Dopamine D1 receptors mediate CREB phosphorylation via phosphorylation of the NMDA receptor at Ser897-NR1

Journal of Neurochemistry

Volumn 87, Issue 4, 2003, Pages 922-934

  Dudman, Joshua T ^a   Eaton, Molly E ^a   Rajadhyaksha, Anjali ^a,b   Macías, Wendy ^c   Taher, Muffadal ^a   Barczak, Amy ^c   Kameyama, Kimihiko ^d   Huganir, Richard ^c   Konradi, Christine ^a,b,c  

^a MCLEAN HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium calmodulin kinase; CREB; Cyclic AMP; Dopamine D1 receptor; NMDA; Protein kinase A

Indexed keywords

CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE 1 RECEPTOR; GLUTAMIC ACID; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT; SERINE 897; SERINE DERIVATIVE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DRUG DEPENDENCE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSFECTION; LONG TERM MEMORY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CELLS, CULTURED; CORPUS STRIATUM; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GLUTAMIC ACID; MUTAGENESIS, SITE-DIRECTED; NEURONS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0345255956     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02067.x     Document Type: Article

References (84)

1. Andersson M., Konradi C. and Cenci M. A. (2001) cAMP response element-binding protein is required for dopamine-dependent gene expression in the intact but not the dopamine-denervated striatum. J. Neurosci. 21, 9930-9943.
2. Bailey C. H., Giustetto M., Huang Y. Y., Hawkins R. D. and Kandel E. R. (2000) Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat. Rev. Neurosci. 1, 11-20.
3. Battisti J. J., Shreffler C. B., Uretsky N. J. and Wallace L. J. (2000) NMDA antagonists block expression of sensitization of amphetamine- and apomorphine-induced stereotypy. Pharmacol. Biochem. Behav. 67, 241-246.
4. Bespalov A. Y. and Zvartau E. E. (1996) Intraaccumbens administration of NMDA receptor antagonist (+/-)-CPP prevents locomotor activation conditioned by morphine and amphetamine in rats. Pharmacol. Biochem. Behav. 55, 203-207.
5. Bristow L. J., Thorn L., Tricklebank M. D. and Hutson P. H. (1994) Competitive NMDA receptor antagonists attenuate the behavioural and neurochemical effects of amphetamine in mice. Eur J. Pharmacol. 264, 353-359.
6. Carlezon W. A. Jr, Thome J., Olson V. G., Lane-Ladd S. B., Brodkin E. S., Hiroi N., Duman R. S., Neve R. L. and Nestler E. J. (1998) Regulation of cocaine reward by CREB. Science 282, 2272-2275.
7. Carr D. B. and Sesack S. R. (2000) Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J. Neurosci. 20, 3864-3873.
8. Carr D. B., O'Donnell P., Card J. P. and Sesack S. R. (1999) Dopamine terminals in the rat prefrontal cortex synapse on pyramidal cells that project to the nucleus accumbens. J. Neurosci. 19, 11049-11060.
9. Centonze D., Picconi B., Gubellini P., Bernardi G. and Calabresi P. (2001) Dopaminergic control of synaptic plasticity in the dorsal striatum. Eur J. Neurosci. 13, 1071-1077.
10. 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.
11. Chao S. Z., Lu W., Lee H. K., Huganir R. L. and Wolf M. E. (2002) D(1) dopamine receptor stimulation increases GluR1 phosphorylation in postnatal nucleus accumbens cultures. J Neurochem 81, 984-992.
12. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356, 521-523.
13. Choe E. S. and McGinty J. F. (2000) N-methyl-D-aspartate receptors and p38 mitogen-activated protein kinase are required for cAMP-dependent cyclase response element binding protein and Elk-1 phosphorylation in the striatum. Neuroscience 101, 607-617.
14. Choe E. S. and McGinty J. F. (2001) Cyclic AMP and mitogen-activated protein kinases are required for glutamate-dependent cyclic AMP response element binding protein and Elk-1 phosphorylation in the dorsal striatum in vivo. J. Neurochem. 76, 401-412.
15. Choe E. S. and Wang J. Q. (2002) CaMKII regulates amphetamine-induced ERK1/2 phosphorylation in striatal neurons. Neuroreport 13, 1013-1016.
