The neurotoxic MEC-4(d) DEG/ENaC sodium channel conducts calcium: Implications for necrosis initiation

Nature Neuroscience

Volumn 7, Issue 12, 2004, Pages 1337-1344

  Bianchi, Laura ^a   Gerstbrein, Beate ^a   Frøkjær Jensen, Christian ^b   Royal, Dewey C ^a   Mukherjee, Gargi ^a   Royal, Mary Anne ^a   Xue, Jian ^a   Schafer, William R ^b   Driscoll, Monica ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALPAIN; SODIUM CHANNEL; SODIUM ION; VOLTAGE GATED CALCIUM CHANNEL; AMILORIDE; CAENORHABDITIS ELEGANS PROTEIN; CALCIUM; CALCIUM CHANNEL; DEGENERIN PROTEIN, C ELEGANS; EPITHELIAL SODIUM CHANNEL; MEC 4 PROTEIN, C ELEGANS; MEC-4 PROTEIN, C ELEGANS; MEMBRANE PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CYTOPLASM; ENDOPLASMIC RETICULUM; ISCHEMIA; MEMBRANE DEPOLARIZATION; MOLECULAR MODEL; NECROSIS; NERVE CELL; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; OOCYTE; PRIORITY JOURNAL; XENOPUS; ANIMAL; BIOSYNTHESIS; CELL CULTURE; COMPARATIVE STUDY; DOSE RESPONSE; GENETICS; METABOLISM; PHYSIOLOGY; XENOPUS LAEVIS;

AMILORIDE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; CALCIUM CHANNELS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL SODIUM CHANNEL; MEMBRANE PROTEINS; NECROSIS; NEURONS; SODIUM CHANNELS; XENOPUS LAEVIS;

EID: 13744255990     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1347     Document Type: Article

References (50)

