Nuclear calcium: A key regulator of gene expression

BioMetals

Volumn 11, Issue 4, 1998, Pages 345-358

  Hardingham, Giles E ^a   Bading, Hilmar ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Calcium; CREB; Gene expression

Indexed keywords

CALCIUM ION; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; TRANSCRIPTION FACTOR;

CALCIUM CELL LEVEL; CELL NUCLEUS; GENE EXPRESSION REGULATION; HUMAN; LEARNING; MAMMAL CELL; MEMORY; NERVE CELL; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CELL NUCLEUS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GENE EXPRESSION REGULATION; HUMANS; LEARNING; MAMMALS; MEMORY; NEURONS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 0032454145     PISSN: 09660844     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1009257909785     Document Type: Review

References (120)

1. Abel, T., Nguyen, P., Barad, M., Deuel, T., and Kandel, E. (1997). Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus based longterm memory. Cell 88, 615-26.
2. Arias, J., Alberts, A. S., Brindle, P., Claret, F. X., Smeal, T., Karin, M., Feramisco, J., and Montminy, M. (1994). Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370, 226-229.
3. Bading, H., Ginty, D. D., and Greenberg, M. E. (1993). Regulation of gene expression in hippocampal neurons by distinct calcium signalling pathways. Science 260, 181-186.
4. Bading, H., and Greenberg, M. E. (1991). Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912-914.
5. Bading, H., Hardingham, G. E., Johnson, C. M., and Chawla, S. (1997). Gene regulation by nuclear and cytoplasmic calcium signals. Biochem. Biophys. Res. Com. 236, 541-543.
6. Bading, H., Segal, M. M., Sucher, N. J., Dudek, H., Lipton, S. A., and Greenberg, M. E. (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. Badminton, M., Kendall, J., Rembold, C., and Campbell, A. (1998). Current evidence suggests independent regulation of nuclear calcium. Cell Calcium 23, 79-86.
8. Bailey, C., and Kandel, E. (1994). Structural changes underlying long-term memory storage in Aplysia: a molecular perspective. Neurosciences 6, 35-44.
9. Bannister, A., and Kouzarides, T. (1996). The CBP coactivator is a histone acetyltransferase. Nature 384, 641-643.
10. Bannister, A. J., Ochler, T., Wilhelm, D., Angel, P., and Kouzarides, T. (1995). Stimulation of c-Jun activity by CBP: c-Jun residues Ser63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene 11, 2509-2514.
11. Bashir, Z., Bortolotto, Z., Davies, C., Berretta, N., Irving, A., Seal, A., Henley, J., Jane, D., Watkins, J., and Collingridge, G. (1993). Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363, 347-350.
12. Berridge, M. (1993). Inositol triphosphate and calcium signalling. Nature 361, 315-325.
13. Bhattacharya, S., Eckner, R., Grossman, S., Oldread, E., Arany, Z., D'Andrea, A., and Livingston, D. (1996). Co-operation of STAT2 and p300/CBP in signalling induced by interferon-a. Nature 383, 226-228.
14. Bito, H., Deisseroth, K., and Tsien, R. (1996). CREB phosphorylation and dephosphorylation: a calcium and stimulus dependent switch for hippocampal gene expression. Cell, 1203-1214.
15. Bliss, T. V. P., and Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-38.
16. Bliss, T. V. P., and Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetised rabbit following stimulation of the perforant path. Journal of Physiology 232, 331-356.
17. Bockaert, J., and Pin, J. (1997). Metabotropic glutamate receptors: 10 years of research. In 'Recombinant cell surface receptors: Focal point for therapeutic intervention' (M. Brown, Ed.). Academic Press, Georgetown, USA.
18. Bonni, A., Ginty, D. D., Dudek, H., and Greenberg, M. E. (1995). Serine 133-phosphorylated CREB induces transcription via a co-operative mechanism that may confer specificity to neurotrophin signals. Molecular and Cellular Neuroscience 6, 168-183.
19. Bootman, M., Berridge, M., and Lipp, P. (1997). Cooking with calcium: the recipes for creating global signals from elementary events. Cell 91, 367-374.
20. Bortolotto, Z., and Collingridge, G. (1993). Characterisation of LTP induced by the activation of glutamate metabotropic receptors in area CA1 of the hippocampus. Neuropharmacology 32, 1-9.
21. 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.
22. Byrne, J., Zwartjes, R., Homayouni, R., Critz, S., and Eskin, A. (1993). Roles of second messenger pathways in neuronal plasticity and in learning and memory. Insights gained from Aplysia. Raven, New York.
