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Section 3: From inputs to outputs

Mechano-gated channels in C. elegans

ORCID Icon & ORCID Icon
Pages 363-368 | Received 31 Mar 2020, Accepted 30 Sep 2020, Published online: 16 Dec 2020

References

  • Al-Sheikh, U., & Kang, L. (2020). Molecular crux of hair cell mechanotransduction machinery. Neuron, 107(3), 404–406. doi:10.1016/j.neuron.2020.07.007
  • Ardiel, E.L., & Rankin, C.H. (2008). Behavioral plasticity in the C. elegans mechanosensory circuit. Journal of Neurogenetics, 22(3), 239–255. doi:10.1080/01677060802298509
  • Arnadottir, J., & Chalfie, M. (2010). Eukaryotic mechanosensitive channels. Annual Review of Biophysics, 39, 111–137. doi:10.1146/annurev.biophys.37.032807.125836
  • Bai, X., Bouffard, J., Lord, A., Brugman, K., Sternberg, P.W., Cram, E.J., & Golden, A. (2019). Caenorhabditis elegans PIEZO channel coordinates multiple reproductive tissues to govern ovulation. 9, bioRxiv, 847392. doi:10.1101/847392
  • Barr, M.M., DeModena, J., Braun, D., Nguyen, C.Q., Hall, D.H., & Sternberg, P.W. (2001). The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Current Biology : CB, 11(17), 1341–1346. doi:10.1016/S0960-9822(01)00423-7
  • Brown, A.L., Liao, Z., & Goodman, M.B. (2008). MEC-2 and MEC-6 in the Caenorhabditis elegans sensory mechanotransduction complex: Auxiliary subunits that enable channel activity. The Journal of General Physiology, 131(6), 605–616. doi:10.1085/jgp.200709910
  • Chalfie, M. (2009). Neurosensory mechanotransduction. Nature Reviews. Molecular Cell Biology, 10(1), 44–52. doi:10.1038/nrm2595
  • Chalfie, M., & Sulston, J. (1981). Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Developmental Biology, 82(2), 358–370. doi:10.1016/0012-1606(81)90459-0
  • Chatzigeorgiou, M., Bang, S., Hwang, S.W., & Schafer, W.R. (2013). tmc-1 encodes a sodium-sensitive channel required for salt chemosensation in C. elegans. Nature, 494(7435), 95–99. doi:10.1038/nature11845
  • Chatzigeorgiou, M., Grundy, L., Kindt, K.S., Lee, W.H., Driscoll, M., & Schafer, W.R. (2010). Spatial asymmetry in the mechanosensory phenotypes of the C. elegans DEG/ENaC gene mec-10. Journal of Neurophysiology, 104(6), 3334–3344. doi:10.1152/jn.00330.2010
  • Chatzigeorgiou, M., & Schafer, W.R. (2011). Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. Neuron, 70(2), 299–309. doi:10.1016/j.neuron.2011.02.046
  • Christensen, A.P., & Corey, D.P. (2007). TRP channels in mechanosensation: Direct or indirect activation? Nature Reviews. Neuroscience, 8(7), 510–521. doi:10.1038/nrn2149
  • Cunningham, C.L., Qiu, X., Wu, Z., Zhao, B., Peng, G., Kim, Y.-H., … Müller, U. (2020). TMIE defines pore and gating properties of the mechanotransduction channel of mammalian cochlear hair cells. Neuron, 107(1), 126–143.e8. doi:10.1016/j.neuron.2020.03.033
  • Dao, J., Lee, A., Drecksel, D.K., Bittlingmaier, N.M., & Nelson, T.M. (2020). Characterization of TMC-1 in C. elegans sodium chemotaxis and sodium conditioned aversion. BMC Genetics, 21(1), 37. doi:10.1186/s12863-020-00844-4
  • Delmas, P., & Coste, B. (2013). Mechano-gated ion channels in sensory systems. Cell, 155(2), 278–284. doi:10.1016/j.cell.2013.09.026
