Acid-sensing ion channel 3 in retinal function and survival

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 5, 2009, Pages 2417-2426

  Ettaiche, Mohammed ^a   Deval, Emmanuel ^a   Pagnotta, Sophie ^b   Lazdunski, Michel ^a   Lingueglia, Eric ^a  

^a INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b Universite Co te d'Azur Parc Valrose   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 3; GLIAL FIBRILLARY ACIDIC PROTEIN; UNCLASSIFIED DRUG; ASIC3 PROTEIN, MOUSE; SODIUM CHANNEL;

A WAVE; AGE DISTRIBUTION; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B WAVE; CELL CULTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; HISTOLOGY; IMMUNOLOCALIZATION; KNOCKOUT MOUSE; MALE; MICROSCOPY; MOUSE; MUELLER CELL; NICK END LABELING; NIGHT VISION; NONHUMAN; OSCILLATORY POTENTIAL; PATCH CLAMP; PHOTORECEPTOR INNER SEGMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA; RETINA AMACRINE CELL; RETINA DEGENERATION; RETINA FUNCTION; RETINA GANGLION CELL; RETINA ROD; RETINA SURVIVAL; RETINAL STRUCTURE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL SURVIVAL; DARK ADAPTATION; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; MOUSE MUTANT; PHOTOTRANSDUCTION; PHYSIOLOGY; RETINA HORIZONTAL NERVE CELL; RETINA ROD INNER SEGMENT;

AMACRINE CELLS; ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; DARK ADAPTATION; ELECTRORETINOGRAPHY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOENZYME TECHNIQUES; IN SITU NICK-END LABELING; LIGHT SIGNAL TRANSDUCTION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; RETINAL GANGLION CELLS; RETINAL HORIZONTAL CELLS; RETINAL PHOTORECEPTOR CELL INNER SEGMENT; SODIUM CHANNELS;

EID: 65549122579     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-3028     Document Type: Article

References (61)

