Acid-sensing ion channels: A novel therapeutic target for pain and anxiety

Current Pharmaceutical Design

Volumn 21, Issue 7, 2015, Pages 885-894

  Li, Wei Guang ^a   Xu, Tian Le ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Acid sensing ion channel; Anxiety; Inflammatory pain; Neuropathic pain; Nociception

Indexed keywords

ACID SENSING ION CHANNEL; PROTEIN ASIC1; PROTEIN ASIC2A; PROTEIN ASIC2B; PROTEIN ASIC3; UNCLASSIFIED DRUG;

ANXIETY DISORDER; ARTICLE; CENTRAL NERVOUS SYSTEM; DYNAMICS; GENE SILENCING; INFLAMMATORY PAIN; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PAIN; PERIPHERAL NERVOUS SYSTEM; PH; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANALGESIA; ANIMAL; ANXIETY; CHEMISTRY; DRUG DELIVERY SYSTEM; GENE TARGETING; GENETICS; HUMAN; METABOLISM; PROTEIN SECONDARY STRUCTURE; THERAPY; TRENDS;

ACID SENSING ION CHANNELS; ANIMALS; ANXIETY; DRUG DELIVERY SYSTEMS; GENE KNOCKDOWN TECHNIQUES; GENE TARGETING; HUMANS; PAIN; PAIN MANAGEMENT; PROTEIN STRUCTURE, SECONDARY;

EID: 84925866922     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612820666141027124506     Document Type: Article

References (148)

1. [1] Bonica JJ. The need of a taxonomy. Pain 1979; 6: 247-8.
2. [2] Woolf CJ, Bennett GJ, Doherty M, Dubner R, Kidd B, Koltzenburg M, Lipton R, Loeser JD, Payne R, Torebjork E. Towards a mechanism-based classification of pain? Pain 1998; 77: 227-9.
3. [3] Woolf CJ. What is this thing called pain? J Clin Invest 2010; 120: 3742-4.
4. [4] Davison GC. Abnormal psychology. Veronica Visentin: Toronto 2008.
5. [5] Zeng WZ, Xu TL. Proton production, regulation and pathophysiological roles in the mammalian brain. Neurosci Bull 2012; 28: 1-13.
6. [6] Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature 1997; 386: 173-7.
7. [7] Krishtal O. The ASICs: signaling molecules? Modulators? Trends Neurosci 2003; 26: 477-83.
8. [8] Wemmie JA, Price MP, Welsh MJ. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 2006; 29: 578-86.
9. [9] Kellenberger S, Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 2002; 82: 735-67.
10. [10] Grunder S, Geissler HS, Bassler EL, Ruppersberg JP. A new member of acid-sensing ion channels from pituitary gland. Neuroreport 2000; 11: 1607-11.
11. [11] Sakai H, Lingueglia E, Champigny G, Mattei MG, Lazdunski M. Cloning and functional expression of a novel degenerin-like Na+ channel gene in mammals. J Physiol 1999; 519 Pt 2: 323-33.
12. [12] Li WG, Xu TL. ASIC3 channels in multimodal sensory perception. ACS Chem Nurosci 2011; 2: 26-37.
13. [13] Wemmie JA, Taugher RJ, Kreple CJ. Acid-sensing ion channels in pain and disease. Nat Rev Neurosci 2013; 14: 461-71.
14. [14] Chen CC, Zimmer A, Sun WH, Hall J, Brownstein MJ. A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc Natl Acad Sci USA 2002; 99: 8992-7.
15. [15] Gautam M, Benson CJ, Sluka KA. Increased response of muscle sensory neurons to decreases in pH after muscle inflammation. Neuroscience 2010; 170: 893-900.
16. [16] Ikeuchi M, Kolker SJ, Burnes LA, Walder RY, Sluka KA. Role of ASIC3 in the primary and secondary hyperalgesia produced by joint inflammation in mice. Pain 2008; 137: 662-9.
17. [17] Ikeuchi M, Kolker SJ, Sluka KA. Acid-sensing ion channel 3 expression in mouse knee joint afferents and effects of carrageenaninduced arthritis. J Pain 2009; 10: 336-42.
