Acid-Sensing Ion Channels and nociception in the peripheral and central nervous systems

Neuropharmacology

Volumn 94, Issue , 2015, Pages 49-57

  Deval, Emmanuel ^a,b,c   Lingueglia, Eric ^a,b,c  

^a INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c Laboratory of Excellence in Ion Channel Science and Therapeutics   (France)

Author keywords

ASICs; Ion channels; Pain; Sensory neurons

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 1; ACID SENSING ION CHANNEL 1A; ACID SENSING ION CHANNEL 1B; ACID SENSING ION CHANNEL 2; ACID SENSING ION CHANNEL 3; AMILORIDE; DICLOFENAC; MAMBALGIN; SEROTONIN; TOXIN; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; CENTRAL NERVOUS SYSTEM; HUMAN; NERVE CELL EXCITABILITY; NOCICEPTION; NONHUMAN; PAIN; PERIPHERAL NERVOUS SYSTEM; PERIPHERAL SENSORY NEURON; PRIMARY SENSORY NEURON; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SECONDARY SENSORY NEURON; SENSORY NERVE CELL; ANIMAL; METABOLISM; PHYSIOLOGY;

ACID SENSING ION CHANNELS; ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; NOCICEPTION; PERIPHERAL NERVOUS SYSTEM;

EID: 84961050726     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.02.009     Document Type: Review

References (121)

1. Alijevic, O., Kellenberger, S., Subtype-specific modulation of acid-sensing ion channel (ASIC) function by 2-guanidine-4-methylquinazoline. J. Biol. Chem. 287 (2012), 36059–36070.
2. Alvarez de la Rosa, D., Zhang, P., Shao, D., White, F., Canessa, C.M., Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 2326–2331.
3. Anzai, N., Deval, E., Schaefer, L., Friend, V., Lazdunski, M., Lingueglia, E., The multivalent PDZ domain-containing protein CIPP is a partner of acid-sensing ion channel 3 in sensory neurons. J. Biol. Chem. 277 (2002), 16655–16661.
4. Babinski, K., Le, K.T., Seguela, P., Molecular cloning and regional distribution of a human proton receptor subunit with biphasic functional properties. J. Neurochem. 72 (1999), 51–57.
5. Baron, A., Lingueglia, E., Pharmacology of acid-sensing ion channels – physiological and therapeutical perspectives. Neuropharmacology 94 (2015), 19–35, 10.1016/j.neuropharm.2015.01.005.
6. Baron, A., Voilley, N., Lazdunski, M., Lingueglia, E., Acid sensing ion channels in dorsal spinal cord neurons. J. Neurosci. 28 (2008), 1498–1508.
7. Baron, A., Waldmann, R., Lazdunski, M., ASIC-like, proton-activated currents in rat hippocampal neurons. J. Physiol. 539 (2002), 485–494.
8. Bassler, E.L., Ngo-Anh, T.J., Geisler, H.S., Ruppersberg, J.P., Grunder, S., Molecular and functional characterization of acid-sensing ion channel (ASIC) 1b. J. Biol. Chem. 276 (2001), 33782–33787.
9. Benson, C.J., Eckert, S.P., McCleskey, E.W., Acid-evoked currents in cardiac sensory neurons: a possible mediator of myocardial ischemic sensation. Circ. Res. 84 (1999), 921–928.
10. Berdiev, B.K., Xia, J., McLean, L.A., Markert, J.M., Gillespie, G.Y., Mapstone, T.B., Naren, A.P., Jovov, B., Bubien, J.K., Ji, H.L., Fuller, C.M., Kirk, K.L., Benos, D.J., Acid-sensing ion channels in malignant gliomas. J. Biol. Chem. 278 (2003), 15023–15034.
11. Birdsong, W.T., Fierro, L., Williams, F.G., Spelta, V., Naves, L.A., Knowles, M., Marsh-Haffner, J., Adelman, J.P., Almers, W., Elde, R.P., McCleskey, E.W., Sensing muscle ischemia: coincident detection of acid and ATP via interplay of two ion channels. Neuron 68 (2010), 739–749.