16. Cole R. L., Konradi C., Douglass J. and Hyman S. E. (1995) Neuronal adaptation to amphetamine and dopamine: molecular mechanisms of prodynorphin gene regulation in rat striatum. Neuron 14, 813-823.
17. Colledge M., Dean R. A., Scott G. K., Langeberg L. K., Huganir R. L. and Scott J. D. (2000) Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 27, 107-119.
18. Dash P. K., Karl K. A., Colicos M. A., Prywes R. and Kandel E. R. (1991) cAMP response element-binding protein is activated by Ca2+/calmodulin- as well as cAMP-dependent protein kinase. Proc. Natl Acad. Sci. USA 88, 5061-5065.
19. Day R. N., Walder J. A. and Maurer R. A. (1989) A protein kinase inhibitor gene reduces both basal and multihormone-stimulated prolactin gene transcription. J. Biol. Chem. 264, 431-436.
20. De Montis M. G., Devoto P., Meloni D., Gambarana C., Giorgi G. and Tagliamonte A. (1992) NMDA receptor inhibition prevents tolerance to cocaine. Pharmacol. Biochem. Behav. 42, 179-182.
21. Dell'Acqua M. L. and Scott J. D. (1997) Protein kinase A anchoring. J. Biol. Chem. 272, 12881-12884.
22. Dolmetsch R. E., Pajvani U., Fife K., Spotts J. M. and Greenberg M. E. (2001) Signaling to the nucleus by an 1-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294, 333-339.
23. Druhan J. P. and Wilent W. B. (1999) Effects of the competitive N-methyl-D-aspartate receptor antagonist, CPP, on the development and expression of conditioned hyperactivity and sensitization induced by cocaine. Behav. Brain Res. 102, 195-210.
24. Ehlers M. D., Tingley W. G. and Huganir R. L. (1995) Regulated subcellular distribution of the NR1 subunit of the NMDA receptor. Science 269, 1734-1737.
25. Fiorentini C., Gardoni F., Spano P., Di Luca M. and Missale C. (2003) Regulation of dopamine D1 receptor trafficking and desensitization by oligomerization with glutamate N-methyl-D-aspartate receptors. J. Biol. Chem. 278, 20196-20202.
26. Fraser I. D. and Scott J. D. (1999) Modulation of ion channels: a 'current' view of AKAPs. Neuron 23, 423-426.
27. 2+/calmodulin-dependent protein kinase II and protein kinase C by glutamate in cultured rat hippocampal neurons. J. Biol. Chem. 267, 22527-22533.
28. Gerfen C. R., Miyachi S., Paletzki R. and Brown P. (2002) D1 dopamine receptor supersensitivity in the dopamine-depleted striatum results from a switch in the regulation of ERK1/2/MAP kinase. J. Neurosci. 22, 5042-5054.
29. Ginty D. D., Kornhauser J. M., Thompson M. A., Bading H., Mayo K. E., Takahashi J. S. and Greenberg M. E. (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and circadian clock. Science 260, 238-241.
30. Gonzalez G. A. and Montminy M. R. (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59, 675-680.
31. Götz T., Kraushaar U., Geiger J., Lübke J., Berger T. and Jonas P. (1997) Functional properties of AMPA and NMDA receptors expressed in identified types of basal ganglia neurons. J. Neurosci. 17, 204-215.
32. Haracz J. L., Belanger S. A., MacDonall J. S. and Sircar R. (1995) Antagonist of N-methyl-D-aspartate receptors partially prevent the development of cocaine sensitization. Life Sci. 57, 2347-2357.
33. Hollmann M., Boulter J., Maron C., Beasley L., Sullivan J., Pecht G. and Heinemann S. (1993) Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10, 943-954.
34. Hu S. C., Chrivia J. and Ghosh A. (1999) Regulation of CBP-mediated transcription by neuronal calcium signaling. Neuron 22, 799-808.
35. Huettner J. E. and Bean B. P. (1988) Block of N-methyl-D-aspartate-activated current by the anticonvulsant MK-801: selective binding to open channels. Proc. Natl Acad. Sci. USA 85, 1307-1311.
36. Hyman S. E. (1996) Addiction to cocaine and amphetamine. Neuron 16, 901-904.
37. Hyman S. E. and Malenka R. C. (2001) Addiction and the brain: the neurobiology of compulsion and its persistence. Nat. Rev. Neurosci. 2, 695-703.
