Acid-sensing ion channels: A new target for pain and CNS diseases

Current Opinion in Drug Discovery and Development

Volumn 12, Issue 5, 2009, Pages 693-704

  Sluka, Kathleen A ^a   Winter, Olivia C ^a,b   Wemmie, John A ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acid sensing ion channel; Anxiety; ASIC; Depression; Pain; Ph

Indexed keywords

A 317567; ACID SENSING ION CHANNEL; ALPRAZOLAM; AMILORIDE; ANTIDEPRESSANT AGENT; ANXIOLYTIC AGENT; GLUTAMATE RECEPTOR ANTAGONIST; MORPHINE; NONSTEROID ANTIINFLAMMATORY AGENT; OPIATE; PROTEIN INHIBITOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACIDOSIS; ANXIETY; BONE CANCER; CENTRAL NERVOUS SYSTEM DISEASE; CEREBROVASCULAR ACCIDENT; CHRONIC PAIN; DEGENERATIVE DISEASE; DEPRESSION; FIBROMYALGIA; HUMAN; HUNTINGTON CHOREA; HYPERALGESIA; IMMUNOFLUORESCENCE; INFLAMMATION; LOW BACK PAIN; MULTIPLE SCLEROSIS; NERVE CELL; NERVE INJURY; NEUROPATHIC PAIN; NEUROPROTECTION; NOCICEPTION; NONHUMAN; PARKINSON DISEASE; PH; POSTOPERATIVE PAIN; RETINA; REVIEW; SEIZURE; SPINAL GANGLION; STROKE; SYNAPSE; TISSUE INJURY; TRAUMATIC BRAIN INJURY; TREATMENT FAILURE; VISCERAL PAIN;

ANALGESICS; ANIMALS; CENTRAL NERVOUS SYSTEM AGENTS; CENTRAL NERVOUS SYSTEM DISEASES; DRUG DESIGN; HUMANS; HYDROGEN-ION CONCENTRATION; NERVE TISSUE PROTEINS; PAIN; SODIUM CHANNELS;

EID: 70149084337     PISSN: 13676733     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (113)

1. Canessa CM: Structural biology: Unexpected opening. Nature (2007) 449(7160):293-294.
2. Wemmie JA, Price MP, Welsh MJ: Acid-sensing ion channels; Advances, questions and therapeutic opportunities. Trends Neurosci (2006) 29(10); 578-586.
3. + channel mechanism revealed by the acid-sensing ion channel 1 structure. IUBMB Life (2008) 60(9); 620-628.
4. 4. Jasti J, Furukawa H, Gonzales EB, Gouaux E: Structure of acidsensing ion channel 1 at 1.9 Å resolution and low pH. Nature (2007) 449(7160):316-323. (Pubitemid 47443482)
5. Qadri YJ, Berdiev BK, Song Y, Lippton HL, Fuller CM, Benos DJ: Psalmotoxin-1 docking to human acid sensing ion channel-1. J Biol Chem (2009) 284(26);17625-17633.
6. Zha XM, Wang R, Collier DM, Snyder PM, Wemmie JA, Welsh MJ: Oxidant regulated inter-subunit disulfide bond formation between ASIC1a subunits. Proc Natl Acad Sci USA (2009) 106(9):3573-3578.
7. 7. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, Wei WL, MacDonald JF, Wemmie JA, Price MP, Welsh MJ, Simon RP; Neuroprotection in ischemia; Blocking calcium-permeable acid-sensing ion channels. Cell (2004) 118(6):687-698. (Pubitemid 39221729)
8. 8. Yermolaieva O, Leonard AS, Schnizler MK, Abboud FM, Welsh MJ: Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc Natl Acad Sci USA (2004) 101(17);6752-6757. (Pubitemid 38586046)
9. 9. Gao J, Duan B, Wang DG, Deng XH, Zhang GY Xu L, Xu TL; Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron (2005) 48(4): 635-646. (Pubitemid 41654684)
10. 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(44):16556-16561.
11. 2+ entry. Cell Calcium (2009)45(4):319-325.
12. 2+ influx in rat cortical neurons. J Pharmacol Exp Ther (2008) 327(2) :491-502.
13. Gründer S, Geissler HS, Bässler EL, Ruppersberg JP: A new member of acid-sensing ion channels from pituitary gland. Neuroreport (2000) 11(8);1607-1611.
