Acid-Sensing ion channels and pain

Pharmaceuticals

Volumn 3, Issue 5, 2010, Pages 1411-1425

  Gu, Qihai ^a   Lee, Lu Yuan ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Acid sensing ion channel; Acidosis; Inflammation; Nociceptor; Pain

Indexed keywords

ACID SENSING ION CHANNEL; AMILORIDE; MESSENGER RNA; POTASSIUM CHANNEL; PURINERGIC P2X RECEPTOR; VANILLOID RECEPTOR 1;

ACIDOSIS; ANGINA PECTORIS; CHRONIC PAIN; DRUG MECHANISM; DRUG TARGETING; GASTROINTESTINAL PAIN; HUMAN; INFLAMMATION; IONTOPHORESIS; NOCICEPTION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SENSORY NERVE CELL; SKIN PAIN;

EID: 77954912734     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph3051411     Document Type: Review

References (117)

1. Reeh, P.W.; Steen, K.H. Tissue acidosis in nociception and pain. Prog. Brain Res. 1996, 113, 143-151.
2. Hunt, J.F.; Fang, K.; Malik, R.; Snyder, A.; Malhotra, N.; Platts-Mills, T.A.; Gaston, B. Endogenous airway acidification: Implications for asthma pathophysiology. Am. J. Respir. Crit. Care Med. 2000, 161, 694-699.
3. Benson, C.J.; Sutherland, S.P. Toward an understanding of the molecules that sense myocardial ischemia. Ann. N. Y. Acad. Sci. 2001, 940, 96-109.
4. Mantyh, P.W.; Clohisy, D.R.; Koltzenburg, M.; Hunt, S.P. Molecular mechanisms of cancer pain. Nat. Rev. Cancer 2002, 2, 201-209.
5. Steen, K.H.; Reeh, P.W. Sustained graded pain and hyperalgesia from harmless experimental tissue acidosis in human skin. Neurosci. Lett. 1993, 154, 113-116.
6. Bevan, S.; Yeats, J. Protons activate a cation conductance in a sub-population of rat dorsal root ganglion neurones. J. Physiol. 1991, 433, 145-161.
7. Waldmann, R.; Lazdunski, M. H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr. Opin. Neurobiol. 1998, 8, 418-424.
8. Caterina, M.J.; Julius, D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu. Rev. Neurosci. 2001, 24, 487-517.
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, 735-767.
10. Krishtal, O. The ASICs: signaling molecules? Modulators? Trends Neurosci. 2003, 26, 477-483.
11. Wemmie, J.A.; Price, M.P.; Welsh, M.J. Acid-sensing ion channels: Advances, questions and therapeutic opportunities. Trends Neurosci. 2006, 29, 578-586.
12. Akopian, A.N.; Chen, C.C.; Ding, Y.; Cesare, P.; Wood, J.N. A new member of the acid-sensing ion channel family. Neuroreport 2000, 11, 2217-2222.
13. Holzer, P. Acid-sensitive ion channels and receptors. Handb. Exp. Pharmacol. 2009, 194, 283-332.
14. Jasti, J.; Furukawa, H.; Gonzales, E.B.; Gouaux, E. Structure of acid-sensing ion channel 1 at 1.9 Ǻ resolution and low pH. Nature 2007, 449, 316-323.
15. Waldmann, R. Proton-gated cation channels-Neuronal acid sensors in the central and peripheral nervous system. Adv. Exp. Med. Biol. 2001, 502, 293-304.
16. Diochot, S.; Salinas, M.; Baron, A.; Escoubas, P.; Lazdunski, M. Peptides inhibitors of acidsensing ion channels. Toxicon 2007, 49, 271-284.
17. Benson, C.J.; Xie, J.; Wemmie, J.A.; Price, M.P.; Henss, J.M.; Welsh, M.J.; Snyder, P.M. Heteromultimers of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc. Natl. Acad. Sci. USA 2002, 99, 2338-2343.
18. Waldmann, R.; Champigny, G.; Lingueglia, E.; De Weille, J.R.; Heurteaux, C.; Lazdunski, M. H(+)-gated cation channels. Ann. N. Y. Acad. Sci. 1999, 868, 67-76.
19. 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. USA. 2002, 99, 2326-2331.
20. Hesselager, M.; Timmermann, D.B.; Ahring, P.K. pH dependency and desensitization kinetics of heterologously expressed combinations of acid-sensing ion channel subunits. J. Biol. Chem. 2004, 279, 11006-11015.