12. Blanchard, M.G., Rash, L.D., Kellenberger, S., Inhibition of voltage-gated Na(+) currents in sensory neurones by the sea anemone toxin APETx2. Br. J. Pharmacol. 165 (2012), 2167–2177.
13. Bohlen, C.J., Chesler, A.T., Sharif-Naeini, R., Medzihradszky, K.F., Zhou, S., King, D., Sanchez, E.E., Burlingame, A.L., Basbaum, A.I., Julius, D., A heteromeric Texas coral snake toxin targets acid-sensing ion channels to produce pain. Nature 479 (2011), 410–414.
14. Brockway, L.M., Zhou, Z.H., Bubien, J.K., Jovov, B., Benos, D.J., Keyser, K.T., Rabbit retinal neurons and glia express a variety of ENaC/DEG subunits. Am. J. Physiol. Cell. Physiol. 283 (2002), C126–C134.
15. Chen, C.C., England, S., Akopian, A.N., Wood, J.N., A sensory neuron-specific, proton-gated ion channel. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 10240–10245.
16. Chen, C.C., Zimmer, A., Sun, W.H., Hall, J., Brownstein, M.J., A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 8992–8997.
17. Chen, J.J., Vasko, M.R., Wu, X., Staeva, T.P., Baez, M., Zgombick, J.M., Nelson, D.L., Multiple subtypes of serotonin receptors are expressed in rat sensory neurons in culture. J. Pharmacol. Exp. Ther. 287 (1998), 1119–1127.
18. Coryell, M.W., Wunsch, A.M., Haenfler, J.M., Allen, J.E., Schnizler, M., Ziemann, A.E., Cook, M.N., Dunning, J.P., Price, M.P., Rainier, J.D., Liu, Z., Light, A.R., Langbehn, D.R., Wemmie, J.A., Acid-sensing ion channel-1a in the amygdala, a novel therapeutic target in depression-related behavior. J. Neurosci. 29 (2009), 5381–5388.
19. Delaunay, A., Gasull, X., Salinas, M., Noel, J., Friend, V., Lingueglia, E., Deval, E., Human ASIC3 channel dynamically adapts its activity to sense the extracellular pH in both acidic and alkaline directions. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 13124–13129.
20. Deval, E., Baron, A., Lingueglia, E., Mazarguil, H., Zajac, J.M., Lazdunski, M., Effects of neuropeptide SF and related peptides on acid sensing ion channel 3 and sensory neuron excitability. Neuropharmacology 44 (2003), 662–671.
21. Deval, E., Gasull, X., Noel, J., Salinas, M., Baron, A., Diochot, S., Lingueglia, E., Acid-sensing ion channels (ASICs): pharmacology and implication in pain. Pharmacol. Ther. 128 (2010), 549–558.
22. Deval, E., Noel, J., Gasull, X., Delaunay, A., Alloui, A., Friend, V., Eschalier, A., Lazdunski, M., Lingueglia, E., Acid-sensing ion channels in postoperative pain. J. Neurosci. 31 (2011), 6059–6066.
23. Deval, E., Noel, J., Lay, N., Alloui, A., Diochot, S., Friend, V., Jodar, M., Lazdunski, M., Lingueglia, E., ASIC3, a sensor of acidic and primary inflammatory pain. Embo J. 27 (2008), 3047–3055.
24. Deval, E., Salinas, M., Baron, A., Lingueglia, E., Lazdunski, M., ASIC2b-dependent regulation of ASIC3, an essential acid-sensing ion channel subunit in sensory neurons via the partner protein PICK-1. J. Biol. Chem. 279 (2004), 19531–19539.
