Scaffolding of Fyn kinase to the NMDA receptor determines brain region sensitivity to ethanol

Journal of Neuroscience

Volumn 23, Issue 9, 2003, Pages 3623-3632

  Yaka, Rami ^a   Phamluong, Khanhky ^a   Ron, Dorit ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^b NONE   (United States)

Author keywords

Ethanol; Fyn; NMDA; RACK1; Scaffolding proteins; Tyrosine phosphorylation

Indexed keywords

ALCOHOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN; PROTEIN KINASE; PROTEIN KINASE FYN; PROTEIN RACK1; RECEPTOR SUBUNIT; SCAFFOLDING PROTEIN; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; FYN PROTEIN, RAT; NR2B NMDA RECEPTOR; ONCOPROTEIN; RECEPTORS FOR ACTIVATED C KINASE;

ALCOHOL ABUSE; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; BRAIN; BRAIN LEVEL; CELL COMPARTMENTALIZATION; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN; BRAIN CHEMISTRY; CELL COMPARTMENTATION; CEREBRAL CORTEX; ETHANOL; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; MALE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FYN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CELL SURFACE; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0037868950     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-09-03623.2003     Document Type: Article

References (41)

1. Ali DW, Salter MW (2001) NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr Opin Neurobiol 11:336-342.
2. Chandler LI, Harris RA, Crews FT (1998) Ethanol tolerance and synaptic plasticity. Trends Pharmacol Sci 19:491-495.
3. Fagni L, Worley PF, Ango F (2002) Homer as both a scaffold and transduction molecule. Sci STKE 2002:RE8.
4. Givens B, McMahon K (1995) Ethanol suppresses the induction of long-term potentiation in vivo. Brain Res 688:27-33.
5. Gonzalez LP, Veatch LM, Ticku MK, Becker HC (2001) Alcohol withdrawal kindling: mechanisms and implications for treatment. Alcohol Clin Exp Res 25:197S-201S.
6. Grant SG, O'Dell TJ, Karl KA, Stein PL, Soriano P, Kandel ER (1992) Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258:1903-1910.
7. Grover CA, Frye GD, Griffith WH (1994) Acute tolerance to ethanol inhibition of NMDA-mediated EPSPs in the CA1 region of the rat hippocampus. Brain Res 642:70-76.
8. He DY, Vagts AJ, Yaka R, Ron D (2002) Ethanol induces gene expression via nuclear compartmentalization of receptor for activated C kinase 1. Mol Pharmacol 62:272-280.
9. Heidinger V, Manzerra P, Wang XQ, Strasser U, Yu SP, Choi DW, Behrens MM (2002) Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J Neurosci 22:5452-5461.
10. Hisatsune C, Umemori H, Inoue T, Michikawa T, Kohda K, Mikoshiba K, Yamamoto T (1997) Phosphorylation-dependent regulation of N-methyl-D-aspartate receptors by calmodulin. J Biol Chem 272:20805-20810.
11. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III: its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96:1374-1388.
12. Kennedy MB (1997) The postsynaptic density at glutamatergic synapses. Trends Neurosci 20:264-268.
13. Kohr G, Seeburg PH (1996) Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the src family. J Physiol (Lond) 492:445-452.
14. Kumari M, Ticku MK (2000) Regulation of NMDA receptors by ethanol. Prog Drug Res 54:152-189.
15. Lau LF, Huganir RL (1995) Differential tyrosine phosphorylation of N-methyl-D-aspartate receptor subunits. J Biol Chem 270:20036-20041.
16. Leonard AS, Hell JW (1997) Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D-aspartate receptors at different sites. J Biol Chem 272:12107-12115.
17. Lovinger DM, White G, Weight FF (1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243:1721-1724.
