Advertisement

CREB-Mediated Memory Enhancement

  • Anne TanenhausEmail author
  • Jiabin Zhang
  • Jerry C. P. Yin
Chapter

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.

Keywords

CREB Long-term memory Memory enhancement Intrinsic excitability Synaptic plasticity Drosophila cAMP signaling Transcription Systems neuroscience 

References

  1. 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 24:757–762PubMedCrossRefGoogle Scholar
  2. 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 30:16699–16708PubMedPubMedCentralCrossRefGoogle Scholar
  3. 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 31:5643–5647PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121–145PubMedCrossRefGoogle Scholar
  5. Alberini CM, Chen DY (2012) Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends Neurosci 35:274–283PubMedPubMedCentralCrossRefGoogle Scholar
  6. Altarejos JY, Montminy M (2011) CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12:141–151PubMedPubMedCentralCrossRefGoogle Scholar
  7. 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 23:6304–6314PubMedGoogle Scholar
  8. 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 108:689–703PubMedCrossRefGoogle Scholar
  9. Barco A, Pittenger C, Kandel ER (2003) CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert Opin Ther Targets 7:101–114PubMedCrossRefGoogle Scholar
  10. 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 83:979–992PubMedCrossRefGoogle Scholar
  11. 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 95:211–223PubMedCrossRefGoogle Scholar
  12. Belvin MP, Zhou H, Yin JC (1999) The Drosophila dCREB2 gene affects the circadian clock. Neuron 22:777–787PubMedCrossRefGoogle Scholar
  13. 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 221:23–29PubMedCrossRefGoogle Scholar
  14. Benito E, Barco A (2010) CREB’s control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33:230–240PubMedCrossRefGoogle Scholar
  15. 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 2:1682–1691PubMedGoogle Scholar
  16. 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 11:3753–3756PubMedCrossRefGoogle Scholar
  17. 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 15:1098–1106PubMedPubMedCentralGoogle Scholar
  18. 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 79:59–68PubMedCrossRefGoogle Scholar
  19. 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 22:109–115PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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 14:195–199PubMedCrossRefGoogle Scholar
  21. 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 72:2272–2277PubMedCrossRefGoogle Scholar
  22. 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 99:221–237PubMedCrossRefGoogle Scholar
  23. 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 2:1673–1681Google Scholar
  24. 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 281:17870–17881PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 469:491–497PubMedPubMedCentralCrossRefGoogle Scholar
  26. 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 335:678–685PubMedCrossRefGoogle Scholar
  27. Chen YC, Hsu WL, Ma YL, Tai DJ, Lee EH (2014) CREB SUMOylation by the E3 ligase PIAS1 enhances spatial memory. J Neurosci 34:9574–9589PubMedCrossRefGoogle Scholar
  28. Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855–859PubMedCrossRefGoogle Scholar
  29. 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 100:986–991PubMedPubMedCentralCrossRefGoogle Scholar
  30. Conkright MD, Montminy M (2005) CREB: the unindicted cancer co-conspirator. Trends Cell Biol 15:457–459PubMedCrossRefGoogle Scholar
  31. 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 11:1101–1108PubMedCrossRefGoogle Scholar
  32. 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 32:13039–13051PubMedCrossRefGoogle Scholar
  33. 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 10:149–159PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 345:718–721PubMedCrossRefGoogle Scholar
  35. Davis RL, Kiger JA Jr (1981) Dunce mutants of Drosophila melanogaster: mutants defective in the cyclic AMP phosphodiesterase enzyme system. J Cell Biol 90:101–107PubMedCrossRefGoogle Scholar
  36. Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC (2006) CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9:475–477PubMedCrossRefGoogle Scholar
  37. Dragunow M (2004) CREB and neurodegeneration. Front Biosci 9:100–103PubMedCrossRefGoogle Scholar
  38. Dubnau J, Chiang A-S (2013) Systems memory consolidation in Drosophila. Curr Opin Neurobiol 23:84–91PubMedCrossRefGoogle Scholar
