Advertisement

Mechanosensory Transduction in the Nematode Caenorhabditis elegans

  • Nikos Kourtis
  • Nektarios Tavernarakis
Part of the Mechanosensitivity in Cells and Tissues book series (MECT, volume 1)

abstract

Mechanotransduction, the process of converting a mechanical stimulus into a biological signal, appeared very early in the evolution and underlies a plethora of fundamental biological processes such as osmosensation, touch, hearing, balance and proprioception. Mechanosensory transduction has been studied extensively in simple animal models such as the nematode Caenorhabditis elegans and the fruit fly Drosophila melanogaster. Genetic and physiological studies have revealed that specialized macromolecular complexes, encompassing mechanically gated ion channels, play a critical role in the conversion of mechanical energy into cellular response. Members of two large ion channel families, the degenerin/epithelial sodium channels (DEG/ENaC) and the transient receptor potential ion channels (TRP), have emerged as candidate mechanosensitive channels. Several auxiliary proteins associate with the core mechanosensitive channels to form the mechanotransducing apparatus in specialized mechanosensory cells. C. elegans displays a variety of mechanosensory behaviours. In this chapter, we survey the mechanisms of mechanosensory transduction in C. elegans. The exceptional amenability of this simple metazoan to genetic and molecular manipulations has facilitated the dissection of the mechanotransduction process to unprecedented detail.

Keywords

Degenerin Ion channels Proprioception Touch receptor neurons TRP channels 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alvarez de la Rosa, D., C. M. Canessa, G. K. Fyfe, and P. Zhang. 2000. Structure and regulation of amiloride-sensitive sodium channels. Annu Rev Physiol 62:573–94.Google Scholar
  2. Ashmore, J. 1998. Mechanosensation: swimming round in circles. Curr Biol 8:425–7.Google Scholar
  3. Avery, L. 1993. The genetics of feeding in Caenorhabditis elegans. Genetics 133:897–917.PubMedGoogle Scholar
  4. Bargmann, C. I., and J. M. Kaplan. 1998. Signal transduction in the Caenorhabditis elegans nervous system. Annu Rev Neurosci 21:279–308.PubMedGoogle Scholar
  5. Bargmann, C. I., J. H. Thomas, and H. R. Horvitz. 1990. Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol 55:529–38.PubMedGoogle Scholar
  6. Barnes, T. M., Y. Jin, H. R. Horvitz, G. Ruvkun, and S. Hekimi. 1996. The Caenorhabditis elegans behavioral gene unc-24 encodes a novel bipartite protein similar to both erythrocyte band 7.2 (stomatin) and nonspecific lipid transfer protein. J Neurochem 67:46–57.PubMedGoogle Scholar
  7. Baumeister, R., and L. Ge. 2002. The worm in us - Caenorhabditis elegans as a model of human disease. Trends Biotechnol 20:147–8.PubMedGoogle Scholar
  8. Block, I., N. Freiberger, O. Gavrilova, and R. Hemmersbach. 1999. Putative graviperception mechanisms of protists. Adv Space Res 24:877–82.PubMedGoogle Scholar
  9. Blount, P., and P. C. Moe. 1999. Bacterial mechanosensitive channels: integrating physiology, structure and function. Trends Microbiol 7:420–4.PubMedGoogle Scholar
  10. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.PubMedGoogle Scholar
  11. Caterina, M. J., T. A. Rosen, M. Tominaga, A. J. Brake, and D. Julius. 1999. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–41.PubMedGoogle Scholar
  12. Caterina, M. J., M. A. Schumacher, M. Tominaga, T. A. Rosen, J. D. Levine, and D. Julius. 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–24.PubMedGoogle Scholar
  13. Chalfie, M. 1995. The differentiation and function of the touch receptor neurons of Caenorhabditis elegans. Prog Brain Res 105:179–82.PubMedGoogle Scholar
  14. Chalfie, M. 1997. A molecular model for mechanosensation in Caenorhabditis elegans. Biol Bull 192:125.PubMedGoogle Scholar
  15. Chalfie, M. 1993. Touch receptor development and function in Caenorhabditis elegans. J Neurobiol 24:1433–41.PubMedGoogle Scholar