18. Lovinger DM, White G, Weight FF (1990) NMDA receptor-mediated synaptic excitation selectively inhibited by ethanol in hippocampal slice from adult rat. J Neurosci 10:1372-1379.
19. Lu WY, Xiong ZG, Lei S, Orser BA, Dudek E, Browning MD, MacDonald JF (1999) G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat Neurosci 2:331-338.
20. Lu YM, Roder JC, Davidow J, Salter MW (1998) Src activation in the induction of long-term potentiation in CA1 hippocampal neurons. Science 279:1363-1367.
21. Ludvig N, George MA, Tang HM, Gonzales RA, Bungay PM (2001) Evidence for the ability of hippocampal neurons to develop acute tolerance to ethanol in behaving rats. Brain Res 900:252-260.
22. Mannaioni G, Marino MI, Valenti O, Traynelis SF, Conn PI (2001) Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J Neurosci 21:5925-5934.
23. Miyakawa T, Yagi T, Kitazawa H, Yasuda M, Kawai N, Tsuboi K, Niki H (1997) Fyn-kinase as a determinant of ethanol sensitivity: relation to NMDA-receptor function. Science 278:698-701.
24. Moon IS, Apperson ML, Kennedy MB (1994) The major tyrosine-phosphorylated protein in the postsynaptic density fraction is N-methyl-D-aspartate receptor subunit 2B. Proc Natl Acad Sci USA 91:3954-3958.
25. 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.
26. Nagahara H, Vocero-Akbani AM, Snyder EL, Ho A, Latham DG, Lissy NA, Becker-Hapak M, Ezhevsky SA, Dowdy SF (1998) Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat Med 4:1449-1452.
27. Nakazawa T, Komai S, Tezuka T, Hisatsune C, Umemori H, Semba K, Mishina M, Manabe T, Yamamoto T (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.
28. Narita M, Soma M, Mizoguchi H, Tseng LF, Suzuki T (2000) Implications of the NR2B subunit-containing NMDA receptor localized in mouse limbic forebrain in ethanol dependence. Eur J Pharmacol 401:191-195.
29. O'Brien RI, Lau LF, Huganir RL (1998) Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr Opin Neurobiol 8:364-369.
30. Ohnishi H, Yamamori S, Ono K, Aoyagi K, Kondo S, Takahashi M (2001) A src family tyrosine kinase inhibits neurotransmitter release from neuronal cells. Proc Natl Acad Sci USA 98:10930-10935.
31. Pandey SC (1998) Neuronal signaling systems and ethanol dependence. Mol Neurobiol 17:1-15.
32. Pawson T, Scott JD (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075-2080.
33. Ron D, Vagts AJ, Dohrman DP, Yaka R, Jiang Z, Yao L, Crabbe J, Grisel JE, Diamond I (2000) Uncoupling of {beta}IIPKC from its targeting protein RACK1 in response to ethanol in cultured cells and mouse brain. FASEB J 14:2303-2314.
34. Sheng M, Pak DT (1999) Glutamate receptor anchoring proteins and the molecular organization of excitatory synapses. Ann NY Acad Sci 868:483-493.
35. Stubbs CD, Slater SJ (1999) Ethanol and protein kinase C. Alcohol Clin Exp Res 23:1552-1560.
36. Sucher NJ, Awobuluyi M, Choi YB, Lipton SA (1996) NMDA receptors: from genes to channels. Trends Pharmacol Sci 17:348-355.
37. Takasu MA, Dalva MB, Zigmond RE, Greenberg ME (2002) Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295:491-495.
38. Wang YT, Salter MW (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369:233-235.
39. Yaka R, Thornton C, Vagts AJ, Phamluong K, Bonci A, Ron D (2002) NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc Natl Acad Sci USA 99:5710-5715.
40. Yu XM, Askalan R, Keil II GJ, Salter MW (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275:674-678.
41. Zheng F, Gingrich MB, Traynelis SF, Conn PJ (1998) Tyrosine kinase potentiates NMDA receptor currents by reducing tonic zinc inhibition. Nat Neurosci 1:185-191.