23. Carafoli, E., and Penniston, J. (1985). The calcium signal. Scientific American 253, 50-58.
24. Cardenas, M., and Heitman, J. (1995). Role of calcium in T-lymphocyte activation. Advances in second messenger and phosphoprotein research 30, 281-298.
25. Carew, T., Walters, E., and Kandel, E. (1981). Classical conditioning in a simple withdrawal reflex in Aplysia californica. Journal of Neuroscience 1, 1426-1437.
26. Chakravarti, D., LaMorte, V. J., Nelson, M. C., Nakajima, T., Schulman, I. G., Juguilon, H., Montminy, M., and Evans, R. M. (1996). Role of CBP/P300 in nuclear receptor signalling. Nature 383, 99-102.
27. Chen, H., Lin, R., Schiltz, R., Chakravati, D., Nash, A., Nagy, L., Privalsky, M., Kakatini, Y., and Evans, R. (1997). Nuclear receptor coactivator ACTR is a novel histone acetyl transferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90, 569-580.
28. Chrivia, J. C., Kwok, R. P. S., Lamb, N., Hagiwara, M., Montminy, M. R., and Goodman, R. H. (1993). Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859.
29. Cole, A. J., Saffen, D. W., Baraban, J. M., and Worley, P. F. (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340, 474-476.
30. Comb, M., Birnberg, N., Seasholtz, A., Herbert, E., and Goodman, H. (1986). A cyclic AMP and phorbol esterinducible DNA element. Nature 323, 353-356.
31. Cruzalegui, F. H., Kapiloff, M. S., Morfin, J. P., Kemp, B. E., Rosenfield, M. G., and Means, A. R. (1992). Regulation of Intrasteric inhibition of the multifunctional calcium/calmodulin-dependent protein kinase. Proceedings of the National Academy of Sciences, USA 89, 12127-12131.
32. Cruzalegui, F. H., and Means, A. R. (1993). Biochemical characterisation of the multifunctional Ca2+/calmodulin dependent protein kinase type IV expressed in insect cells. Journal of Biological Chemistry 268, 26171-26178.
33. Dash, P., Hochner, B., and Kandel, E. (1990). Injection of the CRE into the nucleus of Aplysia sensory neurons blocks long term facilitation. Nature 345, 718-721.
34. Davis, R. (1994). MAPKs: new JNK expands the group. Trends in Biochemical Sciences 19, 470-473.
35. Deisseroth, K., Heist, E., and Tsien, R. (1998). Calmodulin translocation to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392, 198-202.
36. DeKonick, P., and Schulman, H. (1998). Sensitivity of CaM kinase II to the frequency of calcium oscillations. Science 279, 227-230.
37. Drain, P., Folkers, E., and Quinn, W. (1991). cAMP dependent protein kinase and the disruption of learning in transgenic flies. Neuron 6, 71-82.
38. Frey, U., Huang, Y.-Y., and Kandel, E. R. (1993). Effects of cAMP simulate a late stage of LTP in hippocampal CA1 Neurons. Science 260, 1661-1664.
39. Ghosh, A., and Greenberg, M. (1995). Calcium signalling in neurons-molecular mechanisms and cellular consequences. Science 268, 239-247.
40. Giese, K., Fedorov, N., Filipkowski, R., and Silva, A. (1998). Autophosphorylation at Thr 286 of the a calcium/calmodulin dependent kinase II in LTP and Learning. Science 279, 870-873.
41. Ginty, D. D., Bonni, A., and Greenberg, M. E. (1994). Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77, 713-725.
42. Gu, W., Shi, X., and Roeder, R. (1997). Synergistic activation of transcription by CBP and p53. Nature 387, 819-822.
43. Guzowski, G., and McGaugh, J. (1997). Antisense oligodeoxynucleotide-mediated disruption of hippocampal CREB protein levels impairs memory of a spatial task. Proceedings of the National Academy of Sciences USA 94, 2693-98.
44. Hardingham, G. E., Chawla, S., Johnson, C. M., and Bading, H. (1997). Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385, 360-365.
45. Hardingham, G. E., Cruzalegui, F., Chawla, S., and Bading, H. (1998). Mechanisms controlling gene expression by nuclear calcium signals. Cell Calcium 23, 131-134.
46. Harvey, J., and Collingridge, G. (1992). Thapsigargin blocks the induction of LTP in rat hippocampal slices. Neuroscience letters 139, 197-200.
