L-type Ca2+ channels are essential for glutamate-mediated CREB phosphorylation and c-fos gene expression in striatal neurons

Journal of Neuroscience

Volumn 19, Issue 15, 1999, Pages 6348-6359

  Rajadhyaksha, Anjali ^a   Barczak, Amy ^a   Macías, Wendy ^a   Leveque, Jean Christophe ^a   Lewis, Susan E ^a   Konradi, Christine ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

AMPA; c fos; CREB; Glutamate; Kainate; L type Ca2+ channels; NMDA

Indexed keywords

AMPA RECEPTOR; CALCIUM CHANNEL; CALCIUM ION; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUTAMIC ACID; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN C FOS;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; FETUS; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SECOND MESSENGER; SIGNAL TRANSDUCTION;

EID: 0033178426     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-15-06348.1999     Document Type: Article

References (102)

1. Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C (1998) A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol Cell Biol 18:967-977.
2. Aroniadou VA, Maillis A, Stefanis CC (1993) Dihydropyridine-sensitive calcium channels are involved in the induction of N-methyl-D-aspartate receptor-independent long-term potentiation in visual cortex of adult rats. Neurosci Lett 151:77-80.
3. Aronin N, Chase K, Sagar SM, Sharp FR, DiFiglia M (1991) N-MethylD-aspartate receptor activation in the neostriatum increases c-fos and fos-related antigens selectively in medium-sized neurons. Neuroscience 44:409-420.
4. Ascher P, Nowak L (1987) Electrophysiological studies of NMDA receptors. Trends Neurosci 10:284-287.
5. Bading H, Ginty DD, Greenberg ME (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260:181-186.
6. Bading H, Segal MM, Sucher NJ, Dudek H, Lipton SA, Greenberg ME (1995) N-Methyl-D-aspartate receptors are critical for mediating the effects of glutamate on intracellular calcium concentration and immediate early gene expression in cultured hippocampal neurons. Neuroscience 64:653-664.
7. Bailey CH, Bartsch D, Kandel ER (1996) Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93:13445-13452.
8. Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 20:415-455.
9. Bito H, Deisseroth K, Tsien RW (1996) CREB phosphorylation and dephosphorylation: a Ca2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
10. Bonni A, Ginty DD, Dudek H, Greenberg ME (1995) Serine 133-phosphorylated CREB induces transcription via a cooperative mechanism that may confer specificity to neurotrophin signals. Mol Cell Neurosci 6:168-183.
11. Bourtchuladze R, Frenguelli B, Blendie J, Cioffi D, Schütz G, Silva AJ (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
12. Buchsbaum MS, Haier RJ, Potkin SG, Nuechterlein K, Bracha HS, Katz M, Lohr J, Wu J, Lottenberg S, Jerabek PA (1992) Frontostriatal disorder of cerebral metabolism in never-medicated schizophrenics. Arch Gen Psychiatry 49:935-942.
13. Burns RS (1991) Subclinical damage to the nigrostriatal dopamine system by MPTP as a model of preclinical Parkinson's disease: a review. Acta Neurol Scand Suppl 136:29-36.
14. Burt DR, Creese I, Snyder SH (1977) Antischizophrenic drugs: chronic treatment elevates dopamine receptor binding in brain. Science 196:326-328.
15. Busatto GF, Kerwin RW (1997) Schizophrenia, psychosis, and the basal ganglia. Psychiatr Clin North Am 20:897-910.
16. Calne DB, Langston JW, Martin WR, Stoessl AJ, Ruth TJ, Adam MJ, Pate BD, Schulzer M (1985) Positron emission tomography after MPTP: observations relating to the cause of Parkinson's disease. Nature 317:246-248.
17. Catterall WA (1991) Functional subunit structure of voltage-gated calcium channels. Science 253:1499-1500.
18. Catterall WA, Striessnig J (1992) Receptor sites for Ca2+ channel antagonists. Trends Pharmacol Sci 13:256-262.
19. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519.
20. Chetkovich DM, Gray R, Johnston D, Sweatt JD (1991) N-Methyl-D-aspartate receptor activation increases cAMP levels and voltage-gated Ca2+ channel activity in area CA1 of hippocampus. Proc Natl Acad Sci USA 88:6467-6471.
21. Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476.
22. Connor JA, Wadman WJ, Hockberger PE, Wong RK (1988) Sustained dendritic gradients of Ca2+ induced by excitatory amino acids in CA1 hippocampal neurons. Science 240:649-653.
23. Danielson PE, Forss-Petter S, Brow MA, Calavetta L, Douglass J, Milner RJ, Sutcliffe JG (1988) p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7:261-267.
24. Dave JR, Tortella FC (1994) Regional changes in c-fos mRNA in rat brain after i.v. or i.c.v. NMDA injections. NeuroReport 5:1645-1648.
25. Deadwyler SA, Dunwiddie T, Lynch G (1987) A critical level of protein synthesis is required for long-term potentiation. Synapse 1:90-95.
26. Deisseroth K, Tsien RW (1997) Calmodulin translocation to the nucleus mediates rapid synaptic control of CREB phosphorylation in hippocampal neurons. Soc Neurosci Abstr 23:311.
27. Deisseroth K, Heist EK, Tsien RW (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392:198-202.
28. DiFiglia M (1990) Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci 13:286-289.
29. Eastwood SL, Burnet PW, Harrison PJ (1994) Striatal synaptophysin expression and haloperidol-induced synaptic plasticity. NeuroReport 5:677-680.
30. Eastwood SL, Heffernan J, Harrison PJ (1997) Chronic haloperidol treatment differentially affects the expression of synaptic and neuronal plasticity-associated genes. Mol Psychiatry 2:322-329.
31. Egebjerg J, Heinemann SF (1993) Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci USA 90:755-759.
32. Gasic G, Hollmann M (1992) Molecular neurobiology of glutamate receptors. Annu Rev Physiol 54:507-536.
33. Ghosh A, Ginty DD, Bading H, Greenberg ME (1994) Calcium regulation of gene expression in neuronal cells. J Neurobiol 25:294-303.
34. Ginty DD, Kornhauser JM, Thompson MA, Bading H, Mayo KE, Takahashi JS, Greenberg ME (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and circadian clock. Science 260:238-241.
35. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59:675-680.
36. Greenamyre JT, Porter RH (1994) Anatomy and physiology of glutamate in the CNS. Neurology 44:S7-S13.
37. Hardingham GE, Chawla S, Johnson CM, Bading H (1997) Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385:260-265.
38. Heckers S (1997) Neuropathology of schizophrenia: cortex, thalamus, basal ganglia, and neurotransmitter-specific projection systems. Schizophr Bull 23:403-421.
39. Hofmann F, Biel M, Flockerzi V (1994) Molecular basis for Ca2+ channel diversity. Annu Rev Neurosci 17:399-418.
40. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
41. Hollmann M, Hartley M, Heinemann S (1991) Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252:851-853.
42. Hornykiewicz O (1993) Parkinson's disease and the adaptive capacity of the nigrostriatal dopamine system: possible neurochemical mechanisms. Adv Neurol 60:140-147.
43. Hyman SE (1996) Addiction to cocaine and amphetamine. Neuron 16:901-904.
44. Hyman SE, Nestler EJ (1996) Initiation and adaptation: a paradigm for understanding psychotropic drug action. Am J Psychiatry 153:151-162.
45. Impey S, Villacres EC, Poser S, Chavkin C, Storm DR (1996) Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973-982.
46. Jarvis MF, Murphy DE, Williams M (1987) Quantitative autoradiographic localization of NMDA receptors in rat brain using [3H]CPP: comparison with [3H]TCP binding sites. Eur J Pharmacol 141:149-152.
47. Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325:529-531.
48. Kandel ER, Schwartz JH, Jessell TM (1991) Principles of neural science. New York: Elsevier.
49. Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273:1399-1402.
50. Kohler M, Burnashev N, Sakmann B, Seeburg PH (1993) Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 10:491-500.
51. Konradi C, Leveque JC, Hyman SE (1996) Amphetamine and dopamine-induced immediate early gene expression in striatal neurons depends upon postsynaptic NMDA receptors and calcium. J Neurosci 16:4231-4239.
