A presynaptic ENaC channel drives homeostatic plasticity

Neuron

Volumn 79, Issue 6, 2013, Pages 1183-1196

  Younger, MegA ^a   Müller, Martin ^a   Tong, Amy ^a   Pym, EdwardC ^a   Davis, GraemeW ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEGENERIN EPITHELIAL SODIUM CHANNEL SUBUNIT; DEGENERIN SODIUM CHANNEL; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXON; GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; GENOTYPE; HOMEOSTASIS; HOMOZYGOSITY; MOTONEURON; NEUROTRANSMITTER RELEASE; NONHUMAN; PPK11 GENE; PPK16 GENE; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; UPREGULATION;

AMILORIDE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM; CENTRAL NERVOUS SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIAL SODIUM CHANNELS; EXCITATORY POSTSYNAPTIC POTENTIALS; HOMEOSTASIS; LARVA; MUTATION; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; NEUROPROTECTIVE AGENTS; NICOTINIC ANTAGONISTS; PATCH-CLAMP TECHNIQUES; POLYAMINES; PRESYNAPTIC TERMINALS; SODIUM CHANNELS;

EID: 84884289719     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.06.048     Document Type: Article

References (65)

1. Adams C.M., Anderson M.G., Motto D.G., Price M.P., Johnson W.A., Welsh M.J. Ripped pocket and pickpocket, novel Drosophila DEG/ENaC subunits expressed in early development and in mechanosensory neurons. J.Cell Biol. 1998, 140:143-152.
2. Alle H., Geiger J.R.P. Combined analog and action potential coding in hippocampal mossy fibers. Science 2006, 311:1290-1293.
3. Awatramani G.B., Price G.D., Trussell L.O. Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron 2005, 48:109-121.
4. Ben-Shahar Y. Sensory functions for degenerin/epithelial sodium channels (DEG/ENaC). Adv. Genet. 2011, 76:1-26.
5. Benson C.J., Xie J., Wemmie J.A., Price M.P., Henss J.M., Welsh M.J., Snyder P.M. Heteromultimers of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc. Natl. Acad. Sci. USA 2002, 99:2338-2343.
6. Bergquist S., Dickman D.K., Davis G.W. A hierarchy of cell intrinsic and target-derived homeostatic signaling. Neuron 2010, 66:220-234.
7. Bernard C., Anderson A., Becker A., Poolos N.P., Beck H., Johnston D. Acquired dendritic channelopathy in temporal lobe epilepsy. Science 2004, 305:532-535.
8. Bianchi L., Driscoll M. Protons at the gate: DEG/ENaC ion channels help us feel and remember. Neuron 2002, 34:337-340.
9. Blumenthal T. Operons in eukaryotes. Brief. Funct. Genomics Proteomics 2004, 3:199-211.
10. Boiko N., Kucher V., Stockand J.D., Eaton B.A. Pickpocket1 is an ionotropic molecular sensory transducer. J.Biol. Chem. 2012, 287:39878-39886.
11. Bollmann J.H., Sakmann B., Borst J.G. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 2000, 289:953-957.
12. Borst J.G., Sakmann B. Facilitation of presynaptic calcium currents in the rat brainstem. J.Physiol. 1998, 513:149-155.
13. Bouhours B., Trigo F.F., Marty A. Somatic depolarization enhances GABA release in cerebellar interneurons via a calcium/protein kinase C pathway. J.Neurosci. 2011, 31:5804-5815.
14. Chalfie M. Neurosensory mechanotransduction. Nat. Rev. Mol. Cell Biol. 2009, 10:44-52.
15. Chandrashekar J., Kuhn C., Oka Y., Yarmolinsky D.A., Hummler E., Ryba N.J., Zuker C.S. The cells and peripheral representation of sodium taste in mice. Nature 2010, 464:297-301.
16. Chen Z., Wang Q., Wang Z. The amiloride-sensitive epithelial Na+ channel PPK28 is essential for drosophila gustatory water reception. J.Neurosci. 2010, 30:6247-6252.
17. Christie J.M., Chiu D.N., Jahr C.E. Ca(2+)-dependent enhancement of release by subthreshold somatic depolarization. Nat. Neurosci. 2011, 14:62-68.
