Abstract
CREB-responsive transcription is a conserved, important mechanism employed during memory formation. In both Drosophila and mice, overexpression of the activator isoform can enhance this process. However, in both systems, some conflicting data exists, providing a lingering doubt about its universality. In this review, we consider how molecular, cellular and systems parameters affect the fly dCREB2 gene during memory formation. This multi-level analysis provides plausible explanations for some of the discrepant data that exists in the fly system, and perhaps can inform mouse behavioral analysis as well.
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References
Ahmed BY, Husnain O, Stafford R, Howard M, Gujar AS, Moradiya V, Patel KK, Sihotra S (2013) Hyperphosphorylation of CREB in human dopaminergic neurons: a kinetic study of cellular distribution of total CREB and phosphor-CREB following oxidative stress. NeuroReport 24:757–762
Akalal DB, Yu D, Davis RL (2010) A late-phase, long-term memory trace forms in the γ neurons of Drosophila mushroom bodies after olfactory classical conditioning. J Neurosci 30:16699–16708
Akalal DB, Yu D, Davis RL (2011) The long-term memory trace formed in the Drosophila α/β mushroom body neurons is abolished in long-term memory mutants. J Neurosci 31:5643–5647
Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121–145
Alberini CM, Chen DY (2012) Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends Neurosci 35:274–283
Altarejos JY, Montminy M (2011) CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12:141–151
Balschun D, Wolfer DP, Gass P, Mantamadiotis T, Wetzl H, Schutz G, Frey JU, Lipp HP (2003) Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J Neurosci 23:6304–6314
Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689–703
Barco A, Pittenger C, Kandel ER (2003) CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert Opin Ther Targets 7:101–114
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 83:979–992
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 95:211–223
Belvin MP, Zhou H, Yin JC (1999) The Drosophila dCREB2 gene affects the circadian clock. Neuron 22:777–787
Bender W, Akam M, Karch F, Beachy PA, Peifer M, Spierer P, Lewis EB, Hogness DS (1983) Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 221:23–29
Benito E, Barco A (2010) CREB’s control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33:230–240
Bernier L, Castellucci VF, Kandel ER, Schwartz JH (1982) Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′, 5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia. J Neurosci 2:1682–1691
Bevilaqua LR, Cammarota M, Paratcha G, de Stein ML, Izquierdo I, Medina JH (1999) Experience-dependent increase in cAMP-responsive element binding protein in synaptic and nonsynaptic mitochondria of the rat hippocampus. Eur J Neurosci 11:3753–3756
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 15:1098–1106
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
Briand LA, Lee BG, Lelay J, Kaestner KH, Blendy JA (2015) Serine 133 phosphorylation is not required for hippocampal CREB-mediated transcription and behavior. Learn Mem 22:109–115
Brightwell JJ, Smith CA, Neve RL, Colombo PJ (2007) Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn Mem 14:195–199
Cammarota M, Paratcha G, Bevilaqua LR, Levi de Stein M, Lopez M, Pellegrino de Iraldi A, Izquierdo I, Medina JH (1999) Cyclic AM-responsive element binding protein in brain mitochondria. J Neurochem 72:2272–2277
Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bailey CH, Kandel ER (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221–237
Castelluci VF, Nairn A, Greengard P, Schwartz JH, Kandel ER (1982) Inhibitor of adenosine 3′,5′-monophosphate-dependent protein kinase blocks presynaptic facilitation in Alysia. J Neurosci 2:1673–1681
Chalovich EM, Zhu J, Caltagarone J, Bowser R, Chu CT (2006) Functional repression of cAMP response element in 6-hydroxydopamine-treated neuronal cells. J Biol Chem 281:17870–17881
Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, Blitzer RD, Alberini CM (2011) A critical role for IGF-II in memory consolidation and enhancement. Nature 469:491–497
Chen CC, Wu JK, Lin HW, Pai TP, Fu TF, Wu CL, Tully T, Chiang AS (2012) Visualizing long-term memory formation in two neurons of the Drosophila brain. Science 335:678–685
Chen YC, Hsu WL, Ma YL, Tai DJ, Lee EH (2014) CREB SUMOylation by the E3 ligase PIAS1 enhances spatial memory. J Neurosci 34:9574–9589
Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855–859
Comerford KM, Leonard MO, Karhausen J, Carey R, Colgan SP, Taylor CT (2003) Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia. Proc Natl Acad Sci U S A 100:986–991
Conkright MD, Montminy M (2005) CREB: the unindicted cancer co-conspirator. Trends Cell Biol 15:457–459
Conkright MD, Guzman E, Flechner L, Su AI, Hogenesch JB, Montminy M (2003) Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. Mol Cell 11:1101–1108
Correa SA, Hunter CJ, Palygin O, Wauters SC, Martin KJ, McKenzie C, McKelvey K, Morris RG, Pankratov Y, Arthur JS, Frenguelli BG (2012) MSK1 regulates homeostatic and experience-dependent synaptic plasticity. J Neurosci 32:13039–13051
Cox LJ, Hengst U, Gurskaya NG, Lukyanov KA, Jaffrey SR (2008) Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat Cell Biol 10:149–159
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 345:718–721
Davis RL, Kiger JA Jr (1981) Dunce mutants of Drosophila melanogaster: mutants defective in the cyclic AMP phosphodiesterase enzyme system. J Cell Biol 90:101–107
Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC (2006) CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9:475–477
Dragunow M (2004) CREB and neurodegeneration. Front Biosci 9:100–103
Dubnau J, Chiang A-S (2013) Systems memory consolidation in Drosophila. Curr Opin Neurobiol 23:84–91
Dudai Y, Jan YN, Byers D, Quinn WG, Benzer S (1976) Dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci U S A 73:1694–1698
Dudai Y, Uzzan A, Benzer S (1983) Abnormal activity of adenylate cyclase in the Drosophila memory mutant rutabaga. Neurosci Lett 42:207–212
Eckel-Mahan KL, Phan T, Han S, Wang H, Chan GC, Scheiner ZS, Storm DR (2008) Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence. Nat Neurosci 11:1074–1082
Endo A, Sumi D, Iwamoto N, Kumagai Y (2011) Inhibition of DNA binding activity of cAMP response element-binding protein by 1,2-naphthoquinone through chemical modification of cys-286. Chem Biol Interact 192:272–277
Finkbeiner S, Tavazoie SF, Maloratsky A, Jacobs KM, Harris KM, Greenberg ME (1997) CREB: a major mediator of neuronal neurotrophin responses. Neuron 19:1031–1047
Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536
Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661–1664
Fropf R, Tubon TC Jr, Yin JC (2013) Nuclear gating of a Drosophila dCREB2 activator is involved in memory formation. Neurobiol Learn Mem 106:258–267
Fropf R, Zhang J, Tanenhaus AK, Fropf WJ, Siefkes E, Yin JC (2014) Time of day influences memory formation and dCREB2 proteins in Drosophila. Front Syst Neurosci 8:43
Fusco S, Ripoli C, Podda MV, Ranieri SC, Leone L, Toietta G, McBurney MW, Schutz G, Riccio A, Grassi C, Galeotti T, Pani G (2012) A role for neuronal cAMP responsive-element binding (CREB)-1 in brain responses to calorie restriction. Proc Natl Acad Sci U S A 109:621–626
Garat CV, Fankell D, Irickson PF, Reusch JEB, Bauer NN, McMurtry IF, Klemm DJ (2006) Platelet-derived growth factor BB induces nuclear export and proteosomal degradation of CREB via phosphatidylinositol 3-kinase/Akt signaling in pulmonary artery smooth muscle cells. Mol Cell Biol 26:4934–4938
Gass P, Wolfer DP, Balschun D, Rudolph D, Frey U, Lipp HP, Schutz G (1998) Deficits in memory tasks of mice with CREB mutations depend on gene dosage. Learn Mem 5:274–288
Gerstner JR, Lyons LC, Wright KP Jr, Loh DH, Rawashdeh O, Eckel-Mahan KL, Roman GW (2009) Cycling behavior and memory formation. J Neurosci 29:12824–12830
Goren I, Tavor E, Goldblum A, Honigman A (2001) Two cysteine residues in the DNA-binding domain of CREB control binding to CRE and CREB-mediated gene expression. J Mol Biol 313:695–709