  • Ding, G., Zou, W., Zhang, H., Xue, Y., Cai, Y., Huang, G., … Kang, L. (2015). In vivo tactile stimulation-evoked responses in Caenorhabditis elegans amphid sheath glia. PLoS One, 10(2), e0117114. doi:10.1371/journal.pone.0117114
  • Douguet, D., & Honore, E. (2019). Mammalian mechanoelectrical transduction: Structure and function of force-gated ion channels. Cell, 179(2), 340–354. doi:10.1016/j.cell.2019.08.049
  • Fechner, S., D’Alessandro, I., Wang, L., Tower, C., Tao, L., & Goodman, M.B. (2020). Functional and pharmacological characterization of C. elegans DEG/ENaC/ASIC channels. Biophysical Journal, 118(3), 114a. doi:10.1016/j.bpj.2019.11.768
  • Geffeney, S.L., Cueva, J.G., Glauser, D.A., Doll, J.C., Lee, T.H.-C., Montoya, M., … Goodman, M.B. (2011). DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron, 71(5), 845–857. doi:10.1016/j.neuron.2011.06.038
  • Goodman, M.B. (2006). Mechanosensation. WormBook, 1–14. doi:10.1895/wormbook.1.62.1
  • Hall, D.H., Gu, G., Garcı́a-Añoveros, J., Gong, L., Chalfie, M., &., & Driscoll, M. (1997). Neuropathology of degenerative cell death in Caenorhabditis elegans. The Journal of Neuroscience, 17(3), 1033–1045. doi:10.1523/JNEUROSCI.17-03-01033.1997
  • Hill, A.S., & Ben-Shahar, Y. (2018). The synaptic action of Degenerin/Epithelial sodium channels. Channels (Austin, Tex.), 12(1), 262–275. doi:10.1080/19336950.2018.1495006
  • Jia, Y., Zhao, Y., Kusakizako, T., Wang, Y., Pan, C., Zhang, Y., … Yan, Z. (2020). TMC1 and TMC2 proteins are pore-forming subunits of mechanosensitive ion channels. Neuron, 105(2), 310–321.e313. doi:10.1016/j.neuron.2019.10.017
  • Jin, P., Jan, L.Y., & Jan, Y.N. (2020). Mechanosensitive ion channels: Structural features relevant to mechanotransduction mechanisms. Annual Review of Neuroscience, 43, 207–229. doi:10.1146/annurev-neuro-070918-050509
  • Kang, L., Gao, J., Schafer, W.R., Xie, Z., & Xu, X.Z. (2010). C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron, 67(3), 381–391. doi:10.1016/j.neuron.2010.06.032
  • Katta, S., Krieg, M., & Goodman, M.B. (2015). Feeling force: Physical and physiological principles enabling sensory mechanotransduction. Annual Review of Cell and Developmental Biology, 31, 347–371. doi:10.1146/annurev-cellbio-100913-013426
  • Kawashima, Y., Kurima, K., Pan, B., Griffith, A.J., & Holt, J.R. (2015). Transmembrane channel-like (TMC) genes are required for auditory and vestibular mechanosensation. Pflugers Archiv : European Journal of Physiology, 467(1), 85–94. doi:10.1007/s00424-014-1582-3
  • Kung, C. (2005). A possible unifying principle for mechanosensation. Nature, 436(7051), 647–654. doi:10.1038/nature03896
  • Lee, C.H., & Chen, C.C. (2018). Roles of ASICs in nociception and proprioception. Advances in Experimental Medicine and Biology, 1099, 37–47. doi:10.1007/978-981-13-1756-9_4
  • Li, W., Feng, Z., Sternberg, P.W., & Xu, X.Z. (2006). A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature, 440(7084), 684–687. doi:10.1038/nature04538
  • Li, W., Kang, L., Piggott, B.J., Feng, Z., & Xu, X.Z. (2011). The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nature Communications, 2, 315. doi:10.1038/ncomms1308
