ASIC3 Channels Integrate Agmatine and Multiple Inflammatory Signals through the Nonproton Ligand Sensing Domain

Molecular Pain

Volumn 6, Issue , 2010, Pages

  Li, Wei Guang ^a,b   Yu, Ye ^a   Zhang, Zhu Dan ^a,b   Cao, Hui ^a   Xu, Tian Le ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 1B; ACID SENSING ION CHANNEL 3; AGMATINE; ARACHIDONIC ACID; ARCAINE; ARGININE; CALCIUM ION; LACTIC ACID; UNCLASSIFIED DRUG; ASIC CHANNEL; LIGAND; NERVE PROTEIN; SODIUM CHANNEL;

ACIDOSIS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CHELATION; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; HYPEROSMOLARITY; INFLAMMATION; LIGAND BINDING; NEUROPATHOLOGY; NONHUMAN; PAIN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CYTOLOGY; MALE; NERVE CELL; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SPRAGUE DAWLEY RAT;

AGMATINE; ANIMALS; CELLS, CULTURED; INFLAMMATION; LIGANDS; MALE; NERVE TISSUE PROTEINS; NEURONS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SODIUM CHANNELS;

EID: 78649785634     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-6-88     Document Type: Article

References (60)

1. Wemmie JA, Price MP, Welsh MJ. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 2006, 29:578-586. 10.1016/j.tins.2006.06.014, 16891000.
2. Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007, 449:316-323. 10.1038/nature06163, 17882215.
3. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature 1997, 386:173-177. 10.1038/386173a0, 9062189.
4. Babinski K, Le KT, Seguela P. Molecular cloning and regional distribution of a human proton receptor subunit with biphasic functional properties. J Neurochem 1999, 72:51-57. 10.1046/j.1471-4159.1999.0720051.x, 9886053.
5. de Weille JR, Bassilana F, Lazdunski M, Waldmann R. Identification, functional expression and chromosomal localisation of a sustained human proton-gated cation channel. FEBS Lett 1998, 433:257-260. 10.1016/S0014-5793(98)00916-8, 9744806.
6. Waldmann R, Bassilana F, de Weille J, Champigny G, Heurteaux C, Lazdunski M. Molecular cloning of a non-inactivating proton-gated Na+ channel specific for sensory neurons. J Biol Chem 1997, 272:20975-20978. 10.1074/jbc.272.34.20975, 9261094.
7. Salinas M, Lazdunski M, Lingueglia E. Structural elements for the generation of sustained currents by the acid pain sensor ASIC3. J Biol Chem 2009, 284:31851-31859. 10.1074/jbc.M109.043984, 2797256, 19778905.
8. 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 2008, 27:3047-3055. 10.1038/emboj.2008.213, 2585165, 18923424.
9. Li WG, Xu TL. ASIC3 channels in multimodal sensory perception. ACS Chem Neurosci
10. Yu Y, Chen Z, Li WG, Cao H, Feng EG, Yu F, Liu H, Jiang H, Xu TL. A nonproton ligand sensor in the acid-sensing ion channel. Neuron 2010, 68:61-72. 10.1016/j.neuron.2010.09.001, 20920791.
11. Morris SM. Arginine metabolism: boundaries of our knowledge. J Nutr 2007, 137:1602S-1609S.
12. Li G, Regunathan S, Barrow CJ, Eshraghi J, Cooper R, Reis DJ. Agmatine: an endogenous clonidine-displacing substance in the brain. Science 1994, 263:966-969. 10.1126/science.7906055, 7906055.
13. Reis DJ, Regunathan S. Agmatine: an endogenous ligand at imidazoline receptors may be a novel neurotransmitter in brain. J Auton Nerv Syst 1998, 72:80-85. 10.1016/S0165-1838(98)00091-5, 9851555.
14. Yang XC, Reis DJ. Agmatine selectively blocks the N-methyl-D-aspartate subclass of glutamate receptor channels in rat hippocampal neurons. J Pharmacol Exp Ther 1999, 288:544-549.
15. Loring RH. Agmatine acts as an antagonist of neuronal nicotinic receptors. Br J Pharmacol 1990, 99:207-211. 1917502, 2331571.
16. Li Q, Yin JX, He RR. Effect of agmatine on L-type calcium current in rat ventricular myocytes. Acta Pharmacol Sin 2002, 23:219-224.