18. [18] Sluka KA, Price MP, Breese NM, Stucky CL, Wemmie JA, Welsh MJ. Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 2003; 106: 229-39.
19. [19] Sluka KA, Radhakrishnan R, Benson CJ, et al. ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain 2007; 129: 102-12.
20. [20] Sluka KA, Winter OC, Wemmie JA. Acid-sensing ion channels: A new target for pain and CNS diseases. Curr Opin Drug Discov Devel 2009; 12: 693-704.
21. [21] Walder RY, Rasmussen LA, Rainier JD, Light AR, Wemmie JA, Sluka KA. ASIC1 and ASIC3 play different roles in the development of Hyperalgesia after inflammatory muscle injury. J Pain 2010; 11: 210-8.
22. [22] Yen YT, Tu PH, Chen CJ, Lin YW, Hsieh ST, Chen CC. Role of acid-sensing ion channel 3 in sub-acute-phase inflammation. Mol Pain 2009; 5: 1.
23. [23] Page AJ, Brierley SM, Martin CM, Hughes PA, Blackshaw LA. Acid sensing ion channels 2 and 3 are required for inhibition of visceral nociceptors by benzamil. Pain 2007; 133: 150-60.
24. [24] Deval E, Noel J, Lay N, et al. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J 2008; 27: 3047-55.
25. [25] Wultsch T, Painsipp E, Shahbazian A, et al. Deletion of the acidsensing ion channel ASIC3 prevents gastritis-induced acid hyperresponsiveness of the stomach-brainstem axis. Pain 2008; 134: 245-53.
26. [26] 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: 1071-83.
27. [27] Page AJ, Brierley SM, Martin CM, et al. Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 2005; 54: 1408-15.
28. [28] Lee CH, Sun SH, Lin SH, Chen CC. Role of the acid-sensing ion channel 3 in blood volume control. Circ J 2011; 75: 874-83.
29. [29] McCord JL, Tsuchimochi H, Kaufman MP. Acid-sensing ion channels contribute to the metaboreceptor component of the exercise pressor reflex. Am J Physiol Heart Circ Physiol 2009; 297: H443-9.
30. [30] 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: 501-9.
31. [31] Tan ZY, Lu Y, Whiteis CA, et al. Chemoreceptor hypersensitivity, sympathetic excitation, and overexpression of ASIC and TASK channels before the onset of hypertension in SHR. Circ Res 2010; 106: 536-45.
32. [32] Tan ZY, Lu Y, Whiteis CA, Benson CJ, Chapleau MW, Abboud FM. Acid-sensing ion channels contribute to transduction of extracellular acidosis in rat carotid body glomus cells. Circ Res 2007; 101: 1009-19.
33. [33] Sutherland SP, Cook SP, McCleskey EW. Chemical mediators of pain due to tissue damage and ischemia. Prog Brain Res 2000; 129: 21-38.
34. [34] Sutherland SP, Benson CJ, Adelman JP, McCleskey EW. Acidsensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons. Proc Natl Acad Sci USA 2001; 98: 711-6.
35. [35] Immke DC, McCleskey EW. ASIC3: a lactic acid sensor for cardiac pain. ScientificWorldJournal 2001; 1: 510-2.
36. [36] Birdsong WT, Fierro L, Williams FG, et al. Sensing muscle ischemia: coincident detection of acid and ATP via interplay of two ion channels. Neuron 2010; 68: 739-49.
37. [37] Benson CJ, Eckert SP, McCleskey EW. Acid-evoked currents in cardiac sensory neurons: A possible mediator of myocardial ischemic sensation. Cir Res 1999; 84: 921-8.
38. [38] Ettaiche M, Deval E, Pagnotta S, Lazdunski M, Lingueglia E. Acid-sensing ion channel 3 in retinal function and survival. Invest Ophthalmol Vis Sci 2009; 50: 2417-26.
39. [39] Mercado F, Lopez IA, Acuna D, Vega R, Soto E. Acid-sensing ionic channels in the rat vestibular endorgans and ganglia. J Neurophysiol 2006; 96: 1615-24.