52. Landwehrmeyer GB, Standaert DG, Testa CM, Penney Jr JB, Young AB (1995) NMDA receptor subunit mRNA expression by projection neurons and interneurons in rat striatum. J Neurosci 15:5297-5307.
53. Langston JW (1996) The etiology of Parkinson's disease with emphasis on the MPTP story. Neurology 47:S153-S160.
54. Lerea LS, McNamara JO (1993) Ionotropic glutamate receptor subtypes activate c-fos transcription by distinct calcium-requiring intracellular signaling pathways. Neuron 10:31-41.
55. Lomeli H, Mosbacher J, Melcher T, Hoger T, Geiger JR, Kuner T, Monyer H, Higuchi M, Bach A, Seeburg PH (1994) Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266:1709-1713.
56. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321:519-522.
57. Matthies H (1989) In search of cellular mechanisms of memory. Prog Neurobiol 32:277-349.
58. Maxwell IH, Harrison GS, Wood WM, Maxwell F (1989) A DNA cassette containing a trimerized SV40 polyadenylation signal which efficiently blocks spurious plasmid-initiated transcription. Biotechniques 7:276-280.
59. Mayer ML, Westbrook GL, Guthrie PB (1984) Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
60. McCleskey EW (1994) Calcium channels: cellular roles and molecular mechanisms. Curr Opin Neurobiol 4:304-312.
61. Michaelis EK (1998) Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog Neurobiol 54:369-415.
62. Mijnster MJ, Ingham CA, Meredith GE, Docter GJ, Arbuthnott GW (1996) Morphological changes in met(5)-enkephalin-immunoreactive synaptic boutons in the rat neostriatum after haloperidol decanoate treatment. Eur J Neurosci 8:716-726.
63. Misra RP. Bonni A, Miranti CK, Rivera VM, Sheng M, Greenberg ME (1994) L-type voltage-sensitive calcium channel activation stimulates gene expression by a serum response factor-dependent pathway. J Biol Chem 259:25483-25493.
64. Miyoshi R, Kito S, Doudou N, Nomoto T (1991) Influence of age on N-methyl-D-aspartate antagonist binding sites in the rat brain studied by in vitro autoradiography. Synapse 8:212-217.
65. Montminy MR, Bilezikjian LM (1987) Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature 328:175-178.
66. Montminy MR, Gonzalez GA, Yamamoto KK (1990) Regulation of cAMP-inducible genes by CREB. Trends Neurosci 13:184-188.
67. Mosbacher J, Schoepfer R, Monyer H, Burnashev N, Seeburg PH, Ruppersberg JP (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266:1059-1062.
68. Murphy D, Segal M (1997) Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein. Proc Natl Acad Sci USA 94:1482-1487.
69. Murphy TH, Worley PF, Baraban JM (1991) L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron 7:625-635.
70. Mutel V, Buchy D, Klingelschmidt A, Messer J, Bleuel Z, Kemp JA, Richards JG (1998) In vitro binding properties in rat brain of [3H]Ro 25-6981, a potent and selective antagonist of NMDA receptors containing NR2B subunits. J Neurochem 70:2147-2155.
71. Nairn AC, Shenolikar S (1992) The role of protein phosphatases in synaptic transmission, plasticity and neuronal development. Curr Opin Neurobiol 2:296-301.
72. Nestler EJ, Hope BT, Widnell KL (1993) Drug addiction: a model for the molecular basis of neural plasticity. Neuron 11:995-1006.
73. Neve KA, Kozlowski MR, Marshall JF (1982) Plasticity of neostriatal dopamine receptors after nigrostriatal injury: relationship to recovery of sensorimotor functions and behavioral supersensitivity. Brain Res 244:33-44.
74. Ozawa S, Kamiya H, Tsuzuki K (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54:581-618.
75. Patel J, Zinkand WC, Klika AB, Mangano TJ, Keith RA, Salama AI (1990) 6,7-Dinitroquinoxaline-2,3-dione blocks the cytotoxicity of N-methyl-D-aspartate and kainate, but not quisqualate, in cortical cultures. J Neurochem 55:114-121.
76. Pich EM, Pagliusi SR, Tessari M, Talabot-Ayer D, Hooft van Huijsduijnen R, Chiamulera C (1997) Common neural substrates for the addictive properties of nicotine and cocaine. Science 275:83-86.