14. +-gated channels in mouse sensory neurons. Proc Natl Acad Sci USA (2002) 99(4): 2338-2343.
15. 15. Hesselager M, Timmermann DB, Ahring PK; pH-dependency and desensitization kinetics of heterologously expressed combinations of acid-sensing ion channel subunits. J Biol Chem (2004) 279(12);11006-11015. 16. Askwith CC, Wemmie JA, Price MP, Rokhlina T, Welsh MJ: Acid-sensing ion channel 2 (ASIC2) modulates ASIC1 H+-activated currents in hippocampal neurons. J Biol Chem (2003) 279(18):18296-18305. (Pubitemid 38401592)
16. Cadiou H, Studer M, Jones NG, Smith ES, Ballard A, McMahon SB, McNaughton PA: Modulation of acid-sensing ion channel activity by nitric oxide. J Neurosci (2007) 27(48): 13251-13260.
17. Frey Law LA, Sluka KA, McMullen T, Lee J, Arendt-Nielsen L, Graven-Nielsen T: Acidic buffer induced muscle pain evokes referred pain and mechanical hyperalgesia in humans. Pain (2008) 140(2): 254-264.
18. Steen KH, Reeh PW: Sustained graded pain and hyperalgesia from harmless experimental tissue acidosis in human skin. Neurosci Lett (1993) 154(1-2);113-116.
19. Reeh PW, Steen KH: Tissue acidosis in nociception and pain. Prog Brain Res (1996) 113:143-151.
20. Goldie I, Nachemson A: Synovial pH In rheumatoid knee-joints. I. The effect of synovectomy. Acta Orthop Scand (1969) 40(5): 634-641.
21. 22. Geborek P, Saxne T, Pettersson H, Wollheim FA: Synovial fluid acidosis correlates with radiological joint destruction in rheumatoid arthritis knee joints. J Rheumatol (1989) 16(4); 468-472. (Pubitemid 19149402)
22. 23. Sluka KA, Price MP, Bréese 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(3); 229-239. (Pubitemid 37505871)
23. 24. Sluka KA, Radhakrishnan R, Benson CJ, Eshcol JO, Price MP, Babinski K, Audette KM, Yeomans DC, Wilson SP: ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain (2007) 129(1-2):102-112. (Pubitemid 46551372)
24. 25. Issberner U, Reeh PW, Steen KH: Pain due to tissue acidosis: A mechanism for inflammatory and ischemic myalgia? Neurosci Lett (1996) 208(3); 191-194. (Pubitemid 26140154)
25. Steen KH, Reeh PW: Sustained graded pain and hyperalgesia from harmless experimental tissue acidosis in human skin. Neurosci Lett (1993) 154(1-2):113-116.
26. 27. Jones NG, Slater R, Cadiou H, McNaughton P, McMahon SB; Acid-induced pain and its modulation in humans. J Neurosci (2004) 24(48): 10974-10979. (Pubitemid 39602408)
27. Krishtal OA, Pidoplichko VI; A "receptor" for protons in small neurons of trigeminal ganglia: Possible role in nociception. Neurosci Lett (1981) 24(3):243-246.
28. + channel specific for sensory neurons. J Biol Chem (1997) 272(34); 20975-20978.
29. Rehncrona S: Brain acidosis. Ann Emerg Med (1985) 14(8): 770-776.
30. 31. Olson TH, Riedl MS, Vulchanova L, Ortiz-Gonzalez XR, Eide R: An acid sensing ion channel (ASIC) localizes to small primary afferent neurons in rats. Neuron (1998) 9(6):1109-1113. (Pubitemid 28266632)
31. 32. Price MP, McIlwrath SL, Xie J, Cheng C, Qiao J, Tarr DE, Sluka KA, Brennan TJ, Lewin GR, Welsh MJ: The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron (2001) 32(6): 1071-1083. (Pubitemid 34075397)
32. 33. Molliver DC, Immke DC, Fierro L, Paré M, Rice FL, McCleskey EW; ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol Pain (2005) 1:35. (Pubitemid 44848588)
33. 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(3):662-669.
34. Ikeuchi M, Kolker SJ, Sluka KA; Acid-sensing ion channel 3 expression in mouse knee joint afferents and effects of carrageenan-induced arthritis. J Pain (2009) 10(3);336-342.
35. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M; A proton-gated cation channel involved in acid-sensing. Nature (1997) 386(6621): 173-177.