40. [40] Meng QY, Wang W, Chen XN, Xu TL, Zhou JN. Distribution of acid-sensing ion channel 3 in the rat hypothalamus. Neuroscience 2009; 159: 1126-34.
41. [41] Wu WL, Wang CH, Huang EY, Chen CC. Asic3(-/-) female mice with hearing deficit affects social development of pups. PLoS One 2009; 4: e6508.
42. [42] Chen CH, Hsu YT, Chen CC, Huang RC. Acid-sensing ion channels in neurones of the rat suprachiasmatic nucleus. J Physiol 2009; 587: 1727-37.
43. [43] Weng JY, Lin YC, Lien CC. Cell type-specific expression of acidsensing ion channels in hippocampal interneurons. J Neurosci 2010; 30: 6548-58.
44. [44] Petroff EY, Price MP, Snitsarev V, et al. Acid-sensing ion channels interact with and inhibit BK K+ channels. Proc Natl Acad Sci USA 2008; 105: 3140-4.
45. [45] Petroff E, Snitsarev V, Gong H, Abboud FM. Acid sensing ion channels regulate neuronal excitability by inhibiting BK potassium channels. Biochem Biophys Res Commun 2012; 426: 511-5.
46. [46] Wemmie JA, Chen J, Askwith CC, et al. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 2002; 34: 463-77.
47. [47] Cho JH, Askwith CC. Presynaptic release probability is increased in hippocampal neurons from ASIC1 knockout mice. J Neurophysiol 2008; 99: 426-41.
48. [48] Wu PY, Huang YY, Chen CC, et al. Acid-sensing ion channel-1a is not required for normal hippocampal LTP and spatial memory. J Neurosci 2013; 33: 1828-32.
49. [49] Du J, Reznikov LR, Price MP, et al. Protons are a neurotransmitter that regulates synaptic plasticity in the lateral amygdala. Proc Natl Acad Sci USA 2014; 111: 8961-6.
50. [50] Wemmie JA, Askwith CC, Lamani E, Cassell MD, Freeman JH, Jr., Welsh MJ. Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci 2003; 23: 5496-502.
51. [51] Wemmie JA, Coryell MW, Askwith CC, et al. Overexpression of acid-sensing ion channel 1a in transgenic mice increases acquired fear-related behavior. Proc Natl Acad Sci USA 2004; 101: 3621-6.
52. [52] Coryell MW, Ziemann AE, Westmoreland PJ, et al. Targeting ASIC1a reduces innate fear and alters neuronal activity in the fear circuit. Biol Psychiatry 2007; 62: 1140-8.
53. [53] Coryell MW, Wunsch AM, Haenfler JM, et al. Restoring Acidsensing ion channel-1a in the amygdala of knock-out mice rescues fear memory but not unconditioned fear responses. J Neurosci 2008; 28: 13738-41.
54. [54] Ziemann AE, Allen JE, Dahdaleh NS, et al. The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell 2009; 139: 1012-21.
55. [55] Vralsted VC, Price MP, Du J, et al. Expressing acid-sensing ion channel 3 in the brain alters acid-evoked currents and impairs fear conditioning. Genes Brain Behav 2011; 10: 444-50.
56. [56] Ziemann AE, Schnizler MK, Albert GW, et al. Seizure termination by acidosis depends on ASIC1a. Nat Neurosci 2008; 11: 816-22.
57. [57] Gao J, Duan B, Wang DG, et al. Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron 2005; 48: 635-46.
58. [58] Duan B, Wang YZ, Yang T, et al. Extracellular spermine exacerbates ischemic neuronal injury through sensitization of ASIC1a channels to extracellular acidosis. J Neurosci 2011; 31: 2101-12.
59. [59] Xiong ZG, Zhu XM, Chu XP, et al. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 2004; 118: 687-98.
60. [60] Xiong ZG, Chu XP, Simon RP. Ca2+-permeable acid-sensing ion channels and ischemic brain injury. J Mem Biol 2006; 209: 59-68.