47. Hebbes, T., Thorne, A., and Crane-Robinson, C. (1988). A direct link between core histone acetylation and transcriptionally active chromatin. EMBO Journal 7, 1395-1402.
48. Heist, E., and Schulman, H. (1998). The role of Ca2+/calmodulin dependent protein kinases within the nucleus. Cell Calcium 23, 103-114.
49. Hill, C. S., and Treisman, R. (1995a). Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 80, 199-211.
50. Hill, C. S., and Treisman, R. (1995b). Differential activation of c-fos promoter elements by serum, lysophosphatidic acid, G proteins and polypeptide growth factors. The EMBO Journal 14, 5037-5047.
51. Hoeffler, J., Meyer, T., Yun, Y., Jameson, L, and Habener, J. (1988). cAMP responsive DNA-binding protein-structure based on cloned placental cDNA. Science 242, 1430-1433.
52. Humbert, J., Matter, A., Artault, J., Koppler, P., and Malviya, A. (1996). Inositol 1, 4, 5 trisphosphate receptor is located to the inner nuclear membrane vindicating regulation of nuclear calcium signalling by inositol 1, 4, 5 trisphosphate. Journal of Biological Chemistry 271, 478-485.
53. Hummler, E., Cole, T., Blendy, J., Ganss, R., Aguzzi, A., Schmid, W., Beermann, F., and Shultz, G. (1994). Targeted mutation of the cAMP-response element binding protein (CREB) gene: compensation within the CREB/ATF family of transcription factors. Proceedings of the National Academy of Sciences USA 91, 5647-5651.
54. Hunter, T., and Karin, M. (1992). The regulation of transcription by phosphorylation. Cell 70, 375-387.
55. Impey, S., Mark, M., Villacres, E. C., Poser, S., Chavkin, C., and Storm, D. R. (1996). Induction of CRE-mediated gene expression by stimuli that generate longlasting LTP in Area CA1 of the hippocampus. Neuron 16, 973-982.
56. Janknecht, R., and Nordheim, A. (1996a). Regulation of the c-fos promoter by the ternary complex factor Sapla nad its coactivator CBP. Oncogene 12, 1961-1969.
57. Janknecht, R., and Nordheim, A. (1996b). MAP Kinase-dependent transcriptional coactivation by Elk-1 and its cofactor CBP. Biochemical Biophysical Research Communications 228, 831-837.
58. 2+/calmodulin-dependent protein kinase type Gr in rat cerebellar cortex. Proceedings of the National Academy of Sciences USA 88, 2850-2853.
59. Johnson, C. M., Hill, C. S., Chawla, S., Treisman, R., and Bading, H. (1997). Calcium controls gene expression via three distinct pathways that can function independently of the Ras/MAP kinase (ERKs) signalling cascade. Journal of Neuroscience 17, 6189-6202.
60. Kandel, E., and Schwartz, J. (1982). Molecular biology of learning-modulation of transmitter release. 1982 218, 433-443.
61. Kawasaki, H., Morooka, T., Shimohama, S., Kimura, J., Hirano, T., Gotoh, Y., and Nishida, E. (1997). Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J. Biol. Chem. 272, 18518-18521.
62. Kogan, J., Frankland, P., Blendy, J., Coblentz, J., Marowitz, Z., Schutz, G., and Silva, A. (1997). Spaced training induces normal long-term memory in CREB-mutant mice. Current Biology 7, 1-11.
63. Kullman, D. M., and Siegelbaum, S. A. (1995). The site of expression of NMDA-receptor dependent LTP: new fuel for old fire. Neuron 15, 997-1002.
64. Kwok, R. P. S., Lundblad, J. R., Chrivia, J. C., Richards, J. P., Bachinger, H. P., Brennan, R. G., Roberts, S. G. E., Green, M. R., and Goodman, R. H. (1994). Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370, 223-226.
65. Larkman, A., and Jack, J. (1995). Synaptic Plasticityhippocampal LTP. Current Opinion in neurobiology 5, 324-334.
66. Lin, C., Kapiloff, M., Durgerian, S., Tatemoto, K., Russo, A., Hanson, P., Schulman, H., and Rosenfeld, M. (1987). Molecular cloning of a brain specific calcium/calmodulin dependent protein kinase. Proceedings of the National Academy of Sciences USA 84, 5962-5966.
67. Lipp, P., Thomas, D., Berridge, M., and Bootman, M. (1997). Nuclear calcium signalling by individual cytoplasmic calcium puffs. EMBO Journal 16, 7166-7173.
68. Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., and Schottler, F. (1983). Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305, 719-721.