21. Waldmann, R.; Champigny, G.; Bassilana, F.; Heurteaux, C.; Lazdunski, M. A proton-gated cation channel involved in acid-sensing. Nature 1997, 386, 173-177.
22. Yermolaieva, O.; Leonard, A.S.; Schnizler, M.K.; Abboud, F.M.; Welsh, M.J. Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc. Natl. Acad. Sci. USA 2004, 101, 6752-6757.
23. Dubé, G.R.; Elagoz, A.; Mangat, H. Acid sensing ion channels and acid nociception. Curr. Pharm. Des. 2009, 15, 1750-1766.
24. Price, M.P.; Snyder, P.M.; Welsh, M.J. Cloning and expression of a novel human brain Na+ channel. J. Biol. Chem. 1996, 271, 7879-7882.
25. Chen, C.C.; England, S.; Akopian, A.N.; Wood, J.N. A sensory neuron-specific, proton-gated ion channel. Proc. Natl. Acad. Sci. USA. 1998, 95, 10240-10245.
26. 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. USA. 2001, 98, 711-716.
27. 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 2005, 54, 1408-1415.
28. 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. 2007, 500, 863-875.
29. Olson, T.H.; Riedl, M.S.; Vulchanova, L.; Ortiz-Gonzalez, X.R.; Elde, R. An acid sensing ion channel (ASIC) localizes to small primary afferent neurons in rats. Neuroreport 1998, 9, 1109-1113.
30. Ugawa, S.; Ueda, T.; Yamamura, H.; Shimada, S. In situ hybridization evidence for the coexistence of ASIC and TRPV1 within rat single sensory neurons. Brain Res. Mol. Brain Res. 2005, 136, 125-133.
31. 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 2001, 32, 1071-1083.
32. Xie, J.; Price, M.P.; Berger, A.L.; Welsh, M.J. DRASIC contributes to pH-gated currents in large dorsal root ganglion sensory neurons by forming heteromultimeric channels. J. Neurophysiol. 2002, 87, 2835-2843.
33. 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 2002, 34, 463-477.
34. Alvarez de la Rosa, D.; Krueger, S.R.; Kolar, A.; Shao, D.; Fitzsimonds, R.M.; Canessa, C.M. Distribution, subcellular localization and ontogeny of ASIC1 in the mammalian central nervous system. J. Physiol. 2003, 546, 77-87.
35. Jovov, B.; Tousson, A.; McMahon, L.L.; Benos, D.J. Immunolocalization of the acid-sensing ion channel 2a in the rat cerebellum. Histochem. Cell Biol. 2003, 119, 437-446.
36. Askwith, C.C.; Wemmie, J.A.; Price, M.P.; Rokhlina, T.; Welsh, M.J. Acid-sensing ion channel 2 (ASIC2) modulates ASIC1 H+-activated currents in hippocampal neurons. J. Biol. Chem. 2004, 279, 18296-18305.
37. 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. 2004, 279, 43716-43724.
38. Duan, B.; Wu, L.J.; Yu, Y.Q.; Ding, Y.; Jing, L.; Xu, L.; Chen, J.; Xu, T.L. Upregulation of acidsensing ion channel ASIC1a in spinal dorsal horn neurons contributes to inflammatory pain hypersensitivity. J. Neurosci. 2007, 27, 11139-11148.
39. Xu, T.L.; Duan, B. Calcium-permeable acid-sensing ion channel in nociceptive plasticity: A new target for pain control. Prog. Neurobiol. 2009, 87, 171-180.
40. Gründer, S.; Geissler, H.S.; Bässler, E.L.; Ruppersberg, J.P. New member of acid-sensing ion channels from pituitary gland. Neuroreport 2000, 11, 1607-1611.
41. 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. 2002, 283, C126-C134.
42. Lingueglia, E. Acid-sensing ion channels in sensory perception. J. Biol. Chem. 2007, 282, 17325-17329.
43. Basbaum, A.I.; Bautista, D.M.; Scherrer, G.; Julius, D. Cellular and molecular mechanisms of pain. Cell 2009, 139, 267-284.
44. Costigan, M.; Scholz, J.; Woolf, C.J. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu. Rev. Neurosci. 2009, 32, 1-32.
45. McCleskey, E.W.; Gold, M.S. Ion channels of nociception. Annu. Rev. Physiol. 1999, 61, 835-856.
