Beyond the dopamine receptor: The DARPP-32/protein phosphatase-1 cascade

Neuron

Volumn 23, Issue 3, 1999, Pages 435-447

  Greengard, Paul ^a   Allen, Patrick B ^a   Nairn, Angus C ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE RECEPTOR; GLUTAMATE RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE 1;

CENTRAL NERVOUS SYSTEM; DOPAMINE METABOLISM; DOPAMINERGIC TRANSMISSION; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVIEW; TARGET CELL; TISSUE DISTRIBUTION;

EID: 0033166545     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80798-9     Document Type: Review

References (114)

1. Allen, P.B., Ouimet, C.C., and Greengard, P. (1997). Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc. Natl. Acad. Sci. USA 94, 9956-9961.
2. Andreasen, N.C. (1996). Pieces of the schizophrenia puzzle fall into place. Neuron 16, 697-700.
3. Barria, A., Muller, D., Derkach, V., Griffith, L.C., and Soderling, T.R. (1997). Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276, 2042-2045.
4. Bergson, C., Mrzljak, L., Smiley, J.F., Pappy, M., Levenson, R., and Goldman-Rakic, P.S. (1995). Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J. Neurosci. 15, 7821-7836.
5. 2+ and stimulus duration-dependent switch for hippocampal gene expression. Cell 87, 1203-1214.
6. Blank, T., Nijholt, I., Teichert, U., Kugler, H., Behrsing, H., Fienberg, A., Greengard, P., and Spiess, J. (1997). The phosphoprotein DARPP-32 mediates cAMP-dependent potentiation of striatal N-methyl-D-aspartate responses. Proc. Natl. Acad. Sci. USA 94, 14859-14864.
7. Blitzer, R.D., Wong, T., Nouranifar, R., Iyengar, R., and Landau, E.M. (1995). Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15, 1403-1414.
8. Blitzer, R.D., Connor, J.H., Brown, G.P., Wong, T., Shenolikar, S., Iyengar, R., and Landau, E.M. (1998). Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280, 1940-1942.
9. Blumer, K.J., and Johnson, G.L. (1994). Diversity in function and regulation of MAP kinase pathways. Trends Biochem. Sci. 19, 236-240.
10. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., and Silva, A.J. (1994). Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79, 59-68.
11. Burnett, P.E., Blackshaw, S., Lai, M.M., Qureshi, I.A., Burnett, A.F., Sabatini, D.M., and Snyder, S.H. (1998). Neurabin is a synaptic protein linking p70 S6 kinase and the neuronal cytoskeleton. Proc. Natl. Acad. Sci. USA 95, 8351-8356.
12. Calabresi, P., Mercuri, N., Stanzione, P., Stefani, A., and Bernardi, G. (1987). Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: evidence for D1 receptor involvement. Neuroscience 20, 757-771.
13. Calabresi, P., Maj, R., Pisani, A., Mercuri, N.B., and Bernardi, G. (1992). Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J. Neurosci. 12, 4224-4233.
14. Cepeda, C., and Levine, M.S. (1998). Dopamine and N-methyl-D-aspartate receptor interactions in the neostriatum. Dev. Neurosci. 20, 1-18.
15. Cepeda, C., Buchwald, N.A., and Levine, M.S. (1993). Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc. Natl. Acad. Sci. USA 90, 9576-9580.
16. Cepeda, C., Colwell, C.S., Itri, J.N., Chandler, S.H., and Levine, M.S. (1998). Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances. J. Neurophysiol. 79, 82-94.
17. Craven, S.E., and Bredt, D.S. (1998). PDZ proteins organize synaptic signaling pathways. Cell 93, 495-498.
18. Desdouits, F., Cheetham, J.J., Huang, H.B., Kwon, Y.G., da Cruz e Silva, E.F., Denefle, P., Ehrlich, M.E., Nairn, A.C., Greengard, P., and Girault, J.A. (1995a). Mechanism of inhibition of protein phosphatase 1 by DARPP-32: studies with recombinant DARPP-32 and synthetic peptides. Biochem. Biophys. Res. Comm. 206, 652-658.