Greenberg ME, Thompson MA, Sheng M (1992) Calcium regulation of immediate early gene transcription. J Physiol Paris 86:99–108
Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A, Brown RA, Neve RL, Guzowski JF, Silva AJ, Josselyn SA (2007) Neuronal competition and selection during memory formation. Science 316:457–460
Hansen KF, Sakamoto K, Pelz C, Impey S, Obrietan K (2014) Profiling status epilepticus-induced changes in hippocampal RNA expression using high-throughput RNA sequencing. Sci Rep 4:6930
Hirano Y, Masuda T, Naganos S, Matsuno M, Ueno K, Miyashita T, Horiuchi J, Saitoe M (2013) Fasting launches CRTC to facilitate long-term memory formation in Drosophila. Science 339:443–446
Huang YY, Kandel ER (1994) Recruitment of a long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74–82
Huang FL, Huang KP, Wu J, Boucheron C (2006) Environmental enrichment enhances neurogranin expression and hippocampal learning and memory but fails to rescue the impairments of neurogranin null mutant mice. J Neurosci 26:6230–6237
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 91:5647–5651
Jancic D, Lopez de Armentia M, Valor LM, Olivares R, Barco A (2009) Inhibition of cAMP response element-binding protein reduces neuronal excitability and plasticity, and triggers neurodegeneration. Cereb Cortex 19:2535–2547
Johannessen M, Moens U (2007) Multisite phosphorylation of the cAMP response element-binding protein (CREB) by a diversity of protein kinases. Front Biosci 12:1814–1832
Josselyn SA, Shi C, Carlezon WA Jr, Neve RL, Nestler EJ, Davis M (2001) Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 21:2404–2412
Kandel E (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038
Kandel E (2012) The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2 and CPEB. Mol Brain 5:14
Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura M, Takemoto-Kimura S, Worley PF, Bito H (2009) Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc Natl Acad Sci U S A 106:316–321
Kida S, Serita T (2014) Functional roles of CREB as a positive regulator in the formation and enhancement of memory. Brain Res Bull 105:17–24
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
Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 69:2332–2336
Korol DL, Gold PE (1998) Glucose, memory, and aging. Am J Clin Nutr 67:764S–771S
Kuramoto N, Kubo K, Ogita K, Platenik J, Balcar VJ, Takarada T, Nakamichi N, Yoneda Y (2005) Nuclear condensation of cyclic adenosine monophosphate responsive element-binding protein in discrete murine brain structures. J Neurosci Res 80:667–676
Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SG, Green MR, Goodman RH (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370:223–226
Lee J, Kim CH, Simon DK, Aminova LR, Andreyev AY, Kushnareva YE, Murphy AN, Lonze BE, Kim KS, Ginty DD, Ferrante RJ, Ryu H, Ratan RR (2005) Mitochondrial cyclic AMP response element-binding protein (CREB) mediates mitochondrial gene expression and neuronal survival. J Biol Chem 280:40398–40401
Lemberger T, Parkitna JR, Chai M, Schutz G, Engblom D (2008) CREB has a context-dependent role in activity-regulated transcription and maintains neuronal cholesterol homeostasis. FASEB J 22:2872–2879
Lesiak A, Pelz C, Ando H, Zhu M, Davare M, Lambert TJ, Hansen KF, Obrietan K, Appleyard SM, Impey S, Wayman GA (2013) A genome-wide screen of CREB occupancy identifies the RhoA inhibitors Par6C and Rnd3 as regulators of BDNF-induced synaptogenesis. PLoS One 8, e64658
Lewis EB (1994) Homeosis: the first 100 years. Trends Genet 10:341–343
Liu Y, Sun L-Y, Singer DV, Ginnan R, Singer HA (2014) CaMKII delta-dependent inhibition of cAMP-response element binding protein activity in vascular smooth muscle. J Biol Chem 288:33519–33529
Lopez de Armentia M, Jancic D, Olivares R, Alarcon JM, Kandel ER, Barco A (2007) cAMP response element-binding protein-mediated gene expression increases the intrinsic excitability of CA1 pyramidal neurons. J Neurosci 27:13909–13918
Lu Q, Hutchins AE, Doyle CM, Lundblad JR, Kwok RP (2003) Acetylation of cAMP-responsive element-binding protein (CREB) by CREB-binding protein enhances CREB-dependent transcription. J Biol Chem 278:15727–15734