17. Weng XC, Gai XD, Zheng JQ, Li J. Agmatine blocked voltage-gated calcium channel in cultured rat hippocampal neurons. Acta Pharmacol Sin 2003, 24:746-750.
18. Lopatin AN, Makhina EN, Nichols CG. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 1994, 372:366-369. 10.1038/372366a0, 7969496.
19. Ficker E, Taglialatela M, Wible BA, Henley CM, Brown AM. Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science 1994, 266:1068-1072. 10.1126/science.7973666, 7973666.
20. Kamboj SK, Swanson GT, Cull-Candy SG. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 1995, 486(Pt 2):297-303. 1156521, 7473197.
21. Bowie D, Mayer ML. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 1995, 15:453-462. 10.1016/0896-6273(95)90049-7, 7646897.
22. Nilius B, Prenen J, Voets T, Droogmans G. Intracellular nucleotides and polyamines inhibit the Ca2+-activated cation channel TRPM4b. Pflugers Arch 2004, 448:70-75. 10.1007/s00424-003-1221-x, 14758478.
23. Kerschbaum HH, Kozak JA, Cahalan MD. Polyvalent cations as permeant probes of MIC and TRPM7 pores. Biophys J 2003, 84:2293-2305. 10.1016/S0006-3495(03)75035-8, 1302796, 12668438.
24. Ahern GP, Wang X, Miyares RL. Polyamines are potent ligands for the capsaicin receptor TRPV1. J Biol Chem 2006, 281:8991-8995. 10.1074/jbc.M513429200, 16431906.
25. Quinn SJ, Ye CP, Diaz R, Kifor O, Bai M, Vassilev P, Brown E. The Ca2+-sensing receptor: a target for polyamines. Am J Physiol 1997, 273:C1315-1323.
26. Rock DM, Macdonald RL. The polyamine spermine has multiple actions on N-methyl-D-aspartate receptor single-channel currents in cultured cortical neurons. Mol Pharmacol 1992, 41:83-88.
27. Zhang L, Zheng X, Paupard MC, Wang AP, Santchi L, Friedman LK, Zukin RS, Bennett MV. Spermine potentiation of recombinant N-methyl-D-aspartate receptors is affected by subunit composition. Proc Natl Acad Sci USA 1994, 91:10883-10887. 10.1073/pnas.91.23.10883, 45130, 7971977.
28. Rock DM, MacDonald RL. Spermine and related polyamines produce a voltage-dependent reduction of N-methyl-D-aspartate receptor single-channel conductance. Mol Pharmacol 1992, 42:157-164.
29. Babini E, Paukert M, Geisler HS, Grunder S. Alternative splicing and interaction with di- and polyvalent cations control the dynamic range of acid-sensing ion channel 1 (ASIC1). J Biol Chem 2002, 277:41597-41603. 10.1074/jbc.M205877200, 12198124.
30. Duan B, Wang YZ, Yang T, Chu XP, Yu Y, Huang Y, Cao H, Hansen J, Simon RP, Zhu MX, et al. Extracellular spermine exacerbates ischemic neuronal injury through sensitization of ASIC1a channels to extracellular acidosis. J Neurosci
31. Zhang M, Wang H, Tracey KJ. Regulation of macrophage activation and inflammation by spermine: a new chapter in an old story. Crit Care Med 2000, 28:N60-66. 10.1097/00003246-200004001-00007, 10807317.
32. Sastre M, Galea E, Feinstein D, Reis DJ, Regunathan S. Metabolism of agmatine in macrophages: modulation by lipopolysaccharide and inhibitory cytokines. Biochem J 1998, 330(Pt 3):1405-1409. 1219289, 9494113.
33. Cobbe SM, Poole-Wilson PA. The time of onset and severity of acidosis in myocardial ischaemia. J Mol Cell Cardiol 1980, 12:745-760. 10.1016/0022-2828(80)90077-2, 7420422.
34. 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, 15:3982-3989.
35. Issberner U, Reeh PW, Steen KH. Pain due to tissue acidosis: a mechanism for inflammatory and ischemic myalgia?. Neurosci Lett 1996, 208:191-194. 10.1016/0304-3940(96)12576-3, 8733302.
36. Yagi J, Wenk HN, Naves LA, McCleskey EW. Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ Res 2006, 99:501-509. 10.1161/01.RES.0000238388.79295.4c, 16873722.
37. Vakili C, Ruiz-Ortiz F, Burke JF. Chemical and osmolar changes of interstitial fluid in acute inflammatory states. Surg Forum 1970, 21:227-228.