  16. Chalfie, M., and M. Au. 1989. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243:1027–33.PubMedGoogle Scholar
  17. Chalfie, M., E. Dean, E. Reilly, K. Buck, and J. N. Thomson. 1986. Mutations affecting microtubule structure in Caenorhabditis elegans. J Cell Sci Suppl 5:257–71.PubMedGoogle Scholar
  18. Chalfie, M., M. Driscoll, and M. Huang. 1993. Degenerin similarities. Nature 361:504.PubMedGoogle Scholar
  19. Chalfie, M., and J. Sulston. 1981. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82:358–70.PubMedGoogle Scholar
  20. Chalfie, M., J. E. Sulston, J. G. White, E. Southgate, J. N. Thomson, and S. Brenner. 1985. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5:956–64.PubMedGoogle Scholar
  21. Chalfie, M., and J. N. Thomson. 1979. Organization of neuronal microtubules in the nematode Caenorhabditis elegans. J Cell Biol 82:278–89.Google Scholar
  22. Chalfie, M., and J. N. Thomson. 1982. Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans. J Cell Biol 93:15–23.PubMedGoogle Scholar
  23. Chalfie, M., J. N. Thomson, and J. E. Sulston. 1983. Induction of neuronal branching in Caenorhabditis elegans. Science 221:61–3.PubMedGoogle Scholar
  24. Chalfie, M., and E. Wolinsky. 1990. The identification and suppression of inherited neurodegeneration in Caenorhabditis elegans. Nature 345:410–6.PubMedGoogle Scholar
  25. Chelur, D. S., G. G. Ernstrom, M. B. Goodman, C. A. Yao, A. F. Chen, R. O’Hagan, and M. Chalfie. 2002. The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel. Nature 420:669–73.PubMedGoogle Scholar
  26. Chiba, C. M., and C. H. Rankin. 1990. A developmental analysis of spontaneous and reflexive reversals in the nematode Caenorhabditis elegans. J Neurobiol 21:543–54.Google Scholar
  27. Colbert, H. A., T. L. Smith, and C. I. Bargmann. 1997. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17:8259–69.PubMedGoogle Scholar
  28. Corey, D. P. 2003. New TRP channels in hearing and mechanosensation. Neuron 39:585–8.Google Scholar
  29. Corey, D. P., J. Garcia-Anoveros, J. R. Holt, K. Y. Kwan, S. Y. Lin, M. A. Vollrath, A. Amalfitano, E. L. Cheung, B. H. Derfler, A. Duggan, G. S. Geleoc, P. A. Gray, M. P. Hoffman, H. L. Rehm, Tamasauskas, D., and D. S. Zhang. 2004. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723–30.PubMedGoogle Scholar
  30. Coulson, A., R. Waterston, J. Kiff, J. Sulston, and Y. Kohara. 1988. Genome linking with yeast artificial chromosomes. Nature 335:184–6.PubMedGoogle Scholar
  31. Delaunay, J., G. Stewart, and A. Iolascon. 1999. Hereditary dehydrated and overhydrated stomatocytosis: recent advances. Curr Opin Hematol 6:110–4.PubMedGoogle Scholar
  32. Driscoll, M. 1996. Cell death in C. elegans: molecular insights into mechanisms conserved between nematodes and mammals. Brain Pathol 6:411–25.PubMedGoogle Scholar
  33. Driscoll, M., and M. Chalfie. 1991. The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 349: 588–93.PubMedGoogle Scholar
  34. Driscoll, M., and J. M. Kaplan. 1996. Mechanotransduction, p. 645–677. In D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Pries (ed.), The Nematode C. elegans, II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  35. Driscoll, M., and N. Tavernarakis. 1997. Molecules that mediate touch transduction in the nematode Caenorhabditis elegans. Gravit Space Biol Bull 10:33–42.PubMedGoogle Scholar
  36. Drummond, H. A., M. P. Price, M. J. Welsh, and F. M. Abboud. 1998. A molecular component of the arterial baroreceptor mechanotransducer. Neuron 21:1435–41.PubMedGoogle Scholar
  37. Drummond, H. A., M. J. Welsh, and F. M. Abboud. 2001. ENaC subunits are molecular components of the arterial baroreceptor complex. Ann N Y Acad Sci 940:42–7.PubMedGoogle Scholar
  38. Du, H., and M. Chalfie. 2001. Genes regulating touch cell development in Caenorhabditis elegans. Genetics 158:197–207.PubMedGoogle Scholar
