MEC-2 and MEC-6 in the Caenorhabditis elegans sensory mechanotransduction complex: Auxiliary subunits that enable channel activity

Journal of General Physiology

Volumn 131, Issue 6, 2008, Pages 605-616

  Brown, Austin L ^a   Liao, Zhiwen ^a   Goodman, Miriam B ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARYLDIALKYLPHOSPHATASE; CALCIUM; CHOLESTEROL; DIVALENT CATION; MAGNESIUM; MEMBRANE PROTEIN; PROTEIN MEC 2; PROTEIN MEC 6; PROTEIN SUBUNIT; PROTEINASE; STOMATIN;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL FUNCTION; CHANNEL GATING; CONTROLLED STUDY; ENZYME ACTIVATION; ION CURRENT; MECHANOTRANSDUCTION; NONHUMAN; PALMITOYLATION; PATCH CLAMP; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; VOLTAGE CLAMP; XENOPUS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; CHOLESTEROL; CHYMOTRYPSIN; EPITHELIAL SODIUM CHANNEL; GENE EXPRESSION REGULATION; ION CHANNEL GATING; ION TRANSPORT; LIPOYLATION; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MULTIPROTEIN COMPLEXES; OOCYTES; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; PROTEIN SUBUNITS; RNA PROBES; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; XENOPUS LAEVIS;

EID: 44349147323     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200709910     Document Type: Article

References (45)

