Functional characterization of acid-sensing ion channels in cultured neurons of rat inferior colliculus

Neuroscience

Volumn 154, Issue 2, 2008, Pages 461-472

  Zhang, M ^a,b   Gong, N ^c   Lu, Y G ^a,b   Jia, N L ^a   Xu, T L ^c   Chen, L ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

acid sensing ion channel; cell culture; inferior colliculus; whole cell patch clamp

Indexed keywords

ACID SENSING ION CHANNEL; AMILORIDE; CALCIUM ION; PSALMOTOXIN; VENOM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; IC 50; INFERIOR COLLICULUS; NERVE CELL CULTURE; NONHUMAN; PATCH CLAMP; PH; PRIORITY JOURNAL; RAT;

ACIDS; AMILORIDE; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELLS, CULTURED; DIURETICS; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; HYDROGEN-ION CONCENTRATION; INFERIOR COLLICULI; ION CHANNELS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RNA, MESSENGER; SALICYLATES; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SPIDER VENOMS;

EID: 46549084958     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.03.040     Document Type: Article

References (68)

1. Akopian A.N., Chen C.C., Ding Y., Cesare P., and Wood J.N. A new member of the acid-sensing ion channel family. Neuroreport 11 (2000) 2217-2222
2. Araki T., Inoue T., Kato H., Kogure K., and Murakami M. Neuronal damage and calcium accumulation following transient cerebral ischemia in the rat. Mol Chem Neuropathol 12 (1990) 203-213
3. Babinski K., Le K.T., and Seguela P. Molecular cloning and regional distribution of a human proton receptor subunit with biphasic functional properties. J Neurochem 72 (1999) 51-57
4. + are coactivators of acid-sensing ion channels. J Biol Chem 276 (2001) 35361-35367
5. Biagini G., Babinski K., Avoli M., Marcinkiewicz M., and Seguela P. Regional and subunit-specific downregulation of acid-sensing ion channels in the pilocarpine model of epilepsy. Neurobiol Dis 8 (2001) 45-58
6. Chen C.C., England S., Akopian A.N., and Wood J.N. A sensory neuron-specific, proton-gated ion channel. Proc Natl Acad Sci U S A 95 (1998) 10240-10245
7. Chen C.C., Zimmer A., Sun W.H., Hall J., Brownstein M.J., and Zimmer A. A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc Natl Acad Sci U S A 99 (2002) 8992-8997
8. Chesler M., and Kaila K. Modulation of pH by neuronal activity. Trends Neurosci 15 (1992) 396-402
9. Chu X.P., Miesch J., Johnson M., Root L., Zhu X.M., Chen D., Simon R.P., and Xiong Z.G. Proton-gated channels in PC12 cells. J Neurophysiol 87 (2002) 2555-2561
10. Chu X.P., Wemmie J.A., Wang W.Z., Zhu X.M., Saugstad J.A., Price M.P., Simon R.P., and Xiong Z.G. Subunit-dependent high-affinity zinc inhibition of acid-sensing ion channels. J Neurosci 24 (2004) 8678-8689
11. de Weille J., and Bassilana F. Dependence of the acid-sensitive ion channel, ASIC1a, on extracellular Ca(2+) ions. Brain Res 900 (2001) 277-281
12. de Weille J.R., Bassilana F., Lazdunski M., and Waldmann R. Identification, functional expression and chromosomal localisation of a sustained human proton-gated cation channel. FEBS Lett 433 (1998) 257-260
13. 2+ current in mammalian cone photoreceptors. Neuron 32 (2001) 1107-1117
14. Drew L.J., Rohrer D.K., Price M.P., Blaver K.E., Cockayne D.A., Cesare P., and Wood J.N. Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J Physiol 556 (2004) 691-710
15. Duan B., Wu L.J., Yu Y.Q., Ding Y., Jing L., Xu L., Chen J., and Xu T.L. Upregulation of acid-sensing ion channel ASIC1a in spinal dorsal horn neurons contributes to inflammatory pain hypersensitivity. J Neurosci 27 (2007) 11139-11148
16. + channels. J Biol Chem 275 (2000) 25116-25121
17. Ettaiche M., Guy N., Hofman P., Lazdunski M., and Waldmann R. Acid-sensing ion channel 2 is important for retinal function and protects against light-induced retinal degeneration. J Neurosci 24 (2004) 1005-1012
18. Ettaiche M., Deval E., Cougnon M., Lazdunski M., and Voilley N. Silencing acid-sensing ion channel 1a alters cone-mediated retinal function. J Neurosci 26 (2006) 5800-5809
19. Gao J., Duan B., Wang D.G., Deng X.H., Zhang G.Y., Xu L., and Xu T.L. Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron 48 (2005) 635-646