  39. Du, H., G. Gu, C. M. William, and M. Chalfie. 1996. Extracellular proteins needed for C. elegans mechanosensation. Neuron 16:183–94.PubMedGoogle Scholar
  40. Duggan, A., C. Ma, and M. Chalfie. 1998. Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 125:4107–19.PubMedGoogle Scholar
  41. Eberl, D. F. 1999. Feeling the vibes: chordotonal mechanisms in insect hearing. Curr Opin Neurobiol 9:389–93.PubMedGoogle Scholar
  42. Emtage, L., G. Gu, E. Hartwieg, and M. Chalfie. 2004. Extracellular proteins organize the mechanosensory channel complex in C. elegans touch receptor neurons. Neuron 44:795–807.PubMedGoogle Scholar
  43. Fettiplace, R., and P. A. Fuchs. 1999. Mechanisms of hair cell tuning. Annu Rev Physiol 61:809–34.PubMedGoogle Scholar
  44. Finney, M., and G. Ruvkun. 1990. The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63:895–905.Google Scholar
  45. Finney, M., G. Ruvkun, and H. R. Horvitz. 1988. The C. elegans cell lineage and differentiation gene unc-86 encodes a protein with a homeodomain and extended similarity to transcription factors. Cell 55:757–69.PubMedGoogle Scholar
  46. Fire, A., S. Xu, M. K. Montgomery, S. A. Kostas, S. E. Driver, and C. C. Mello. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–11.PubMedGoogle Scholar
  47. Francis, R., and R. H. Waterston. 1991. Muscle cell attachment in Caenorhabditis elegans. J Cell Biol 114:465–79.PubMedGoogle Scholar
  48. French, A. S. 1992. Mechanotransduction. Annu Rev Physiol 54:135–52.PubMedGoogle Scholar
  49. Fukushige, T., Z. K. Siddiqui, M. Chou, J. G. Culotti, C. B. Gogonea, S. S. Siddiqui, and M. Hamelin. 1999. MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J Cell Sci 112:395–403.PubMedGoogle Scholar
  50. Garcia-Anoveros, J., and D. P. Corey. 1997. The molecules of mechanosensation. Annu Rev Neurosci 20:567–94.PubMedGoogle Scholar
  51. Garcia-Anoveros, J., and D. P. Corey. 1996. Touch at the molecular level. Mechanosensation. Curr Biol 6:541–3.PubMedGoogle Scholar
  52. Garcia-Anoveros, J., J. A. Garcia, J. D. Liu, and D. P. Corey. 1998. The nematode degenerin UNC-105 forms ion channels that are activated by degeneration- or hypercontraction-causing mutations. Neuron 20:1231–41.PubMedGoogle Scholar
  53. Gebauer, M., D. Watzke, and H. Machemer. 1999. The gravikinetic response of Paramecium is based on orientation-dependent mechanotransduction. Naturwissenschaften 86:352–6.PubMedGoogle Scholar
  54. Gillespie, P. G. 1995. Molecular machinery of auditory and vestibular transduction. Curr Opin Neurobiol 5:449–55.PubMedGoogle Scholar
  55. Gillespie, P. G., and R. G. Walker. 2001. Molecular basis of mechanosensory transduction. Nature 413:194–202.PubMedGoogle Scholar
  56. Golden, J. W., and D. L. Riddle. 1984. The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev Biol 102:368–78.PubMedGoogle Scholar
  57. Gong, Z., W. Son, Y. D. Chung, J. Kim, D. W. Shin, C. A. McClung, Y. Lee, H. W. Lee, D. J. Chang, B. K. Kaang, H. Cho, U. Oh, J. Hirsh, M. J. Kernan, and C. Kim. 2004. Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 24:9059–66.PubMedGoogle Scholar
  58. Goodman, M. B., G. G. Ernstrom, D. S. Chelur, R. O’Hagan, C. A. Yao, and M. Chalfie. 2002. MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature 415:1039–42.PubMedGoogle Scholar
  59. Gu, G., G. Caldwell, and M. Chalfie. 1996. Genetic interactions affecting touch sensitivity in Caenorhabditis elegans. Proc Natl Acad Sci U S A 93:6577 - 82.PubMedGoogle Scholar
  60. Hackney, C. M., and D. N. Furness. 1995. Mechanotransduction in vertebrate hair cells: structure and function of the stereociliary bundle. Am J Physiol 268:C1–13.PubMedGoogle Scholar
  61. Hall, D. H., G. Gu, J. Garcia-Anoveros, L. Gong, M. Chalfie, and M. Driscoll. 1997. Neuropathology of degenerative cell death in Caenorhabditis elegans. J Neurosci 17:1033–45.Google Scholar
  62. Hamelin, M., I. M. Scott, J. C. Way, and J. G. Culotti. 1992. The mec-7 beta-tubulin gene of Caenorhabditis elegans is expressed primarily in the touch receptor neurons. Embo J 11:2885–93.PubMedGoogle Scholar