1. Anishkin, A., and C. Kung. 2005. Microbial mechanosensation. Curr. Opin. Neurobiol. 15:397-405.
2. + channel by trypsin. J. Biol. Chem. 282:26884-26896.
3. Bianchi, L., B. Gerstbrein, C. Frokjaer-Jensen, D.C. Royal, G. Mukherjee, M.A. Royal, J. Xue, W.R. Schafer, and M. Driscoll. 2004. The neurotoxic MEC-4(d) DEG/ENaC sodium channel conducts calcium: implications for necrosis initiation. Nat. Neurosci. 7:1337-1344.
4. Brown, A.L., S.M. Fernandez-Illescas, Z. Liao, and M.B. Goodman. 2007. Gain-of-function mutations in the MEC-4 DEG/ENaC sensory mechanotransduction channel alter gating and drug blockade. J. Gen. Physiol. 129:161-173.
5. + channels. Am. J. Physiol. Cell Physiol. 286:C190-C194.
6. Cantor, R.S. 1999. Lipid composition and the lateral pressure profile in bilayers. Biophys. J. 76:2625-2639.
7. Chalfie, M., and E. Wolinsky. 1990. The identification and suppression of inherited neurodegeneration in Caenorhabditis elegans. Nature. 345:410-416.
8. Chelur, D.S., G.G. Ernstrom, M.B. Goodman, C.A. Yao, L. 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. 420:669-673.
9. Chillaron, J., R. Estevez, I. Samarzija, S. Waldegger, X. Testar, F. Lang, A. Zorzano, A. Busch, and M. Palacin. 1997. An intracellular trafficking defect in type I cystinuria rBAT mutants M467T and M467K. J. Biol. Chem. 272:9543-9549.
10. Chraibi, A., V. Vallet, D. Firsov, S.K. Hess, and J.D. Horisberger. 1998. Protease modulation of the activity of the epithelial sodium channel expressed in Xenopus oocytes. J. Gen. Physiol. 111:127-138.
11. 2+ ions. Brain Res. 900:277-281.
12. Draganov, D.I., P.L. Stetson, C.E. Watson, S.S. Billecke, and B.N. La Du. 2000. Rabbit serum paraoxonase 3 (PON3) is a high density lipoprotein- associated lactonase and protects low density lipoprotein against oxidation. J. Biol. Chem. 275:33435-33442.
13. 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. 349:588-593.
14. Gandhavadi, M., D. Allende, A. Vidal, S.A. Simon, and T.J. McIntosh. 2002. Structure, composition, and peptide binding properties of detergent soluble bilayers and detergent resistant rafts. Biophys. J. 82:1469-1482.
15. Goodman, M.B., and S.R. Lockery. 2000. Pressure polishing: a method for re-shaping patch pipettes during fire polishing. J. Neurosci. Methods. 100:13-15.
16. Goodman, M.B., G.G. Ernstrom, D.S. Chelur, R. O'Hagan, C.A. Yao, and M. Chalfie. 2002a. MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature. 415:1039-1042.
17. Goodman, M.B., G.G. Ernstrom, D.S. Chelur, R. O'Hagan, C.A. Yao, and M. Chalfie. 2002b. Corrigendum: MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature. 417:880.
18. Harel, M., A. Aharoni, L. Gaidukov, B. Brumshtein, O. Khersonsky, R. Meged, H. Dvir, R.B. Ravelli, A. McCarthy, L. Toker, et al. 2004. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat. Struct. Mol. Biol. 11:412-419.
19. Huang, M., and M. Chalfie. 1994. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature. 367:467-470.
20. Huang, M., G. Gu, E.L. Ferguson, and M. Chalfie. 1995. A stomatin-like protein necessary for mechanosensation in C. elegans. Nature. 378:292-295.
21. Huber, T.B., B. Schermer, R.U. Muller, M. Hohne, M. Bartram, A. Calixto, H. Hagmann, C. Reinhardt, F. Koos, K. Kunzelmann, et al. 2006. Inaugural article: podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels. Proc. Natl. Acad. Sci. USA. 103:17079-17086.
22. Hughey, R.P., J.B. Bruns, C.L. Kinlough, K.L. Harkleroad, Q. Tong, M.D. Carattino, J.P. Johnson, J.D. Stockand and T.R. Kleyman. 2004. Epithelial sodium channels are activated by furin-dependent proteolysis. J. Biol. Chem. 279:18111-18114.
23. Jasti, J., H. Furukawa, E.B. Gonzales, and E. Gouaux. 2007. Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature. 449:316-323.
24. Johansson, R.S., and A.B. Vallbo. 1979. Detection of tactile stimuli. Thresholds of afferent units related to psychophysical thresholds in the human hand. J. Physiol. 297:405-422.
25. Kellenberger, S., and L. Schild. 2002. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82:735-767.
26. Lai, C.C., K. Hong, M. Kinnell, M. Chalfie, and M. Driscoll. 1996. Sequence and transmembrane topology of MEC-4, an ion channel subunit required for mechanotransduction in Caenorhabditis elegans. J. Cell Biol. 133:1071-1081.
27. Levina, N., S. Totemeyer, N.R. Stokes, P. Louis, M.A. Jones, and I.R. Booth. 1999. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J. 18:1730-1737.
28. Lewis, C.A. 1984. Divalent cation effects on acetylcholine-activated channels at the frog neuromuscular junction. Cell. Mol. Neurobiol. 4:273-284.
29. Mannsfeldt, A.G., P. Carroll, C.L. Stucky, and G.R. Lewin. 1999. Stomatin, a MEC-2 like protein, is expressed by mammalian sensory neurons. Mol. Cell. Neurosci. 13:391-404.
30. Markin, V.S., and F. Sachs. 2004. Thermodynamics of mechanosensitivity. Phys. Biol. 1:110-124.
31. Martinez-Salgado, C., A.G. Benckendorff, L.Y. Chiang, R. Wang, N. Milenkovic, C. Wetzel, J. Hu, C.L. Stucky, M.G. Parra, N. Mohandas, and G.R. Lewin. 2007. Stomatin and sensory neuron mechanotransduction. J. Neurophysiol. 98:3802-3808.
32. Moe, P., and P. Blount. 2005. Assessment of potential stimuli for mechano-dependent gating of MscL: effects of pressure, tension, and lipid headgroups. Biochemistry. 44:12239-12244.
33. Niemela, P.S., S. Ollila, M.T. Hyvonen, M. Karttunen, and I. Vattulainen. 2007. Assessing the nature of lipid raft membranes. PLoS Comput. Biol. 3:e34.
34. 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.
35. + channel by peptidases. Curr. Top. Dev. Biol. 78:23-46.
36. Porter, J.A., K.E. Young, and P.A. Beachy. 1996. Cholesterol modification of hedgehog signaling proteins in animal development. Science. 274:255-259.
37. Schild, L., E. Schneeberger, I. Gautschi, and D. Firsov. 1997. Identification of amino acid residues in the α, β, and γ subunits of the epithelial sodium channel (ENaC) involved in amiloride block and ion permeation. J. Gen. Physiol. 109:15-26.
38. Sedensky, M.M., J.M. Siefker, J.Y. Koh, D.M. Miller III, and P.G. Morgan. 2004. A stomatin and a degenerin interact in lipid rafts of the nervous system of Caenorhabditis elegans. Am. J. Physiol. Cell Physiol. 287:C468-C474.
39. Sigworth, F.J., and S.M. Sine. 1987. Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys. J. 52:1047-1054.
40. Vallet, V., C. Pfister, J. Loffing, and B.C. Rossier. 2002. Cell-surface expression of the channel activating protease xCAP-1 is required for activation of ENaC in the Xenopus oocyte. J. Am. Soc. Nephrol. 13:588-594.
41. Waldmann, R., G. Champigny, F. Bassilana, C. Heurteaux, and M. Lazdunski. 1997. A proton-gated cation channel involved in acid-sensing. Nature. 386:173-177.
42. Wetzel, C., J. Hu, D. Riethmacher, A. Benckendorff, L. Harder, A. Eilers, R. Moshourab, A. Kozlenkov, D. Labuz, O. Caspani, et al. 2007. A stomatin-domain protein essential for touch sensation in the mouse. Nature. 445:206-209.
43. Yeung, D.T., D.E. Lenz, and D.M. Cerasoli. 2005. Analysis of active-site amino-acid residues of human serum paraoxonase using competitive substrates. FEBS J. 272:2225-2230.
44. Zhang, S., J. Arnadottir, C. Keller, G.A. Caldwell, C.A. Yao, and M. Chalfie. 2004a. MEC-2 is recruited to the putative mechanosensory complex in C. elegans touch receptor neurons through its stomatin-like domain. Curr. Biol. 14:1888-1896.
45. Zhang, S., C. Ma, and M. Chalfie. 2004b. Combinatorial marking of cells and organelles with reconstituted fluorescent proteins. Cell. 119:137-144.