19. Desdouits, F., Cohen, D., Nairn, A.C., Greengard, P., and Girault, J.A. (1995b). Phosphorylation of DARPP-32, a dopamine-and cAMP-regulated phosphoprotein, by casein kinase I in vitro and in vivo. J. Biol. Chem. 270, 8772-8778.
20. Desdouits, F., Siciliano, J.C., Greengard, P., and Girault, J.A. (1995c). Dopamine-and cAMP-regulated phosphoprotein DARPP-32: phosphorylation of Ser-137 by casein kinase I inhibits dephosphorylation of Thr-34 by calcineurin. Proc. Natl. Acad. Sci. USA 92, 2682-2685.
21. Desdouits, F., Siciliano, J.C., Nairn, A.C., Greengard, P., and Girault, J.A. (1998). Dephosphorylation of Ser-137 in DARPP-32 by protein phosphatases 2A and 2C: different roles in vitro and in striatonigral neurons. Biochem. J. 330, 211-216.
22. Egloff, M.P., Cohen, P.T., Reinemer, P., and Barford, D. (1995). Crystal structure of the catalytic subunit of human protein phosphatase 1 and its complex with tungstate. J. Mol. Biol. 254, 942-959.
23. Egloff, M.P., Johnson, D.F., Moorhead, G., Cohen, P.T., Cohen, P., and Barford, D. (1997). Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. EMBO J. 16, 1876-1887.
24. Faux, M.C., and Scott, J.D. (1996). More on target with protein phosphorylation: conferring specificity by location. Trends Biochem. Sci. 21, 312-315.
25. Fernandez, A., Brautigan, D.L., Mumby, M., and Lamb, N.J. (1990). Protein phosphatase type-1, not type-2A, modulates actin microfilament integrity and myosin light chain phosphorylation in living non-muscle cells. J. Cell Biol. 111, 103-112.
26. Ferraro, L., Antonelli, T., O'Connor, W.T., Fuxe, K., Soubrie, P., and Tanganelli, S. (1998). The striatal neurotensin receptor modulates striatal and pallidal glutamate and GABA release: functional evidence for a pallidal glutamate-GABA interaction via the pallidal-subthalamic nucleus loop. J. Neurosci. 18, 6977-6989.
27. Ferre, S., Fredholm, B.B., Morelli, M., Popoli, P., and Fuxe, K. (1997). Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia. Trends Neurosci. 20, 482-487.
28. Fienberg, A.A., Hiroi, N., Mermelstein, P.G., Song, W., Snyder, G.L., Nishi, A., Cheramy, A., O'Callaghan, J.P., Miller, D.B., Cole, D.G., et al. (1998). DARPP-32: regulator of the efficacy of dopaminergic neurotransmission. Science 281, 838-842.
29. Figueredo-Cardenas, G., Morello, M., Sancesario, G., Bernardi, G., and Reiner, A. (1996). Colocalization of somatostatin, neuropeptide Y, neuronal nitric oxide synthase and NADPH-diaphorase in striatal interneurons in rats. Brain Res. 735, 317-324.
30. Frey, U., Matthies, H., Reymann, K.G., and Matthies, H. (1991). The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci. Lett. 129, 111-114.
31. Fuxe, K., Li, X.M., Tanganelli, S., Hedlund, P., O'Connor, W.T., Ferraro, L., Ungerstedt, U., and Agnati, L.F. (1995). Receptor-receptor interactions and their relevance for receptor diversity. Focus on neuropeptide/dopamine interactions. Ann. NY Acad. Sci. 10, 365-376.
32. Gerfen, C.R. (1992). The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci. 15, 133-139.
33. Gerfen, C.R., Engber, T.M., Mahan, L.C., Susel, Z., Chase, T.N., Monsma, F.J., Jr., and Sibley, D.R. (1990). D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429-1432.
34. Girault, J.A., Shalaby, I.A., Rosen, N.L., and Greengard, P. (1988). Regulation by cAMP and vasoactive intestinal peptide of phosphorylation of specific proteins in striatal cells in culture. Proc. Natl. Acad. Sci. USA 85, 7790-7794.
35. Girault, J.A., Hemmings, H.C., Jr., Williams, K.R., Nairn, A.C., and Greengard, P. (1989). Phosphorylation of DARPP-32, a dopamine-and cAMP-regulated phosphoprotein, by casein kinase II. J. Biol. Chem. 264, 21748-21759.