69. Malenka, R. (1994). Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78, 535-538.
70. Malenka, R., Kauer, J., Zucker, R., and Nicoll, R. (1988). Post-synaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242, 81-84.
71. Malinow, R., Schulman, H., and Tsien, R. W. (1989). Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245, 862-866.
72. Martinez-Balbas, M. A., Bannister, A., Martin, K., Haus-Seuffert, P., Meisterernst, M., and Kouzarides, T. (1998). The acetyltransferase activity of CBP stimulates transcription. EMBO Journal 17, 2886-2893.
73. Matthews, R. P., Guthrie, C. R., Wailes, L. M., Zhao, X., Means, A. R., and McKnight, G. S. (1994). Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Molecular and Cellular Biology 14, 6107-6116.
74. Mayford, M., Bach, N., Huang, Y., Wang, L., Hawkins, R., and Kandel, E. (1996). Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678-1683.
75. Meyer, T., Hanson, P., Stryer, L., and Schulman, H. (1992). Calmodulin trapping by CaM kinase II. Science 256, 1199-1202.
76. Miller, S., and Kennedy, M. (1986). Regulation of brain type-II calcium/calmodulin dependent protein kinase by autophosphorylation-a calcium/calmodulin dependent molecular switch. Cell 44, 861-870.
77. Milner, B., Corkin, S., and Teurber, H. (1968). Further analysis of the hippocampal amnesic syndrome: 14 year follow-up study of H.M. Neurophysiologia 6, 215-234.
78. Misra, R. P., Bonni, A., Miranti, C. K., Rivera, V. M., Sheng, M., and Greenberg, M. E. (1994). L-type voltage-sensitive calcium channel activation stimulates gene expression by a serum response factor-dependent pathway. The Journal of Biological Chemistry 269, 25483-25493.
79. Montarolo, P., Goelet, P., Castelucci, J., Morgan, J., Kandel, E., and Schacher, S. (1986). A critical period fro macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234, 1249-1254.
80. Montminy, M. R., and Bilezikjian, L. M. (1987). Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature 328, 175-178.
81. Montminy, M. R., Sevarino, K. A., Wagner, J. A., Mandel, G., and Goodman, R. H. (1986). Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proceedings of the National Academy of Sciences, USA 83, 6682-6686.
82. Morgan, J. I., and Curran, T. (1986). Role of ion influx in the control of c-fos expression. Nature 322, 552-555.
83. Morris, R., Anderson, E., Lynch, G., and Baudry, M. (1986). Selective impairment of learning and blockade of long-term potentiation by an NMDA receptor antagonist, AP5. Nature 319, 774-776.
84. Nadel, L., and Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinion in Neurobiology 7, 217-227.
85. Nakajima, T., Uchida, C., Anderson, S. E., Parvin, J. D., and Montminy, M. (1997). Analysis of a cAMP-responsive activator reveals a two component mechanism for transcriptional induction via signal-dependent factors. Genes and Development 11, 738-747.
86. Neylon, C., Hoyland, J., Mason, W., and Irvine, R. (1990). Spatial dynamics of intracellular calcium in agoniststimulated vascular smooth muscle cells. American Journal of Physiology 259, C675-C686.
87. Nguyen, P. V., Abel, T., and Kandel, E. R. (1994). Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265, 1104-1107.
88. Norman, C., Runswick, M., Pollock, R., and Treisman, R. (1988). Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55, 989-1003.
89. 2+/Calmodulin-dependent protein kinase enriched in cerebellar granule cells. Journal of Biological Chemistry 264, 5866-5875.
90. Parker, D., Ferreri, K., Nakajima, T., Lamorte, V. J., Evans, R., Koerber, S. C., Hoeger, C., and Montminy, M. R. (1996). Phosphorylation of CREB at ser-133 induces complex formation with the CREB-binding protein via a direct mechanism. Molecular and Cellular Biology 16, 694-703.
91. Ptashne, M., and Gann, A. (1997). Transcriptional activation by recruitment. Nature 386, 569-577.
92. Robertson, E., English, J., and Sweatt, J. (1996). A biochemists view of LTP. Learning and memory 3, 1-24.
93. Roeder, R. G. (1996). The role of general initiation factors in transcription by RNA polymerase II. Trends in Biochemical Sciences 21, 327-334.
94. Rosen, L. B., Ginty, D. D., Weber, M. J., and Greenberg, M. E. (1994). Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12, 1207-1221.
95. Rouse, J., Cohen, P., Trigon, S., Morange, M., Liamazares, A., Zamanillo, D., Hunt, T., and Nebrada, A. (1994). A novel kinase cascade triggered by stress and heat shock that stimulates MAP KAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78, 1027-1037.