18. Chu Y., Fioravante D., Thanawala M., Leitges M., Regehr W.G. Calcium-dependent isoforms of protein kinase C mediate glycine-induced synaptic enhancement at the calyx of Held. J.Neurosci. 2012, 32:13796-13804.
19. Cuthbert A.W., Fanelli G.M. Effects of some pyrazinecarboxamides on sodium transport in frog skin. Br. J. Pharmacol. 1978, 63:139-149.
20. Cuttle M.F., Tsujimoto T., Forsythe I.D., Takahashi T. Facilitation of the presynaptic calcium current at an auditory synapse in rat brainstem. J.Physiol. 1998, 512:723-729.
21. Davis G.W. Homeostatic control of neural activity: from phenomenology to molecular design. Annu. Rev. Neurosci. 2006, 29:307-323.
22. Davis G.W., Bezprozvanny I. Maintaining the stability of neural function: a homeostatic hypothesis. Annu. Rev. Physiol. 2001, 63:847-869.
23. Davis G.W., Goodman C.S. Synapse-specific control of synaptic efficacy at the terminals of a single neuron. Nature 1998, 392:82-86.
24. Davis G.W., Schuster C.M., Goodman C.S. Genetic analysis of the mechanisms controlling target selection: target-derived Fasciclin II regulates the pattern of synapse formation. Neuron 1997, 19:561-573.
25. DiAntonio A., Petersen S.A., Heckmann M., Goodman C.S. Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J.Neurosci. 1999, 19:3023-3032.
26. Dickman D.K., Davis G.W. The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis. Science 2009, 326:1127-1130.
27. Drummond H.A., Price M.P., Welsh M.J., Abboud F.M. A molecular component of the arterial baroreceptor mechanotransducer. Neuron 1998, 21:1435-1441.
28. Frank C.A., Kennedy M.J., Goold C.P., Marek K.W., Davis G.W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 2006, 52:663-677.
29. Frank C.A., Pielage J., Davis G.W. A presynaptic homeostatic signaling system composed of the Eph receptor, ephexin, Cdc42, and CaV2.1 calcium channels. Neuron 2009, 61:556-569.
30. Garty H., Palmer L.G. Epithelial sodium channels: function, structure, and regulation. Physiol. Rev. 1997, 77:359-396.
31. Gonzalez-Islas C., Chub N., Garcia-Bereguiain M.A., Wenner P. GABAergic synaptic scaling in embryonic motoneurons is mediated by a shift in the chloride reversal potential. J.Neurosci. 2010, 30:13016-13020.
32. Goold C.P., Davis G.W. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron 2007, 56:109-123.
33. Houweling A.R., Bazhenov M., Timofeev I., Steriade M., Sejnowski T.J. Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cereb. Cortex 2005, 15:834-845.
34. Jakubs K., Nanobashvili A., Bonde S., Ekdahl C.T., Kokaia Z., Kokaia M., Lindvall O. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 2006, 52:1047-1059.
35. Jasti J., Furukawa H., Gonzales E.B., Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007, 449:316-323.
36. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron 2003, 37:925-937.
37. Katz B., Miledi R. Further study of the role of calcium in synaptic transmission. J.Physiol. 1970, 207:789-801.
38. Kim S.H., Ryan T.A. CDK5 serves as a major control point in neurotransmitter release. Neuron 2010, 67:797-809.
39. Kleyman T.R., Cragoe E.J. Amiloride and its analogs as tools in the study of ion transport. J.Membr. Biol. 1988, 105:1-21.
40. Liu L., Johnson W.A., Welsh M.J. Drosophila DEG/ENaC pickpocket genes are expressed in the tracheal system, where they may be involved in liquid clearance. Proc. Natl. Acad. Sci. USA 2003, 100:2128-2133.
41. Liu L., Leonard A.S., Motto D.G., Feller M.A., Price M.P., Johnson W.A., Welsh M.J. Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 2003, 39:133-146.