25. Diochot, S., Baron, A., Rash, L.D., Deval, E., Escoubas, P., Scarzello, S., Salinas, M., Lazdunski, M., A new sea anemone peptide, APETx2, inhibits ASIC3, a major acid-sensitive channel in sensory neurons. Embo J. 23 (2004), 1516–1525.
26. Diochot, S., Baron, A., Salinas, M., Douguet, D., Scarzello, S., Dabert-Gay, A.S., Debayle, D., Friend, V., Alloui, A., Lazdunski, M., Lingueglia, E., Black mamba venom peptides target acid-sensing ion channels to abolish pain. Nature 490 (2012), 552–555.
27. Du, J., Reznikov, L.R., Price, M.P., Zha, X.M., Lu, Y., Moninger, T.O., Wemmie, J.A., Welsh, M.J., Protons are a neurotransmitter that regulates synaptic plasticity in the lateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 8961–8966.
28. Duan, B., Liu, D.S., Huang, Y., Zeng, W.Z., Wang, X., Yu, H., Zhu, M.X., Chen, Z.Y., Xu, T.L., PI3-kinase/Akt pathway-regulated membrane insertion of acid-sensing ion channel 1a underlies BDNF-induced pain hypersensitivity. J. Neurosci. 32 (2012), 6351–6363.
29. Duan, B., Wu, L.J., Yu, Y.Q., Ding, Y., Jing, L., Xu, L., Chen, J., 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.
30. Dube, G.R., Lehto, S.G., Breese, N.M., Baker, S.J., Wang, X., Matulenko, M.A., Honore, P., Stewart, A.O., Moreland, R.B., Brioni, J.D., Electrophysiological and in vivo characterization of A-317567, a novel blocker of acid sensing ion channels. Pain 117 (2005), 88–96.
31. Durham, P.L., Masterson, C.G., Two mechanisms involved in trigeminal CGRP release: implications for migraine treatment. Headache 53 (2013), 67–80.
32. Dusenkova, S., Ru, F., Surdenikova, L., Nassenstein, C., Hatok, J., Dusenka, R., Banovcin, P. Jr., Kliment, J., Tatar, M., Kollarik, M., The expression profile of acid-sensing ion channel (ASIC) subunits ASIC1a, ASIC1b, ASIC2a, ASIC2b, and ASIC3 in the esophageal vagal afferent nerve subtypes. Am. J. Physiol. Gastrointest. Liver Physiol. 307 (2014), G922–G930.
33. Dussor, G., ASICs as therapeutic targets for migraine. Neuropharmacology 94 (2015), 64–71, 10.1016/j.neuropharm2014.12.015.
34. Escoubas, P., De Weille, J.R., Lecoq, A., Diochot, S., Waldmann, R., Champigny, G., Moinier, D., Menez, A., Lazdunski, M., Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J. Biol. Chem. 275 (2000), 25116–25121.
35. Ettaiche, M., Deval, E., Cougnon, M., Lazdunski, M., Voilley, N., Silencing acid-sensing ion channel 1a alters cone-mediated retinal function. J. Neurosci. 26 (2006), 5800–5809.
36. Ettaiche, M., Deval, E., Pagnotta, S., Lazdunski, M., Lingueglia, E., Acid-sensing ion channel 3 in retinal function and survival. Invest. Ophthalmol. Vis. Sci. 50 (2009), 2417–2426.
37. 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. 24 (2004), 1005–1012.
38. Friese, M.A., Craner, M.J., Etzensperger, R., Vergo, S., Wemmie, J.A., Welsh, M.J., Vincent, A., Fugger, L., Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat. Med. 13 (2007), 1483–1489.
39. Fromy, B., Lingueglia, E., Sigaudo-Roussel, D., Saumet, J.L., Lazdunski, M., Asic3 is a neuronal mechanosensor for pressure-induced vasodilation that protects against pressure ulcers. Nat. Med. 18 (2012), 1205–1207.