36. + channel specific for sensory neurons. J Biol Chem (1997) 272(34):20975-20978.
37. 38. Molliver DC, Immke DC, Fierro L, Paré M, Rice FL, McCleskey EW: ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol Pain (2005) 1:35. (Pubitemid 44848588)
38. 39. Wu LJ, Duan B, Mei YD, Gao J, Chen JG, Zhuo M, Xu L, Wu M, Xu TL; Characterization of acid-sensing ion channels in dorsal horn neurons of rat spinal cord. J Biol Chem (2004) 279(42);43716-43724. (Pubitemid 39390676)
39. 40. Duan B, Wu U, Yu YQ, Ding Y, Jing L, Xu L, Chen J, Xu TL: Upregulation of acid-sensing ion channel ASIC1a in spinal dorsal horn neurons contributes to inflammatory pain hypersensitivity. J Neurosci (2007) 27(41): 11139-11148. (Pubitemid 47577376)
40. 41. Baron A, Voilley N, Lazdunski M, Lingueglia E; Acid sensing ion channels In dorsal spinal cord neurons. J Neurosci (2008) 28(6):1498-1508. (Pubitemid 351231523)
41. 42. Ferreira J, Santos AR, Calixto JB: Antinociception produced by systemic, spinal and supraspinal administration of amiloride in mice. Life Sci (1999) 65(10); 1059-1066. (Pubitemid 29410390)
42. 43. Coryell M, Ziemann AE, Westmoreland PJ, Haenfler JM, Kurjakovic Z, Zha XM, Price M, Schnizler MK, Wemmie JA; Targeting ASIC1a reduces innate fear and alters neuronal activity in the fear circuit. Biol Psychiatry (2007) 62(10): 1140-1148. (Pubitemid 350029730)
43. 44. Mazzuca M, Heurteaux C, Alloui A, Diochot S, Baron A, Voilley N, Blondeau N, Escoubas P, Gélot A, Cupo A, Zimmer A et al: A tarantula peptide against pain via ASIC1a channels and opioid mechanisms. Nat Neurosci (2007) 10(8);943-945. (Pubitemid 47185208)
44. + channel. J Biol Chem (1996) 271(14): 7879-7882.
45. 46. García-Añoveros J, Derfler B, Neville-Golden J, Hyman BT, Corey DP: BNaC1 and BNaC2 constitute a new family of human neuronal sodium channels related to degenerins and epithelial sodium channels. Proc Natl Acad Sci USA (1997) 94(4): 1459-1464. (Pubitemid 27087873)
46. Meng QY, Wang W, Chen XN, Xu TL, Zhou JN: Distribution of acid-sensing ion channel 3 in the rat hypothalamus. Neuroscience (2009) 159(3); 1126-1134.
47. 48. Jahr H, van Driel M, van Osch GJ, Weinans H, van Leeuwen JP: Identification of acid-sensing ion channels in bone. Biochem Biophys Res Commun (2005) 337(1): 349-354. (Pubitemid 41393801)
48. 49. 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(10);1009-1019. (Pubitemid 350084978)
49. 50. Ohtori S, Inoue G, Koshi T, Ito T, Doya H, Saito T, Moriya H, Takahashi K; Up-regulation of acid-sensing ion channel 3 in dorsal root ganglion neurons following application of nucleus pulposus on nerve root in rats. Spine (2006) 31(18): 2048-2052. (Pubitemid 44246376)
50. 51. Gitterman DP, Wilson J, Randall AD: Functional properties and pharmacological inhibition of ASIC channels in the human SJ-RH30 skeletal muscle cell line. J Physiol (2005) 562(Pt 3): 759-769. (Pubitemid 40246791)
51. 52. Voilley N, de Weille J, Mamet J, Lazdunski M: Nonsteroid antiinflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci (2001) 21(20):8026-8033. (Pubitemid 32952759)
52. Nagae M, Hiraga T, Wakabayashi H, Wang L, Iwata K, Yoneda T: Osteoclasts play a part in pain due to the inflammation adjacent to bone. Bone (2006) 39(5):1107-1115.