61. [61] Hey JG, Chu XP, Seeds J, Simon RP, Xiong ZG. Extracellular zinc protects against acidosis-induced injury of cells expressing Ca2+-permeable acid-sensing ion channels. Stroke 2007; 38: 670-3.
62. [62] Pignataro G, Simon RP, Xiong ZG. Prolonged activation of ASIC1a and the time window for neuroprotection in cerebral ischaemia. Brain 2007; 130: 151-8.
63. [63] Xiong ZG, Chu XP, Simon RP. Acid sensing ion channels--novel therapeutic targets for ischemic brain injury. Front Biosci 2007; 12: 1376-86.
64. [64] Chai S, Li M, Branigan D, Xiong ZG, Simon RP. Activation of acid-sensing ion channel 1a (ASIC1a) by surface trafficking. J Biol Chem 2010; 285: 13002-11.
65. [65] Li M, Inoue K, Branigan D, et al. Acid-sensing ion channels in acidosis-induced injury of human brain neurons. J Cereb Blood Flow Metab 2010; 30: 1247-60.
66. [66] Wang YZ, Xu TL. Acidosis, acid-sensing ion channels, and neuronal cell death. Mol Neurobiol 2011; 44: 350-8.
67. [67] Wu LJ, Duan B, Mei YD, et al. Characterization of acid-sensing ion channels in dorsal horn neurons of rat spinal cord. J Bio Chem 2004; 279: 43716-24.
68. [68] Duan B, Wu LJ, Yu YQ, et al. Upregulation of acid-sensing ion channel ASIC1a in spinal dorsal horn neurons contributes to inflammatory pain hypersensitivity. J Neurosci 2007; 27: 11139-48.
69. [69] Xu TL, Duan B. Calcium-permeable acid-sensing ion channel in nociceptive plasticity: a new target for pain control. Prog Neurobiol 2009; 87: 171-80.
70. [70] Mazzuca M, Heurteaux C, Alloui A, et al. A tarantula peptide against pain via ASIC1a channels and opioid mechanisms. Nat Neurosci 2007; 10: 943-5.
71. [71] Baron A, Voilley N, Lazdunski M, Lingueglia E. Acid sensing ion channels in dorsal spinal cord neurons. J Neurosci 2008; 28: 1498-508.
72. [72] Deval E, Noel J, Gasull X, et al. Acid-sensing ion channels in postoperative pain. J Neurosci 2011; 31: 6059-66.
73. [73] Diochot S, Baron A, Salinas M, et al. Black mamba venom peptides target acid-sensing ion channels to abolish pain. Nature 2012; 490: 552-5.
74. [74] Jiang Q, Wang CM, Fibuch EE, Wang JQ, Chu XP. Differential regulation of locomotor activity to acute and chronic cocaine administration by acid-sensing ion channel 1a and 2 in adult mice. Neuroscience 2013; 246: 170-8.
75. [75] Kreple CJ, Lu Y, Taugher RJ, et al. Acid-sensing ion channels contribute to synaptic transmission and inhibit cocaine-evoked plasticity. Nat Neurosci 2014; 17: 1083-91.
76. [76] Friese MA, Craner MJ, Etzensperger R, et al. Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med 2007; 13: 1483-9.
77. [77] Vergo S, Craner MJ, Etzensperger R, et al. Acid-sensing ion channel 1 is involved in both axonal injury and demyelination in multiple sclerosis and its animal model. Brain 2011; 134: 571-84.
78. [78] Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acidsensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007; 449: 316-23.
79. [79] Gonzales EB, Kawate T, Gouaux E. Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 2009; 460: 599-604.
80. [80] Baconguis I, Gouaux E. Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes. Nature 2012; 489: 400-5.
81. [81] Dawson RJ, Benz J, Stohler P, et al. Structure of the acid-sensing ion channel 1 in complex with the gating modifier Psalmotoxin 1. Nat Commun 2012; 3: 936.
82. [82] Baconguis I, Bohlen CJ, Goehring A, Julius D, Gouaux E. X-ray structure of acid-sensing ion channel 1-snake toxin complex reveals open state of a Na(+)-selective channel. Cell 2014; 156: 717-29.