1. Demaurex, N. & Distelhorst, C. Apoptosis - the calcium connection. Science 300, 65-67 (2003).
2. Leist, M. & Nicotera, P. Apoptosis, excitotoxicity, and neuropathology. Exp. Cell Res. 239, 183-201 (1998).
3. 2+ homeostasis and neuronal death. J. Cell. Mol. Med. 7, 351-361 (2003).
4. Mattson, M.P. et al. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23, 222-229 (2000).
5. 2+ release from the endoplasmic reticulum. Neuron 31, 957-971 (2001).
6. Driscoll, M. & Chalfie, M. The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 349, 588-593 (1991).
7. Heintz, N. & Zoghbi, H.Y. Insights from mouse models into the molecular basis of neurodegeneration. Annu. Rev. Physiol. 62, 779-802 (2000).
8. Driscoll, M. & Gerstbrein, B. Dying for a cause: invertebrate genetics takes on human neurodegeneration. Nat. Rev. Gen. 4, 181-194 (2003).
9. Lai, C.C., Hong, K., Kinnell, M., Chalfie, M. & Driscoll, M. Sequence and transmembrane topology of MEC-4, an ion channel subunit required for mechanotransduction in Caenorhabditis elegans. J. Cell Biol. 133, 1071-1081 (1996).
10. Goodman, M.B. et al. MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature 415, 1039-1042 (2002).
11. Chelur, D.S. et al. The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel. Nature 420, 669-673 (2002).
12. Bianchi, L. & Driscoll, M. The molecular basis of touch sensation as modeled in Caenorhabditis elegans. in Transduction Channels in Sensory Cells (eds Frings, S. & Bradely, J.) 1-29 (Wiley-VCH, Weinheim, Germany, 2004).
13. Suzuki, H. et al. 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, 1005-1017 (2003).
14. Waldmann, R., Champigny, G., Voilley, N., Lauritzen, I. & Lazdunski, M. The mammalian degenerin MDEG, an amiloride-sensitive cation channel activated by mutations causing neurodegeneration in Caenorhabditis elegans. J. Biol. Chem. 271, 10433-10436 (1996).
15. + channel 1 by inducing a conformational change that exposes a residue associated with neurodegeneration. J. Biol. Chem. 273, 30204-30207 (1998).
16. Chalfie, M. & Wolinsky, E. The identification and suppression of inherited neurodegeneration in Caenorhabditis elegans. Nature 345, 410-416 (1990).
17. Hong, K. & Driscoll, M. A transmembrane domain of the putative channel subunit MEC-4 influences mechanotransduction and neurodegeneration in C. elegans. Nature 367, 470-473 (1994).
18. Price, M.P. et al. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407, 1007-1011 (2000).
19. Wemmie, J.A. et al. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning and memory. Neuron 34, 463-477 (2002).
20. Wemmie, J.A. et al. Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J. Neurosci. 23, 5496-5502 (2003).
21. Yermolaieva, O., Leonard, A.S., Schnizler, M.K., Abboud, F.M. & Welsh, M.J. Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc. Natl. Acad. Sci. USA 101, 6752-6757 (2004).
22. Xiong, Z.G. et al. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118, 687-698 (2004).
23. Syntichaki, P., Xu, K., Driscoll, M. & Tavernarakis, N. Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419, 939-944 (2002).
24. Metzstein, M.M., Stanfield, G.M. & Horvitz, H.R. Genetics of programmed cell death in C. elegans: past, present and future. Trends Genet. 14, 410-416 (1998).
25. Berridge, M.J. Inositol trisphosphate and calcium signalling. Nature 361, 315-325 (1993).
26. Verkhratsky, A. & Shmigol, A. Calcium-induced calcium release in neurones. Cell Calcium 19, 1-14 (1996).
27. Bargmann, C.I. Neurobiology of the Caenorhabditis elegans genome. Science 282, 2028-2033 (1998).
28. 2+ channels. J. Exp. Biol. 203, 841-856 (2000).
29. Kuruma, A. & Hartzell, H.C. Dynamics of calcium regulation of chloride currents in Xenopus oocytes. Am. J. Physiol. 276, C161-C175 (1999).
30. - channel in Xenopus laevis oocytes. J. Membr. Biol. 172, 169-179 (1999).
31. Weber, W. Ion currents of Xenopus laevis oocytes: state of the art. Biochim. Biophys. Acta 1421, 213-233 (1999).
32. Woodhull, A.M. Ionic blockage of sodium channels in nerve. J. Gen. Physiol. 61, 687-708 (1973).
33. Sheng, S., Li, J., McNulty, K.A., Avery, D. & Kleyman, T.R. Characterization of the selectivity filter of the epithelial sodium channel. J. Biol. Chem. 275, 8572-8581 (2000).
34. Sheng, S., McNulty, K.A., Harvey, J.M. & Kleyman, T.R. Second transmembrane domains of ENaC subunits contribute to ion permeation and selectivity. J. Biol. Chem. 276, 44091-44098 (2001).
35. + channel. J. Gen. Physiol. 114, 13-30 (1999).
36. Hong, K., Mano, I. & Driscoll, M. In vivo structure-function analyses of Caenorhabditis elegans MEC-4, a candidate mechanosensory ion channel subunit. J. Neurosci. 20, 2575-2588 (2000).
37. 2+ channel cause myotonia in Caenorhabditis elegans. EMBO J. 16, 6066-6076 (1997).
38. Garcia-Anoveros, J., Garcia, J.A., Liu, J.D. & Corey, D.P. The nematode degenerin UNC-105 forms ion channels that are activated by degeneration- or hypercontraction-causing mutations. Neuron 20, 1231-1241 (1998).
39. Waldmann, R., Champigny, G., Bassilana, F., Heurteaux, C. & Lazdunski, M. A proton-gated cation channel involved in acid-sensing. Nature 386, 173-177 (1997).
40. Chu, X.P. et al. Proton-gated channels in PC12 cells. J. Neurophysiol. 87, 2555-2561 (2002).
41. Gunthorpe, M.J., Smith, G.D., Davis, J.B. & Randall, A.D. Characterisation of a human acid-sensing ion channel (hASIC1a) endogenously expressed in HEK293 cells. Pflugers Arch. 442, 668-674 (2001).
42. Sutherland, S.P., Benson, C.J., Adelman, J.P. & McCleskey, E.W. Acid-sensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons. Proc. Natl. Acad. Sci. USA 98, 711-716 (2001).
43. Zhang, P. & Canessa, C.M. Single channel properties of rat acid-sensitive ion channel-1α, -2a, and -3 expressed in Xenopus oocytes. J. Gen. Physiol. 120, 553-566 (2002).
44. Bassler, E.L., Ngo-Anh, T.J., Geisler, H.S., Ruppersberg, J.P. & Grunder, S. Molecular and functional characterization of acid-sensing ion channel (ASIC) 1b. J. Biol. Chem. 276, 33782-33787 (2001).
45. Mesaeli, N. et al. Calreticulin is essential for cardiac development. J. Cell Biol. 144, 857-868 (1999).
46. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
47. Ks suppression in LQT1 mutants. Am. J. Physiol, 279, H3003-H3011 (2000).
48. Christensen, M. et al. A primary culture system for functional analysis of C. elegans neurons and muscle cells. Neuron 33, 503-514 (2002).
49. 2+ signals. Cell Calcium 28, 213-223 (2000).
50. Kerr, R. et al. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26, 583-594 (2000).