NLF-1 Delivers a Sodium Leak Channel to Regulate Neuronal Excitability and Modulate Rhythmic Locomotion

Neuron

Volumn 77, Issue 6, 2013, Pages 1069-1082

  Xie, Lin ^a,b   Gao, Shangbang ^b   Alcaire, Salvador M ^a,b   Aoyagi, Kyota ^c   Wang, Ying ^b   Griffin, Jennifer K ^d   Stagljar, Igor ^a   Nagamatsu, Shinya ^c   Zhen, Mei ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CATION CHANNEL; MEMBRANE PROTEIN; SODIUM ION; SODIUM LEAK CHANNEL; SODIUM LEAK CHANNEL LOCALIZATION FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CHANNEL GATING; CONTROLLED STUDY; IN VITRO STUDY; INTERNEURON; LOCOMOTION; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; PREMOTOR CORTEX; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SODIUM CURRENT;

ANIMALS; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELLS, CULTURED; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; LOCOMOTION; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NEURONS; PERIODICITY; SODIUM CHANNELS; TRANSCRIPTION FACTORS;

EID: 84875509376     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.01.018     Document Type: Article

References (52)

1. Altier C., Garcia-Caballero A., Simms B., You H., Chen L., Walcher J., Tedford H.W., Hermosilla T., Zamponi G.W. The Cavβ subunit prevents RFP2-mediated ubiquitination and proteasomal degradation of L-type channels. Nat. Neurosci. 2011, 14:173-180.
2. Arellano-Carbajal F., Briseño-Roa L., Couto A., Cheung B.H., Labouesse M., de Bono M. Macoilin, a conserved nervous system-specific ER membrane protein that regulates neuronal excitability. PLoS Genet. 2011, 7:e1001341.
3. Basham S.E., Rose L.S. The Caenorhabditis elegans polarity gene ooc-5 encodes a Torsin-related protein of the AAA ATPase superfamily. Development 2001, 128:4645-4656.
4. Borgese N., Fasana E. Targeting pathways of C-tail-anchored proteins. Biochim. Biophys. Acta 2011, 1808:937-946.
5. Brockie P.J., Mellem J.E., Hills T., Madsen D.M., Maricq A.V. The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 2001, 31:617-630.
6. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25.
7. 2+ channels. Annu. Rev. Cell Dev. Biol. 2000, 16:521-555.
8. Crill W.E. Persistent sodium current in mammalian central neurons. Annu. Rev. Physiol. 1996, 58:349-362.
9. Denecke J., De Rycke R., Botterman J. Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J. 1992, 11:2345-2355.
10. Deribe Y.L., Wild P., Chandrashaker A., Curak J., Schmidt M.H., Kalaidzidis Y., Milutinovic N., Kratchmarova I., Buerkle L., Fetchko M.J., et al. Regulation of epidermal growth factor receptor trafficking by lysine deacetylase HDAC6. Sci. Signal. 2009, 2:ra84.
11. Deutsch C. The birth of a channel. Neuron 2003, 40:265-276.
12. Gao S., Zhen M. Action potentials drive body wall muscle contractions in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2011, 108:2557-2562.
13. Gendrel M., Rapti G., Richmond J.E., Bessereau J.L. A secreted complement-control-related protein ensures acetylcholine receptor clustering. Nature 2009, 461:992-996.
14. Gisler S.M., Kittanakom S., Fuster D., Wong V., Bertic M., Radanovic T., Hall R.A., Murer H., Biber J., Markovich D., et al. Monitoring protein-protein interactions between the mammalian integral membrane transporters and PDZ-interacting partners using a modified split-ubiquitin membrane yeast two-hybrid system. Mol. Cell. Proteomics 2008, 7:1362-1377.
15. Gong Q., Keeney D.R., Molinari M., Zhou Z. Degradation of trafficking-defective long QT syndrome type II mutant channels by the ubiquitin-proteasome pathway. J. Biol. Chem. 2005, 280:19419-19425.
16. Grunwald M.E., Kaplan J.M. Mutations in the ligand-binding and pore domains control exit of glutamate receptors from the endoplasmic reticulum in C. elegans. Neuropharmacology 2003, 45:768-776.
17. Halevi S., McKay J., Palfreyman M., Yassin L., Eshel M., Jorgensen E., Treinin M. The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J. 2002, 21:1012-1020.
18. Helenius A., Aebi M. Intracellular functions of N-linked glycans. Science 2001, 291:2364-2369.
19. Hille B. Ion Channels of Excitable Membranes 2001, Sinauer, Sunderland, MA. Third Edition.
20. Hodgkin A.L., Katz B. The effect of sodium ions on the electrical activity of giant axon of the squid. J. Physiol. 1949, 108:37-77.
21. Humphrey J.A., Hamming K.S., Thacker C.M., Scott R.L., Sedensky M.M., Snutch T.P., Morgan P.G., Nash H.A. A putative cation channel and its novel regulator: cross-species conservation of effects on general anesthesia. Curr. Biol. 2007, 17:624-629.
22. Iossifov I., Ronemus M., Levy D., Wang Z., Hakker I., Rosenbaum J., Yamrom B., Lee Y.H., Narzisi G., Leotta A., et al. De novo gene disruptions in children on the autistic spectrum. Neuron 2012, 74:285-299.
23. Johnsson N., Varshavsky A. Split ubiquitin as a sensor of protein interactions in vivo. Proc. Natl. Acad. Sci. USA 1994, 91:10340-10344.