20. Grunder S., Geissler H.S., Bassler E.L., and Ruppersberg J.P. A new member of acid-sensing ion channels from pituitary gland. Neuroreport 11 (2000) 1607-1611
21. Hakim A.M. The induction and reversibility of cerebral acidosis in thiamine deficiency. Ann Neurol 16 (1984) 673-679
22. Hesselager M., Timmermann D.B., and Ahring P.K. pH Dependency and desensitization kinetics of heterologously expressed combinations of acid-sensing ion channel subunits. J Biol Chem 279 (2004) 11006-11015
23. 2+-permeable acid-sensing ion channels. Stroke 38 (2007) 670-673
24. Hildebrand M.S., de Silva M.G., Klockars T., Rose E., Price M., Smith R.J., McGuirt W.T., Christopoulos H., Petit C., and Dahl H.H. Characterisation of DRASIC in the mouse inner ear. Hear Res 190 (2004) 149-160
25. 2+ blockade. Neuron 37 (2003) 75-84
26. Jasti J., Furukawa H., Gonzales E.B., and Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 449 (2007) 316-323
27. Jia Z., Agopyan N., Miu P., Xiong Z., Henderson J., Gerlai R., Taverna F.A., Velumian A., MacDonald J., Carlen P., Abramow-Newerly W., and Roder J. Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17 (1996) 945-956
28. Krishtal O.A., Osipchuk Y.V., Shelest T.N., and Smirnoff S.V. Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices. Brain Res 436 (1987) 352-356
29. Lin W., Ogura T., and Kinnamon S.C. Acid-activated cation currents in rat vallate taste receptor cells. J Neurophysiol 88 (2002) 133-141
30. Lingueglia E., de Weille J.R., Bassilana F., Heurteaux C., Sakai H., Waldmann R., and Lazdunski M. A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglion cells. J Biol Chem 272 (1997) 29778-29783
31. Mair R.G., Knoth R.L., Rabchenuk S.A., and Langlais P.J. Impairment of olfactory, auditory, and spatial serial reversal learning in rats recovered from pyrithiamine-induced thiamine deficiency. Behav Neurosci 105 (1991) 360-374
32. Mercado F., Lopez I.A., Acuna D., Vega R., and Soto E. Acid-sensing ionic channels in the rat vestibular endorgans and ganglia. J Neurophysiol 96 (2006) 1615-1624
33. Miesenbock G., De Angelis D.A., and Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394 (1998) 192-195
34. Murase K., Ryu P.D., and Randic M. Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103 (1989) 56-63
35. N′Gouemo P., and Morad M. Voltage-gated calcium channels in adult rat inferior colliculus neurons. Neuroscience 120 (2003) 815-826
36. Nedergaard M., Kraig R.P., Tanabe J., and Pulsinelli W.A. Dynamics of interstitial and intracellular pH in evolving brain infarct. Am J Physiol 260 (1991) R581-R588
37. Palmer M.J., Hull C., Vigh J., and von Gersdorff H. Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J Neurosci 23 (2003) 11332-11341
38. 2+ blocking site of acid-sensing ion channel (ASIC) 1: implications for channel gating. J Gen Physiol 124 (2004) 383-394
39. Peng B.G., Ahmad S., Chen S., Chen P., Price M.P., and Lin X. Acid-sensing ion channel 2 contributes a major component to acid-evoked excitatory responses in spiral ganglion neurons and plays a role in noise susceptibility of mice. J Neurosci 24 (2004) 10167-10175
40. + channel. J Biol Chem 271 (1996) 7879-7882
41. Price M.P., McIlwrath S.L., Xie J., Cheng C., Qiao J., Tarr D.E., Sluka K.A., Brennan T.J., Lewin G.R., and Welsh M.J. The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32 (2001) 1071-1083
42. Price M.P., Lewin G.R., McIlwrath S.L., Cheng C., Xie J., Heppenstall P.A., Stucky C.L., Mannsfeldt A.G., Brennan T.J., Drummond H.A., Qiao J., Benson C.J., Tarr D.E., Hrstka R.F., Yang B., Williamson R.A., and Welsh M.J. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407 (2000) 1007-1011
43. Roza C., Puel J.L., Kress M., Baron A., Diochot S., Lazdunski M., and Waldmann R. Knockout of the ASIC2 channel in mice does not impair cutaneous mechanosensation, visceral mechanonociception and hearing. J Physiol 558 (2004) 659-669
44. Shigematsu Y., Nakai A., Kuriyama M., Kikawa Y., Konishi I., Sudo M., and Itokawa Y. Delayed auditory brainstem response in thiamin-deficient rats. J Nutr Sci Vitaminol (Tokyo) 36 (1990) 209-215