36. Goldberg, J., Huang, H.B., Kwon, Y.G., Greengard, P., Nairn, A.C., and Kuriyan, J. (1995). Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature 376, 745-753.
37. Goto, S., Matsukado, Y., Mihara, Y., Inoue, N., and Miyamoto, E. (1986). The distribution of calcineurin in rat brain by light and electron microscopic immunohistochemistry and enzyme-immunoassay. Brain Res. 397, 161-172.
38. Gray, E.G. (1959). Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J. Anat. 93, 420-433.
39. Greengard, P., Jen, J., Nairn, A.C., and Stevens, C.F. (1991). Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253, 1135-1138.
40. Guitart, X., and Nestler, E.J. (1992). Chronic administration of lithium or other antidepressants increases levels of DARPP-32 in rat frontal cortex. J. Neurochem. 59, 1164-1167.
41. Hagiwara, M., Alberts, A., Brindle, P., Meinkoth, J., Feramisco, J., Deng, T., Karin, M., Shenolikar, S., and Montminy, M. (1992). Transcriptional attenuation following cAMP induction requires PP-1-mediated dephosphorylation of CREB. Cell 70, 105-113.
42. Halpain, S., Girault, J.A., and Greengard, P. (1990). Activation of NMDA receptors induces dephosphorylation of DARPP-32 in rat striatal slices. Nature 343, 369-372.
43. Harris, K.M., and Kater, S.B. (1994). Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 17, 341-371.
44. Harsing, L.G., Jr., and Zigmond, M.J. (1997). Influence of dopamine on GABA release in striatum: evidence for D1-D2 interactions and non-synaptic influences. Neuroscience 77, 419-429.
45. Hemmings, H.C., Jr., Greengard, P., Tung, H.Y., and Cohen, P. (1984a). DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature 310, 503-505.
46. Hemmings, H.C., Jr., Nairn, A.C., and Greengard, P. (1984b). DARPP-32, a dopamine-and adenosine 3′:5′-monophosphate-regulated neuronal phosphoprotein. II. Comparison of the kinetics of phosphorylation of DARPP-32 and phosphatase inhibitor 1. J. Biol. Chem. 259, 14491-14497.
47. Hemmings, H.C., Jr., Nairn, A.C., Elliott, J.I., and Greengard, P. (1990). Synthetic peptide analogs of DARPP-32 (Mr 32,000 dopamine-and cAMP-regulated phosphoprotein), an inhibitor of protein phosphatase-1. Phosphorylation, dephosphorylation, and inhibitory activity. J. Biol. Chem. 265, 20369-20376.
48. 2+ conductance. J. Neurosci. 17, 3334-3342.
49. Hersch, S.M., Ciliax, B.J., Gutekunst, C.A., Rees, H.D., Heilman, C.J., Yung, K.K., Bolam, J.P., Ince, E., Yi, H., and Levey, A.I. (1995). Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents. J. Neurosci. 15, 5222-5237.
50. Hiroi, N., Fienberg, A.A., Haile, C.N., Alburges, M., Hanson, G.R., Greengard, P., and Nestler, E.J. (1999). Neuronal and behavioral abnormalities in striatal function in DARPP-32-mutant mice. Eur. J. Neurosci. 11, 1114-1118.
51. Hsieh-Wilson, L.C., Allen, P.B., Watanabe, T., Nairn, A.C., and Greengard, P. (1999). Characterization of the neuronal targeting protein spinophilin and its interactions with protein phosphatase 1. Biochemistry 38, 4365-4373.
52. Huang, Y.Y., and Kandel, E.R. (1995). D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc. Natl. Acad. Sci. USA 92, 2446-2450.
53. Huang, H.-B., Horiuchi, A., Watanabe, T., Shih, S.R., Tsay, H.J., Li, H.C., Greengard, P., and Nairn, A.C. (1999). Characterization of the inhibition of protein phosphatase-1 by DARPP-32 and inhibitor-2. J. Biol. Chem. 274, 7870-7878.