42. Mahr A., Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 2006, 6:299-309.
43. Marder E., Goaillard J.-M. Variability, compensation and homeostasis in neuron and network function. Nat. Rev. Neurosci. 2006, 7:563-574.
44. Martin A.R. A further study of the statistical composition on the end-plate potential. J.Physiol. 1955, 130:114-122.
45. Metaxakis A., Oehler S., Klinakis A., Savakis C. Minos as a genetic and genomic tool in Drosophila melanogaster. Genetics 2005, 171:571-581.
46. 2+ influx achieves homeostatic potentiation of neurotransmitter release. Curr. Biol. 2012, 22:1102-1108.
47. Müller M., Pym E.C., Tong A., Davis G.W. Rab3-GAP controls the progression of synaptic homeostasis at a late stage of vesicle release. Neuron 2011, 69:749-762.
48. Müller M., Liu K.S., Sigrist S.J., Davis G.W. RIM controls homeostatic plasticity through modulation of the readily-releasable vesicle pool. J.Neurosci. 2012, 32:16574-16585.
49. Petersen S.A., Fetter R.D., Noordermeer J.N., Goodman C.S., DiAntonio A. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 1997, 19:1237-1248.
50. Piedras-Rentería E.S., Pyle J.L., Diehn M., Glickfeld L.L., Harata N.C., Cao Y., Kavalali E.T., Brown P.O., Tsien R.W. Presynaptic homeostasis at CNS nerve terminals compensates for lack of a key Ca2+ entry pathway. Proc. Natl. Acad. Sci. USA 2004, 101:3609-3614.
51. Plomp J.J., van Kempen G.T., Molenaar P.C. Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in alpha-bungarotoxin-treated rats. J.Physiol. 1992, 458:487-499.
52. Ramocki M.B., Zoghbi H.Y. Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 2008, 455:912-918.
53. Schild L. The epithelial sodium channel and the control of sodium balance. Biochim. Biophys. Acta 2010, 1802:1159-1165.
54. Schneggenburger R., Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 2000, 406:889-893.
55. Schuster C.M., Davis G.W., Fetter R.D., Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 1996, 17:655-667.
56. Shapiro E., Castellucci V.F., Kandel E.R. Presynaptic membrane potential affects transmitter release in an identified neuron in Aplysia by modulating the Ca2+ and K+ currents. Proc. Natl. Acad. Sci. USA 1980, 77:629-633.
57. Shu Y., Hasenstaub A., Duque A., Yu Y., McCormick D.A. Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 2006, 441:761-765.
58. Thiagarajan T.C., Lindskog M., Malgaroli A., Tsien R.W. LTP and adaptation to inactivity: overlapping mechanisms and implications for metaplasticity. Neuropharmacology 2007, 52:156-175.
59. Turrigiano G.G. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008, 135:422-435.
60. Wagh D.A., Rasse T.M., Asan E., Hofbauer A., Schwenkert I., Dürrbeck H., Buchner S., Dabauvalle M.C., Schmidt M., Qin G., et al. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 2006, 49:833-844.
61. Waldmann R., Champigny G., Bassilana F., Heurteaux C., Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature 1997, 386:173-177.
62. Weyhersmüller A., Hallermann S., Wagner N., Eilers J. Rapid active zone remodeling during synaptic plasticity. J.Neurosci. 2011, 31:6041-6052.
63. Wojtowicz J.M., Atwood H.L. Maintained depolarization of synaptic terminals facilitates nerve-evoked transmitter release at a crayfish neuromuscular junction. J.Neurobiol. 1983, 14:385-390.
64. Wojtowicz J.M., Atwood H.L. Presynaptic membrane potential and transmitter release at the crayfish neuromuscular junction. J.Neurophysiol. 1984, 52:99-113.
65. Zhao C., Dreosti E., Lagnado L. Homeostatic synaptic plasticity through changes in presynaptic calcium influx. J.Neurosci. 2011, 31:7492-7496.