Molecular mechanism of constitutive endocytosis of acid-sensing ion channel 1a and its protective function in acidosis-induced neuronal death

Journal of Neuroscience

Volumn 33, Issue 16, 2013, Pages 7066-7078

  Zeng, Wei Zheng ^a,b   Liu, Di Shi ^b   Duan, Bo ^a,e   Song, Xing Lei ^b   Wang, Xiang ^b   Wei, Dong ^c   Jiang, Wen ^c   Zhu, Michael X ^d   Li, Yong ^b   Xu, Tian Le ^b  

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

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

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; ADAPTOR PROTEIN; CLATHRIN; DYNAMIN; SHORT HAIRPIN RNA; TYRPHOSTIN;

ACIDOSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CELL FRACTIONATION; CELL MIGRATION; CONTROLLED STUDY; DNA SEQUENCE; DNA TRANSFECTION; ELECTROPHYSIOLOGY; EMBRYO; ENDOCYTOSIS; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NERVE INJURY; NONHUMAN; PATHOPHYSIOLOGY; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE;

ACID SENSING ION CHANNELS; ACIDOSIS; ADAPTOR PROTEIN COMPLEX 2; ANIMALS; BIOTINYLATION; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; CLATHRIN; CRICETINAE; DYNAMINS; ELECTRIC STIMULATION; EMBRYO, MAMMALIAN; ENDOCYTOSIS; GREEN FLUORESCENT PROTEINS; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; NEURONS; PATCH-CLAMP TECHNIQUES; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPIDER VENOMS; SUBCELLULAR FRACTIONS; TRANSFECTION; TYRPHOSTINS;

EID: 84876258536     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5206-12.2013     Document Type: Article

References (59)