  63. Hamill, O. P., J. W. Lane, and D. W. McBride, Jr. 1992. Amiloride: a molecular probe for mechanosensitive channels. Trends Pharmacol Sci 13:373–6.PubMedGoogle Scholar
  64. Hamill, O. P., and B. Martinac. 2001. Molecular basis of mechanotransduction in living cells. Physiol Rev 81:685–740.PubMedGoogle Scholar
  65. Hamill, O. P., and D. W. McBride, Jr. 1996. The pharmacology of mechanogated membrane ion channels. Pharmacol Rev 48:231–52.PubMedGoogle Scholar
  66. Harbinder, S., N. Tavernarakis, L. A. Herndon, M. Kinnell, S. Q. Xu, A. Fire, and M. Driscoll. 1997. Genetically targeted cell disruption in Caenorhabditis elegans. Proc Natl Acad Sci U S A 94:13128–33.PubMedGoogle Scholar
  67. Hart, A. C., J. Kass, J. E. Shapiro, and J. M. Kaplan. 1999. Distinct signaling pathways mediate touch and osmosensory responses in a polymodal sensory neuron. J Neurosci 19:1952–8.PubMedGoogle Scholar
  68. Hart, A. C., S. Sims, and J. M. Kaplan. 1995. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378:82–5.PubMedGoogle Scholar
  69. Harteneck, C., T. D. Plant, and G. Schultz. 2000. From worm to man: three subfamilies of TRP channels. Trends Neurosci 23:159–66.PubMedGoogle Scholar
  70. Hemmersbach, R., B. Bromeis, I. Block, R. Braucker, M. Krause, N. Freiberger, C. Stieber, and M. Wilczek. 2001. Paramecium–a model system for studying cellular graviperception. Adv Space Res 27:893–8.PubMedGoogle Scholar
  71. Herman, R. K. 1996. Touch sensation in Caenorhabditis elegans. Bioessays 18:199–206.PubMedGoogle Scholar
  72. Hilliard, M. A., A. J. Apicella, R. Kerr, H. Suzuki, P. Bazzicalupo, and W. R. Schafer. 2005. In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. Embo J 24:63–72.PubMedGoogle Scholar
  73. Hoger, U., P. H. Torkkeli, E. A. Seyfarth, and A. S. French. 1997. Ionic selectivity of mechanically activated channels in spider mechanoreceptor neurons. J Neurophysiol 78:2079–85.PubMedGoogle Scholar
  74. Hresko, M. C., B. D. Williams, and R. H. Waterston. 1994. Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans. J Cell Biol 124:491–506.PubMedGoogle Scholar
  75. Huang, M., and M. Chalfie. 1994. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature 367:467–70.PubMedGoogle Scholar
  76. Huang, M., G. Gu, E. L. Ferguson, and M. Chalfie. 1995. A stomatin-like protein necessary for mechanosensation in C. elegans. Nature 378:292–5.PubMedGoogle Scholar
  77. Hudspeth, A. J. 1989. How the ear’s works work. Nature 341:397–404.PubMedGoogle Scholar
  78. Hudspeth, A. J., Y. Choe, A. D. Mehta, and P. Martin. 2000. Putting ion channels to work: mechanoelectrical transduction, adaptation, and amplification by hair cells. Proc Natl Acad Sci U S A 97:11765–72.PubMedGoogle Scholar
  79. Ingber, D. E. 1997. Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 59:575–99.PubMedGoogle Scholar
  80. Jaramillo, F., and A. J. Hudspeth. 1991. Localization of the hair cell’s transduction channels at the hair bundle’s top by iontophoretic application of a channel blocker. Neuron 7:409–20.PubMedGoogle Scholar
  81. Jospin, M., M. C. Mariol, L. Segalat, and B. Allard. 2004. Patch clamp study of the UNC-105 degenerin and its interaction with the LET-2 collagen in Caenorhabditis elegans muscle. J Physiol 557:379–88.PubMedGoogle Scholar
  82. Kahn-Kirby, A. H., and C. I. Bargmann. 2006. TRP channels in C. elegans. Annu Rev Physiol 68:719–36.PubMedGoogle Scholar
  83. Kahn-Kirby, A. H., J. L. Dantzker, A. J. Apicella, W. R. Schafer, J. Browse, C. I. Bargmann, and J. L. Watts. 2004. Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell 119:889–900.PubMedGoogle Scholar
  84. Kaplan, J. M., and H. R. Horvitz. 1993. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc Natl Acad Sci U S A 90:2227–31.PubMedGoogle Scholar
  85. Kellenberger, S., and L. Schild. 2002. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 82:735–67.PubMedGoogle Scholar