45. Siesjo B.K. Acidosis and ischemic brain damage. Neurochem Pathol 9 (1988) 31-88
46. Siesjo B.K., von Hanwehr R., Nergelius G., Nevander G., and Ingvar M. Extra- and intracellular pH in the brain during seizures and in the recovery period following the arrest of seizure activity. J Cereb Blood Flow Metab 5 (1985) 47-57
47. Siman R., Zhang C., Roberts V.L., Pitts-Kiefer A., and Neumar R.W. Novel surrogate markers for acute brain damage: cerebrospinal fluid levels correlate with severity of ischemic neurodegeneration in the rat. J Cereb Blood Flow Metab 25 (2005) 1433-1444
48. Tang Z.Q., Lu Y.G., Zhou K.Q., Xu T.L., and Chen L. Amiloride attenuates glycine-induced currents in cultured neurons of rat inferior colliculus. Biochem Biophys Res Commun 350 (2006) 900-904
49. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., and Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21 (1998) 531-543
50. Ugawa S. Identification of sour-taste receptor genes. Anat Sci Int 78 (2003) 205-210
51. Ugawa S., Ueda T., Ishida Y., Nishigaki M., Shibata Y., and Shimada S. Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J Clin Invest 110 (2002) 1185-1190
52. Ugawa S., Inagaki A., Yamamura H., Ueda T., Ishida Y., Kajita K., Shimizu H., and Shimada S. Acid-sensing ion channel-1b in the stereocilia of mammalian cochlear hair cells. Neuroreport 17 (2006) 1235-1239
53. Varming T. Proton-gated ion channels in cultured mouse cortical neurons. Neuropharmacology 38 (1999) 1875-1881
54. Voilley N., de Weille J., Mamet J., and Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci 21 (2001) 8026-8033
55. Vortmeyer A.O., and Colmant H.J. Differentiation between brain lesions in experimental thiamine deficiency. Virchows Arch A Pathol Anat Histopathol 414 (1988) 61-67
56. Vukicevic M., and Kellenberger S. Modulatory effects of acid-sensing ion channels on action potential generation in hippocampal neurons. Am J Physiol Cell Physiol 287 (2004) C682-C690
57. Waldmann R., and Lazdunski M. H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol 8 (1998) 418-424
58. Waldmann R., Champigny G., Voilley N., Lauritzen I., and Lazdunski M. The mammalian degenerin MDEG, an amiloride-sensitive cation channel activated by mutations causing neurodegeneration in Caenorhabditis elegans. J Biol Chem 271 (1996) 10433-10436
59. Waldmann R., Champigny G., Bassilana F., Heurteaux C., and Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature 386 (1997) 173-177
60. + channel specific for sensory neurons. J Biol Chem 272 (1997) 20975-20978
61. Waldmann R., Champigny G., Lingueglia E., De Weille J.R., Heurteaux C., and Lazdunski M. H(+)-gated cation channels. Ann N Y Acad Sci 868 (1999) 67-76
62. Wang W., Duan B., Xu H., Xu L., and Xu T.L. Calcium-permeable acid-sensing ion channel is a molecular target of the neurotoxic metal ion lead. J Biol Chem 281 (2006) 2497-2505
63. Wemmie J.A., Askwith C.C., Lamani E., Cassell M.D., Freeman Jr. J.H., and Welsh M.J. Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci 23 (2003) 5496-5502
64. Wemmie J.A., Coryell M.W., Askwith C.C., Lamani E., Leonard A.S., Sigmund C.D., and Welsh M.J. Overexpression of acid-sensing ion channel 1a in transgenic mice increases acquired fear-related behavior. Proc Natl Acad Sci U S A 101 (2004) 3621-3626
65. Wemmie J.A., Chen J., Askwith C.C., Hruska-Hageman A.M., Price M.P., Nolan B.C., Yoder P.G., Lamani E., Hoshi T., Freeman Jr. J.H., and Welsh M.J. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34 (2002) 463-477
66. Wu L.J., Duan B., Mei Y.D., Gao J., Chen J.G., Zhuo M., Xu L., Wu M., and Xu T.L. Characterization of acid-sensing ion channels in dorsal horn neurons of rat spinal cord. J Biol Chem 279 (2004) 43716-43724
67. Xiong Z.G., Zhu X.M., Chu X.P., Minami M., Hey J., Wei W.L., MacDonald J.F., Wemmie J.A., Price M.P., Welsh M.J., and Simon R.P. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118 (2004) 687-698
68. Yermolaieva O., Leonard A.S., Schnizler M.K., Abboud F.M., and Welsh M.J. Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc Natl Acad Sci U S A 101 (2004) 6752-6757