  • Lin, S.H., Sun, W.H., & Chen, C.C. (2015). Genetic exploration of the role of acid-sensing ion channels. Neuropharmacology, 94, 99–118. doi:10.1016/j.neuropharm.2014.12.011
  • Liu, H., Qin, L.W., Li, R., Zhang, C., Al-Sheikh, U., & Wu, Z.X. (2019). Reciprocal modulation of 5-HT and octopamine regulates pumping via feedforward and feedback circuits in C. elegans. Proceedings of the National Academy of Sciences of the United States of America, 116(14), 7107–7112. doi:10.1073/pnas.1819261116
  • Liu, S., Wang, S., Zou, L., Li, J., Song, C., Chen, J., … Xiong, W. (2019). TMC1 is an essential component of a leak channel that modulates tonotopy and excitability of auditory hair cells in mice. eLife, 8. doi:10.7554/eLife.47441
  • Lumpkin, E.A., Marshall, K.L., & Nelson, A.M. (2010). The cell biology of touch. The Journal of Cell Biology, 191(2), 237–248. doi:10.1083/jcb.201006074
  • Marshall, K.L., & Lumpkin, E.A. (2012). The molecular basis of mechanosensory transduction. Advances in Experimental Medicine and Biology, 739, 142–155. doi:10.1007/978-1-4614-1704-0_9
  • Montell, C. (2005). The TRP superfamily of cation channels. Science Signaling, 2005(272), re3. doi:10.1126/stke.2722005re3
  • Nilius, B., Voets, T., & Peters, J. (2005). TRP channels in disease. Science’s STKE : Signal Transduction Knowledge Environment, 2005(295), re8. doi:10.1126/stke.2952005re8
  • O’Hagan, R., Chalfie, M., & Goodman, M.B. (2005). The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nature Neuroscience, 8(1), 43–50. doi:10.1038/nn1362
  • Pan, B., Géléoc, G.S., Asai, Y., Horwitz, G.C., Kurima, K., Ishikawa, K., … Holt, J.R. (2013). TMC1 and TMC2 are components of the mechanotransduction channel in hair cells of the mammalian inner ear. Neuron, 79(3), 504–515. doi:10.1016/j.neuron.2013.06.019
  • Prole, D.L., & Taylor, C.W. (2013). Identification and analysis of putative homologues of mechanosensitive channels in pathogenic protozoa. PLoS One, 8(6), e66068. doi:10.1371/journal.pone.0066068
  • Ranade, S.S., Syeda, R., & Patapoutian, A. (2015). Mechanically activated ion channels. Neuron, 87(6), 1162–1179. doi:10.1016/j.neuron.2015.08.032
  • Rasmussen, T., & Rasmussen, A. (2018). Bacterial mechanosensitive channels. Sub-cellular Biochemistry, 87, 83–116. doi:10.1007/978-981-10-7757-9_4
  • Rhoades, J.L., Nelson, J.C., Nwabudike, I., Yu, S.K., McLachlan, I.G., Madan, G.K., … Flavell, S.W. (2019). ASICs mediate food responses in an enteric serotonergic neuron that controls foraging behaviors. Cell, 176(1–2), 85–97.e14. doi:10.1016/j.cell.2018.11.023
  • Rivard, L., Srinivasan, J., Stone, A., Ochoa, S., Sternberg, P.W., & Loer, C.M. (2010). A comparison of experience-dependent locomotory behaviors and biogenic amine neurons in nematode relatives of Caenorhabditis elegans. BMC Neuroscience, 11, 22. doi:10.1186/1471-2202-11-22
  • Suzuki, H., Kerr, R., Bianchi, L., Frøkjaer-Jensen, C., Slone, D., Xue, J., … Schafer, W.R. (2003). In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron, 39(6), 1005–1017. doi:10.1016/j.neuron.2003.08.015
  • Takeishi, A., Takagaki, N., & Kuhara, A. (2020). Temperature signaling underlying thermotaxis and cold tolerance in Caenorhabditis elegans. J Neurogenet, 1–12. doi:10.1080/01677063.2020.1734001