38. Karler R., Calder L. D., Chaudhry I. A. and Turkanis S. A. (1989) Blockade of 'reverse tolerance' to cocaine and amphetamine by MK-801. Life Sci. 45, 599-606.
39. Kim H. S., Park W. K., Jang C. G. and Oh S. (1996) Inhibition by MK-801 of cocaine-induced sensitization, conditioned place preference, and dopamine-receptor supersensitivity in mice. Brain Res. Bull. 40, 201-207.
40. Konradi C. (1998) The molecular basis of dopamine and glutamate interactions in the striatum. Adv. Pharmacol. 42, 729-733.
41. Konradi C., Cole R. L., Heckers S. and Hyman S. E. (1994) Amphetamine regulates gene expression in rat striatum via transcription factor CREB. J. Neurosci. 14, 5623-5634.
42. Konradi C., Leveque J. C. and Hyman S. E. (1996) Amphetamine and dopamine-induced immediate early gene expression in striatal neurons depends on postsynaptic NMDA receptors and calcium. J. Neurosci. 16, 4231-4239.
43. Koob G. F., Sanna P. P. and Bloom F. E. (1998) Neuroscience of addiction. Neuron 21, 467-476.
44. Leveque J. C., Macias W., Rajadhyaksha A., Carlson R. R., Barczak A., Kang S., Li X. M., Coyle J. T., Huganir R. L., Heckers S. and Konradi C. (2000) Intracellular modulation of NMDA receptor function by antipsychotic drugs. J. Neurosci. 20, 4011-4020.
45. Li Y., Hu X. T., Berney T. G., Vartanian A. J., Stine C. D., Wolf M. E. and White F. J. (1999) Both glutamate receptor antagonists and prefrontal cortex lesions prevent induction of cocaine sensitization and associated neuroadaptations. Synapse 34, 169-180.
46. Lonze B. E. and Ginty D. D. (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623.
47. MacDermott A. B., Mayer M. L., Westbrook G. L., Smith S. J. and Barker J. L. (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321, 519-522.
48. Maldve R. E., Zhang T. A., Ferrani-Kile K., Schreiber S. S., Lippmann M. J., Snyder G. L., Fienberg A. A., Leslie S. W., Gonzales R. A. and Morrisett R. A. (2002) DARPP-32 and regulation of the ethanol sensitivity of NMDA receptors in the nucleus accumbens. Nat. Neurosci. 5, 641-648.
49. Maxwell I. H., Harrison G. S., Wood W. M. and Maxwell F. (1989) A DNA cassette containing a trimerized SV40 polyadenylation signal which efficiently blocks spurious plasmid-initiated transcription. Biotechniques 7, 276-280.
50. Mayer M. L. and Westbrook G. L. (1987) The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28, 197-276.
51. Monsma F. J. Jr, Mahan L. C., McVittie L. D., Gerfen C. R. and Sibley D. R. (1990) Molecular cloning and expression of a D1 dopamine receptor linked to adenylyl cyclase activation. Proc. Natl Acad. Sci. USA 87, 6723-6727.
52. Montminy M. R., Gonzalez G. A. and Yamamoto K. K. (1990) Regulation of cAMP-inducible genes by CREB. Trends Neurosci. 13, 184-188.
53. Nestler E. J. (2001) Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2, 119-128.
54. Pliakas A. M., Carlson R. R., Neve R. L., Konradi C., Nestler E. J. and Carlezon W. A. Jr (2001) Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J. Neurosci. 21, 7397-7403.
55. Price C. J., Kim P. and Raymond L. A. (1999) D1 dopamine receptor-induced cyclic AMP-dependent protein kinase phosphorylation and potentiation of striatal glutamate receptors. J. Neurochem. 73, 2441-2446.
56. Pulvirenti L., Swerdlow N. R. and Koob G. F. (1991) Nucleus accumbens NMDA antagonist decreases locomotor activity produced by cocaine, heroin or accumbens dopamine, but not caffeine. Pharmacol. Biochem. Behav. 40, 841-845.
57. Rajadhyaksha A., Barczak A., Macias W., Leveque J. C., Lewis S. E. and Konradi C. (1999) L-Type Ca (2+) channels are essential for glutamate-mediated CREB phosphorylation and c-fos gene expression in striatal neurons. J. Neurosci. 19, 6348-6359.
58. Rajadhyaksha A., Leveque J., Macias W., Barczak A. and Konradi C. (1998) Molecular components of striatal plasticity: the various routes of cyclic AMP pathways. Dev. Neurosci. 20, 204-215.
59. Robinson T. E. and Berridge K. C. (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95, S91-S117.