46. Steen, K.H.; Issberner, U.; Reeh, P.W. Pain due to experimental acidosis in human skin: Evidence for non-adapting nociceptor excitation. Neurosci. Lett. 1995, 199, 29-32.
47. 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, 1185-1190.
48. Jones, N.G.; Slater, R.; Cadiou, H.; McNaughton, P.; McMahon, S.B. Acid-induced pain and its modulation in humans. J. Neurosci. 2004, 24, 10974-10979.
49. 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.
50. Deval, E.; Noël, 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, 3047-3055.
51. Escoubas, P.; De Weille, J.R.; Lecoq, A.; Diochot, S.; Waldmann, R.; Champigny, G.; Moinier, D.; Ménez, A.; Lazdunski, M. Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J. Biol. Chem. 2000, 275, 25116-25121.
52. 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, 10662-10670.
53. 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 2003, 106, 229-239.
54. 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 2007, 129, 102-112.
55. 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, 292-304.
56. 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 2008, 137, 662-669.
57. Walder, R.Y.; Rasmussen, L.A.; Rainier, J.D.; Light, A.R.; Wemmie, J.A.; Sluka, K.A. ASIC1 and ASIC3 play different roles in the development of Hyperalgesia after inflammatory muscle injury. J. Pain 2010, 11, 210-218.
58. Radhakrishnan, R.; Moore, S.A.; Sluka, K.A. Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats. Pain 2003, 104, 567-577.
59. 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 2009, 10, 336-342.
60. Drew, L.J.; Rohrer, D.K.; Price, M.P.; Blaver, K.E.; Cockayne, D.A.; Cesare, P.; Wood, J.N. Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J. Physiol. 2004, 556, 691-710.
61. 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. 2005, 25, 9893-9901.
62. Staniland, A.A.; McMahon, S.B. 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, 554-563.
63. Sluka, K.A.; Winter, O.C.; Wemmie, J.A. Acid-sensing ion channels: A new target for pain and CNS diseases. Curr. Opin. Drug Discov. Devel. 2009, 12, 693-704.
64. Cervero, F.; Laird, J.M. Understanding the signaling and transmission of visceral nociceptive events. J. Neurobiol. 2004, 61, 45-54.
65. 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. 2006, 99, 501-509.
66. 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. 1999, 84, 921-928.
67. Naves, L.A.; McCleskey, E.W. An acid-sensing ion channel that detects ischemic pain. Braz. J. Med. Biol. Res. 2005, 38, 1561-1569.
68. Immke, D.C.; McCleskey, E.W. Lactate enhances the acid-sensing Na+ channel on ischemiasensing neurons. Nat. Neurosci. 2001, 4, 869-870.
69. Immke, D.C.; McCleskey, E.W. Protons open acid-sensing ion channels by catalyzing relief of Ca2+ blockade. Neuron 2003, 37, 75-84.
70. 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. 2009, 105, 279-286.
71. Holzer, P. Taste receptors in the gastrointestinal tract. V. Acid sensing in the gastrointestinal tract. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292, G699-G705.
72. Schicho, R.; Florian, W.; Liebmann, I.; Holzer, P.; Lippe, I.T. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur. J. Neurosci. 2004, 19, 1811-1818.
73. Yiangou, Y.; Facer, P.; Smith, J.A.; Sangameswaran, L.; Eglen, R.; Birch, R.; Knowles, C.; Williams, N.; Anand, P. Increased acid-sensing ion channel ASIC-3 in inflamed human intestine. Eur. J. Gastroenterol. Hepatol. 2001, 13, 891-896.