54. Hubbard, M.J., and Cohen, P. (1993). On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18, 172-177.
55. Huff, R.M., Chio, C.L., Lajiness, M.E., and Goodman, L.V. (1998). Signal transduction pathways modulated by D2-like dopamine receptors. Adv. Pharmacol. 42, 454-457.
56. Kaibuchi, K. (1999). Regulation of cytoskeleton and cell adhesion by Rho targets. Prog. Mol. Subcell. Biol. 22, 23-38.
57. Kauer, J.A., Malenka, R.C., and Nicoll, R.A. (1988). A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron 1, 911-917.
58. King, M.M., Huang, C.Y., Chock, P.B., Nairn, A.C., Hemmings, H.C., Jr., Chan, K.F., and Greengard, P. (1984). Mammalian brain phosphoproteins as substrates for calcineurin. J. Biol. Chem. 259, 8080-8083.
59. Koob, G.F., Sanna, P.P., and Bloom, F.E. (1998). Neuroscience of addiction. Neuron 21, 467-476.
60. Kolter, R. (1994). Postsynaptic integration of glutamatergic and dopaminergic signals in the striatum. Prog. Neurobiol. 44, 163-196.
61. Kusuki, T., Imahori, Y., Ueda, S., and Inokuchi, K. (1997). Dopaminergic modulation of LTP induction in the dentate gyrus of intact brain. Neuroreport 8, 2037-2040.
62. Kwon, Y.G., Huang, H.B., Desdouits, F., Girault, J.A., Greengard, P., and Nairn, A.C. (1997). Characterization of the interaction between DARPP-32 and protein phosphatase 1 (PP-1): DARPP-32 peptides antagonize the interaction of PP-1 with binding proteins. Proc. Natl. Acad. Sci. USA 94, 3536-3541.
63. Le Moine, C., Svenningsson, P., Fredholm, B.B., and Bloch, B. (1997). Dopamine-adenosine interactions in the striatum and the globus pallidus: inhibition of striatopallidal neurons through either D2 or A2A receptors enhances D1 receptor-mediated effects on c-fos expression. J. Neurosci. 17, 8038-8048.
64. Li, M., West, J.W., Lai, Y., Scheuer, T., and Catterall, W.A. (1992). Functional modulation of brain sodium channels by cAMP-dependent phosphorylation. Neuron 8, 1151-1159.
65. Lindskog, M., Svenningsson, P., Fredholm, B.B., Greengard, P., and Fisone, G. (1998). Activation of dopamine D2 receptors decreases DARPP-32 phosphorylation. Neuroscience 88, 1005-1008.
66. Lindskog, M., Svenningson, P., Fredholm, B., Greengard, P., and Fisone, G. (1999). μ-and δ-opioid receptor agonists inhibit DARPP-32 phosphorylation in distinct populations of striatal projection neurons. Eur. J. Neurosci. 11, 2182-2186.
67. Lledo, P.M., Hjelmstad, G.O., Mukherji, S., Soderling, T.R., Malenka, R.C., and Nicoll, R.A. (1995). Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc. Natl. Acad. Sci. USA 92, 11175-11179.
68. Lovinger, D.M.,andTyler, E. (1996). Synaptic transmission and modulation in the neostriatum. Int. Rev. Neurobiol. 39, 77-111.
69. Mansour, A., Khachaturian, H., Lewis, M.E., Akil, H., and Watson, S.J. (1987). Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J. Neurosci. 7, 2445-2464.
70. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D., and Kandel, E.R. (1996). Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678-1683.
71. McAvoy, T., Allen, P.B., Obaishi, H., Nakanishi, H., Takai, Y., Greengard, P., Nairn, A.C., and Hemmings, H.C. (1999). Regulation of Neurabin 1 interaction with protein phosphatase 1 by phosphorylation. Biochemistry, in press.
72. Mulkey, R.M., Endo, S., Shenolikar, S., and Malenka, R.C. (1994). Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486-488.
73. Muller, D., and Lynch, G. (1988). Long-term potentiation differentially affects two components of synaptic responses in hippocampus. Proc. Natl. Acad. Sci. USA 85, 9346-9350.