83. [83] Yu Y, Chen Z, Li WG, et al. A nonproton ligand sensor in the acidsensing ion channel. Neuron 2010; 68: 61-72.
84. [84] Li WG, Yu Y, Zhang ZD, Cao H, Xu TL. ASIC3 channels integrate agmatine and multiple inflammatory signals through the nonproton ligand sensing domain. Mol Pain 2010; 6: 88.
85. [85] Yu Y, Li WG, Chen Z, et al. Atomic level characterization of the nonproton ligand-sensing domain of ASIC3 channels. J Biol Chem 2011; 286: 24996-5006.
86. [86] Li WG, Yu Y, Huang C, Cao H, Xu TL. Nonproton ligand sensing domain is required for paradoxical stimulation of acid-sensing ion channel 3 (ASIC3) channels by amiloride. J Biol Chem 2011; 286: 42635-46.
87. [87] Wang X, Li WG, Yu Y, et al. Serotonin facilitates peripheral pain sensitivity in a manner that depends on the nonproton ligand sensing domain of ASIC3 channel. J Neurosci 2013; 33: 4265-79.
88. [88] Bohlen CJ, Chesler AT, Sharif-Naeini R, et al. A heteromeric Texas coral snake toxin targets acid-sensing ion channels to produce pain. Nature 2011; 479: 410-4.
89. [89] Delaunay A, Gasull X, Salinas M, et al. Human ASIC3 channel dynamically adapts its activity to sense the extracellular pH in both acidic and alkaline directions. Proc Natl Acad Sci USA 2012; 109: 13124-9.
90. [90] Babinski K, Le KT, Seguela P. Molecular cloning and regional distribution of a human proton receptor subunit with biphasic functional properties. J Neurochem 1999; 72: 51-7.
91. [91] 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: 257-60.
92. [92] Waldmann R, Bassilana F, de Weille J, Champigny G, Heurteaux C, Lazdunski M. Molecular cloning of a non-inactivating protongated Na+ channel specific for sensory neurons. J Biol Chem 1997; 272: 20975-8.
93. [93] Voilley N, de Weille J, Mamet J, Lazdunski M. Nonsteroid antiinflammatory drugs inhibit both the activity and the inflammationinduced expression of acid-sensing ion channels in nociceptors. J Neurosci 2001; 21: 8026-33.
94. [94] 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 2002; 22: 10662-70.
95. [95] Steen KH, Steen AE, Reeh PW. A dominant role of acid pH in inflammatory excitation and sensitization of nociceptors in rat skin, in vitro. J Neurosci 1995; 15: 3982-9.
96. [96] Vakili C, Ruiz-Ortiz F, Burke JF. Chemical and osmolar changes of interstitial fluid in acute inflammatory states. Surg Forum 1970; 21: 227-8.
97. [97] Smith ES, Cadiou H, McNaughton PA. Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action. Neuroscience 2007; 145: 686-98.
98. [98] Immke DC, McCleskey EW. Lactate enhances the acid-sensing Na+ channel on ischemia-sensing neurons. Nat Neurosci 2001; 4: 869-70.
99. [99] Immke DC, McCleskey EW. Protons open acid-sensing ion channels by catalyzing relief of Ca2+ blockade. Neuron 2003; 37: 75-84.
100. [100] Askwith CC, Cheng C, Ikuma M, Benson C, Price MP, Welsh MJ. Neuropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/ENaC channels. Neuron 2000; 26: 133-41.
101. [101] Drew LJ, Rohrer DK, Price MP, et al. Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J Physiol 2004; 556: 691-710.
102. [102] Mogil JS, Breese NM, Witty MF, et al. Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci 2005; 25: 9893-901.
103. [103] Jones RC, 3rd, Xu L, Gebhart GF. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acidsensing ion channel 3. J Neurosci 2005; 25: 10981-9.
104. [104] Jones RC, 3rd, Otsuka E, Wagstrom E, Jensen CS, Price MP, Gebhart GF. Short-term sensitization of colon mechanoreceptors is associated with long-term hypersensitivity to colon distention in the mouse. Gastroenterology 2007; 133: 184-94.