40. Fukuda, T., Ichikawa, H., Terayama, R., Yamaai, T., Kuboki, T., Sugimoto, T., ASIC3-immunoreactive neurons in the rat vagal and glossopharyngeal sensory ganglia. Brain Res. 1081 (2006), 150–155.
41. Garcia-Anoveros, J., Derfler, B., Neville-Golden, J., Hyman, B.T., Corey, D.P., BNaC1 and BNaC2 constitute a new family of human neuronal sodium channels related to degenerins and epithelial sodium channels. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 1459–1464.
42. Garcia-Anoveros, J., Samad, T.A., Zuvela-Jelaska, L., Woolf, C.J., Corey, D.P., Transport and localization of the DEG/ENaC ion channel BNaC1alpha to peripheral mechanosensory terminals of dorsal root ganglia neurons. J. Neurosci. 21 (2001), 2678–2686.
43. Grifoni, S.C., Jernigan, N.L., Hamilton, G., Drummond, H.A., ASIC proteins regulate smooth muscle cell migration. Microvasc. Res. 75 (2008), 202–210.
44. Grunder, S., Geissler, H.S., Bassler, E.L., Ruppersberg, J.P., A new member of acid-sensing ion channels from pituitary gland. Neuroreport 11 (2000), 1607–1611.
45. Grunder, S., Push, M., Biophysical properties of acid-sensing ion channels (ASICs). Neuropharmacology 94 (2015), 9–18, 10.1016/j.neuropharm.2014.12.016.
46. Hattori, T., Chen, J., Harding, A.M., Price, M.P., Lu, Y., Abboud, F.M., Benson, C.J., ASIC2a and ASIC3 heteromultimerize to form pH-sensitive channels in mouse cardiac dorsal root ganglia neurons. Circ. Res. 105 (2009), 279–286.
47. Hildebrand, M.S., de Silva, M.G., Klockars, T., Rose, E., Price, M., Smith, R.J., McGuirt, W.T., Christopoulos, H., Petit, C., Dahl, H.H., Characterisation of DRASIC in the mouse inner ear. Hear. Res. 190 (2004), 149–160.
48. Holzer, P., Acid sensing by visceral afferent neurons. Acta Physiol. (Oxf), 2010.
49. Holzer, P., Acid-sensing ion channels in gastrointestinal function. Neuropharmacology 94 (2015), 72–79, 10.1016/j.neuropharm.2014.12.009.
50. Huang, C., Hu, Z.L., Wu, W.N., Yu, D.F., Xiong, Q.J., Song, J.R., Shu, Q., Fu, H., Wang, F., Chen, J.G., Existence and distinction of acid-evoked currents in rat astrocytes. Glia 58 (2010), 1415–1424.
51. Huang, S.J., Yang, W.S., Lin, Y.W., Wang, H.C., Chen, C.C., Increase of insulin sensitivity and reversal of age-dependent glucose intolerance with inhibition of ASIC3. Biochem. Biophys. Res. Commun. 371 (2008), 729–734.
52. Hughes, P.A., Brierley, S.M., Young, R.L., Blackshaw, L.A., Localization and comparative analysis of acid-sensing ion channel (ASIC1, 2, and 3) mRNA expression in mouse colonic sensory neurons within thoracolumbar dorsal root ganglia. J. Comp. Neurol. 500 (2007), 863–875.
53. Ikeuchi, M., Kolker, S.J., Burnes, L.A., Walder, R.Y., Sluka, K.A., Role of ASIC3 in the primary and secondary hyperalgesia produced by joint inflammation in mice. Pain 137 (2008), 662–669.
54. Ikeuchi, M., Kolker, S.J., Sluka, K.A., Acid-sensing ion channel 3 expression in mouse knee joint afferents and effects of carrageenan-induced arthritis. J. Pain 10 (2009), 336–342.
55. Immke, D.C., McCleskey, E.W., ASIC3: a lactic acid sensor for cardiac pain. ScientificWorldJournal 1 (2001), 510–512.