Lyons LC, Collado MS, Khabour O, Green CL, Eskin A (2006) The circadian clock modulates core steps in long-term memory formation in Aplysia. J Neurosci 26:8662–8671
Marie H, Morishita W, Yu X, Calakos N, Malenka RC (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741–752
Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927–938
Mayr B, Montminy M (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2:599–609
Montminy M (1997) Transcriptional regulation by cyclic AMP. Annu Rev Biochem 2:599–609
Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801
Perazzona B, Isabel G, Preat T, Davis RL (2004) The role of cAMP response element-binding protein in Drosophila long-term memory. J Neurosci 24:8823–8828
Restivo L, Tafi E, Ammassari-Teule M, Marie H (2009) Viral-mediated expression of a constitutively active form of CREB in hippocampal neurons increases memory. Hippocampus 19:228–234
Rexach JE, Clark PM, Mason DE, Neve RL, Peters EC, Hsieh-Wilson LC (2012) Dynamic O-GlcNAc modification regulates CREB-mediated gene expression and memory formation. Nat Chem Biol 8:253–261
Ruby NF, Hwang CE, Wessells C, Fernandez F, Zhang P, Sapolsky R, Heller HC (2008) Hippocampal-dependent learning requires a functional circadian system. Proc Natl Acad Sci U S A 105:15593–15598
Ryu H, Lee J, Impey S, Ratan RR, Ferrante RJ (2005) Antioxidants modulate mitochondrial PKA and increase CREB binding to D-loop DNA of the mitochondrial genome in neurons. Proc Natl Acad Sci U S A 102:13915–13920
Salinas JA, Gold PE (2005) Glucose regulation of memory for reward reduction in young and aged rats. Neurobiol Aging 26:45–52
Sargin D, Mercaldo V, Yiu AP, Higgs G, Han JH, Frankland PW, Josselyn SA (2013) CREB regulates spine density of lateral amygdala neurons: implications for memory allocation. Front Behav Neurosci 7:209
Sassone-Corsi P (2012) The cyclic AMP pathway. Cold Spring Har Perspect Biol 4:a011148
Scott R, Bourtchuladze R, Gossweiler S, Dubnau J, Tully T (2002) CREB and the discovery of cognitive enhancers. J Mol Neurosci 19:171–177
Sekeres MJ, Mercaldo V, Richards B, Sargin D, Mahadevan V, Woodin MA, Frankland PW, Josselyn SA (2012) Increasing CRTC2 function in the dentate gyrus during memory formation or reactivation increases memory strength without compromising memory quality. J Neurosci 32:17857–17868
Shanware NP, Trinh AT, Williams LM, Tibbetts RS (2007) Coregulated ataxia telangiectasia-mutated and casein kinase sites modulate cAMP-response element-binding protein-coactivator interactions in response to DNA damage. J Biol Chem 282:6283–6291
Shanware NP, Zhan L, Hutchinson JA, Kim SH, Williams LM, Tibbetts RS (2010) Conserved and distinct modes of CREB/ATF transcription factor regulation by PP2A/B56gamma and genotoxic stress. PLoS One 5:e12173. doi:10.1371/journal.pone.0012173
Shaywitz AJ, Greenberg ME (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821–861
Shen H, Tong L, Balazs R, Cotman CW (2001) Physical activity elicits sustained activation of the cyclic AMP response element-binding protein and mitogen-activated protein kinase in the rat hippocampus. Neuroscience 107:219–229
Sheng M, Thompson MA, Greenberg ME (1991) CREB: a Ca2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252:1427–1430
Skalhegg BS, Tasken K (2000) Specificity in the cAMP/PKA signaling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA. Front Biosci 5:D678–D693
Stern SA, Alberini CM (2013) Mechanisms of memory enhancement. Wiley Interdiscip Rev Syst Biol Med 5:37–53
Stern SA, Chen DY, Alberini CM (2014) The effect of insulin and insulin-like growth factors on hippocampus- and amydgala-dependent long-term memory formation. Learn Mem 21:556–563
Sun P, Enslen H, Myung PS, Maurer RA (1994) Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev 8:2527–2539
Sun P, Maurer RA (1995) An inactivating point mutation demonstrates that interaction of cAMP response element binding protein (CREB) with the CREB binding protein is not sufficient for transcriptional activation. J Biol Chem 270:7041–7044.