77. Rajadhyaksha A, Leveque J, Macias W, Barczak A, Konradi C (1998) Molecular components of striatal plasticity: the various routes of cyclic AMP pathways. Dev Neurosci 20:204-215.
78. Robertson LM, Kerppola TK, Vendrell M, Luk D, Smeyne RJ, Bocchiaro C, Morgan JI, Curran T (1995) Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron 14:241-252.
79. Ruppersberg JP, Mosbacher J, Gunther W, Schoepfer R, Fakler B (1993) Studying block in cloned N-methyl-D-aspartate (NMDA) receptors. Biochem Pharmacol 46:1877-1885.
80. Sakurai SY, Cha JH, Penney JB, Young AB (1991) Regional distribution and properties of [3H]MK-801 binding sites determined by quantitative autoradiography in rat brain. Neuroscience 40:533-543.
81. Sanna E, Head GA, Hanbauer I (1986) Evidence for a selective localization of voltage-sensitive Ca2+ channels in nerve cell bodies of corpus striatum. J Neurochem 47:1552-1557.
82. Schild D, Geiling H, Bischofberger J (1995) Imaging of L-type Ca2+ channels in olfactory bulb neurones using fluorescent dihydropyridine and a styryl dye. J Neurosci Methods 59:183-190.
83. Schoepfer R, Monyer H, Sommer B, Wisden W, Sprengel R, Kuner T, Lomeli H, Herb A, Kohler M, Burnashev N, Günther W, Ruppersberg P, Seeburg P (1994) Molecular biology of glutamate receptors. Prog Neurobiol 42:353-357.
84. Schulman H (1995) Protein phosphorylation in neuronal plasticity and gene expression. Curr Opin Neurobiol 5:375-381.
85. Self DW, Nestler EJ (1995) Molecular mechanisms of drug reinforcement and addiction. Annu Rev Neurosci 18:463-495.
86. Sheng M, McFadden G, Greenberg ME (1990) Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4:571-582.
87. Sheng M, Thompson MA, Greenberg ME (1991) CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252:1427-1430.
88. Siegel Jr BV, Buchsbaum MS, Bunney Jr WE, Gottschalk LA, Haier RJ, Lohr JB, Lottenberg S, Najafi A, Nuechterlein KH, Potkin SG, Wu JC (1993) Cortical-striatal-thalamic circuits and brain glucose metabolic activity in 70 unmedicated male schizophrenic patients. Am J Psychiatry 150:1325-1336.
89. Standaert DG, Testa CM, Young AB, Penney Jr JB (1994) Organization of N-methyl-D-aspartate glutamate receptor gene expression in the basal ganglia of the rat. J Comp Neurol 343:1-16.
90. Stanton PK, Sarvey JM (1984) Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J Neurosci 4:3080-3088.
91. Sucher NJ, Lei SZ, Lipton SA (1991) Calcium channel antagonists attenuate NMDA receptor-mediated neurotoxicity of retinal ganglion cells in culture. Brain Res 551:297-302.
92. 2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev 8:2527-2539.
93. Thayer SA, Murphy SN, Miller RJ (1986) Widespread distribution of dihydropyridine-sensitive calcium channels in the central nervous system. Mol Pharmacol 30:505-509.
94. Thompson MA, Ginty DD, Bonni A, Greenberg ME (1995) L-type voltage-sensitive Ca2+ channel activation regulates c-fos transcription at multiple levels. J Biol Chem 270:4224-4235.
95. Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP (1988) Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11:431-438.
96. Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Hitzemann R, Chen AD, Dewey SL, Pappas N (1997) Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 386:830-833.
97. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson Jr EP (1985) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44:559-577.
98. Walker D, De Waard M (1998) Subunit interaction sites in voltage-dependent Ca2+ channels: role in channel function. Trends Neurosci 21:148-154.
99. Weiss JH, Hartley DM, Koh J, Choi DW (1990) The calcium channel blocker nifedipine attenuates slow excitatory amino acid neurotoxicity. Science 247:1474-1477.
100. Westenbroek RE, Ahlijanian MK, Catterall WA (1990) Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons. Nature 347:281-284.
101. Xia Z, Dudek H, Miranti CK, Greenberg ME (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16:5425-5436.
102. Yin JCP, Wallach JS, Del Vecchio M, Wilder EL, Zhou H, Quinn WG, Tully T (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49-58.