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2003 | 50 | 3 | 775-782
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The relation of transcription to memory formation.

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A distinction between short-term memories lasting minutes to hours and long-term memories lasting for many days is that the formation of long-term memories requires new gene expression. In this review, the focus is on the current understanding of the relation of transcription to memory consolidation based on the data collected from behavioral studies performed primarily on genetically altered animals. Studies in Drosophila and Aplysia indicate that the transcription factor cAMP/Ca2+ response element binding protein (CREB) is critical in mediating the conversion from short- to long-term memory. More recent genetic studies in mice also demonstrated CREB and inducible transcription factor Zif268 involvement in information storage processes. Transcription seems to play essential role in memory formation but the mechanisms for activation of transcription and downstream processes during memory consolidation remain unclear.
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  • University of California San Diego, Department of Neurosciences, 9500 Gilman Drive (M/C 0986), La Jolla, CA 92093-0986, U.S.A.
  • Abel T, Martin KC, Bartsch D, Kandel ER. (1998) Memory suppressor genes: inhibitory constraints on the storage of long-term memory. Science.; 279: 338-41.
  • Alberini CM, Ghirardi M, Metz R, Kandel ER. (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell.; 76: 1099-114.
  • Allweis C. (1991) The congruity of rat and chick multiphasic memory consolidation models. In neural and behavioural plasticity: the use of the domestic chick as a model. Andrew RJ. ed, pp 370-93. Oxford University Press, Oxford.
  • Andrew RJ. (1980) The functional organization of phases of memory consolidation. In Advances in the Study of Behaviour. Hinde RA, Beer C, Bunsel M. eds, pp 337-67. Academic Press, New York.
  • Baddeley AD. (1976) The psychology of memory. New York Basic Books.
  • Bartsch D, Casadio A, Karl KA, Serodio P, Kandel ER. (1998) CREB1 encodes a nuclear activator a repressor and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell.; 95: 211-23.
  • Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER. (1995) Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell.; 83: 979-92.
  • Bito H, Deisseroth K, Tsien RW. (1996) CREB phosphorylation and dephosphorylation: a Ca2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell.; 87: 1203-14.
  • Blendy JA, Kaestner KH, Schmid W, Gass P, Schutz G. (1996) Targeting of the CREB gene leads to up-regulation of a novel CREB mRNA isoform. EMBO J.; 15: 1098-106.
  • Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz 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.
  • Bozon B, Davis S, Laroche S. (2002) Regulated transcription of the immediate-early gene Zif268: mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation. Hippocampus.; 12: 570-7.
  • Brindle PK, Montminy MR. (1992) The CREB family of transcription activators. Curr Opin Genet Dev.; 2: 199-204.
  • Brunelli M, Castellucci V, Kandel ER. (1976) Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science.; 194: 1178-81.
  • Byrne JH, Kandel ER. (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci.; 16: 425-35.
  • Castellucci VF, Kandel ER, Schwartz JH, Wilson FD, Nairn AC, Greengard P. (1980) Intracellular injection of the catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. Proc Natl Acad Sci U S A.; 77: 7492-6.
  • Castellucci VF, Nairn A, Greengard P, Schwartz JH, Kandel ER. (1982) Inhibitor of adenosine 3':5'-monophosphate-dependent protein kinase blocks presynaptic facilitation in Aplysia. J Neurosci.; 2: 1673-81.
  • Chawla S, Hardingham GE, Quinn DR, Bading H. (1998) CBP: a signal-regulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV. Science.; 281: 1505-9.
  • Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH. (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature.; 365: 855-9.
  • 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: 474-6.
  • Dash PK, Hochner B, Kandel ER. (1990) Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature.; 345: 718-21.
  • Davis HP, Squire LR. (1984) Protein synthesis and memory: a review. Psychol Bull.; 96: 518-59.
  • Deisseroth K, Bito H, Tsien RW. (1996) Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron.; 16: 89-101.
  • Dubnau J, Tully T. (1998) Gene discovery in Drosophila: new insights for learning and memory. Annu Rev Neurosci.; 21: 407-44.
  • Gass P, Wolfer DP, Balschun D, Rudolph D, Frey U, Lipp HP, Schutz G. (1998) Deficits in memory tasks on mice with CREB mutations depend on gene dosage. Learning & Memory.; 5: 274-88.
