Friedrich RW, Nicolson T 2003. NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:562996–99
     [Google Scholar]
  149. Sloan-Heggen CM, Bierer AO, Shearer AE, Kolbe DL, Nishimura CJ et al. 2016. Comprehensive genetic testing in the clinical evaluation of 1119 patients with hearing loss. Hum. Genet. 135:4441–50
     [Google Scholar]
  150. Solis AG, Bielecki P, Steach HR, Sharma L, Harman CCD et al. 2019. Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity. Nature 573:69–74
     [Google Scholar]
  151. Song Y, Li D, Farrelly O, Miles L, Li F et al. 2019. The mechanosensitive ion channel Piezo inhibits axon regeneration. Neuron 102:2373–89.e6
     [Google Scholar]
  152. Spassova MA, Hewavitharana T, Xu W, Soboloff J, Gill DL 2006. A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. PNAS 103:4416586–91
     [Google Scholar]
  153. Sugimoto A, Miyazaki A, Kawarabayashi K, Shono M, Akazawa Y et al. 2017. Piezo type mechanosensitive ion channel component 1 functions as a regulator of the cell fate determination of mesenchymal stem cells. Sci. Rep. 7:17696
     [Google Scholar]
  154. Sun L, Gao Y, He J, Cui L, Meissner J et al. 2019. Ultrastructural organization of NompC in the mechanoreceptive organelle of Drosophila campaniform mechanoreceptors. PNAS 116:157343–52
     [Google Scholar]
  155. Syeda R, Florendo MN, Cox CD, Kefauver JM, Santos JS et al. 2016. Piezo1 channels are inherently mechanosensitive. Cell Rep 17:71739–46
     [Google Scholar]
  156. Taberner FJ, Prato V, Schaefer I, Schrenk-Siemens K, Heppenstall PA, Lechner SG 2019. Structure-guided examination of the mechanogating mechanism of PIEZO2. PNAS 116:2814260–69
     [Google Scholar]
  157. Teng J, Loukin S, Anishkin A, Kung C 2014. The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflugers Arch 467:127–37
     [Google Scholar]
  158. Turner HN, Armengol K, Patel AA, Himmel NJ, Sullivan L et al. 2016. The TRP channels Pkd2, NompC, and Trpm act in cold-sensing neurons to mediate unique aversive behaviors to noxious cold in Drosophila. Curr. Biol 26:233116–28
     [Google Scholar]
  159. Walker RG, Willingham AT, Zuker CS 2000. A Drosophila mechanosensory transduction channel. Science 287:54612229–34
     [Google Scholar]
  160. Wang L, Zhou H, Zhang M, Liu W, Deng T et al. 2019. Structure and mechanogating of the mammalian tactile channel PIEZO2. Nature 573:225–29
     [Google Scholar]
  161. Wang X, Li G, Liu J, Liu J, Xu XZS 2016. TMC-1 mediates alkaline sensation in C. elegans through nociceptive neurons. Neuron 91:1146–54
     [Google Scholar]
  162. Wang Y, Guo Y, Liu C, Wang L, Zhang A et al. 2019. Push-to-open: the gating mechanism of the tethered mechanosensitive ion channel NompC. bioRxiv 853721. https://doi.org/10.1101/853721
    [Crossref]
  163. Whitlock JM, Hartzell HC. 2016. Anoctamins/TMEM16 proteins: chloride channels flirting with lipids and extracellular vesicles. Annu. Rev. Physiol. 79:119–43
     [Google Scholar]
  164. Wilson ME, Maksaev G, Haswell ES 2013. MscS-like mechanosensitive channels in plants and microbes. Biochemistry 52:345708–22
     [Google Scholar]
  165. Woo SH, 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. Wu J, Goyal R, Grandl J 2016. Localized force application reveals mechanically sensitive domains of Piezo1. Nat. Commun. 7:12939
     [Google Scholar]
  167. Wu Z, Grillet N, Zhao B, Cunningham C, Harkins-Perry S et al. 2017. Mechanosensory hair cells express two molecularly distinct mechanotransduction channels. Nat. Neurosci. 20:124–33
     [Google Scholar]
  168. Wu Z, Müller U. 2016. Molecular identity of the mechanotransduction channel in hair cells: not quiet there yet. J. Neurosci. 36:4310927–34
     [Google Scholar]