1. Kleinschmidt J. Signal transmission at the photoreceptor synapse: role of calcium ions and protons. Ann N Y Acad Sci. 1991;635:468-470.
2. Harsanyi K, Mangel SC. Modulation of cone to horizontal cell transmission by calcium and pH in the fish retina. Vis Neurosci. 1993;10:81-91.
3. Barnes S, Merchant V, Mahmud F. Modulation of transmission gain by protons at the photoreceptor output synapse. Proc Natl Acad Sci U S A. 1993;90:10081-10085.
4. Gedney C, Ostroy SE. Hydrogen ion effects of the vertebrate photoreceptor: the pK's of ionizable groups affecting cell permeability. Arch Biochem Biophys. 1978;188:105-113.
5. Liebman PA, Mueller P, Pugh EN Jr. Protons suppress the dark current of frog retinal rods. J Physiol. 1984;347:85-110.
6. Meyertholen EP, Wilson MJ, Ostroy SE. The effects of HEPES, bicarbonate and calcium on the cGMP content of vertebrate rod photoreceptors and the isolated electrophysiological effects of cGMP and calcium. Vision Res. 1986;26:521-533.
7. 2 current in mammalian cone photoreceptors. Neuron. 2001;32: 1107-1117.
8. Hosoi N, Arai I, Tachibana M. Group III metabotropic glutamate receptors and exocytosed protons inhibit L-type calcium currents in cones but not in rods. J Neurosci. 2005;25:4062-4072.
9. Dmitriev AV, Mangel SC. Circadian clock regulation of pH in the rabbit retina. J Neurosci. 2001;21:2897-2902.
10. Brockway LM, Zhou ZH, Bubien JK, Jovov B, Benos DJ, Keyser KT. Rabbit retinal neurons and glia express a variety of ENaC/DEG subunits. Am J Physiol Cell Physiol. 2002;283:C126-C134.
11. Maubaret C, Delettre C, Sola S, Hamel CP. Identification of preferentially expressed mRNAs in retina and cochlea. DNA Cell Biol. 2002;21:781-791.
12. Ettaiche M, Guy N, Hofman P, Lazdunski M, Waldmann R. Acid-sensing ion channel 2 is important for retinal function and protects against light-induced retinal degeneration. J Neurosci. 2004;24:1005-1012.
13. Ettaiche M, Deval E, Cougnon M, Lazdunski M, Voilley N. Silencing acid-sensing ion channel 1a alters cone-mediated retinal function. J Neurosci. 2006;26:5800-5809.
14. Brockway LM, Benos DJ, Keyser KT, Kraft TW. Blockade of amiloride-sensitive sodium channels alters multiple components of the mammalian electroretinogram. Vis Neurosci. 2005;22:143-151.
15. Lilley S, LeTissier P, Robbins J. The discovery and characterization of a proton-gated sodium current in rat retinal ganglion cells. J Neurosci. 2004;24:1013-1022.
16. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature. 1997;386:173-177.
17. Lingueglia E. Acid-sensing ion channels in sensory perception. J Biol Chem. 2007;282:17325-17329.
18. Wemmie JA, Price MP, Welsh MJ. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci. 2006;29:578-586.
19. Krishtal O. The ASICs: signaling molecules? modulators? Trends Neurosci. 2003;26:477-483.
20. Lingueglia E, de Weille JR, Bassilana F, et al. A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglion cells. J Biol Chem. 1997;272:29778-29783.
21. Grunder S, Geissler HS, Bassler EL, Ruppersberg JP. A new member of acid-sensing ion channels from pituitary gland. Neuroreport. 2000;11:1607-1611.
22. Chen CC, England S, Akopian AN, Wood JN. A sensory neuron-specific, proton-gated ion channel. Proc Natl Acad Sci U S A. 1998;95:10240-10245.
23. Akopian AN, Chen CC, Ding Y, Cesare P, Wood JN. A new member of the acid-sensing ion channel family. Neuroreport. 2000;11: 2217-2222.
24. Bassler EL, Ngo-Anh TJ, Geisler HS, Ruppersberg JP, Grunder S. Molecular and functional characterization of acid-sensing ion chan- nel (ASIC) 1b. J Biol Chem. 2001;276:33782-33787.
25. Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature. 2007;449:316-323.
26. Benson CJ, Xie J, Wemmie JA, et al. Heteromultimers of DEG/EnaC subunits form H -gated channels in mouse sensory neurons. Proc Natl Acad Sci U S A. 2002;99:2338-2343.
27. Baron A, Voilley N, Lazdunski M, Lingueglia E. Acid sensing ion channels (ASICs) in dorsal spinal cord neurons. J Neurosci. 2008; 28:1498-1508.
28. Waldmann R, Bassilana F, de Weille J, Champigny G, Heurteaux C, Lazdunski M. Molecular cloning of a non-inactivating proton-gated Na channel specific for sensory neurons. J Biol Chem. 1997;272: 20975-20978.
29. Deval E, Noel J, Lay N, et al. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J. 2008;27:3047-3055.
30. Chen CC, Zimmer A, Sun WH, Hall J, Brownstein MJ, Zimmer A. A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc Natl Acad Sci U S A. 2002;99:8992-8997.
31. Price MP, McIlwrath SL, Xie J, et al. The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron. 2001;32:1071-1083.