60. Robinson T. E. and Kolb B. (1999) Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur. J. Neurosci. 11, 1598-1604.
61. Scott D. B., Blanpied T. A., Swanson G. T., Zhang C. and Ehlers M. D. (2001) An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J. Neurosci. 21, 3063-3072.
62. Seamon K. B., Padgett W. and Daly J. W. (1981) Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc. Natl Acad. Sci. USA 78, 3363-3367.
63. Self D. W., Genova L. M., Hope B. T., Barnhart W. J., Spencer J. J. and Nestler E. J. (1998) Involvement of cAMP-dependent protein kinase in the nucleus accumbens in cocaine self-administration and relapse of cocaine-seeking behavior. J. Neurosci, 18, 1848-1859.
64. Sheng M., Thompson M. A. and Greenberg M. E. (1991) CREB: a Ca (2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252, 1427-1430.
65. Smith A. D. and Bolam J. P. (1990) The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci. 13, 259-265.
66. Snyder G. L., Fienberg A. A., Huganir R. L. and Greengard P. (1998) A dopamine/D1 receptor/protein kinase A/dopamine- and cAMP-regulated phosphoprotein (Mr 32 kDa) /protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor. J. Neurosci. 18, 10297-10303.
67. Soderling T. R. (2000) CaM-kinases: modulators of synaptic plasticity. Curr. Opin. Neurobiol. 10, 375-380.
68. Sugihara H., Moriyoshi K., Ishii T., Masu M. and Nakanishi S. (1992) Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem. Biophys. Res. Comm 185, 826-832.
69. Thornburg J. E. and Moore K. E. (1975) Supersensitivity to dopamine agonists following unilateral, 6-hydroxydopamine-induced striatal lesions in mice. J. Pharm. Exp. Ther. 192, 42-49.
70. 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.
71. Tingley W. G., Roche K. W., Thompson A. K. and Huganir R. L. (1993) Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364, 70-73.
72. Torres G. and Rivier C. (1993) Cocaine-induced expression of striatal c-fos in the rat is inhibited by NMDA receptor antagonists. Brain Res. Bull. 30, 173-176.
73. Tzschentke T. M. and Schmidt W. J. (1998) Does the noncompetitive NMDA receptor antagonist dizocilpine (MK801) really block behavioural sensitization associated with repeated drug administration? Trends Pharmacol. Sci. 19, 447-451.
74. Uzbay I. T., Wallis C. J., Lal H. and Forster M. J. (2000) Effects of NMDA receptor blockers on cocaine-stimulated locomotor activity in mice. Behav. Brain Res. 108, 57-61.
75. Vanderschuren L. J. and Kalivas P. W. (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology 151, 99-120.
76. Westphal R. S., Tavalin S. J., Lin J. W., Alto N. M., Fraser I. D., Langeberg L. K., Sheng M. and Scott J. D. (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285, 93-96.
77. Wise R. A. (1984) Neural mechanisms of the reinforcing action of cocaine. NIDA Res. Monogr. 50, 15-33.
78. Wise R. A. (1996) Neurobiology of addiction. Curr. Opin. Neurobiol. 6, 243-251.
79. Wolf M. E. (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog. Neurobiol. 54, 679-720.
80. Wolf M. E. and Jeziorski M. (1993) Co-administration of MK-801 with amphetamine, cocaine or morphine prevents rather than transiently masks the development of behavioral sensitization. Brain Res. 613, 291-294.
81. Xia Z., Dudek H., Miranti C. K. and Greenberg M. E. (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16, 5425-5436.
82. Xing J., Ginty D. D. and Greenberg M. E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963.
83. Xing J., Kornhauser J. M., Xia Z., Thiele E. A. and Greenberg M. E. (1998) Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell Biol. 18, 1946-1955.
84. Zhen X., Uryu K., Wang H. Y. and Friedman E. (1998) D1 dopamine receptor agonists mediate activation of p38 mitogen-activated protein kinase and c-Jun amino-terminal kinase by a protein kinase A-dependent mechanism in SK-N-MC human neuroblastoma cells. Mol. Pharmacol. 54, 453-458.