Alcohol inhibition of the NMDA receptor function, long-term potentiation, and fear learning requires striatal-enriched protein tyrosine phosphatase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 16, 2011, Pages 6650-6655

  Hicklin, Tianna R ^a   Wu, Peter H ^b,c   Radcliffe, Richard A ^a   Freund, Ronald K ^b   Goebel Goody, Susan M ^a,d   Correa, Paulo R ^d   Proctor, William R ^b,c   Lombroso, Paul J ^d   Browning, Michael D ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c DEPARTMENT OF VETERANS AFFAIRS   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Null mutant mice; Whole cell currents

Indexed keywords

ALCOHOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN TYROSINE PHOSPHATASE; STRIATAL ENRICHED PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

ALCOHOLISM; AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; ENZYME INHIBITION; FEAR; HIPPOCAMPUS; IMMUNOPRECIPITATION; LEARNING; LONG TERM POTENTIATION; MOUSE; NONHUMAN; POINT MUTATION; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING;

AMNESIA; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; FEAR; HUMANS; LEARNING; LONG-TERM POTENTIATION; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC POTENTIALS;

MUS;

EID: 79955580396     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1017856108     Document Type: Article

References (55)

1. White AM, Matthews DB, Best PJ (2000) Ethanol, memory, and hippocampal function: A review of recent findings. Hippocampus 10(1):88-93. (Pubitemid 30107594)
2. Bliss TV, Collingridge GL (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361(6407):31-39. (Pubitemid 23020772)
3. Morris RG, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776. (Pubitemid 16145031)
4. Lovinger DM, White G, Weight FF (1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243:1721-1724. (Pubitemid 19106970)
5. Hoffman PL, Moses F, Tabakoff B (1989) Selective inhibition by ethanol of glutamatestimulated cyclic GMP production in primary cultures of cerebellar granule cells. Neuropharmacology 28:1239-1243. (Pubitemid 19277039)
6. Krystal JH, Petrakis IL, Mason G, Trevisan L, D'Souza DC (2003) N-methyl-D-aspartate glutamate receptors and alcoholism: Reward, dependence, treatment, and vulnerability. Pharmacol Ther 99(1):79-94. (Pubitemid 36694751)
7. Kauer JA, Malenka RC (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8: 844-858. (Pubitemid 350006216)
8. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540. (Pubitemid 24100885)
9. Nakanishi N, Axel R, Shneider NA (1992) Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 89:8552-8556.
10. Chu B, Anantharam V, Treistman SN (1995) Ethanol inhibition of recombinant heteromeric NMDA channels in the presence and absence of modulators. J Neurochem 65(1):140-148.
11. Masood K, Wu C, Brauneis U, Weight FF (1994) Differential ethanol sensitivity of recombinant N-methyl-D-aspartate receptor subunits. Mol Pharmacol 45:324-329. (Pubitemid 24063088)
12. Salter MW, Kalia LV (2004) Src kinases: A hub for NMDA receptor regulation. Nat Rev Neurosci 5:317-328. (Pubitemid 38478658)
13. Alvestad RM, et al. (2003) Tyrosine dephosphorylation and ethanol inhibition of NMethyl- D-aspartate receptor function. J Biol Chem 278:11020-11025. (Pubitemid 36792651)
14. Roche KW, et al. (2001) Molecular determinants of NMDA receptor internalization. Nat Neurosci 4:794-802. (Pubitemid 32702511)
15. Prybylowski K, et al. (2005) The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 47:845-857. (Pubitemid 41266951)
16. Ferrani-Kile K, Randall PK, Leslie SW (2003) Acute ethanol affects phosphorylation state of the NMDA receptor complex: Implication of tyrosine phosphatases and protein kinase A. Brain Res Mol Brain Res 115(1):78-86. (Pubitemid 36725038)