56. Immke, D.C., McCleskey, E.W., Lactate enhances the acid-sensing Na+ channel on ischemia-sensing neurons. Nat. Neurosci. 4 (2001), 869–870.
57. Izumi, M., Ikeuchi, M., Ji, Q., Tani, T., Local ASIC3 modulates pain and disease progression in a rat model of osteoarthritis. J. Biomed. Sci., 19, 2012, 77.
58. Jahr, H., van Driel, M., van Osch, G.J., Weinans, H., van Leeuwen, J.P., Identification of acid-sensing ion channels in bone. Biochem. Biophys. Res. Commun. 337 (2005), 349–354.
59. Jensen, J.E., Cristofori-Armstrong, B., Anangi, R., Rosengren, K.J., Lau, C.H., Mobli, M., Brust, A., Alewood, P.F., King, G.F., Rash, L.D., Understanding the molecular basis of toxin Promiscuity: the analgesic sea anemone peptide APETx2 Interacts with acid-sensing ion channel 3 and hERG channels via overlapping Pharmacophores. J. Med. Chem. 57 (2014), 9195–9203.
60. Jones, N.G., Slater, R., Cadiou, H., McNaughton, P., McMahon, S.B., Acid-induced pain and its modulation in humans. J. Neurosci. 24 (2004), 10974–10979.
61. Kang, S., Jang, J.H., Price, M.P., Gautam, M., Benson, C.J., Gong, H., Welsh, M.J., Brennan, T.J., Simultaneous disruption of mouse ASIC1a, ASIC2 and ASIC3 genes enhances cutaneous mechanosensitivity. PLoS One, 7, 2012, e35225.
62. Karczewski, J., Spencer, R.H., Garsky, V.M., Liang, A., Leitl, M.D., Cato, M.J., Cook, S.P., Kane, S., Urban, M.O., Reversal of acid-induced and inflammatory pain by the selective ASIC3 inhibitor, APETx2. Br. J. Pharmacol. 161 (2010), 950–960.
63. Kolker, S.J., Walder, R.Y., Usachev, Y., Hillman, J., Boyle, D.L., Firestein, G.S., Sluka, K.A., Acid-sensing ion channel 3 expressed in type B synoviocytes and chondrocytes modulates hyaluronan expression and release. Ann. Rheum. Dis. 69 (2010), 903–909.
64. Kreple, C.J., Lu, Y., Taugher, R.J., Schwager-Gutman, A.L., Du, J., Stump, M., Wang, Y., Ghobbeh, A., Fan, R., Cosme, C.V., Sowers, L.P., Welsh, M.J., Radley, J.J., LaLumiere, R.T., Wemmie, J.A., Acid-sensing ion channels contribute to synaptic transmission and inhibit cocaine-evoked plasticity. Nat. Neurosci. 17 (2014), 1083–1091.
65. Krishtal, O.A., Receptor for protons: first observations of acid-sensing ion channels. Neuropharmacology 94 (2015), 4–8, 10.1016/j.neuropharm.2014.12.014.
66. Krishtal, O.A., Pidoplichko, V.I., Receptor for protons in the membrane of sensory neurons. Brain Res. 214 (1981), 150–154.
67. Krishtal, O.A., Pidoplichko, V.I., A receptor for protons in the membrane of sensory neurons may participate in nociception. Neuroscience 6 (1981), 2599–2601.
68. Krishtal, O.A., Pidoplichko, V.I., A “receptor” for protons in small neurons of trigeminal ganglia: possible role in nociception. Neurosci. Lett. 24 (1981), 243–246.
69. Leffler, A., Monter, B., Koltzenburg, M., The role of the capsaicin receptor TRPV1 and acid-sensing ion channels (ASICS) in proton sensitivity of subpopulations of primary nociceptive neurons in rats and mice. Neuroscience 139 (2006), 699–709.
70. Li, W.G., Yu, Y., Zhang, Z.D., Cao, H., Xu, T.L., ASIC3 channels integrate agmatine and multiple inflammatory signals through the nonproton ligand sensing domain. Mol. Pain, 6, 2010, 88.