38. Nicholson C, Bruggencate GT, Steinberg R, Stockle H. Calcium modulation in brain extracellular microenvironment demonstrated with ion-selective micropipette. Proc Natl Acad Sci USA 1977, 74:1287-1290. 10.1073/pnas.74.3.1287, 430669, 265573.
39. Immke DC, McCleskey EW. Lactate enhances the acid-sensing Na+ channel on ischemia-sensing neurons. Nat Neurosci 2001, 4:869-870. 10.1038/nn0901-869, 11528414.
40. Satriano J. Arginine pathways and the inflammatory response: interregulation of nitric oxide and polyamines: review article. Amino Acids 2004, 26:321-329. 10.1007/s00726-004-0078-4, 15290337.
41. Grillo MA, Colombatto S. Metabolism and function in animal tissues of agmatine, a biogenic amine formed from arginine. Amino Acids 2004, 26:3-8. 10.1007/s00726-003-0030-z, 14752610.
42. Raasch W, Regunathan S, Li G, Reis DJ. Agmatine is widely and unequally distributed in rat organs. Ann N Y Acad Sci 1995, 763:330-334. 10.1111/j.1749-6632.1995.tb32419.x, 7677343.
43. Halaris A, Piletz JE. Relevance of imidazoline receptors and agmatine to psychiatry: a decade of progress. Ann N Y Acad Sci 2003, 1009:1-20. 10.1196/annals.1304.001, 15028565.
44. Chen X, Kalbacher H, Grunder S. The tarantula toxin psalmotoxin 1 inhibits acid-sensing ion channel (ASIC) 1a by increasing its apparent H+ affinity. J Gen Physiol 2005, 126:71-79. 10.1085/jgp.200509303, 2266618, 15955877.
45. Chen X, Kalbacher H, Grunder S. Interaction of acid-sensing ion channel (ASIC) 1 with the tarantula toxin psalmotoxin 1 is state dependent. J Gen Physiol 2006, 127:267-276. 10.1085/jgp.200509409, 2151504, 16505147.
46. Steen KH, Reeh PW. Sustained graded pain and hyperalgesia from harmless experimental tissue acidosis in human skin. Neurosci Lett 1993, 154:113-116. 10.1016/0304-3940(93)90184-M, 8361622.
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. 150796, 12393854.
48. Jones NG, Slater R, Cadiou H, McNaughton P, McMahon SB. Acid-induced pain and its modulation in humans. J Neurosci 2004, 24:10974-10979. 10.1523/JNEUROSCI.2619-04.2004, 15574747.
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. 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.
51. 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, 10:336-342. 10.1016/j.jpain.2008.10.010, 2675631, 19185546.
52. Yiangou Y, Facer P, Smith JA, 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. 10.1097/00042737-200108000-00003, 11507351.
53. 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, 129:102-112. 10.1016/j.pain.2006.09.038, 1941845, 17134831.
54. Smith ES, Cadiou H, McNaughton PA. Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action. Neuroscience 2007, 145:686-698. 10.1016/j.neuroscience.2006.12.024, 17258862.
55. Allen NJ, Attwell D. Modulation of ASIC channels in rat cerebellar Purkinje neurons by ischaemia-related signals. J Physiol 2002, 543:521-529. 10.1113/jphysiol.2002.020297, 2290513, 12205186.
56. Immke DC, McCleskey EW. Protons open acid-sensing ion channels by catalyzing relief of Ca2+ blockade. Neuron 2003, 37:75-84. 10.1016/S0896-6273(02)01130-3, 12526774.
57. Benson CJ, Xie J, Wemmie JA, Price MP, Henss JM, Welsh MJ, Snyder PM. Heteromultimers of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc Natl Acad Sci USA 2002, 99:2338-2343. 10.1073/pnas.032678399, 122366, 11854527.
58. Xie J, Price MP, Wemmie JA, Askwith CC, Welsh MJ. ASIC3 and ASIC1 mediate FMRFamide-related peptide enhancement of H+-gated currents in cultured dorsal root ganglion neurons. J Neurophysiol 2003, 89:2459-2465. 10.1152/jn.00707.2002, 12612000.
59. Birdsong WT, Fierro L, Williams FG, Spelta V, Naves LA, Knowles M, Marsh-Haffner J, Adelman JP, Almers W, Elde RP, McCleskey EW. Sensing muscle ischemia: coincident detection of acid and ATP via interplay of two ion channels. Neuron 2010, 68:739-749. 10.1016/j.neuron.2010.09.029, 21092862.
60. 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