53. 54. Dorofeeva NA, Barygin OI, Staruschenko A, Bolshakov KV, Magazanik LG: Mechanisms of non-steroid anti-inflammatory drugs action on ASICs expressed in hippocampal interneurons. J Neurochem (2008) 106(1):429-441. 55. Coryell MW, Wunsch AM, Haenfler JM, Allen JE, Schnizler M, Ziemann AE, Cook MN, Dunning JP, Price MP, Rainier JD, Liu Z et al: Acid-sensing ion channel-la in the amygdala, a novel therapeutic target in depression-related behavior, J Neurosci (2009) 29(17):5381-5388. (Pubitemid 351840226)
54. 56. Page AJ, Brierley SM, Martin CM, Price MP, Symonds E, Butler R, Wemmie JA, Blackshaw LA; Different contributions of ASIC channels la, 2, and 3 in gastrointestinal mechanosensory function. Gut (2005) 54(10): 1408-1415. (Pubitemid 41375197)
55. Walder RY, Rasmussen LA, Rainier JD, Light AR, Wemmie JA, Sluka, KA; ASIC1 and ASIC3 play different roles in the development of hyperalgesia following inflammatory muscle injury, J Pain (2009): in press.
56. 58. Mogil JS, Breese NM, Witty MF, Ritchie J, Rainville ML, Ase A, Abbadi N, Stucky CL, Séguéla P; Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci (2005) 25(43):9893-9901. (Pubitemid 41528026)
57. 59. 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 USA (2002) 99(13):8992-8997. (Pubitemid 34693671)
58. Staniland AA, McMahon SB: Mice lacking acid-sensing ion channels (ASIC) 1 or 2, but not ASIC3, show increased pain behaviour in the formalin test. Eur J Pain (2009) 13(6):554-563.
59. 61. Dube GR, Lehto SG, Breese NM, Baker SJ, Wang X, Matulenko MA, Honoré P, Stewart AO, Moreland RB, Brioni JD: Electrophysiological and in vivo characterization of A-317567, a novel blocker of acid sensing ion channels. Pain (2005) 117(1-2):88-96. (Pubitemid 41764775)
60. Deval E, Noë 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 (2008) 27(22):3047-3055.
61. Rocha-Gonzalez HI, Herrejon-Abreu EB, López-Santillán FJ, García-López BE, Murbartián J, Granados-Soto V: Acid increases inflammatory pain in rats: Effect of local peripheral ASICs inhibitors. Eur J Pharmacol (2009) 603(1-3):56-61.
62. Yen YT, Tu PH, Chen CJ, Lin YW, Hsieh ST, Chen CC: Role of acid-sensing ion channel 3 in sub-acute-phase inflammation. Moi Pain (2009) 5:1.
63. Fujii Y, Ozaki N, Taguchi T, Mizumura K, Furukawa K, Sugiura Y: TRP channels and ASICs mediate mechanical hyperalgesia in models of inflammatory muscle pain and delayed onset muscle soreness. Pain (2008) 140(2);292-304.
64. Sluka KA, Price MP, Wemmie JA, Welsh MJ; ASIC3, but not ASIC1, channels are involved in the development of chronic muscle pain. In: Proceedings of the 10th World Congress on Pain, Progress in Pain Research and Management, Volume 24. Dostrovsky JO, Carr DB, Koltzenburg M (Eds), IASP Press, Seattle, USA (2003); 71-79.
65. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z, Lee J; Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol (2008) 100(3):1184-1201.
66. Woo YC, Park SS, Subieta AR, Brennan TJ: Changes in tissue pH and temperature after incision indicate acidosis may contribute to postoperative pain. Anesthesiology (2004) 101(2);468-475.
67. Benson CJ, Eckert SP, McCleskey EW: Acid-evoked currents in cardiac sensory neurons: A possible mediator of myocardial ischemic sensation. Circ Res (1999) 84(8);921-928.
68. Sutherland SP, Benson CJ, Adelman JP, McCleskey EW: Acid-sensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons. Proc Natl Acad Sci USA (2001) 98(2):711-716.
69. Page AJ, Brierley SM, Martin CM, Martinez-Salgado C, Wemmie JA, Brennan TJ, Symonds E, Omari T, Lewin GR, Welsh MJ, Blackshaw LA: The ion channel ASIC1 contributes to visceral but not cutaneous mechanoreceptor function. Gastroenterology (2004) 127(6): 1739-1747.
70. 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 acid-sensing ion channel 3. J Neurosci (2005) 25(47): 10981-10989.