  86. Kitamura, K. I., S. Amano, and R. Hosono. 2001. Contribution of neurons to habituation to mechanical stimulation in Caenorhabditis elegans. J Neurobiol 46:29–40.PubMedGoogle Scholar
  87. Kloda, A., and B. Martinac. 2001. Molecular identification of a mechanosensitive channel in archaea. Biophys J 80:229–40.PubMedGoogle Scholar
  88. Ko, K. S., and C. A. McCulloch. 2001. Intercellular mechanotransduction: cellular circuits that coordinate tissue responses to mechanical loading. Biochem Biophys Res Commun 285:1077–83.PubMedGoogle Scholar
  89. Koch, A. L. 1994. Development and diversification of the Last Universal Ancestor. J Theor Biol 168:269–80.PubMedGoogle Scholar
  90. Koch, R., H. G. van Luenen, M. van der Horst, K. L. Thijssen, and R. H. Plasterk. 2000. Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Res 10:1690–6.PubMedGoogle Scholar
  91. Koprowski, P., and A. Kubalski. 2001. Bacterial ion channels and their eukaryotic homologues. their eukaryotic homologues. Bioessays 23:1148–58. Bioessays 23:1148–58.Google Scholar
  92. Lane, J. W., D. W. McBride, Jr., and O. P. Hamill. 1991. Amiloride block of the mechanosensitive cation channel in Xenopus oocytes. J Physiol 441:347–66.PubMedGoogle Scholar
  93. Lee, R. T., and H. Huang. 2000. Mechanotransduction and arterial smooth muscle cells: new insight into hypertension and atherosclerosis. Ann Med 32:233–5.Google Scholar
  94. Li, W., Z. Feng, P. W. Sternberg, and X. Z. Xu. 2006. A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:684–7.PubMedGoogle Scholar
  95. Liedtke, W., D. M. Tobin, C. I. Bargmann, and J. M. Friedman. 2003. Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc Natl Acad Sci U S A 100 Suppl 2:14531–6.Google Scholar
  96. Liu, D. W., and J. H. Thomas. 1994. Regulation of a periodic motor program in C. elegans. J Neurosci 14:1953–62.PubMedGoogle Scholar
  97. Liu, J., B. Schrank, and R. H. Waterston. 1996. Interaction between a putative mechanosensory membrane channel and a collagen. Science 273:361–4.PubMedGoogle Scholar
  98. Liu, K. S., and P. W. Sternberg. 1995. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14:79–89.PubMedGoogle Scholar
  99. Lynch, T. M., P. M. Lintilhac, and D. Domozych. 1998. Mechanotransduction molecules in the plant gravisensory response: amyloplast/statolith membranes contain a beta 1 integrin-like protein. Protoplasma 201:92–100.PubMedGoogle Scholar
  100. Mah, K. B., and C. H. Rankin. 1992. An analysis of behavioral plasticity in male Caenorhabditis elegans. Behav Neural Biol 58:211–21.PubMedGoogle Scholar
  101. Marino, M. J., T. G. Sherman, and D. C. Wood. 2001. Partial cloning of putative G-proteins modulating mechanotransduction in the ciliate stentor. J Eukaryot Microbiol 48:527–36.PubMedGoogle Scholar
  102. Martinac, B. 2001. Mechanosensitive channels in prokaryotes. Cell Physiol Biochem 11:61–76.PubMedGoogle Scholar
  103. Mello, C., and A. Fire. 1995. DNA transformation. Methods Cell Biol 48:451–82.PubMedGoogle Scholar
  104. Minke, B., and B. Cook. 2002. TRP channel proteins and signal transduction. Physiol Rev 82: 429–72.PubMedGoogle Scholar
  105. Moerman, D. G., H. Hutter, G. P. Mullen, and R. Schnabel. 1996. Cell autonomous expression of perlecan and plasticity of cell shape in embryonic muscle of Caenorhabditis elegans. Dev Biol 173:228–42.PubMedGoogle Scholar
  106. Montell, C. 2001. Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Sci STKE 2001.Google Scholar
  107. Montell, C. 2005. The TRP superfamily of cation channels. Sci STKE 2005.Google Scholar
  108. Nauli, S. M., F. J. Alenghat, Y. Luo, E. Williams, P. Vassilev, X. Li, A. E. Elia, W. Lu, E. M. Brown, S. J. Quinn, D. E. Ingber, and J. Zhou. 2003. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129–37.PubMedGoogle Scholar
  109. Norris, V., M. S. Madsen, and P. Freestone. 1996. Elements of a unifying theory of biology. Acta Biotheor 44:209–18.PubMedGoogle Scholar
  110. O’Hagan, R., and M. Chalfie. 2006. Mechanosensation in Caenorhabditis elegans. Int Rev Neurobiol 69:169–203.PubMedGoogle Scholar