96. Schröter, H., Shaw, P. E., and Nordheim, A. (1987). Purification of intercalator-released p67, a polypeptide that interacts specifically with the c-fos serum response element. Nucleic Acids Research 15, 10145-10157.
97. 2+/calmodulin-dependent protein kinases. Current Opinion in Cell Biology 5, 247-253.
98. Shankar, G., Davison, I., Helfrich, M. H., Mason, W. T., and Horton, M. A. (1993). Integrin receptor-mediated mobilization of intranuclear calcium in rat osteoclasts. Journal of Cell Science 105, 61-68.
99. Shen, S. (1995). Mechanisms of calcium regulation in seaurchin eggs and their activities during fertilisation. Current topics in developmental biology 30, 63-101.
100. Sheng, M., Dougan, S. T., McFadden, G., and Greenberg, M. E. (1988). Calcium and growth factor pathways of c-fos transcriptional activation require distinct upstream regulatory sequences. Molecular and Cellular Biology 8, 2787-2796.
101. Sheng, M., McFadden, G., and Greenberg, M. E. (1990a). Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4, 571-582.
102. 2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252, 1427-1430.
103. Silva, A. J., Paylor, R., Wehner, J. M., and Tonegawa, S. (1992b). Impaired spatial learning in a-calcium-calmodulin kinase II mutant mice. Science 257, 206-211.
104. Silva, A. J., Stevens, C. F., Tonegawa, S., and Wang, Y. (1992a). Deficient hippocampal long-term potentiation in a-calcium-calmodulin kinase II mutant mice. Science 257, 201-206.
105. 2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes & Development 8, 2527-2539.
106. Swope, D., Mueller, C., and Chrivia, J. (1996). CREB-binding protein activates transcription through multiple domains. Journal of Biological Chemistry 271, 28138-28145.
107. Tan, Y., Rouse, J., Zhang, A., Cariati, S., Cohen, P., and Comb, M. J. (1996). FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. The EMBO Journal, 4629-4642.
108. Treisman, R. (1985). Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5′ element and c-fos 3′ sequences. Cell 42, 889-902.
109. Treisman, R. (1987). Identification and purification of a polypeptide that binds to the c-fos serum response element. The EMBO Journal 6, 2711-2717.
110. Tully, T., Preat, T., Boynton, S. C., and Del Vecchio, M. (1994). Genetic dissection of consolidated memory in Drosophila. Cell 79, 35-47.
111. Turner, B., and O'Neill, L. (1995). Histone acetylation on chromatin and chromosomes. Seminars in Cell Biology 6, 229-236.
112. Verkhratsky, A., and Schmigol, A. (1996). Calcium induced calcium release in neurons. Cell Calcium 19, 1-14.
113. Whishaw, I., McKenna, J., and Maaswinkel, H. (1997). Hippocampal lesions and path integration. Current Opinion in Neurobiology 7, 228-234.
114. Williams, D., Fogarty, K., Tsien, R., and Fay, F. (1985). Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using Fura-2. Nature 318, 558-561.
115. Wisden, W., Errington, M. L., Williams, S., Dunnett, S. B., Waters, C., Hitchcock, D., Evan, G., Bliss, T. V. P., and Hunt, S. P. (1990). Differential expression of imme-diate early genes in the hippocampus and spinal cord. Neuron 4, 603-614.
116. Worley, P. F., Bhat, R. V., Barban, J. M., Erickson, C. A., McNaughton, B. L., and Barnes, C. A. (1993). Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement. The Journal of Neuroscience 13, 4776-4786.
117. Xing, J., Ginty, D. D., and Greenberg, M. E. (1996). Coupling of the RAS-MAPK pathway to gene activa-tion by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963.
118. Yao, T., Ku, G., Zhou, N., Scully, R., and Livingston, D. (1996). The nuclear hormone receptor coactivator SRC-1 is a specific target of p300. Proceedings of the National Academy of Sciences USA 93, 319-324.
119. Yin, J., Vecchio, M. D., Zhou, H., and Tully, T. (1995b). CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long term memory in Drosophila. Cell 81, 107-115.
120. Yin, J., Wallach, J., Wilder, E., Klingensmith, J., Dang, D., Perrimon, N., Zhou, H., Tully, T., and Quinn, W. (1995a). A Drosophila CREB/CREM homologue encodes multiple isoforms, including a cAMP dependent protein kinase responsive transcriptional activator and antagonist. Molecular Cell Biology, 5123-5130.