74. Wultsch, T.; Painsipp, E.; Shahbazian, A.; Mitrovic, M.; Edelsbrunner, M.; Lazdunski, M.; Waldmann, R.; Holzer, P. Deletion of the acid-sensing ion channel ASIC3 prevents gastritisinduced acid hyperresponsiveness of the stomach-brainstem axis. Pain 2008, 134, 245-253.
75. Page, A.J.; Brierley, S.M.; Martin, C.M.; Hughes, P.A.; Blackshaw, L.A. Acid sensing ion channels 2 and 3 are required for inhibition of visceral nociceptors by benzamil. Pain 2007, 133, 150-160.
76. Hobson, A.R.; Aziz, Q. Modulation of visceral nociceptive pathways. Curr. Opin. Pharmacol. 2007, 7, 593-597.
77. Coleridge, H.M.; Coleridge, J.C. Pulmonary reflexes: neural mechanisms of pulmonary defense. Annu. Rev. Physiol. 1994, 56, 69-91.
78. Lee, L.Y.; Pisarri, T.E. Afferent properties and reflex functions of bronchopulmonary C-fibers. Respir. Physiol. 2001, 125, 47-65.
79. Fisher, J.T. The TRPV1 ion channel: implications for respiratory sensation and dyspnea. Respir. Physiol. Neurobiol. 2009, 167, 45-52.
80. Lee, L.Y. Respiratory sensations evoked by activation of bronchopulmonary C-fibers. Respir. Physiol. Neurobiol. 2009, 167, 26-35.
81. Ricciardolo, F.L.; Steinhoff, M.; Amadesi, S.; Guerrini, R.; Tognetto, M.; Trevisani, M.; Creminon, C.; Bertrand, C.; Bunnett, N.W.; Fabbri, L.M.; Salvadori, S.; Geppetti, P. Presence and bronchomotor activity of protease-activated receptor-2 in guinea pig airways. Am. J. Respir. Crit. Care Med. 2000, 161, 1672-1680.
82. Kodric, M.; Shah, A.N.; Fabbri, L.M.; Confalonieri, M. An investigation of airway acidification in asthma using induced sputum: A study of feasibility and correlation. Am. J. Respir. Crit. Care Med. 2007, 175, 905-910.
83. Ricciardolo, F.L.; Gaston, B.; Hunt, J. Acid stress in the pathology of asthma. J. Allergy Clin. Immunol. 2004, 113, 610-619.
84. Kollarik, M.; Ru, F.; Undem, B.J. Acid-sensitive vagal sensory pathways and cough. Pulm. Pharmacol. Ther. 2007, 20, 402-411.
85. Gu, Q.; Lee, L.Y. Characterization of acid-signaling in rat vagal pulmonary sensory neurons. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291, L58-L65.
86. Gu, Q.; Lee, L.Y. Regulation of acid signaling in rat pulmonary sensory neurons by proteaseactivated receptor-2. Am. J. Physiol. Lung. Cell Mol. Physiol. 2010, 298, L454-L461.
87. Woolf, C.J.; Salter, M.W. Neuronal plasticity: increasing the gain in pain. Science 2000, 288, 1765-1769.
88. Treede, R.D.; Jensen, T.S.; Campbell, J.N.; Cruccu, G.; Dostrovsky, J.O.; Griffin, J.W.; Hansson, P.; Hughes, R.; Nurmikko, T.; Serra, J. Neuropathic pain: redefinition and a grading system for clinical and research purposes. Neurology 2008, 70, 1630-1635.
89. Jensen, T.S.; Madsen, C.S.; Finnerup, N.B. Pharmacology and treatment of neuropathic pains. Curr. Opin. Neurol. 2009, 22, 467-474.
90. O'Connor, A.B.; Dworkin, R.H. Treatment of neuropathic pain: an overview of recent guidelines. Am. J. Med. 2009, 122, S22-S32.
91. Harvey, V.L.; Dickenson, A.H. Mechanisms of pain in nonmalignant disease. Curr. Opin. Support Palliat Care. 2008, 2, 133-139.
92. Jarvis, M.F.; Boyce-Rustay, J.M. Neuropathic pain: models and mechanisms. Curr. Pharm. Des. 2009, 15, 1711-1716.
93. Sommer, C. Painful neuropathies. Curr. Opin. Neurol. 2003, 16, 623-628.
94. Schaible, H.G.; Schmelz, M.; Tegeder, I. Pathophysiology and treatment of pain in joint disease. Adv. Drug Deliv. Rev. 2006, 58, 323-342.
95. Ohtori, S.; Inoue, G.; Koshi, T.; Ito, T.; Doya, H.; Saito, T.; Moriya, H.; Takahashi, K. Upregulation of acid-sensing ion channel 3 in dorsal root ganglion neurons following application of nucleus pulposus on nerve root in rats. Spine 2006, 31, 2048-2052.