  111. O’Hagan, R., M. Chalfie, and M. B. Goodman. 2005. The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat Neurosci 8:43–50.PubMedGoogle Scholar
  112. Park, E. C., and H. R. Horvitz. 1986. C. elegans unc-105 mutations affect muscle and are suppressed by other mutations that affect muscle. Genetics 113:853–67.PubMedGoogle Scholar
  113. Park, E. C., and H. R. Horvitz. 1986. Mutations with dominant effects on the behavior and morphology of the nematode Caenorhabditis elegans. Genetics 113:821–52.PubMedGoogle Scholar
  114. Peier, A. M., A. J. Reeve, D. A. Andersson, A. Moqrich, T. J. Earley, A. C. Hergarden, G. M. Story, S. Colley, J. B. Hogenesch, P. McIntyre, S. Bevan, and A. Patapoutian. 2002. A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046–9.PubMedGoogle Scholar
  115. Perkins, L. A., E. M. Hedgecock, J. N. Thomson, and J. G. Culotti. 1986. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117:456–87.PubMedGoogle Scholar
  116. Pickard, B. G., and J. P. Ding. 1993. The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control centre? Aust J Plant Physiol 20:439–59.PubMedGoogle Scholar
  117. Pickles, J. O., and D. P. Corey. 1992. Mechanoelectrical transduction by hair cells. Trends Neurosci 15:254–9.PubMedGoogle Scholar
  118. Pickles, J. O., G. W. Rouse, and M. von Perger. 1991. Morphological correlates of mechanotransduction in acousticolateral hair cells. Scanning Microsc 5:1115–24.PubMedGoogle Scholar
  119. Price, M. P., G. R. Lewin, S. L. McIlwrath, C. Cheng, J. Xie, P. A. Heppenstall, C. L. Stucky, A. G. Mannsfeldt, T. J. Brennan, H. A. Drummond, J. Qiao, C. J. Benson, D. E. Tarr, R. F. Hrstka, B. Yang, R. A. Williamson, and M. J. Welsh. 2000. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407:1007–11.PubMedGoogle Scholar
  120. Price, M. P., P. M. Snyder, and M. J. Welsh. 1996. Cloning and expression of a novel human brain Na+ channel. J Biol Chem 271:7879–82.PubMedGoogle Scholar
  121. Rankin, C. H. 1991. Interactions between two antagonistic reflexes in the nematode Caenorhabditis elegans. J Comp Physiol [A] 169:59–67.Google Scholar
  122. Rankin, C. H., T. Gannon, and S. R. Wicks. 2000. Developmental analysis of habituation in the Nematode C. elegans. Dev Psychobiol 36:261–70.PubMedGoogle Scholar
  123. Roayaie, K., J. G. Crump, A. Sagasti, and C. I. Bargmann. 1998. The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20:55–67.PubMedGoogle Scholar
  124. Rossier, B. C., C. M. Canessa, L. Schild, and J. D. Horisberger. 1994. Epithelial sodium channels. Curr Opin Nephrol Hypertens 3:487–96.PubMedGoogle Scholar
  125. Rupp, F., W. Hoch, J. T. Campanelli, T. Kreiner, and R. H. Scheller. 1992. Agrin and the organization of the neuromuscular junction. Curr Opin Neurobiol 2:88–93.Google Scholar
  126. Rupp, F., T. Ozcelik, M. Linial, K. Peterson, U. Francke, and R. Scheller. 1992. Structure and chromosomal localization of the mammalian agrin gene. J Neurosci 12:3535–44.PubMedGoogle Scholar
  127. Rupp, F., D. G. Payan, C. Magill-Solc, D. M. Cowan, and R. H. Scheller. 1991. Structure and expression of a rat agrin. Neuron 6:811–23.PubMedGoogle Scholar
  128. Sackin, H. 1995. Mechanosensitive channels. Annu Rev Physiol 57:333–53.PubMedGoogle Scholar
  129. Sadoshima, J., T. Takahashi, L. Jahn, and S. Izumo. 1992. Roles of mechano-sensitive ion channels, cytoskeleton, and contractile activity in stretch-induced immediate-early gene expression and hypertrophy of cardiac myocytes. Proc Natl Acad Sci USA 89:9905–9.PubMedGoogle Scholar
  130. Savage, C., M. Hamelin, J. G. Culotti, A. Coulson, D. G. Albertson, and M. Chalfie. 1989. mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 3:870–81.PubMedGoogle Scholar
  131. Savage, C., Y. Xue, S. Mitani, D. Hall, R. Zakhary, and M. Chalfie. 1994. Mutations in the Caenorhabditis elegans beta-tubulin gene mec-7: effects on microtubule assembly and stability and on tubulin autoregulation. J Cell Sci 107:2165–75.PubMedGoogle Scholar