74. Nakanishi, H., Obaishi, H., Satoh, A., Wada, M., Mandai, K., Satoh, K., Nishioka, H., Matsuura, Y., Mizoguchi, A., and Takai, Y. (1997). Neurabin: a novel neural tissue-specific actin filament-binding protein involved in neurite formation. J. Cell Biol. 139, 951-961.
75. Nicola, S.M., and Malenka, R.C. (1998). Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J. Neurophysiol. 79, 1768-1776.
76. Nicola, S.M., Surmeier, J.D., and Malenka, R.C. (1999). Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu. Rev. Neurosci., in press.
77. Nishi, A., Snyder, G.L., and Greengard, P. (1997). Bidirectional regulation of DARPP-32 phosphorylation by dopamine. J. Neurosci. 17, 8147-8155.
78. Nishi, A., Snyder, G.L., Nairn, A.C., and Greengard, P. (1999). Role of calcineurin and protein phosphatase-2A in the regulation of DARPP-32 dephosphorylation. J. Neurochem. 72, 2015-2021.
79. O'Brien, R.J., Lau, L.F., and Huganir, R.L. (1998). Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr. Opin. Neurobiol. 8, 364-369.
80. Otmakhova, N.A., and Lisman, J.E. (1996). D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 16, 7478-7486.
81. Ouimet, C.C., Miller, P.E., Hemmings, H.C., Jr., Walaas, S.I., and Greengard, P. (1984). DARPP-32, a dopamine-and adenosine 3′:5′-monophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. III. Immunocytochemical localization. J. Neurosci. 4, 111-124.
82. Ouimet, C.C., da Cruz e Silva, E.F., and Greengard, P. (1995). The alpha and gamma 1 isoforms of protein phosphatase 1 are highly and specifically concentrated in dendritic spines. Proc. Natl. Acad. Sci. USA 92, 3396-3400.
83. Ouimet, C.C., Langley-Gullion, K.C., and Greengard, P. (1998). Quantitative immunocytochemistry of DARPP-32-expressing neurons in the rat caudatoputamen. Brain Res. 808, 8-12.
84. Roche, K.W., O'Brien, R.J., Mammen, A.L., Bernhardt, J., and Huganir, R.L. (1996). Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16, 1179-1188.
85. Rosenmund, C., Carr, D.W., Bergeson, S.E., Nilaver, G., Scott, J.D., and Westbrook, G.L. (1994). Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature 368, 853-856.
86. Rotenberg, A., Mayford, M., Hawkins, R.D., Kandel, E.R., and Muller, R.U. (1996). Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87, 1351-1361.
87. Satoh, A., Nakanishi, H., Obaishi, H., Wada, M., Takahashi, K., Satoh, K., Hirao, K., Nishioka, H., Hata, Y., Mizoguchi, A., and Takai, Y. (1998). Neurabin-II/spinophilin. An actin filament-binding protein with one PDZ domain localized at cadherin-based cell-cell adhesion sites. J. Biol. Chem. 273, 3470-3475.
88. Schiffmann, S.N., Lledo, P.M., and Vincent, J.D. (1995). Dopamine D1 receptor modulates the voltage-gated sodium current in rat striatal neurones through protein kinase A. J. Physiol. 483, 95-107.
89. Schiffmann, S.N., Desdouits, F., Menu, R., Greengard, P., Vincent, J.D., Vanderhaeghen, J.J., and Girault, J.A. (1998). Modulation of the voltage-gated sodium current in rat striatal neurons by DARPP-32, an inhibitor of protein phosphatase. Eur. J. Neurosci. 10, 1312-1320.
90. Self, D.W., and Nestler, E.J. (1995). Molecular mechanisms of drug reinforcement and addiction. Annu. Rev. Neurosci. 18, 463-495.
91. Sheng, M., and Wyszynski, M. (1997). Ion channel targeting in neurons. Bioessays 19, 847-853.
92. Shields, S.M., Ingebritsen, T.S., and Kelly, P.T. (1985). Identification of protein phosphatase 1 in synaptic junctions: dephosphorylation of endogenous calmodulin-dependent kinase II and synapse-enriched phosphoproteins. J. Neurosci. 5, 3414-3422.
93. Sibley, D.R., and Monsma, F.J., Jr. (1992). Molecular biology of dopamine receptors. Trends Pharmacol. Sci. 13, 61-69.