  169. Xiong W, Grillet N, Elledge HM, Wagner TFJ, Zhao B et al. 2012. TMHS is an integral component of the mechanotransduction machinery of cochlear hair cells. Cell 151:61283–95
     [Google Scholar]
  170. Xu J, Mathur J, Vessières E, Hammack S, Nonomura K et al. 2018. GPR68 senses flow and is essential for vascular physiology. Cell 173:3762–75.e16
     [Google Scholar]
  171. Yan C, Wang F, Peng Y, Williams CR, Jenkins B et al. 2018. Microtubule acetylation is required for mechanosensation in Drosophila. . Cell Rep 25:41051–65.e6
     [Google Scholar]
  172. 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]
  173. Yang H, Kim A, David T, Palmer D, Jin T et al. 2012. TMEM16F forms a Ca2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 151:1111–22
     [Google Scholar]
  174. Yang YD, Cho H, Koo JY, Tak MH, Cho Y et al. 2008. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:72171210–15
     [Google Scholar]
  175. Yoder N, Gouaux E. 2018. Divalent cation and chloride ion sites of chicken acid sensing ion channel 1a elucidated by x-ray crystallography. PLOS ONE 13:8e0202134
     [Google Scholar]
  176. Yoder N, Yoshioka C, Gouaux E 2018. Gating mechanisms of acid-sensing ion channels. Nature 555:7696397–401
     [Google Scholar]
  177. Yuan F, Yang H, Xue Y, Kong D, Ye R et al. 2014. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. . Nature 514:7522367–71
     [Google Scholar]
  178. Zhang M, Li X, Zheng H, Wen X, Chen S et al. 2018a. Brv1 is required for Drosophila larvae to sense gentle touch. Cell Rep 23:123–31
     [Google Scholar]
  179. Zhang M, Wang D, Kang Y, Wu JX, Yao F et al. 2018b. Structure of the mechanosensitive OSCA channels. Nat. Struct. Mol. Biol. 25:9850–58
     [Google Scholar]
  180. Zhang W, Cheng LE, Kittelmann M, Li J, Petkovic M et al. 2015. Ankyrin repeats convey force to gate the NOMPC mechanotransduction channel. Cell 162:61391–403
     [Google Scholar]
  181. Zhang W, Yan Z, Li B, Jan LY, Jan YN 2014. Identification of motor neurons and a mechanosensitive sensory neuron in the defecation circuitry of Drosophila larvae. eLife 3:e03293
     [Google Scholar]
  182. Zhang WK, Wang D, Duan Y, Loy MMT, Chan HC, Huang P 2010. Mechanosensitive gating of CFTR. Nat. Cell Biol. 12:5507–12
     [Google Scholar]
  183. Zhang YV, Aikin TJ, Li Z, Montell C 2016. The basis of food texture sensation in Drosophila. . Neuron 91:4863–77
     [Google Scholar]
  184. Zhang Z, Chen J. 2016. Atomic structure of the cystic fibrosis transmembrane conductance regulator. Cell 167:61586–97.e9
     [Google Scholar]
  185. Zhao B, Wu Z, Grillet N, Yan L, Xiong W et al. 2014. TMIE is an essential component of the mechanotransduction machinery of cochlear hair cells. Neuron 84:5954–67
     [Google Scholar]
  186. Zhao Q, Wu K, Chi S, Geng J, Xiao B 2017. Heterologous expression of the Piezo1-ASIC1 chimera induces mechanosensitive currents with properties distinct from Piezo1. Neuron 94:2274–77
     [Google Scholar]
  187. Zhao Q, Zhou H, Chi S, Wang Y, Wang J et al. 2018. Structure and mechanogating mechanism of the Piezo1 channel. Nature 554:7693487–92
     [Google Scholar]
  188. Zhou Y, Cao L-H, Sui X-W, Guo X-Q, Luo D-G 2019. Mechanosensory circuits coordinate two opposing motor actions in Drosophila feeding. Sci. Adv. 5:eaaw5141
     [Google Scholar]
/content/journals/10.1146/annurev-neuro-070918-050509
Loading
Mechanosensitive Ion Channels: Structural Features Relevant to Mechanotransduction Mechanisms
Annual Review of Neuroscience 43, 207 (2020); https://doi.org/10.1146/annurev-neuro-070918-050509
/content/journals/10.1146/annurev-neuro-070918-050509
/content/journals/10.1146/annurev-neuro-070918-050509
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error