  132. Sawin, E. R., R. Ranganathan, and H. R. Horvitz. 2000. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26:619–31.PubMedGoogle Scholar
  133. Sedensky, M. M., J. M. Siefker, and P. G. Morgan. 2001. Model organisms: new insights into ion channel and transporter function. Stomatin homologues interact in Caenorhabditis elegans. Am J Physiol Cell Physiol 280:1340–8.Google Scholar
  134. Shreffler, W., T. Magardino, K. Shekdar, and E. Wolinsky. 1995. The unc-8 and sup-40 genes regulate ion channel function in Caenorhabditis elegans motorneurons. Genetics 139:1261–72.PubMedGoogle Scholar
  135. Sidi, S., R. W. Friedrich, and T. Nicolson. 2003. NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–9.PubMedGoogle Scholar
  136. Smotherman, M. S., and P. M. Narins. 2000. Hair cells, hearing and hopping: a field guide to hair cell physiology in the frog. J Exp Biol 203:2237–46.PubMedGoogle Scholar
  137. Snyers, L., E. Umlauf, and R. Prohaska. 1998. Oligomeric nature of the integral membrane protein stomatin. J Biol Chem 273:17221–6.PubMedGoogle Scholar
  138. Stewart, G. W. 1997. Stomatin. Int J Biochem Cell Biol 29:271–4.PubMedGoogle Scholar
  139. Stewart, G. W., A. C. Argent, and B. C. Dash. 1993. Stomatin: a putative cation transport regulator in the red cell membrane. Biochim Biophys Acta 1225:15–25.PubMedGoogle Scholar
  140. Sulston, J. E., D. G. Albertson, and J. N. Thomson. 1980. The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev Biol 78:542–76.PubMedGoogle Scholar
  141. Sulston, J. E., and H. R. Horvitz. 1977. Post embriyonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 56:110–156.PubMedGoogle Scholar
  142. Suzuki, H., R. Kerr, L. Bianchi, C. Frokjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer. 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 39:1005–17.PubMedGoogle Scholar
  143. Syntichaki, P., and N. Tavernarakis. 2004. Genetic models of mechanotransduction: the nematode Caenorhabditis elegans. Physiol Rev 84:1097–153.PubMedGoogle Scholar
  144. Tavernarakis, N., and M. Driscoll. 2001. Degenerins. At the core of the metazoan mechanotransducer? Ann N Y Acad Sci 940:28–41.PubMedGoogle Scholar
  145. Tavernarakis, N., and M. Driscoll. 2001. Mechanotransduction in Caenorhabditis elegans: the role of DEG/ENaC ion channels. Cell Biochem Biophys 35:1–18.PubMedGoogle Scholar
  146. Tavernarakis, N., and M. Driscoll. 1997. Molecular modeling of mechanotransduction in the nematode Caenorhabditis elegans. Annu Rev Physiol 59:659–89.PubMedGoogle Scholar
  147. Tavernarakis, N., M. Driscoll, and N. C. Kyrpides. 1999. The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends Biochem Sci 24:425–7.PubMedGoogle Scholar
  148. Tavernarakis, N., W. Shreffler, S. Wang, and M. Driscoll. 1997. unc-8, a DEG/ENaC family member, encodes a subunit of a candidate mechanically gated channel that modulates C. elegans locomotion. Neuron 18:107–19.PubMedGoogle Scholar
  149. Tavernarakis, N., S. L. Wang, M. Dorovkov, A. Ryazanov, and M. Driscoll. 2000. Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nat Genet 24:180–3.PubMedGoogle Scholar
  150. Tavi, P., M. Laine, M. Weckstrom, and H. Ruskoaho. 2001. Cardiac mechanotransduction: from sensing to disease and treatment. Trends Pharmacol Sci 22:254–60.PubMedGoogle Scholar
  151. Thomas, J. H., M. J. Stern, and H. R. Horvitz. 1990. Cell interactions coordinate the development of the C. elegans egg-laying system. Cell 62:1041–52.PubMedGoogle Scholar
  152. Tobin, D., D. Madsen, A. Kahn-Kirby, E. Peckol, G. Moulder, R. Barstead, A. Maricq, and C. Bargmann. 2002. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:307–18.PubMedGoogle Scholar
  153. Tracey, W. D., Jr., R. I. Wilson, G. Laurent, and S. Benzer. 2003. painless, a Drosophila gene essential for nociception. Cell 113:261–73.PubMedGoogle Scholar
  154. Troemel, E. R., J. H. Chou, N. D. Dwyer, H. A. Colbert, and C. I. Bargmann. 1995. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83: 207–18.PubMedGoogle Scholar