96. Mazzuca, M.; Heurteaux, C.; Alloui, A.; Diochot, S.; Baron, A.; Voilley, N.; Blondeau, N.; Escoubas, P.; Gélot, 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. 2007, 10, 943-945.
97. 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.; Simon, R.P. Neuroprotection in ischemia: Blocking calcium-permeable acid-sensing ion channels. Cell 2004, 118, 687-698.
98. Xiong, Z.G.; Chu, X.P.; Simon, R.P. Ca2+-permeable acid-sensing ion channels and ischemic brain injury. J. Membr. Biol. 2006, 209, 59-68.
99. 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. 2007, 13, 1483-1489.
100. Askwith, C.C.; Cheng, C.; Ikuma, M.; Benson, C.; Price, M.P.; Welsh, M.J. Neuropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/ENaC channels. Neuron 2000, 26, 133-141.
101. Catarsi, S.; Babinski, K.; Séguéla, P. Selective modulation of heteromeric ASIC proton-gated channels by neuropeptide FF. Neuropharmacology 2001, 41, 592-600.
102. 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 2003, 44, 662-671.
103. Xie, J.; Price, M.P.; Wemmie, J.A.; Askwith, C.C.; Welsh, M.J. ASIC3 and ASIC1 mediate FMRFamide-related peptide enhancement of H+-gated currents in cultured dorsal root ganglion neurons. J. Neurophysiol. 2003, 89, 2459-2465.
104. Lingueglia, E.; Deval, E.; Lazdunski, M. FMRFamide-gated sodium channel and ASIC channels: A new class of ionotropic receptors for FMRFamide and related peptides. Peptides 2006, 27, 1138-1152.
105. Yang, H.Y.T.; Tao, T.; Iadarola, M.J. Modulatory role of neuropeptide FF system in nociception and opiate analgesia. Neuropeptides 2008, 42, 1-18.
106. Allen, N.J.; Attwell, D. Modulation of ASIC channels in rat cerebellar Purkinje neurons by ischaemia-related signals. J. Physiol. 2002, 543, 521-529.
107. Poirot, O.; Vukicevic, M.; Boesch, A.; Kellenberger, S. Selective regulation of acid-sensing ion channel 1 by serine proteases. J. Biol. Chem. 2004, 279, 38448-38457.
108. Vukicevic, M.; Weder, G.; Boillat, A.; Boesch, A.; Kellenberger, S. Trypsin cleaves acid-sensing ion channel 1a in a domain that is critical for channel gating. J. Biol. Chem. 2006, 281, 714-722.
109. Andrey, F.; Tsintsadze, T.; Volkova, T.; Lozovaya, N.; Krishtal, O. Acid sensing ionic channels: modulation by redox reagents. Biochim. Biophys. Acta 2005, 1745, 1-6.
110. Chu, X.P.; Close, N.; Saugstad, J.A.; Xiong, Z.G. ASIC1a-specific modulation of acid-sensing ion channels in mouse cortical neurons by redox reagents. J. Neurosci. 2006, 26, 5329-5339.
111. Cadiou, H.; Studer, M.; Jones, N.G.; Smith, E.S.; Ballard, A.; McMahon, S.B.; McNaughton, P.A. Modulation of acid-sensing ion channel activity by nitric oxide. J. Neurosci. 2007, 27, 13251-13260.
112. Smith, E.S.; Cadiou, H.; McNaughton, P.A. Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action. Neuroscience 2007, 145, 686-698.
113. Xu, T.L.; Xiong, Z.G. Dynamic regulation of acid-sensing ion channels by extracellular and intracellular modulators. Curr. Med. Chem. 2007, 14, 1753-1763.
114. Rocha-González, H.I.; Herrejon-Abreu, E.B.; López-Santillán, F.J.; García-López, B.E.; Murbartián, J.; Granados-Soto, V. Acid increases inflammatory pain in rats: effect of local peripheral ASICs inhibitors. Eur. J. Pharmacol. 2009, 603, 56-61.
115. Voilley, N. Acid-sensing ion channels (ASICs): New targets for the analgesic effects of nonsteroid anti-inflammatory drugs (NSAIDs). Curr. Drug Targets Inflamm. Allergy 2004, 3, 71-79.
116. 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, 1332-1343.
117. 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. 2004, 23, 1516-1525.