1. Arias RL, Sung ML, Vasylyev D, Zhang MY, Albinson K, Kubek K, Kagan N, Beyer C, Lin Q, Dwyer JM, Zaleska MM, Bowlby MR, Dunlop J, Mon-aghan M (2008) Amiloride is neuroprotective in an MPTP model of Parkinson's disease. Neurobiol Dis 31:334-341.
2. Banbury DN, Oakley JD, Sessions RB, Banting G (2003) Tyrphostin A23 inhibits internalization of the transferrin receptor by perturbing the interaction between tyrosine motifs and the medium chain subunit of the AP-2 adaptor complex. JBiolChem 278:12022-12028.
3. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, von Zastrow M, Malenka RC (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3:1291-1300.
4. Chai S, Li M, Branigan D, Xiong ZG, Simon RP (2010) Activation of acid-sensing ion channel 1a (ASIC1a) by surface trafficking. J Biol Chem 285: 13002-13011.
5. Chen X, Gründer S (2007) Permeating protons contribute to tachyphylaxis of the acid-sensing ion channel (ASIC) 1a. J Physiol 579:657-670.
6. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127:915-934.
7. Daukas G, Zigmond SH (1985) Inhibition of receptor-mediated but not fluid-phase endocytosis in polymorphonuclear leukocytes. J CellBiol 101: 1673-1679.
8. Duan B, Wu LJ, Yu YQ, Ding Y, Jing L, Xu L, Chen J, Xu TL (2007) Upregulation of acid-sensing ion channel ASIC1a in spinal dorsal horn neurons contributes to inflammatory pain hypersensitivity. J Neurosci 27:11139-11148.
9. Duan B, Wang YZ, Yang T, Chu XP, Yu Y, Huang Y, Cao H, Hansen J, Simon RP, Zhu MX, Xiong ZG, Xu TL (2011) Extracellular spermine exacerbates ischemic neuronal injury through sensitization of ASIC1a channels to extracellular acidosis. J Neurosci 31:2101-2112.
10. Duan B, Liu DS, Huang Y, Zeng WZ, Wang X, Yu H, Zhu MX, Chen ZY, Xu TL (2012) PI3-kinase/Akt pathway-regulated membrane insertion of acid-sensing ion channel 1a underlies BDNF-induced pain hypersensitivity. J Neurosci 32:6351-6363.
11. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
12. Escoubas P, De Weille JR, Lecoq A, Diochot S, Waldmann R, Champigny G, Moinier D, Menez A, Lazdunski M (2000) Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J Biol Chem 275: 25116-25121.
13. Fang L, Garuti R, Kim BY, Wade JB, Welling PA (2009) The ARH adaptor protein regulates endocytosis of the ROMK potassium secretory channel in mouse kidney. J Clin Invest 119:3278-3289.
14. Ferguson SM, Brasnjo G, Hayashi M, Wolfel M, Collesi C, Giovedi S, Rai-mondi A, Gong LW, Ariel P, Paradise S, O'Toole E, Flavell R, Cremona O, Miesenbock G, Ryan TA, De Camilli P (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316:570-574.
15. Friese MA, Craner MJ, Etzensperger R, Vergo S, Wemmie JA, Welsh MJ, Vincent A, Fugger L (2007) Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med 13:1483-1489.
16. Gao J, Duan B, Wang DG, Deng XH, Zhang GY, Xu L, Xu TL (2005) Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron 48:635-646.
17. Green EM, Barrett CF, Bultynck G, Shamah SM, Dolmetsch RE (2007) The tumor suppressor eIF3e mediates calcium-dependent internalization of the L-type calcium channel CaV1.2. Neuron 55:615-632.
18. Gründer S, Chen X (2010) Structure, function, and pharmacology of acid-sensing ion channels (ASICs): focus on ASIC1a. Int J Physiol Patho-physiol Pharmacol 2:73-94.
19. Hallett PJ, Collins TL, Standaert DG, Dunah AW (2008) Biochemical fractionation of brain tissue for studies of receptor distribution and trafficking. Curr Protoc Neurosci Chapter 1:Unit 1.16.
20. Henry PC, Kanelis V, O'Brien MC, Kim B, Gautschi I, Forman-Kay J, Schild L, Rotin D (2003) Affinity and specificity of interactions between Nedd4 isoforms and the epithelial Na+ channel. J Biol Chem 278:20019-20028.
21. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006) PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314:1458-1461.
22. Heuser JE, Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389-400.
23. Hill TA, Gordon CP, McGeachie AB, Venn-Brown B, Odell LR, Chau N, Quan A, Mariana A, Sakoff JA, Chircop M, Robinson PJ, McCluskey A (2009) Inhibition of dynamin mediated endocytosis by the dynoles: synthesis and functional activity of a family of indoles. J Med Chem 52:3762-3773.
24. Hruska-Hageman AM, Wemmie JA, Price MP, Welsh MJ (2002) Interaction of the synaptic protein PICK1 (protein interacting with C kinase 1) with the non-voltage gated sodium channels BNC1 (brain Na+ channel 1) and ASIC (acid-sensing ion channel). Biochem J 361:443-450.
25. Kellenberger S, Schild L (2002) Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 82:735-767.
26. Kelly BL, Ferreira A (2006) /3-Amyloid-induced dynamin 1 degradation is mediated by N-methyl-D-aspartate receptors in hippocampal neurons. J Biol Chem 281:28079-28089.
27. Knight KK, Olson DR, Zhou R, Snyder PM (2006) Liddle's syndrome mutations increase Na+ transport through dual effects on epithelial Na+ channel surface expression and proteolytic cleavage. Proc Natl Acad Sci USA 103:2805-2808.
28. Lingueglia E (2007) Acid-sensing ion channels in sensory perception. J Biol Chem 282:17325-17329.
