Cloning and functional expression of a new epithelial sodium channel δ subunit isoform differentially expressed in neurons of the human and monkey telencephalon

Journal of Neurochemistry

Volumn 102, Issue 4, 2007, Pages 1304-1315

  Giraldez, Teresa ^a,b   Afonso Oramas, Domingo ^a   Cruz Muros, Ignacio ^a   Garcia Marin, Victor ^c   Pagel, Philipp ^d   González Hernández, Tomás ^a   De La Rosa, Diego Alvarez ^b  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

^c HOSPITAL UNIVERSITARIO DE CANARIAS   (Spain)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Alternative splicing; Degenerin epithelial sodium channel family; Epithelial sodium channel; Human cerebral cortex; Pyramidal neurons; Xenopus oocytes

Indexed keywords

EPITHELIUM SODIUM CHANNEL BETA; EPITHELIUM SODIUM CHANNEL DELTA; EPITHELIUM SODIUM CHANNEL GAMMA; ISOPROTEIN; SODIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASAL GANGLION; BRAIN CORTEX; CONTROLLED STUDY; EXON; FEMALE; MOLECULAR CLONING; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SPLICEOSOME; TELENCEPHALON; TRANSCRIPTION INITIATION SITE;

ANIMALS; CLONING, MOLECULAR; EPITHELIAL SODIUM CHANNEL; FEMALE; GENE EXPRESSION; HAPLORHINI; HUMANS; IN SITU HYBRIDIZATION; MALE; MEMBRANE POTENTIALS; MICROINJECTIONS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NEURONS; OOCYTES; PATCH-CLAMP TECHNIQUES; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TELENCEPHALON; XENOPUS LAEVIS;

EID: 34547455298     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04622.x     Document Type: Article

References (39)