  • Ghirardi M, Braha O, Hochner B, Montarolo PG, Kandel ER, Dale N. (1992) Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons. Neuron.; 9: 479-89.
  • Gonzalez GA, Montminy MR. (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell.; 59: 675-80.
  • Hall J, Thomas KL, Everitt BJ. (2001) Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci.; 21: 2186-93.
  • Hardingham GE, Chawla S, Cruzalegui FH, Bading H. (1999) Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron.; 22: 789-98.
  • Hardingham GE, Chawla S, Johnson CM, Bading H. (1997) Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature.; 385: 260-5.
  • Hu SC, Chrivia J, Ghosh A. (1999) Regulation of CBP-mediated transcription by neuronal calcium signaling. Neuron.; 22: 799-808.
  • Hummler E, Cole TJ, Blendy JA, Ganss R, Aguzzi A, Schmid W, Beermann F, Schutz G. (1994) Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. Proc Natl Acad Sci U S A.; 91: 5647-51.
  • Impey S, Mark M, 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: 973-82.
  • Impey S, Obrietan K, Wong ST, Poser S, Yano S, Wayman G, Deloulme JC, Chan G, Storm DR. (1998a) Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron.; 21: 869-83.
  • Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR. (1998b) Stimulation of cAMP response element. (CRE)-mediated transcription during contextual learning [see comments]. Nat Neurosci.; 1: 595-601.
  • Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, Charnay P, Bozon B, Laroche S, Davis S. (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci.; 4: 289-96.
  • Kaang BK, Kandel ER, Grant SG. (1993) Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron.; 10: 427-35.
  • Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, Masushige S, Silva AJ. (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci.; 5: 348-55.
  • Kogan JH, Frankland PW, Blendy JA, Coblentz J, Marowitz Z, Schutz G, Silva AJ. (1997) Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol.; 7: 1-11.
  • Korzus E, Torchia J, Rose DW, Xu L, Kurokawa R, McInerney EM, Mullen TM, Glass CK, Rosenfeld MG. (1998) Transcription factor-specific requirements for coactivators and their acetyltransferase functions. Science.; 279: 703-7.
  • Matthies H. (1989) In search of cellular mechanisms of memory. Prog Neurobiol.; 32: 277-349.
  • Mayford M, Korzus E. (2002) Genetics of memory in the mouse. In Neuropsychology of memory. Squire LR. ed, Guilford Publications Inc., New York.
  • McGaugh JL, Hertz MJ. (1972) Memory Consolidation. San Francisco Albion.
  • Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S. (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science.; 234: 1249-54.
  • Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y. (1996) The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell.; 87: 953-9.
  • Phillips RG, LeDoux JE. (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci.; 106: 274-85.
  • Pittenger C, Huang YY, Paletzki RF, Bourtchouladze R, Scanlin H, Vronskaya S, Kandel ER. (2002) Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron.; 34: 447-62.
  • Rosenzweig MR, Bennett EL. (1984) Direct processes and modulatory influences in the stages of memory formation. In Neurobiology of learning and memory. Lynch G, McGaugh JL, Weinberger NM. eds, pp 263-88. Guilford Press, New York.
  • Rudolph D, Tafuri A, Gass P, Hämmerling GJ, Arnold B, Schütz G. (1998) Impaired fetal T cell development and perinatal lethality in mice lacking the cAMP response element binding protein. Proc Natl Acad Sci U S A.; 95: 4481-6.
  • Schacher S, Castellucci VF, Kandel ER. (1988) cAmp evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis. Science.; 240: 1667-9.
  • Squire LR. (1987) Memory and brain. New York Oxford.
  • Squire LR, Davis HP, Spanis CW. (1980) Neurobiology of amnesia [letter]. Science.; 209: 836-7.
  • Squire LR, Zola SM. (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci U S A.; 93: 13515-22.
  • Tischmeyer W, Grimm R. (1999) Activation of immediate early genes and memory formation. Cell Mol Life Sci.; 55: 564-74.
  • Tully T. (1996) Discovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proc Natl Acad Sci U S A.; 93: 13460-7.
  • Worley PF, Cole AJ, Murphy TH, Christy BA, Nakabeppu Y, Baraban JM. (1990) Synaptic regulation of immediate-early genes in brain. Cold Spring Harb Symp Quant Biol.; 55: 213-23.
  • Yin JC, Del Vecchio M, Zhou H, Tully T. (1995) CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell.; 81: 107-15.
  • Yin JC, 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.
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