71. Lilley, S., LeTissier, P., Robbins, J., The discovery and characterization of a proton-gated sodium current in rat retinal ganglion cells. J. Neurosci. 24 (2004), 1013–1022.
72. Lin, S.H., Sun, W.H., Chen, C.C., Genetic exploration of the role of acid-sensing ion channels. Neuropharmacology, 2015, 10.1016/j.neuropharm.2014.12.011.
73. Lingueglia, E., de Weille, J.R., Bassilana, F., Heurteaux, C., Sakai, H., Waldmann, R., Lazdunski, M., A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglion cells. J. Biol. Chem. 272 (1997), 29778–29783.
74. Liu, L., Simon, S.A., Acidic stimuli activates two distinct pathways in taste receptor cells from rat fungiform papillae. Brain Res. 923 (2001), 58–70.
75. Mamet, J., Baron, A., Lazdunski, M., Voilley, N., Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J. Neurosci. 22 (2002), 10662–10670.
76. Mazzuca, M., Heurteaux, C., Alloui, A., Diochot, S., Baron, A., Voilley, N., Blondeau, N., Escoubas, P., Gelot, A., Cupo, A., Zimmer, A., Zimmer, A.M., Eschalier, A., Lazdunski, M., A tarantula peptide against pain via ASIC1a channels and opioid mechanisms. Nat. Neurosci. 10 (2007), 943–945.
77. Meng, Q.Y., Wang, W., Chen, X.N., Xu, T.L., Zhou, J.N., Distribution of acid-sensing ion channel 3 in the rat hypothalamus. Neuroscience 159 (2009), 1126–1134.
78. Mogil, J.S., Breese, N.M., Witty, M.F., Ritchie, J., Rainville, M.L., Ase, A., Abbadi, N., Stucky, C.L., Seguela, P., Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J. Neurosci. 25 (2005), 9893–9901.
79. Molliver, D.C., Immke, D.C., Fierro, L., Pare, M., Rice, F.L., McCleskey, E.W., ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol. Pain, 1, 2005, 35.
80. Morgan, D.L., Borys, D.J., Stanford, R., Kjar, D., Tobleman, W., Texas coral snake (Micrurus tener) bites. South Med. J. 100 (2007), 152–156.
81. Omerbasic, D., Shuhmadrer, L.N., Bernal Sierra, Y.A., Smith, E.S., Lewin, E.R., ASICs and mammalian mechanoreceptor function. Neuropharmacology, 2015, 10.1016/j.neuropharm.2014.12.007.
82. Page, A.J., Brierley, S.M., Martin, C.M., Martinez-Salgado, C., Wemmie, J.A., Brennan, T.J., Symonds, E., Omari, T., Lewin, G.R., Welsh, M.J., Blackshaw, L.A., The ion channel ASIC1 contributes to visceral but not cutaneous mechanoreceptor function. Gastroenterology 127 (2004), 1739–1747.
83. Page, A.J., Brierley, S.M., Martin, C.M., Price, M.P., Symonds, E., Butler, R., Wemmie, J.A., Blackshaw, L.A., Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 54 (2005), 1408–1415.
84. Peigneur, S., Beress, L., Moller, C., Mari, F., Forssmann, W.G., Tytgat, J., A natural point mutation changes both target selectivity and mechanism of action of sea anemone toxins. FASEB J. 26 (2012), 5141–5151.
85. Peng, B.G., Ahmad, S., Chen, S., Chen, P., Price, M.P., 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.
86. Poirot, O., Berta, T., Decosterd, I., Kellenberger, S., Distinct ASIC currents are expressed in rat putative nociceptors and are modulated by nerve injury. J. Physiol. 576 (2006), 215–234.
87. 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., Welsh, M.J., The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407 (2000), 1007–1011.