Suzuki A, Fukushima H, Mukawa T, Toyoda H, Wu LJ, Zhao MG, Xiu H, Shang Y, Endoh K, Iwamoto T, Mamiya N, Okano E, Hasegawa S, Mercaldo V, Zhang Y, Maeda R, Ohta M, Josselyn SA, Kida S (2011) Upregulation of CREB-mediated transcription enhances both short- and long-term memory. J Neurosci 31:8786–8802
Takahashi M, Obayashi M, Ishiguro T, Sato N, Niimi Y, Ozaki K, Mogushi K, Mahmut Y, Tanaka H, Tsuruta F, Dolmetsch R, Yamada M, Takahashi H, Kato T, Mori O, Eishi Y, Mizusawa H, Ishikawa K (2013) Cytoplasmic location of alpha1A voltage-gated calcium channel C-terminal fragment (Cav2.1-CTF) aggregate is sufficient to cause cell death. PLoS One 8:e50121
Tanenhaus AK, Zhang J, Yin JC (2012) In vivo circadian oscillation of dCREB2 and NF-kappaB activity in the Drosophila nervous system. PLoS One 7:45130. doi:10.1371/journal.pone.0045130
Tubon TC Jr, Zhang J, Friedman EL, Jin H, Gonzales ED, Zhou H, Drier D, Gerstner JR, Paulson EA, Fropf R, Yin JC (2013) dCREB2-mediated enhancement of memory formation. J Neurosci 33:7475–7487
Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35–47
Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590
Vecsey CG, Hawk JD, Lattal MK, Stein JM, Fabian SA, Attner MA, Cabrera SM, McDonough CB, Brindle PK, Abel T, Wood MA (2007) Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J Neurosci 27:6128–6140
Viosca J, Lopez de Armentia M, Jancic D, Barco A (2009) Enhanced CREB-dependent gene expression increases the excitability of neurons in the basal amygdala and primes the consolidation of contextual and cued fear memory. Learn Mem 16:193–197
Wen AY, Sakamoto KM, Miller LS (2010) The role of the transcription factor CREB in immune function. J Immunol 185:6413–6419
West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, Takasu MA, Tao X, Greenberg ME (2001) Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A 98:11024–11031
Williams BM, Luo Y, Ward C, Redd K, Gibson R, Kuczaj SA, McCoy JG (2001) Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiol Behav 73:649–658
Wu X, McMurray CT (2001) Calmodulin kinase II attenuation of gene transcription by preventing cAMP response element-binding protein (CREB) dimerization and binding of the CREB-binding protein. J Biol Chem 276:1735–1741
Wu CL, Xia S, Fu TF, Wang H, Chen YH, Leong D, Chiang AS, Tully T (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10:1578–1586
Yang JL, Lin YT, Chuang PC, Bohr VA, Mattson MP (2014) BDNF and exercise enhance neuronal DNA repair by stimulating CREB-mediated production of apurinic/apyrimidinic endonuclease 1. Neuromolecular Med 16:161–174
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
Yin JC, Del Vecchio M, Zhou H, Tully T (1995a) CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81:107–115
Yin JC, Wallach JS, Wilder EL, Klingensmith J, Dang D, Perrimon N, Zhou H, Tully T, Quinn WG (1995b) A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist. Mol Cell Biol 15:123–130
Yiu AP, Mercaldo V, Yan C, Richards B, Rashid AJ, Hsiang HL, Pressey J, Mahadevan V, Tran MM, Kushner SA, Woodin MA, Frankland PW, Josselyn SA (2014) Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training. Neuron 83:722–735
Yu D, Akalal DB, Davis RL (2006) Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52:845–855
Zhang X, Odom DT, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci U S A 102:4459–4464
Zhang J, Tanenhaus AK, Davis JC, Hanlon BM, Yin JC (2015) Spatio-temporal in vivo recording of dCREB2 dynamics in Drosophila long-term memory processing. Neurobiol Learn Mem 118:80–88
Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T, Balaji J, Neve R, Poirazi P, Silva AJ (2009) CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci 12:1438–1443
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Tanenhaus, A., Zhang, J., Yin, J.C.P. (2016). CREB-Mediated Memory Enhancement. In: Giese, K., Radwanska, K. (eds) Novel Mechanisms of Memory. Springer, Cham. https://doi.org/10.1007/978-3-319-24364-1_7
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