17. Lombroso PJ, Naegele JR, Sharma E, Lerner M (1993) A protein tyrosine phosphatase expressed within dopaminoceptive neurons of the basal ganglia and related structures. J Neurosci 13:3064-3074. (Pubitemid 23199231)
18. Pelkey KA, et al. (2002) Tyrosine phosphatase STEP is a tonic brake on induction of long-term potentiation. Neuron 34(1):127-138. (Pubitemid 34270704)
19. Paul S, et al. (2007) The striatal-enriched protein tyrosine phosphatase gates long-term potentiation and fear memory in the lateral amygdala. Biol Psychiatry 61:1049-1061. (Pubitemid 46551973)
20. Wu PH, Coultrap SJ, Browning MD, Proctor WR (2010) Correlated changes in NMDA receptor phosphorylation, functional activity, and sedation by chronic ethanol consumption. J Neurochem 115:1112-1122.
21. Venkitaramani DV, et al. (2009) Knockout of striatal enriched protein tyrosine phosphatase in mice results in increased ERK1/2 phosphorylation. Synapse 63(1):69-81.
22. Wehner JM, Bowers BJ, Paylor R (1996) The use of null mutant mice to study complex learning and memory processes. Behav Genet 26:301-312. (Pubitemid 26234783)
23. Morrisett RA, Swartzwelder HS (1993) Attenuation of hippocampal long-term potentiation by ethanol: A patch-clamp analysis of glutamatergic and GABAergic mechanisms. J Neurosci 13:2264-2272. (Pubitemid 23113432)
24. Durand D, Carlen PL (1984) Impairment of long-term potentiation in rat hippocampus following chronic ethanol treatment. Brain Res 308:325-332. (Pubitemid 14061965)
25. Sinclair JG, Lo GF (1986) Ethanol blocks tetanic and calcium-induced long-term potentiation in the hippocampal slice. Gen Pharmacol 17:231-233. (Pubitemid 16131101)
26. Schummers J, Bentz S, Browning MD (1997) Ethanol's inhibition of LTP may not be mediated solely via direct effects on theNMDAreceptor. Alcohol Clin Exp Res 21:404-408. (Pubitemid 27217182)
27. Ren H, et al. (2008) Functional interactions of alcohol-sensitive sites in the N-methyl-Daspartate receptor M3 and M4 domains. J Biol Chem 283:8250-8257.
28. Miyakawa T, et al. (1997) Fyn-kinase as a determinant of ethanol sensitivity: Relation to NMDA-receptor function. Science 278:698-701. (Pubitemid 27464970)
29. Kalluri HSG, Ticku MK (1999) Effect of ethanol on phosphorylation of the NMDAR2B subunit in mouse cortical neurons. Brain Res Mol Brain Res 68(1-2):159-168. (Pubitemid 29244004)
30. Anders DL, et al. (1999) Fyn tyrosine kinase reduces the ethanol inhibition of recombinant NR1/NR2A but not NR1/NR2B NMDA receptors expressed in HEK 293 cells. J Neurochem 72:1389-1393. (Pubitemid 29140807)
31. Snyder EM, et al. (2005) Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 8:1051-1058. (Pubitemid 41061516)
32. Zhang Y, et al. (2008) The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation. J Neurosci 28:10561-10566.
33. Yaka R, Phamluong K, Ron D (2003) Scaffolding of Fyn kinase to the NMDA receptor determines brain region sensitivity to ethanol. J Neurosci 23:3623-3632. (Pubitemid 36958470)
34. Wang J, et al. (2007) Ethanol induces long-term facilitation of NR2B-NMDA receptor activity in the dorsal striatum: Implications for alcohol drinking behavior. J Neurosci 27:3593-3602. (Pubitemid 46515141)
35. Nguyen TH, Liu J, Lombroso PJ (2002) Striatal enriched phosphatase 61 dephosphorylates Fyn at phosphotyrosine 420. J Biol Chem 277:24274-24279. (Pubitemid 34951945)
36. Nakazawa T, et al. (2001) Characterization of Fyn-mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J Biol Chem 276:693-699. (Pubitemid 32050862)