1. Alvarez de la Rosa D., Canessa C. M., Fyfe G. K. Zhang P. (2000) Structure and regulation of amiloride-sensitive sodium channels. Annu. Rev. Physiol. 62, 573 594.
2. Alvarez de la Rosa D., Zhang P., Shao D., White F. Canessa C. M. (2002) Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc. Natl Acad. Sci. USA 99, 2326 2331.
3. Alvarez de la Rosa D., Krueger S. R., Kolar A., Shao D., Fitzsimonds R. M. Canessa C. M. (2003) Distribution, subcellular localization and ontogeny of ASIC1 in the mammalian central nervous system. J. Physiol. 546, 77 87.
4. Amin M. S., Wang H. W., Reza E., Whitman S. C., Tuana B. S. Leenen F. H. (2005) Distribution of epithelial sodium channels and mineralocorticoid receptors in cardiovascular regulatory centers in rat brain. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1787 R1797.
5. Blom N., Sicheritz-Ponten T., Gupta R., Gammeltoft S. Brunak S. (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633 1649.
6. Canessa C. M., Merillat A. M. Rossier B. C. (1994a) Membrane topology of the epithelial sodium channel in intact cells. Am. J. Physiol. 267, C1682 C1690.
7. Canessa C. M., Schild L., Buell G., Thorens B., Gautschi I., Horisberger J. D. Rossier B. C. (1994b) Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 367, 463 467.
8. Chen C., England S., Akopian A. N. Wood J. N. (1998) A sensory neuron-specific, proton-gated ion channel. Proc. Natl Acad. Sci. USA 95, 10240 10245.
9. Coric T., Hernandez N., Alvarez de la Rosa D., Shao D., Wang T. Canessa C. M. (2004) Expression of ENaC and serum- and glucocorticoid-induced kinase 1 in the rat intestinal epithelium. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G663 G670.
10. Duggan A., Garcia-Añoveros J. Corey D. P. (2002) The PDZ domain protein PICK1 and the sodium channel BNaC1 interact and localize at mechanosensory terminals of dorsal root ganglion neurons and dendrites of central neurons. J. Biol. Chem. 277, 5203 5208.
11. Dyka F. M., May C. A. Enz R. (2005) Subunits of the epithelial sodium channel family are differentially expressed in the retina of mice with ocular hypertension. J. Neurochem. 94, 120 128.
12. Garcia-Añoveros J., Derfler B., Neville-Golden J., Hyman B. T. Corey D. P. (1997) BNaC1 and BNaC2 constitute a new family of human neuronal sodium channels related to degenerins and epithelial sodium channels. Proc. Natl Acad. Sci. USA 94, 1459 1464.
13. Giraldez T., Hughes T. E. Sigworth F. J. (2005) Generation of functional fluorescent BK channels by random insertion of GFP variants. J. Gen. Physiol. 126, 429 438.
14. Gonzalez M. C., Abreu P., Barroso-Chinea P., Cruz-Muros I. Gonzalez-Hernandez T. (2004) Effect of intracerebroventricular injection of lipopolysaccharide on the tuberoinfundibular dopaminergic system of the rat. Neuroscience 127, 251 259.
15. Hernandez-Gonzalez E. O., Sosnik J., Edwards J. et al. (2006) Sodium and epithelial sodium channels participate in the regulation of the capacitation-associated hyperpolarization in mouse sperm. J. Biol. Chem. 281, 5623 5633.
16. Hesselager M., Timmermann D. B. Ahring P. K. (2004) pH Dependency and desensitization kinetics of heterologously expressed combinations of acid-sensing ion channel subunits. J. Biol. Chem. 279, 11006 11015.
17. Hubbard T., Andrews D., Caccamo M. et al. (2005) Ensembl 2005. Nucleic Acids Res. 33, D447 D453.
18. Ji H. L. Benos D. J. (2004) Degenerin sites mediate proton activation of delta-beta-gamma-ENaC. J. Biol. Chem. 279, 26939 26947.
19. Ji H. L., Bishop L. R., Anderson S. J., Fuller C. M. Benos D. J. (2004) The role of Pre-H2 domains of alpha- and delta-epithelial Na+ channels in ion permeation, conductance, and amiloride sensitivity. J. Biol. Chem. 279, 8428 8440.
20. Ji H. L., Su X. F., Kedar S., Li J., Barbry P., Smith P. R., Matalon S. Benos D. J. (2006) Delta-subunit confers novel biophysical features to alpha beta gamma-human epithelial sodium channel (ENaC) via a physical interaction. J. Biol. Chem. 281, 8233 8241.
21. Kellenberger S. Schild L. (2002) Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82, 735 767.
22. Krishtal O. (2003) The ASICs: signaling molecules? Modulators? Trends Neurosci. 26, 477 483.
23. Lennon G., Auffray C., Polymeropoulos M. Soares M. B. (1996) The I.M.A.G.E. Consortium: an integrated molecular analysis of genomes and their expression. Genomics 33, 151 152.
24. Lingueglia E., de Weille J. R., Bassilana F., Heurteaux C., Sakai H., Waldmann R. Lazdunski M. (1997) A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglia. J. Biol. Chem. 272, 29778 29783.
25. McDonald F. J., Snyder P. M., McCray P. B. J. Welsh M. J. (1994) Cloning, expression, and tissue distribution of a human amiloride-sensitive Na+ channel. Am. J. Physiol. 266, L728 L734.
26. McNicholas C. M. Canessa C. M. (1997) Diversity of channels generated by different combinations of epithelial sodium channel subunits. J. Gen. Physiol. 109, 681 692.
27. Ota T., Suzuki Y., Nishikawa T. et al. (2004) Complete sequencing and characterization of 21 243 full-length human cDNAs. Nat. Genet. 36, 40 45.
28. Price M. P., Snyder P. M. Welsh M. J. (1996) Cloning and expression of a novel human brain Na+ channel. J. Biol. Chem. 271, 7879 7882.
29. Puntervoll P., Linding R., Gemund C. et al. (2003) ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res. 31, 3625 3630.
30. Saugstad J. A., Roberts J. A., Dong J., Zeitouni S. Evans R. J. (2004) Analysis of the membrane topology of the acid-sensing ion channel 2a. J. Biol. Chem. 279, 55514 55519.
31. Thompson J. D., Higgins D. G. Gibson T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673 4680.
32. Viloria C. G., Barros F., Giraldez T., Gomez-Varela D. de la Pena P. (2000) Differential effects of amino-terminal distal and proximal domains in the regulation of human erg K(+) channel gating. Biophys. J. 79, 231 246.
33. Voilley N., Bassilana F., Mignon C., Merscher S., Mattei M. G., Carle G. F., Lazdunski M. Barbry P. (1995) Cloning, chromosomal localization, and physical linkage of the beta and gamma subunits (SCNN1B and SCNN1G) of the human epithelial amiloride-sensitive sodium channel. Genomics 28, 560 565.
34. Vukicevic M. Kellenberger S. (2004) Modulatory effects of acid-sensing ion channels on action potential generation in hippocampal neurons. Am. J. Physiol. Cell Physiol. 287, C682 C690.
35. Waldmann R., Champigny G., Bassilana F., Voilley N. Lazdunski M. (1995) Molecular cloning and functional expression of a novel amiloride-sensitive Na+ channel. J. Biol. Chem. 270, 27411 27414.
36. Waldmann R., Champigny G., Bassilana F., Heurteaux C. Lazdunski M. (1997) A proton-gated cation channel involved in acid-sensing. Nature 386, 173 177.
37. Yamamura H., Ugawa S., Ueda T., Nagao M. Shimada S. (2004) Protons activate the delta-subunit of the epithelial Na+ channel in humans. J. Biol. Chem. 279, 12529 12534.
38. Yamamura H., Ugawa S., Ueda T., Nagao M. Shimada S. (2006) A novel spliced variant of the epithelial Na+ channel delta-subunit in the human brain. Biochem. Biophys Res. Commun. 349, 317 321.
39. Zhang P. Canessa C. M. (2002) Single channel properties of rat acid-sensitive ion channel-1alpha, -2a, and -3 expressed in Xenopus oocytes. J. Gen. Physiol. 120, 553 566.