29. Ma D, Taneja TK, Hagen BM, Kim BY, Ortega B, Lederer WJ, Welling PA (2011) Golgi export of the Kir2.1 channel is driven by a trafficking signal located within its tertiary structure. Cell 145:1102-1115.
30. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10:839-850.
31. Mankouri J, Taneja TK, Smith AJ, Ponnambalam S, Sivaprasadarao A (2006) Kir6.2 mutations causing neonatal diabetes prevent endocytosis of ATP-sensitive potassium channels. EMBO J 25:4142-4151.
32. Martin S, Henley JM (2004) Activity-dependent endocytic sorting of kainate receptors to recycling or degradation pathways. EMBO J 23: 4749-4759.
33. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533.
34. Nixon RA (2005) Endosome function and dysfunction in Alzheimer's disease and other neurodegenerative diseases. Neurobiol Aging 26:373-382.
35. Piwon N, Günther W, Schwake M, Bosl MR, Jentsch TJ (2000) ClC-5 Cl--channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 408:369-373.
36. Praefcke GJ, McMahon HT (2004) The dynamin super family: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5:133-147.
37. Rudinskiy N, Grishchuk Y, Vaslin A, Puyal J, Delacourte A, Hirling H, Clarke PG, Luthi-Carter R (2009) Calpain hydrolysis of a- and /32-adaptins decreases clathrin-dependent endocytosis and may promote neurodegen-eration. J Biol Chem 284:12447-12458.
38. 2+ entry. Cell Calcium 45: 319-325.
39. Schild L, Lu Y, Gautschi I, Schneeberger E, Lifton RP, Rossier BC (1996) Identification of a PY motif in the epithelial Na channel subunits as a target sequence for mutations causing channel activation found in Liddle syndrome. EMBO J 15:2381-2387.
40. Sherwood TW, Askwith CC (2009) Dynorphin opioid peptides enhance acid-sensing ion channel 1a activity and acidosis-induced neuronal death. J Neurosci 29:14371-14380.
41. Sherwood TW, Lee KG, Gormley MG, Askwith CC (2011) Heteromeric acid-sensing ion channels (ASICs) composed of ASIC2b and ASIC1a display novel channel properties and contribute to acidosis-induced neuronal death. J Neurosci 31:9723-9734.
42. Shimkets RA, Warnock DG, Bositis CM, Nelson-Williams C, Hansson JH, Schambelan M, Gill JR Jr, Ulick S, Milora RV, Findling JW, et al. (1994) Liddle's syndrome: heritable human hypertension caused by mutations in the /3 subunitofthe epithelial sodium channel. Cell 79:407-414.
43. Snyder PM, Price MP, McDonald FJ, Adams CM, Volk KA, Zeiher BG, Stokes JB, Welsh MJ (1995) Mechanism by which Liddle's syndrome mutations increase activity of a human epithelial Na+ channel. Cell 83:969-978.
44. Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609-622.
45. Tai CY, Mysore SP, Chiu C, Schuman EM (2007) Activity-regulated N-cadherin endocytosis. Neuron 54:771-785.
46. Traub LM (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10:583-596.
47. Troulinaki K, Tavernarakis N (2012) Endocytosis and intracellular trafficking contribute to necrotic neurodegeneration in C. elegans. EMBO J 31: 654-666.
48. van der Bliek AM, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, Schmid SL (1993) Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol 122:553-563.
49. von Heijne G (1992) Membrane protein structure prediction: hydropho-bicity analysis and the positive-inside rule. J Mol Biol 225:487-494.
50. Wang H, Traub LM, Weixel KM, Hawryluk MJ, Shah N, Edinger RS, Perry CJ, Kester L, Butterworth MB, Peters KW, Kleyman TR, Frizzell RA, Johnson JP (2006) Clathrin-mediated endocytosis of the epithelial sodium channel: role of epsin. J Biol Chem 281:14129-14135.
51. Wang YZ, Xu TL (2011) Acidosis, acid-sensing ion channels, and neuronal cell death. Mol Neurobiol 44:350-358.
52. Wemmie JA, Price MP, Welsh MJ (2006) Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 29: 578-586.
53. Wong HK, Bauer PO, Kurosawa M, Goswami A, Washizu C, Machida Y, Tosaki A, Yamada M, Knöpfel T, Nakamura T, Nukina N (2008) Blocking acid-sensing ion channel 1 alleviates Huntington's disease pathology via an ubiquitin-proteasome system-dependent mechanism. Hum Mol Genet 17:3223-3235.
54. Wu Y, Liang S, Oda Y, Ohmori I, Nishiki T, Takei K, Matsui H, Tomizawa K (2007) Truncations of amphiphysin I by calpain inhibit vesicle endocy-tosis during neural hyperexcitation. EMBO J 26:2981-2990.
55. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, Wei WL, MacDonald JF, Wemmie JA, Price MP, Welsh MJ, Simon RP (2004) Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118:687-698.
56. Xiong ZG, Pignataro G, Li M, Chang SY, Simon RP (2008) Acid-sensing ion channels (ASICs) as pharmacological targets for neurodegenerative diseases. Curr Opin Pharmacol 8:25-32.
57. Xu TL, Duan B (2009) Calcium-permeable acid-sensing ion channel in no-ciceptive plasticity: a new target for pain control. Prog Neurobiol 87:171-180.
58. Yang Y, Yu Y, Cheng J, Liu Y, Liu DS, Wang J, Zhu MX, Wang R, Xu TL (2012) Highly conserved salt bridge stabilizes rigid signal patch at extracellular loop critical for surface expression of acid-sensing ion channels. J Biol Chem 287:14443-14455.
59. Yermolaieva O, Leonard AS, Schnizler MK, Abboud FM, Welsh MJ (2004) Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc Natl Acad Sci USA 101:6752-6757.