  155. Voglis and Tavernarakis. 2005. Transduction in the nematode Caenorhabditis elegans. In: Mechanosensitivity in Cells and Tissues. Ed. Kamkin, Andre and Kiseleva, Irina. Academia Publishing House Ltd, Moscow, p. 23–56.Google Scholar
  156. Voilley, N., A. Galibert, F. Bassilana, S. Renard, E. Lingueglia, S. Coscoy, G. Champigny, P. Hofman, M. Lazdunski, and P. Barbry. 1997. The amiloride-sensitive Na+ channel: from primary structure to function. Comp Biochem Physiol A Physiol 118:193–200.PubMedGoogle Scholar
  157. Waldmann, R., G. Champigny, N. Voilley, I. Lauritzen, and M. Lazdunski. 1996. The mammalian degenerin MDEG, an amiloride-sensitive cation channel activated by mutations causing neurodegeneration in Caenorhabditis elegans. J Biol Chem 271:10433–6.PubMedGoogle Scholar
  158. Waldmann, R., and M. Lazdunski. 1998. H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol 8:418–24.PubMedGoogle Scholar
  159. Walker, R. G., A. T. Willingham, and C. S. Zuker. 2000. A Drosophila mechanosensory transduction channel. Science 287:2229–34.PubMedGoogle Scholar
  160. Ward, S., N. Thomson, J. G. White, and S. Brenner. 1975. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160:313–37.PubMedGoogle Scholar
  161. Waterston, R., and J. Sulston. 1995. The genome of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 92:10836–10840.PubMedGoogle Scholar
  162. Waterston, R. H., J. N. Thomson, and S. Brenner. 1980. Mutants with altered muscle structure of Caenorhabditis elegans. Dev Biol 77:271–302.PubMedGoogle Scholar
  163. Way, J. C., and M. Chalfie. 1989. The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev 3:1823–33.PubMedGoogle Scholar
  164. Way, J. C., and M. Chalfie. 1988. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54:5–16.PubMedGoogle Scholar
  165. Weinbaum, S., P. Guo, and L. You. 2001. A new view of mechanotransduction and strain amplification in cells with microvilli and cell processes. Biorheology 38:119–42.PubMedGoogle Scholar
  166. Welsh, M. J., M. P. Price, and J. Xie. 2002. Biochemical basis of touch perception: mechanosensory function of degenerin/epithelial Na+ channels. J Biol Chem 277:2369–72.PubMedGoogle Scholar
  167. White, J. G., E. Southgate, J. N. Thomson, and S. Brenner. 1986. The structure of the nervous system of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1–340.Google Scholar
  168. White, J. G., E. Southgate, J. N. Thomson, and S. Brenner. 1976. The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275:327–48.PubMedGoogle Scholar
  169. Wicks, S. R., and C. H. Rankin. 1997. Effects of tap withdrawal response habituation on other withdrawal behaviors: the localization of habituation in the nematode Caenorhabditis elegans. Behav Neurosci 111:342–53.PubMedGoogle Scholar
  170. Wicks, S. R., and C. H. Rankin. 1995. Integration of mechanosensory stimuli in Caenorhabditis elegans. J Neurosci 15:2434–44.PubMedGoogle Scholar
  171. Wicks, S. R., R. T. Yeh, W. R. Gish, R. H. Waterston, and R. H. Plasterk. 2001. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28:160–4.Google Scholar
  172. Williams, B. D., and R. H. Waterston. 1994. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124:475–90.PubMedGoogle Scholar
  173. Wolinsky, E., and J. Way. 1990. The behavioral genetics of Caenorhabditis elegans. Behav Genet 20:169–89.PubMedGoogle Scholar
  174. Xue, D., M. Finney, G. Ruvkun, and M. Chalfie. 1992. Regulation of the mec-3 gene by the C.elegans homeoproteins UNC-86 and MEC-3. Embo J 11:4969–79.PubMedGoogle Scholar
  175. Zhang, S., J. Arnadottir, C. Keller, G. A. Caldwell, C. A. Yao, and M. Chalfie. 2004. MEC-2 is recruited to the putative mechanosensory complex in C. elegans touch receptor neurons through its stomatin-like domain. Curr Biol 14:1888–96.PubMedGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Nikos Kourtis
  • Nektarios Tavernarakis

There are no affiliations available

Personalised recommendations