94. Silva, A.J., Stevens, C.F., Tonegawa, S., and Wang, Y. (1992). Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 201-206.
95. Sim, A.T., Ratcliffe, E., Mumby, M.C., Villa-Moruzzi, E., and Rostas, J.A. (1994). Differential activities of protein phosphatase types 1 and 2A in cytosolic and paniculate fractions from rat forebrain. J. Neurochem. 62, 1552-1559.
96. Smith, Y., Bevan, M.D., Shink, E., and Bolam, J.P. (1998). Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86, 353-387.
97. Snyder, G.L., Fisone, G., Morino, P., Gundersen, V., Ottersen, O.P., Hokfelt, T., and Greengard, P. (1993). Regulation by the neuropeptide cholecystokinin (CCK-8S) of protein phosphorylation in the neostriatum. Proc. Natl. Acad. Sci. USA 90, 11277-11281.
98. Snyder, G.L., Fisone, G., and Greengard, P. (1994). Phosphorylation of DARPP-32 is regulated by GABA in rat striatum and substantia nigra. J. Neurochem. 63, 1766-1771.
99. r 32 kDa)/protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor. J. Neurosci. 18, 10297-10303.
100. Steward, O. (1997). mRNA localization in neurons: a multipurpose mechanism? Neuron 18, 9-12.
101. Stoof, J.C., and Kebabian, J.W. (1981). Opposing roles for D-1 and D-2 dopamine receptors in efflux of cyclic AMP from rat neostriatum. Nature 294, 366-368.
102. Surmeier, D.J., and Kitai, S.T. (1993). D1 and D2 dopamine receptor modulation of sodium and potassium currents in rat neostriatal neurons. Prog. Brain Res. 99, 309-324.
103. Surmeier, D.J., Bargas, J., Hemmings, H.C., Jr., Nairn, A.C., and Greengard, P. (1995). Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron 14, 385-397.
104. Surmeier, D.J., Song, W.J., and Yan, Z. (1996). Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci. 16, 6579-6591.
105. Svenningsson, P., Le Moine, C., Kull, B., Sunahara, R., Bloch, B., and Fredholm, B.B. (1997). Cellular expression of adenosine A2A receptor messenger RNA in the rat central nervous system with special reference to dopamine innervated areas. Neuroscience 80, 1171-1185.
106. Svenningsson, P., Lindskog, M., Rognoni, F., Fredholm, B.B., Greengard, P., and Fisone, G. (1998). Activation of adenosine A2A and dopamine D1 receptors stimulates cyclic AMP-dependent phosphorylation of DARPP-32 in distinct populations of striatal projection neurons. Neuroscience 84, 223-228.
107. Tiedge, H., Bloom, F.E., and Richter, D. (1999). RNA, whither goest thou? Science 283, 186-187.
108. Tingley, W.G., Ehlers, M.D., Kameyama, K., Doherty, C., Ptak, J.B., Riley, C.T., and Huganir, R.L. (1997). Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J. Biol. Chem. 272, 5157-5166.
109. Tsou, K., Snyder, G.L., and Greengard, P. (1993). Nitric oxide/cGMP pathway stimulates phosphorylation of DARPP-32, a dopamine-and cAMP-regulated phosphoprotein, in the substantia nigra. Proc. Natl. Acad. Sci. USA 90, 3462-3465.
110. Wang, L.Y., Salter, M.W., and MacDonald, J.F. (1991). Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253, 1132-1135.
111. Wilson, C.J. (1993). The generation of natural firing patterns in neostriatal neurons. Prog. Brain Res. 99, 277-297.
112. Wilson, C.J., and Kawaguchi, Y. (1996). The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 16, 2397-2410.
113. Van, Z., Hsieh-Wilson, L., Feng, J., Tomizawa, K., Allen, P.B., Fienberg, A.A., Nairn, A.C., and Greengard, P. (1999). Regulation of AMPA channels by protein phosphatase 1 in neostriatum. Nat. Neurosci. 2, 13-17.
114. Yung, K.K., Bolam, J.P., Smith, A.D., Hersch, S.M., Ciliax, B.J., and Levey, A.I. (1995). Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience 65, 709-730.