24. Jospin M., Watanabe S., Joshi D., Young S., Hamming K., Thacker C., Snutch T.P., Jorgensen E.M., Schuske K. UNC-80 and the NCA ion channels contribute to endocytosis defects in synaptojanin mutants. Curr. Biol. 2007, 17:1595-1600.
25. Kawano T., Po M.D., Gao S., Leung G., Ryu W.S., Zhen M. An imbalancing act: gap junctions reduce the backward motor circuit activity to bias C. elegans for forward locomotion. Neuron 2011, 72:572-586.
26. Lansdell S.J., Gee V.J., Harkness P.C., Doward A.I., Baker E.R., Gibb A.J., Millar N.S. RIC-3 enhances functional expression of multiple nicotinic acetylcholine receptor subtypes in mammalian cells. Mol. Pharmacol. 2005, 68:1431-1438.
27. Lear B.C., Lin J.M., Keath J.R., McGill J.J., Raman I.M., Allada R. The ion channel narrow abdomen is critical for neural output of the Drosophila circadian pacemaker. Neuron 2005, 48:965-976.
28. Lee R.Y., Lobel L., Hengartner M., Horvitz H.R., Avery L. Mutations in the alpha1 subunit of an L-type voltage-activated Ca2+ channel cause myotonia in Caenorhabditis elegans. EMBO J. 1997, 16:6066-6076.
29. Lu T.Z., Feng Z.P. A sodium leak current regulates pacemaker activity of adult central pattern generator neurons in Lymnaea stagnalis. PLoS ONE 2011, 6:e18745.
30. Lu B., Su Y., Das S., Liu J., Xia J., Ren D. The neuronal channel NALCN contributes resting sodium permeability and is required for normal respiratory rhythm. Cell 2007, 129:371-383.
31. Lu B., Su Y., Das S., Wang H., Wang Y., Liu J., Ren D. Peptide neurotransmitters activate a cation channel complex of NALCN and UNC-80. Nature 2009, 457:741-744.
32. Lu B., Zhang Q., Wang H., Wang Y., Nakayama M., Ren D. Extracellular calcium controls background current and neuronal excitability via an UNC79-UNC80-NALCN cation channel complex. Neuron 2010, 68:488-499.
33. + channels. J. Neurosci. 1996, 16:7117-7127.
34. Manganas L.N., Wang Q., Scannevin R.H., Antonucci D.E., Rhodes K.J., Trimmer J.S. Identification of a trafficking determinant localized to the Kv1 potassium channel pore. Proc. Natl. Acad. Sci. USA 2001, 98:14055-14059.
35. Morgan P.G., Sedensky M., Meneely P.M. Multiple sites of action of volatile anesthetics in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 1990, 87:2965-2969.
36. Nash H.A., Scott R.L., Lear B.C., Allada R. An unusual cation channel mediates photic control of locomotion in Drosophila. Curr. Biol. 2002, 12:2152-2158.
37. Nicholls J.G., Martin R.A., Wallace B.G. From Neuron to Brain 2001, Sinauer, Sunderland, MA. Fourth Edition.
38. Palty R., Raveh A., Kaminsky I., Meller R., Reuveny E. SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 2012, 149:425-438.
39. Pierce-Shimomura J.T., Chen B.L., Mun J.J., Ho R., Sarkis R., McIntire S.L. Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proc. Natl. Acad. Sci. USA 2008, 105:20982-20987.
40. Raman I.M., Gustafson A.E., Padgett D. Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J. Neurosci. 2000, 20:9004-9016.
41. Ren D. Sodium leak channels in neuronal excitability and rhythmic behaviors. Neuron 2011, 72:899-911.
42. Richmond J.E., Jorgensen E.M. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 1999, 2:791-797.
43. Saheki Y., Bargmann C.I. Presynaptic CaV2 calcium channel traffic requires CALF-1 and the alpha(2)delta subunit UNC-36. Nat. Neurosci. 2009, 12:1257-1265.
44. Semenza J.C., Hardwick K.G., Dean N., Pelham H.R. ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 1990, 61:1349-1357.
45. Shao S., Hegde R.S. Membrane protein insertion at the endoplasmic reticulum. Annu. Rev. Cell Dev. Biol. 2011, 27:25-56.
46. Simms B.A., Zamponi G.W. Trafficking and stability of voltage-gated calcium channels. Cell. Mol. Life Sci. 2012, 69:843-856.
47. Sinke A.P., Caputo C., Tsaih S.W., Yuan R., Ren D., Deen P.M., Korstanje R. Genetic analysis of mouse strains with variable serum sodium concentrations identifies the Nalcn sodium channel as a novel player in osmoregulation. Physiol. Genomics 2011, 43:265-270.
48. Swayne L.A., Mezghrani A., Varrault A., Chemin J., Bertrand G., Dalle S., Bourinet E., Lory P., Miller R.J., Nargeot J., Monteil A. The NALCN ion channel is activated by M3 muscarinic receptors in a pancreatic beta-cell line. EMBO Rep. 2009, 10:873-880.
49. V)2.2 channels by reducing their proteasomal degradation. J. Biol. Chem. 2011, 286:9598-9611.
50. Wattenberg B., Lithgow T. Targeting of C-terminal (tail)-anchored proteins: understanding how cytoplasmic activities are anchored to intracellular membranes. Traffic 2001, 2:66-71.
51. Yeh E., Ng S., Zhang M., Bouhours M., Wang Y., Wang M., Hung W., Aoyagi K., Melnik-Martinez K., Li M., et al. A putative cation channel, NCA-1, and a novel protein, UNC-80, transmit neuronal activity in C. elegans. PLoS Biol. 2008, 6:e55.
52. Zhang L., Chung B.Y., Lear B.C., Kilman V.L., Liu Y., Mahesh G., Meissner R.A., Hardin P.E., Allada R. DN1(p) circadian neurons coordinate acute light and PDF inputs to produce robust daily behavior in Drosophila. Curr. Biol. 2010, 20:591-599.