37. Zhao Y, Zhang ZY (1996) Reactivity of alcohols toward the phosphoenzyme intermediate in the protein-tyrosine phosphatase-catalyzed reaction: Probing the transition state of the dephosphorylation step. Biochemistry 35:11797-11804. (Pubitemid 26303698)
38. Kojima N, Sakamoto T, Endo S, Niki H (2005) Impairment of conditioned freezing to tone, but not to context, in Fyn-transgenic mice: relationship to NMDA receptor subunit 2B function. Eur J Neurosci 21:1359-1369. (Pubitemid 40516634)
39. Sah P, Westbrook RF, Lüthi A (2008) Fear conditioning and long-term potentiation in the amygdala: What really is the connection? Ann N Y Acad Sci 1129:88-95.
40. Melia KR, Ryabinin AE, Corodimas KP, Wilson MC, Ledoux JE (1996) Hippocampaldependent learning and experience-dependent activation of the hippocampus are preferentially disrupted by ethanol. Neuroscience 74:313-322. (Pubitemid 26274203)
41. Gould TJ (2003) Ethanol disrupts fear conditioning in C57BL/6 mice. J Psychopharmacol 17(1):77-81.
42. Kim JJ, Jung MW (2006) Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review. Neurosci Biobehav Rev 30:188-202. (Pubitemid 41821808)
43. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24: 897-931.
44. Poulos AM, Ponnusamy R, Dong HW, Fanselow MS (2010) Compensation in the neural circuitry of fear conditioning awakens learning circuits in the bed nuclei of the stria terminalis. Proc Natl Acad Sci USA 107:14881-14886.
45. Smothers CT, Woodward JJ (2006) Effects of amino acid substitutions in transmembrane domains of the NR1 subunit on the ethanol inhibition of recombinant N-methyl-D-aspartate receptors. Alcohol Clin Exp Res 30:523-530.
46. Wright JM, Peoples RW, Weight FF (1996) Single-channel and whole-cell analysis of ethanol inhibition of NMDA-activated currents in cultured mouse cortical and hippocampal neurons. Brain Res 738:249-256. (Pubitemid 26378919)
47. Peoples RW, Stewart RR (2000) Alcohols inhibit N-methyl-D-aspartate receptors via a site exposed to the extracellular environment. Neuropharmacology 39:1681-1691. (Pubitemid 30398473)
48. Khanna JM, Shah G, Weiner J, Wu PH, Kalant H (1993) Effect of NMDA receptor antagonists on rapid tolerance to ethanol. Eur J Pharmacol 230(1):23-31. (Pubitemid 23024976)
49. Hölter SM, Danysz W, Spanagel R (2000) Novel uncompetitive N-methyl-D-aspartate (NMDA)-receptor antagonist MRZ 2/579 suppresses ethanol intake in long-term ethanol-experienced rats and generalizes to ethanol cue in drug discrimination procedure. J Pharmacol Exp Ther 292:545-552. (Pubitemid 30067417)
50. Wu PH, Poelchen W, Proctor WR (2005) Differential GABAB receptor modulation of ethanol effects on GABA(A) synaptic activity in hippocampal CA1 neurons. J Pharmacol Exp Ther 312:1082-1089. (Pubitemid 40293767)
51. Wehner JM, et al. (1997) Quantitative trait locus analysis of contextual fear conditioning in mice. Nat Genet 17:331-334. (Pubitemid 27475999)
52. Wehner JM, Radcliffe RA (2003) Cued and contextual fear conditioning in mice. Current Protocols in Neuroscience (J. Wiley, New York).
53. Radcliffe RA, et al. (2006) Confirmation of quantitative trait loci for ethanol sensitivity and neurotensin receptor density in crosses derived from the inbred high and low alcohol sensitive selectively bred rat lines. Psychopharmacology (Berl) 188:343-354. (Pubitemid 44387462)
54. Coultrap SJ, Nixon KM, Alvestad RM, Valenzuela CF, Browning MD (2005) Differential expression of NMDA receptor subunits and splice variants among the CA1, CA3 and dentate gyrus of the adult rat. Brain Res Mol Brain Res 135(1-2):104-111. (Pubitemid 40602403)
55. Goebel-Goody SM, Davies KD, Alvestad Linger RM, Freund RK, Browning MD (2009) Phospho-regulation of synaptic and extrasynaptic N-methyl-D-aspartate receptors in adult hippocampal slices. Neuroscience 158:1446-1459.