NMDA and β1-adrenergic receptors differentially signal phosphorylation of glutamate receptor type 1 in area CA1 of hippocampus

Journal of Neuroscience

Volumn 23, Issue 13, 2003, Pages 5827-5834

  Vanhoose, Amanda M ^a   Winder, Danny G ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA receptor; Long term potentiation; LTP; Neuromodulation; Neuromodulatory; PKA; Synaptic plasticity

Indexed keywords

BETA 1 ADRENERGIC RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHATASE; PROTEIN SUBUNIT; ADRENERGIC RECEPTOR BLOCKING AGENT; AMINO ACID; AMPA RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; N METHYLASPARTIC ACID;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME INHIBITION; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANIMAL; C57BL MOUSE; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ADRENERGIC ANTAGONISTS; ADRENERGIC BETA-AGONISTS; AMINO ACIDS, CYCLIC; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; N-METHYLASPARTATE; NEURONAL PLASTICITY; PHOSPHORYLATION; RECEPTORS, ADRENERGIC, BETA-1; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

EID: 0038721940     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-13-05827.2003     Document Type: Article

References (40)

1. Bailey CH, Giustetto M, Huang YY, Hawkins RD, Kandel ER (2000) Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat Rev Neurosci 1:11-20.
2. Baker LP, Nielsen MD, Impey S, Hacker BM, Poser SW, Chan MY, Storm DR (1999) Regulation and immunohistochemical localization of βγ-stimulated adenylyl cyclases in mouse hippocampus. J Neurosci 19:180-192.
3. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, Traynelis SF (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20:89-102.
4. Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, Iyengar R, Landau EM (1998) Gating of CAMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280:1940-1942.
5. Blitzer RD, Wong T, Nouranifar R, Iyengar R, Landau EM (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15:1403-1414.
6. Booze RM, Crisostomo EA, Davis JN (1993) β-adrenergic receptors in the hippocampal and retrohippocampal regions of rats and guinea pigs: autoradiographic and immunohistochemical studies. Synapse 13:206-214.
7. Brown GP, Blitzer RD, Connor JH, Wong T, Shenolikar S, Iyengar R, Landau EM (2000) Long-term potentiation induced by theta frequency stimulation is regulated by a protein phosphatase-1-operated gate. J Neurosci 20:7880-7887.
8. Chao SZ, Ariano MA, Peterson DA, Wolf ME (2002a) D1 dopamine receptor stimulation increases GluR1 surface expression in nucleus accumbens neurons. J Neurochem 83:704-712.
9. 1 dopamine receptor stimulation increases GluR1 phosphorylation in postnatal nucleus accumbens cultures. J Neurochem 81:984-992.
10. 2+ channel activity in area CA1 of hippocampus. Proc Natl Acad Sci USA 88:6467-6471.
11. Chetkovich DM, Sweatt JD (1993) nMDA receptor activation increases cyclic AMP in area CAl of the hippocampus via calcium/calmodulin stimulation of adenylyl cyclase. J Neurochem 61:1933-1942.
12. Colledge M, Dean RA, Scott GK, Langeberg LK, Huganir RL, Scott JD (2000) Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 27:107-119.
13. 2+ channel Cav1.2 Science 293:98-101.
14. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
15. English JD, Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271:24329-24332.
16. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 21:21.
17. 2+/calmodulin-dependent protein kinase II in long-term potentiation. J Neurosci 21:7053-7062.
18. Gomez LL, Alam S, Smith KE, Horne E, Dell'Acqua ML (2002) Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin. J Neurosci 22:7027-7044.
19. Hu LA, Tang Y, Miller WE, Cong M, Lau AG, Lefkowitz RJ, Hall RA (2000) beta 1-adrenergic receptor association with PSD-95: inhibition of receptor internalization and facilitation of beta 1-adrenergic receptor interaction with N-methyl-D-aspartate receptors. J Biol Chem 275:38659-38666.
20. Kameyama K, Lee HK, Bear MF, Huganir RL (1998) Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression. Neuron 21:1163-1175.
21. Lee HK, Kameyama K, Huganir RL, Bear MF (1998) NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21:1151-1162.
22. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405:955-959.
23. Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Yu S, Ding L, He C, Petralia RS,Wenthold RJ, Gallagher M, Huganir RL (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112:631-643.
24. Mack V, Burnashev N, Kaiser KM, Rozov A, Jensen V, Hvalby O, Seeburg PH, Sakmann B, Sprengel R (2001) Conditional restoration of hippocampal synaptic potentiation in GluR-A-deficient mice. Science 292:2501-2504.
25. Mons N, Harry A, Dubourg P, Premont RT, Iyengar R, Cooper DM (1995) Immunohistochemical localization of adenylyl cyclase in rat brain indicates a highly selective concentration at synapses. Proc Natl Acad Sci USA 92:8473-8477.
26. 1 dopamine receptor-induced cyclic AMP-dependent protein kinase phosphorylation and potentiation of striatal glutamate receptors. J Neurochem 73:2441-2446.
27. Roberson ED, Sweatt JD (1996) Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation. J Biol Chem 271:30436-30441.
28. Roche KW, O'Brien RJ, Mammen AL, Bernhardt J, Huganir RL (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16:1179-1188.
29. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
30. Snyder GL, Allen PB, Fienberg AA, Valle CG, Huganir RL, Nairn AC, Greengard P (2000) Regulation of phosphorylation of the GluR1 AMPA receptor in the neostriatum by dopamine and psychostimulants in vivo. J Neurosci 20:4480-4488.
31. Suvarna NU, O'Donnell JM (2002) Hydrolysis of N-methyl-D-aspartate receptor-stimulated cAMP and cGMP by PDE4 and PDE2 phosphodiesterases in primary neuronal cultures of rat cerebral cortex and hippocampus. J Pharmacol Exp Ther 302:249-256.
32. Tavalin SJ, Colledge M, Hell M, Langeberg LK, Huganir RL, Scott JD (2002) Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J Neurosci 22:3044-3051.
33. Thomas MJ, Moody TD, Makhinson M, O'Dell TJ (1996) Activity- dependent β-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17:475-482.
34. Vanhoose AM, Emery M, Jimenez L, Winder DG (2002) ERK activation by G-protein-coupled receptors in mouse brain is receptor identity-specific. J Biol Chem 277:9049-9053.
35. Watabe AM, O'Dell TJ (2003) Age-related changes in theta frequency stimulation-induced long-term potentiation. Neurobiol Aging 24:267-272.
36. Winder DG, Sweatt JD (2001) Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Nat Rev Neurosci 2:461-474.
37. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by β-adrenergic receptors. Neuron 24:715-726.
38. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, Muglia LJ, Storm DR (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23:787-798.
39. Xia Z, Storm DR (1997) Calmodulin-regulated adenylyl cyclases and neuromodulation. Curr Opin Neurobiol 7:391-396.
40. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T, Worley P, Lubke J, Frotscher M, Kelly PH, Sommer B, Andersen P, Seeburg PH, Sakmann B (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284:1805-1811.