32. Wultsch T, Painsipp E, Shahbazian A, et al. Deletion of the acid-sensing ion channel ASIC3 prevents gastritis-induced acid hyper- responsiveness of the stomach-brainstem axis. Pain. 2008;134: 245-253.
33. Molliver DC, Immke DC, Fierro L, Pare M, Rice FL, McCleskey EW. ASIC3, an acid-sensing ion channel, is expressed in metaborecep- tive sensory neurons. Mol Pain. 2005;1:35.
34. Jeon CJ, Strettoi E, Masland RH. The major cell populations of the mouse retina. J Neurosci. 1998;18:8936-8946.
35. Perez De Sevilla Muller L, Shelley J, Weiler R. Displaced amacrine cells of the mouse retina. J Comp Neurol. 2007;505:177-189.
36. Toda K, Bush RA, Humphries P, Sieving PA. The electroretinogram of the rhodopsin knockout mouse. Vis Neurosci. 1999;16:391-398.
37. Bignami A, Dahl D. The radial glia of Muller in the rat retina and their response to injury: an immunofluorescence study with anti- bodies to the glial fibrillary acidic (GFA) protein. Exp Eye Res. 1979;28:63-69.
38. Eisenfeld AJ, Bunt-Milam AH, Sarthy PV. Muller cell expression of glial fibrillary acidic protein after genetic and experimental photoreceptor degeneration in the rat retina. Invest Ophthalmol Vis Sci. 1984;25:1321-1328.
39. Hong DH, Pawlyk BS, Shang J, Sandberg MA, Berson EL, Li T. A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc Natl Acad Sci USA.2000;97:3649-3654.
40. Reme CE, Grimm C, Hafezi F, Marti A, Wenzel A. Apoptotic cell death in retinal degenerations. Prog Retin Eye Res. 1998;17:443-464.
41. Green CB, Cahill GM, Besharse JC. Regulation of tryptophan hydroxylase expression by a retinal circadian oscillator in vitro. Brain Res. 1995;677:283-290.
42. de Weille JR, Bassilana F, Lazdunski M, Waldmann R. Identification, functional expression and chromosomal localisation of a sustained human proton-gated cation channel. FEBS Lett. 1998;433:257-260.
43. Yagi J, Wenk HN, Naves LA, McCleskey EW. Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ Res. 2006;99:501-509.
44. Immke DC, McCleskey EW. Lactate enhances the acid-sensing Na channel on ischemia-sensing neurons. Nat Neurosci. 2001;4:869-870.
45. Poitry-Yamate CL, Poitry S, Tsacopoulos M. Lactate released by Muller glial cells is metabolized by photoreceptors from mamma- lian retina. J Neurosci. 1995;15:5179-5191.
46. Cadiou H, Studer M, Jones NG, et al. Modulation of acid-sensing ion channel activity by nitric oxide. J Neurosci. 2007;27:13251-13260.
47. Goldstein IM, Ostwald P, Roth S. Nitric oxide: a review of its role in retinal function and disease. Vision Res. 1996;36:2979-2994.
48. Hagins WA, Penn RD, Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970;10:380-412.
49. Pinto LH, Enroth-Cugell C. Tests of the mouse visual system. Mamm Genome. 2000;11:531-536.
50. Ziemann AE, Schnizler MK, Albert GW, et al. Seizure termination by acidosis depends on ASIC1a. Nat Neurosci. 2008;11:816-822.
51. Davis PK, Carlini WG, Ransom BR, Black JA, Waxman SG. Carbonic anhydrase activity develops postnatally in the rat optic nerve. Brain Res. 1987;428:291-298.
52. Palmer MJ, Hull C, Vigh J, von Gersdorff H. Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J Neurosci. 2003;23:11332-11341.
53. Wachtmeister L. Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res. 1998;17:485-521.
54. Peachey NS, Roveri L, Messing A, McCall MA. Functional consequences of oncogene-induced horizontal cell degeneration in the retinas of transgenic mice. Vis Neurosci. 1997;14:627-632.
55. May CA, Mittag T. Neuronal nitric oxide synthase (nNOS) positive retinal amacrine cells are altered in the DBA/2NNia mouse, a murine model for angle-closure glaucoma. J Glaucoma. 2004;13: 496-499.
56. El-Amraoui A, Petit C. Usher I syndrome: unravelling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells. J Cell Sci. 2005;118:4593-4603.
57. Liu X, Bulgakov OV, Darrow KN, et al. Usherin is required for maintenance of retinal photoreceptors and normal development of cochlear hair cells. Proc Natl Acad Sci U S A. 2007;104:4413-4418.
58. Hildebrand MS, de Silva MG, Klockars T, et al. Characterisation of DRASIC in the mouse inner ear. Hear Res. 2004;190:149-160.
59. Alvarez BV, Vithana EN, Yang Z, et al. Identification and characterization of a novel mutation in the carbonic anhydrase IV gene that causes retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2007; 48:3459-3468.
60. Simone JN, Whitacre MM. Effects of anti-inflammatory drugs following cataract extraction. Curr Opin Ophthalmol. 2001;12:63-67.
61. Voilley N, de Weille J, Mamet J, Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci. 2001;21:8026-8033.