88. Price, M.P., McIlwrath, S.L., Xie, J., Cheng, C., Qiao, J., Tarr, D.E., Sluka, K.A., Brennan, T.J., Lewin, G.R., Welsh, M.J., The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32 (2001), 1071–1083.
89. Price, M.P., Snyder, P.M., Welsh, M.J., Cloning and expression of a novel human brain Na+ channel. J. Biol. Chem. 271 (1996), 7879–7882.
90. Qiu, F., Qiu, C.Y., Liu, Y.Q., Wu, D., Li, J.D., Hu, W.P., Potentiation of acid-sensing ion channel activity by the activation of 5-HT(2) receptors in rat dorsal root ganglion neurons. Neuropharmacology 63 (2012), 494–500.
91. Richter, T.A., Dvoryanchikov, G.A., Roper, S.D., Chaudhari, N., Acid-sensing ion channel-2 is not necessary for sour taste in mice. J. Neurosci. 24 (2004), 4088–4091.
92. Salinas, M., Lazdunski, M., Lingueglia, E., Structural elements for the generation of sustained currents by the acid pain sensor ASIC3. J. Biol. Chem. 284 (2009), 31851–31859.
93. Sluka, K.A., Gregory, N.S., The dichotomized role for acid-sensing ion channels in musculoskeletal pain and inflammation. Neuropharmacology, 2015, 10.1016/j.neuropharm.2014.12.013.
94. Sluka, K.A., Price, M.P., Breese, N.M., Stucky, C.L., Wemmie, J.A., Welsh, M.J., Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 106 (2003), 229–239.
95. Sluka, K.A., Radhakrishnan, R., Benson, C.J., Eshcol, J.O., Price, M.P., Babinski, K., Audette, K.M., Yeomans, D.C., Wilson, S.P., ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain 129 (2007), 102–112.
96. Smith, E.S., Cadiou, H., McNaughton, P.A., Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action. Neuroscience 145 (2007), 686–698.
97. Sole-Magdalena, A., Revuelta, E.G., Menenez-Diaz, I., Calavia, M.G., Cobo, T., Garcia-Suarez, O., Perez-Pinera, P., De Carlos, F., Cobo, J., Vega, J.A., Human odontoblasts express transient receptor protein and acid-sensing ion channel mechanosensor proteins. Microsc. Res. Tech. 74 (2011), 457–463.
98. Su, X., Li, Q., Shrestha, K., Cormet-Boyaka, E., Chen, L., Smith, P.R., Sorscher, E.J., Benos, D.J., Matalon, S., Ji, H.L., Interregulation of proton-gated Na(+) channel 3 and cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 281 (2006), 36960–36968.
99. Sugiura, T., Dang, K., Lamb, K., Bielefeldt, K., Gebhart, G.F., Acid-sensing properties in rat gastric sensory neurons from normal and ulcerated stomach. J. Neurosci. 25 (2005), 2617–2627.
100. Sutherland, S.P., Benson, C.J., Adelman, J.P., McCleskey, E.W., Acid-sensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 711–716.
101. Tan, Z.Y., Lu, Y., Whiteis, C.A., Benson, C.J., Chapleau, M.W., Abboud, F.M., Acid-sensing ion channels contribute to transduction of extracellular acidosis in rat carotid body glomus cells. Circ. Res. 101 (2007), 1009–1019.
102. Ugawa, S., Inagaki, A., Yamamura, H., Ueda, T., Ishida, Y., Kajita, K., Shimizu, H., Shimada, S., Acid-sensing ion channel-1b in the stereocilia of mammalian cochlear hair cells. Neuroreport 17 (2006), 1235–1239.
103. Ugawa, S., Ueda, T., Ishida, Y., Nishigaki, M., Shibata, Y., Shimada, S., Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J. Clin. Invest. 110 (2002), 1185–1190.
104. Ugawa, S., Yamamoto, T., Ueda, T., Ishida, Y., Inagaki, A., Nishigaki, M., Shimada, S., Amiloride-insensitive currents of the acid-sensing ion channel-2a (ASIC2a)/ASIC2b heteromeric sour-taste receptor channel. J. Neurosci. 23 (2003), 3616–3622.