  • Tang, Y.Q., Lee, S.A., Rahman, M., Vanapalli, S.A., Lu, H., & Schafer, W.R. (2020). Ankyrin is an intracellular tether for TMC mechanotransduction channels. Neuron, 107(4), 759–761. doi:10.1016/j.neuron.2020.03.026
  • Tao, L., Porto, D., Li, Z., Fechner, S., Lee, S.A., Goodman, M.B., … Shen, K. (2019). Parallel processing of two mechanosensory modalities by a single neuron in C. elegans. Developmental Cell, 51(5), 617–631.e3. doi:10.1016/j.devcel.2019.10.008
  • Tobin, D.M., Madsen, D.M., Kahn-Kirby, A., Peckol, E.L., Moulder, G., Barstead, R., … Bargmann, C.I. (2002). Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron, 35(2), 307–318. doi:10.1016/S0896-6273(02)00757-2
  • Venkatachalam, K., Luo, J., & Montell, C. (2014). Evolutionarily conserved, multitasking TRP channels: Lessons from worms and flies. Handbook of Experimental Pharmacology, 223, 937–962. doi:10.1007/978-3-319-05161-1_9
  • Walker, R.G., Willingham, A.T., & Zuker, C.S. (2000). A Drosophila mechanosensory transduction channel. Science (New York, N.Y.), 287(5461), 2229–2234. doi:10.1126/science.287.5461.2229
  • Wang, X., Li, G., Liu, J., Liu, J., & Xu, X.Z. (2016). TMC-1 mediates alkaline sensation in C. elegans through nociceptive neurons. Neuron, 91(1), 146–154. doi:10.1016/j.neuron.2016.05.023
  • Woo, S.-H., Ranade, S., Weyer, A.D., Dubin, A.E., Baba, Y., Qiu, Z., … Patapoutian, A. (2014). Piezo2 is required for Merkel-cell mechanotransduction. Nature, 509(7502), 622–626. doi:10.1038/nature13251
  • Wu, Z., Grillet, N., Zhao, B., Cunningham, C., Harkins-Perry, S., Coste, B., … Mueller, U. (2017). Mechanosensory hair cells express two molecularly distinct mechanotransduction channels. Nature Neuroscience, 20(1), 24–33. doi:10.1038/nn.4449
  • Xiao, R., & Xu, X.Z. (2010). Mechanosensitive channels: In touch with Piezo. Current Biology : CB, 20(21), R936–R938. doi:10.1016/j.cub.2010.09.053
  • Yan, Z., Su, Z., Cheng, X., & Liu, J. (2020). Caenorhabditis elegans body wall muscles sense mechanical signals with an amiloride-sensitive cation channel. Biochemical and Biophysical Research Communications, 527(2), 581–587. doi:10.1016/j.bbrc.2020.04.130
  • Yue, X., Zhao, J., Li, X., Fan, Y., Duan, D., Zhang, X., … Kang, L. (2018). TMC proteins modulate egg laying and membrane excitability through a background leak conductance in C. elegans. Neuron, 97(3), 571–585.e575. doi:10.1016/j.neuron.2017.12.041
  • Zhang, H., Yue, X., Cheng, H., Zhang, X., Cai, Y., Zou, W., … Kang, L. (2018). OSM-9 and an amiloride-sensitive channel, but not PKD-2, are involved in mechanosensation in C. elegans male ray neurons. Scientific Reports, 8(1), 7192. doi:10.1038/s41598-018-25542-1
  • Zhong, M., Komarova, Y., Rehman, J., & Malik, A.B. (2018). Mechanosensing Piezo channels in tissue homeostasis including their role in lungs. Pulmonary Circulation, 8(2), 2045894018767393. doi:10.1177/2045894018767393
  • Zou, W., Cheng, H., Li, S., Yue, X., Xue, Y., Chen, S., & Kang, L. (2017). Polymodal responses in C. elegans phasmid neurons rely on multiple intracellular and intercellular signaling pathways. Scientific Reports, 7, 42295. doi:10.1038/srep42295

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