105. [105] Wu WL, Lin YW, Min MY, Chen CC. Mice lacking Asic3 show reduced anxiety-like behavior on the elevated plus maze and reduced aggression. Genes Brain Behav 2010; 9: 603-14.
106. [106] Huang SJ, Yang WS, Lin YW, Wang HC, Chen CC. Increase of insulin sensitivity and reversal of age-dependent glucose intolerance with inhibition of ASIC3. Biochem Biophys Res Commun 2008; 371: 729-34.
107. [107] Wu WL, Cheng CF, Sun WH, Wong CW, Chen CC. Targeting ASIC3 for pain, anxiety, and insulin resistance. Pharmacol Ther 2012; 134: 127-38.
108. [108] 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 2010; 128: 549-58.
109. [109] Diochot S, Baron A, Rash LD, et al. A new sea anemone peptide, APETx2, inhibits ASIC3, a major acid-sensitive channel in sensory neurons. EMBO J 2004; 23: 1516-25.
110. [110] Chagot B, Escoubas P, Diochot S, Bernard C, Lazdunski M, Darbon H. Solution structure of APETx2, a specific peptide inhibitor of ASIC3 proton-gated channels. Protein Sci 2005; 14: 2003-10.
111. [111] Diochot S, Salinas M, Baron A, Escoubas P, Lazdunski M. Peptides inhibitors of acid-sensing ion channels. Toxicon 2007; 49: 271-84.
112. [112] Bassler EL, Ngo-Anh TJ, Geisler HS, Ruppersberg JP, Grunder S. Molecular and functional characterization of acid-sensing ion channel (ASIC) 1b. J Biol Chem 2001; 276: 33782-7.
113. [113] Hoagland EN, Sherwood TW, Lee KG, Walker CJ, Askwith CC. Identification of a calcium permeable human acid-sensing ion channel 1 transcript variant. J Biol Chem 2010; 285: 41852-62.
114. [114] Zha XM, Wemmie JA, Green SH, Welsh MJ. Acid-sensing ion channel 1a is a postsynaptic proton receptor that affects the density of dendritic spines. Proc Natl Acad Sci USA 2006; 103: 16556-61.
115. [115] 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 2006; 576: 215-34.
116. [116] Page AJ, Brierley SM, Martin CM, et al. The ion channel ASIC1 contributes to visceral but not cutaneous mechanoreceptor function. Gastroenterology 2004; 127: 1739-47.
117. [117] Escoubas P, De Weille JR, Lecoq A, et al. Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J Biol Chem 2000; 275: 25116-21.
118. [118] Escoubas P, Bernard C, Lambeau G, Lazdunski M, Darbon H. Recombinant production and solution structure of PcTx1, the specific peptide inhibitor of ASIC1a proton-gated cation channels. Protein Sci 2003; 12: 1332-43.
119. [119] Sherwood TW, Lee KG, Gormley MG, Askwith CC. Heteromeric acid-sensing ion channels (ASICs) composed of ASIC2b and ASIC1a display novel channel properties and contribute to acidosis-induced neuronal death. J Neurosci 2011; 31: 9723-34.
120. [120] Schroeder CI, Rash LD, Vila-Farres X, et al. Chemical synthesis, 3D structure, and ASIC binding site of the toxin mambalgin-2. Angew Chem Int Ed Engl 2014; 53: 1017-20.
121. [121] Jones NG, Slater R, Cadiou H, McNaughton P, McMahon SB. Acid-induced pain and its modulation in humans. J Neurosci 2004; 24: 10974-9.
122. [122] 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 2002; 110: 1185-90.
123. [123] Price MP, Lewin GR, McIlwrath SL, et al. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 2000; 407: 1007-11.
124. [124] Roza C, Puel JL, Kress M, et al. Knockout of the ASIC2 channel in mice does not impair cutaneous mechanosensation, visceral mechanonociception and hearing. J Physiol 2004; 558: 659-69.
125. [125] Lu Y, Ma X, Sabharwal R, et al. The ion channel ASIC2 is required for baroreceptor and autonomic control of the circulation. Neuron 2009; 64: 885-97.