71. 73. Sluka KA, Kalra A, Moore SA; Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve (2001) 24(1);37-46. (Pubitemid 32038025)
72. 74. Yokoyama T, Maeda Y, Audette KM, Sluka KA; Pregabalin reduces muscle and cutaneous hyperalgesia in two models of chronic muscle pain in rats. J Pain (2007) 8(5):422-429. (Pubitemid 46678933)
73. 75. Miranda A, Peles S, Rudolph C, Shaker R, Sengupta JN; Altered visceral sensation in response to somatic pain in the rat. Gastroenterology (2004) 126(4);1082-1089. (Pubitemid 38451179)
74. Wemmie JA, Zha X-M, Welsh MJ; Acid-sensing ion channels (ASICs) and pH in synapse physiology. In: Structural and functional organization of the synapse. Hell JW, Ehlers MD (Eds) Springer Science+Business Media LLC, New York, NY, USA (2008): 661-682.
75. 2+ current in mammalian cone photoreceptors. Neuron (2001) 32(6): 1107-1117.
76. 78. Vessey JP, Stratis AK, Daniels BA, Da Silva N, Jonz MG, Lalonde MR, Baldridge WH, Barnes S; Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photoreceptor synapse. J Neurosci (2005) 25(16):4108-4117. (Pubitemid 40563386)
77. 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(36):11332-11341. (Pubitemid 37549689)
78. Demaurex N, Poburko D, Frieden M: Regulation of plasma membrane calcium fluxes by mitochondria. Biochim Biophys Acta (2009):doi:10.1016/j.bbabio.2008. 12.012.
79. 1H-MRS study. Mol Psychiatry (2008) 14(5): 537-545.
80. Stewart PA: Independent and dependent variables of acid-base control. Respir Physiol (1978) 33(1);9-26.
81. 83. Pellerin L, Pellegri G, Bittar PG, Charnay Y, Bouras C, Martin JL, Stella N, Magistretti PJ: Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci (1998) 20(4-5):291-299. (Pubitemid 28495523)
82. Beg AA, Ernstrom GG, Nix P, Davis MW, Jorgensen EM: Protons act as a transmitter for muscle contraction in C elegans. Cell (2008) 132(1);149-160.
83. Voglis G, Tavernarakis N; A synaptic DEG/ENaC ion channel mediates learning in C elegans by facilitating dopamine Signalling. EMBO J (2008) 27(24); 3288-3299.
84. Zha XM, Costa V, Harding AM, Reznikov L, Benson CJ, Welsh MJ; ASIC2 subunits target acid-sensing ion channels to the synapse via an association with PSD-95. J Neurosci (2009) 29(26) :8438-8446.
85. 87. Wemmie JA, Chen J, Askwith CC, Hruska-Hageman AM, Price MP, Nolan BC, Yoder PG, Lamani E, Hoshi T, Freeman JH Jr, Welsh MJ; The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron (2002) 34(3);463-477. (Pubitemid 34465503)
86. Cho JH, Askwith CC: Presynaptic release probability is increased in hippocampal neurons from ASIC1 knockout mice. J Neurophysiol (2008) 99(2);426-441.
87. 89. 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(13):5496-5502. 90. Wemmie J, Coryell M, Askwith C, Lamani E, Leonard S, Sigmund C, Welsh M: Overexpression of acid-sensing ion channel la in transgenic mice increases fear-related behavior. Proc Natl Acad Sci USA (2004) 101(10):3621-3626. (Pubitemid 36807824)
88. Coryell MW, Wunsch AM, Haenfler JM, Allen JE, McBride JL, Davidson BL, Wemmie JA: Restoring acid-sensing ion channel-la in the amygdala of knock-out mice rescues fear memory but not unconditioned fear responses. J Neurosci (2008) 28(51);13738-13741.
89. Dwyer JM, Rizzo SJ, Neal SJ, Lin Q, Jow F, Arias RL, Rosenzweig-Lipson S, Dunlop J, Beyer CE: Acid sensing ion channel (ASIC) inhibitors exhibit anxiolytic-like activity in preclinical pharmacological models. Psychopharmacology (Berl) (2009) 203(1):41-52.
90. 93. Obrenovitch TP, Serieller D, Matsumoto T, Tegtmeier F, Höller M, Symon L: A rapid redistribution of hydrogen ions is associated with depolarization and repolarization subsequent to cerebral ischemia reperfusion. J Neurophysiol (1990) 64(4);1125-1133. (Pubitemid 20338957)
91. 2+ concentration changes in cultured postnatal rat hippocampal neurons. Neuroscience (1999) 93(3); 1003-1016.