105. Vidt, D.G., Mechanism of action, pharmacokinetics, adverse effects, and therapeutic uses of amiloride hydrochloride, a new potassium-sparing diuretic. Pharmacotherapy 1 (1981), 179–187.
106. 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. 21 (2001), 8026–8033.
107. Walder, R.Y., Gautam, M., Wilson, S.P., Benson, C.J., Sluka, K.A., Selective targeting of ASIC3 using artificial miRNAs inhibits primary and secondary hyperalgesia after muscle inflammation. Pain 152 (2011), 2348–2356.
108. 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. 272 (1997), 20975–20978.
109. Waldmann, R., Champigny, G., Bassilana, F., Heurteaux, C., Lazdunski, M., A proton-gated cation channel involved in acid-sensing. Nature 386 (1997), 173–177.
110. Waldmann, R., Champigny, G., Voilley, N., Lauritzen, I., 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.
111. Wang, X., Li, W.G., Yu, Y., Xiao, X., Cheng, J., Zeng, W.Z., Peng, Z., Xi Zhu, M., Xu, T.L., Serotonin facilitates peripheral pain sensitivity in a manner that depends on the nonproton ligand sensing domain of ASIC3 channel. J. Neurosci. 33 (2013), 4265–4279.
112. Wemmie, J.A., Askwith, C.C., Lamani, E., Cassell, M.D., Freeman, J.H. Jr., 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.
113. 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, J.H. Jr., Welsh, M.J., The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34 (2002), 463–477.
114. Wu, L.J., Duan, B., Mei, Y.D., Gao, J., Chen, J.G., Zhuo, M., Xu, L., Wu, M., Xu, T.L., Characterization of acid-sensing ion channels in dorsal horn neurons of rat spinal cord. J. Biol. Chem. 279 (2004), 43716–43724.
115. Yagi, J., Wenk, H.N., Naves, L.A., McCleskey, E.W., Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ. Res. 99 (2006), 501–509.
116. Yan, J., Edelmayer, R.M., Wei, X., De Felice, M., Porreca, F., Dussor, G., Dural afferents express acid-sensing ion channels: a role for decreased meningeal pH in migraine headache. Pain 152 (2011), 106–113.
117. Yan, J., Wei, X., Bischoff, C., Edelmayer, R.M., Dussor, G., pH-evoked dural afferent signaling is mediated by ASIC3 and is sensitized by mast cell mediators. Headache 53 (2013), 1250–1261.
118. Yen, Y.T., Tu, P.H., Chen, C.J., Lin, Y.W., Hsieh, S.T., Chen, C.C., Role of acid-sensing ion channel 3 in sub-acute-phase inflammation. Mol. Pain, 5, 2009, 1.
119. Young, G.T., Gutteridge, A., Fox, H.D., Wilbrey, A.L., Cao, L., Cho, L.T., Brown, A.R., Benn, C.L., Kammonen, L.R., Friedman, J.H., Bictash, M., Whiting, P., Bilsland, J.G., Stevens, E.B., Characterizing human stem cell-derived sensory neurons at the single-cell level reveals their ion channel expression and utility in pain research. Mol. Ther. 22 (2014), 1530–1543.
120. Yu, X.W., Hu, Z.L., Ni, M., Fang, P., Zhang, P.W., Shu, Q., Fan, H., Zhou, H.Y., Ni, L., Zhu, L.Q., Chen, J.G., Wang, F., Acid-sensing ion channels promote the inflammation and migration of cultured rat microglia. Glia, 2014.
121. Yu, Y., Chen, Z., Li, W.G., Cao, H., Feng, E.G., Yu, F., Liu, H., Jiang, H., Xu, T.L., A nonproton ligand sensor in the acid-sensing ion channel. Neuron 68 (2010), 61–72.