126. [126] Ji RR, Kohno T, Moore KA, Woolf CJ. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 2003; 26: 696-705.
127. [127] Sandkuhler J. Learning and memory in pain pathways. Pain 2000; 88: 113-8.
128. [128] Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science 2000; 288: 1765-9.
129. [129] Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell 2009; 139: 267-84.
130. [130] Sandkuhler J. Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 2009; 89: 707-58.
131. [131] Ikeda H, Stark J, Fischer H, et al. Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 2006; 312: 1659-62.
132. [132] Sandkuhler J. Understanding LTP in pain pathways. Mol Pain 2007; 3: 9.
133. [133] Highstein SM, Holstein GR, Mann MA, Rabbitt RD. Evidence that protons act as neurotransmitters at vestibular hair cell-calyx afferent synapses. Proc Natl Acad Sci USA 2014; 111: 5421-6.
134. [134] Duan B, Liu DS, Huang Y, et al. PI3-kinase/Akt pathway-regulated membrane insertion of acid-sensing ion channel 1a underlies BDNF-induced pain hypersensitivity. J Neurosci 2012; 32: 6351-63.
135. [135] Melzack R, Casey KL. Sensory motivational and central control determinants of pain: A new conceptual model. In: D. Kenshalo (Ed.), The Skin Senses 1968; pp. 423-443, Springfield: Thomas.
136. [136] Price MP, Gong H, Parsons MG, et al. Localization and behaviors in null mice suggest that ASIC1 and ASIC2 modulate responses to aversive stimuli. Genes Brain Behav 2014; 13: 179-94.
137. [137] Taugher RJ, Lu Y, Wang Y, et al. The bed nucleus of the stria terminalis is critical for anxiety-related behavior evoked by CO2 and acidosis. J Neurosci 2014; 34: 10247-55.
138. [138] Gregersen N, Dahl HA, Buttenschon HN, et al. A genome-wide study of panic disorder suggests the amiloride-sensitive cation channel 1 as a candidate gene. Eur J Hum Genet 2012; 20: 84-90.
139. [139] Smoller JW, Gallagher PJ, Duncan LE, et al. The human ortholog of acid-sensing ion channel gene ASIC1a is associated with panic disorder and amygdala structure and function. Biol Psychiatry 2014; in press.
140. [140] Magnotta VA, Johnson CP, Follmer R, Wemmie JA. Functional t1rho imaging in panic disorder. Biol Psychiatry 2014; 75: 884-91.
141. [141] Wohleb ES, Powell ND, Godbout JP, Sheridan JF. Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J Neurosci 2013; 33: 13820-33.
142. [142] Pidoplichko VI, Aroniadou-Anderjaska V, Prager EM, Figueiredo TH, Almeida-Suhett CP, Miller SL, Braga MF. ASIC1a activation enhances inhibition in the basolateral amygdala and reduces anxiety. J Neurosci 2014; 34: 3130-41.
143. [143] Dube GR, Lehto SG, Breese NM, et al. Electrophysiological and in vivo characterization of A-317567, a novel blocker of acid sensing ion channels. Pain 2005; 117: 88-96.
144. [144] Kuduk SD, Di Marco CN, Chang RK, et al. Amiloride derived inhibitors of acid-sensing ion channel-3 (ASIC3). Bioorg Med Chem Lett 2009; 19: 2514-8.
145. [145] Kuduk SD, Chang RK, Wai JM, et al. Amidine derived inhibitors of acid-sensing ion channel-3 (ASIC3). Bioorg Med Chem Lett 2009; 19: 4059-63.
146. [146] Kuduk SD, Chang RK, Di Marco CN, et al. Identification of nonamidine inhibitors of acid-sensing ion channel-3 (ASIC3). Bioorg Med Chem Lett 2011; 21: 4255-8.
147. [147] Chen X, Qiu L, Li M, et al. Diarylamidines: high potency inhibitors of acid-sensing ion channels. Neuropharmacology 2010; 58: 1045-53.
148. [148] Li WG, Xu TL. Emerging approaches to probing ion channel structure and function. Neurosci Bull 2012; 28: 351-74.