92. Allen NJ, Attwell D; Modulation of ASIC channels in rat cerebellar Purkinje neurons by ischaemia-related signals. J Physiol (2002) 543(Pt 2):521-529.
93. Katsura K, Siesjǒ BK; Acid-base metabolism in ischemia. In: pH and brain function. Kaila K, Ransom BR (Eds) Wiley-Liss, New York, NY, USA (1998);563-582.
94. Siesjo BK, Katsura K, Kristián T: Acidosis-related damage. Adv Neurol (1996) 71:209-233; discussion 234-236.
95. 98. Immke DC, McCleskey EW: Lactate enhances the acid-sensing Na+ channel on ischemia-sensing neurons. Nat Neurosci (2001) 4(9); 869-870. (Pubitemid 32801586)
96. 99. Smith ES, Cadiou H, McNaughton PA: Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action. Neuroscience (2007) 145(2):686-698. (Pubitemid 46341668)
97. 100. Pignataro G, Simon RP, Xiong ZG; Prolonged activation of ASIC1a and the time window for neuroprotection in cerebral ischaemia. Brain (2007) 130(Pt 1); 151-158. (Pubitemid 46026231)
98. 101. Ajmo CT Jr, Vernon DO, Collier L, Pennypacker KR, Cuevas J: o receptor activation reduces infarct size at 24 hours after permanent middle cerebral artery occlusion in rats. Curr Neurovasc Res (2006) 3(2):89-98. (Pubitemid 43778702)
99. 102. Friese MA, Craner MJ, Etzensperger R, Vergo S, Wemmie JA, Welsh MJ, Vincent A, Fugger L: Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med (2007) 13(12): 1483-1489. (Pubitemid 350224241)
100. Arias RL, Sung ML, Vasylyev D, Zhang MY, Albinson K, Kubek K, Kagan N, Beyer C, Lin Q, Dwyer JM, Zaleska MM et al: Amiloride is neuroprotective in an MPTP model of Parkinson's disease. Neurobiol Dis (2008) 31(3);334-341.
101. Wong HK, Bauer PO, Kurosawa M, Goswami A, Washizu C, Machida Y, Tosaki A, Yamada M, Knopfel T, Nakamura T, Nukina N; Blocking acid-sensing ion channel 1 alleviates Huntington's disease pathology via an ubiquitin-proteasome systemdependent mechanism. Hum Mol Genet (2008) 17(20): 3223-3235.
102. Zhao X, Gorin FA, Berman RF, Lyeth BG: Differential hippocampal protection when blocking intracellular sodium and calcium entry during traumatic brain injury in rats. J Neurotrauma (2008) 25(10);1195-1205.
103. Ziemann AE, Schnizler MK, Albert GW, Severson MA, Howard MA 3rd, Welsh MJ, Wemmie JA: Seizure termination by acidosis depends on ASIC1a. Nat Neurosci (2008) 11(7):816-822.
104. 107. 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(1);C126-C134. (Pubitemid 34670555)
105. 108. 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(5): 1005-1012. (Pubitemid 38177007)
106. 109. Ettaiche M, Deval E, Cougnon M, Lazdunski M, Voilley N; Silencing acid-sensing ion channel la alters cone-mediated retinal function. J Neurosci (2006) 26(21):5800-5809. (Pubitemid 44315273)
107. 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(2);143-151.
108. 111. 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(5); 1013-1022. (Pubitemid 38177008)
109. 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(5):2417-2426.
110. Chu Y, Su X, Huang Q, Zhang X; Patterns of DNA sequence variation at candidate gene loci in black poplar [Populus nigra L) as revealed by single nucleotide polymorphisms. Genetica (2009):doi:10.1007/s10709-009-9371-1.
111. 114. Scott G, Rusak B; Activation of hamster suprachiasmatic neurons in vitro via metabotropic glutamate receptors. Neuroscience (1996) 71(2);533-541. (Pubitemid 26068432)
112. 115. 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(8);1185-1190. (Pubitemid 35215899)
113. Kuduk SD, Di Marco CN, Chang RK, Dipardo RM, Cook SP, Cato MJ, Jovanovska A, Urban MO, Leitl M, Spencer RH, Kane SA et al: Amiloride derived inhibitors of acid-sensing ion channel-3 (ASIC3). Bioorg Med Chem Lett (2009) 19(9); 2514-2518.