  39. 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 73:1694–1698CrossRefGoogle Scholar
  40. Dudai Y, Uzzan A, Benzer S (1983) Abnormal activity of adenylate cyclase in the Drosophila memory mutant rutabaga. Neurosci Lett 42:207–212PubMedCrossRefGoogle Scholar
  41. 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 11:1074–1082PubMedPubMedCentralCrossRefGoogle Scholar
  42. 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 192:272–277PubMedCrossRefGoogle Scholar
  43. Finkbeiner S, Tavazoie SF, Maloratsky A, Jacobs KM, Harris KM, Greenberg ME (1997) CREB: a major mediator of neuronal neurotrophin responses. Neuron 19:1031–1047PubMedCrossRefGoogle Scholar
  44. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536PubMedCrossRefGoogle Scholar
  45. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661–1664PubMedCrossRefGoogle Scholar
  46. Fropf R, Tubon TC Jr, Yin JC (2013) Nuclear gating of a Drosophila dCREB2 activator is involved in memory formation. Neurobiol Learn Mem 106:258–267PubMedCrossRefGoogle Scholar
  47. 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 8:43PubMedPubMedCentralCrossRefGoogle Scholar
  48. 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 109:621–626PubMedCrossRefGoogle Scholar
  49. 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 26:4934–4938PubMedPubMedCentralCrossRefGoogle Scholar
  50. 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 5:274–288PubMedPubMedCentralGoogle Scholar
  51. Gerstner JR, Lyons LC, Wright KP Jr, Loh DH, Rawashdeh O, Eckel-Mahan KL, Roman GW (2009) Cycling behavior and memory formation. J Neurosci 29:12824–12830PubMedPubMedCentralCrossRefGoogle Scholar
  52. 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 313:695–709PubMedCrossRefGoogle Scholar
  53. Greenberg ME, Thompson MA, Sheng M (1992) Calcium regulation of immediate early gene transcription. J Physiol Paris 86:99–108Google Scholar
  54. 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 316:457–460PubMedCrossRefGoogle Scholar
  55. 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 4:6930PubMedPubMedCentralCrossRefGoogle Scholar
  56. 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 339:443–446PubMedCrossRefGoogle Scholar
  57. 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 1:74–82PubMedGoogle Scholar
  58. 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 26:6230–6237PubMedCrossRefGoogle Scholar
  59. 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 91:5647–5651PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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 19:2535–2547PubMedCrossRefGoogle Scholar
  61. Johannessen M, Moens U (2007) Multisite phosphorylation of the cAMP response element-binding protein (CREB) by a diversity of protein kinases. Front Biosci 12:1814–1832PubMedCrossRefGoogle Scholar
  62. 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 21:2404–2412PubMedGoogle Scholar
  63. Kandel E (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038PubMedCrossRefGoogle Scholar
  64. Kandel E (2012) The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2 and CPEB. Mol Brain 5:14PubMedPubMedCentralCrossRefGoogle Scholar
  65. 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 106:316–321PubMedCrossRefGoogle Scholar
  66. Kida S, Serita T (2014) Functional roles of CREB as a positive regulator in the formation and enhancement of memory. Brain Res Bull 105:17–24PubMedCrossRefGoogle Scholar
  67. 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 7:1–11PubMedCrossRefGoogle Scholar
  68. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 69:2332–2336Google Scholar
  69. Korol DL, Gold PE (1998) Glucose, memory, and aging. Am J Clin Nutr 67:764S–771SPubMedGoogle Scholar
  70. 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 80:667–676PubMedCrossRefGoogle Scholar
  71. 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 370:223–226PubMedCrossRefGoogle Scholar
  72. 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 280:40398–40401PubMedPubMedCentralCrossRefGoogle Scholar
  73. 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 22:2872–2879PubMedCrossRefGoogle Scholar
  74. 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, e64658PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lewis EB (1994) Homeosis: the first 100 years. Trends Genet 10:341–343PubMedCrossRefGoogle Scholar
  76. 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 288:33519–33529CrossRefGoogle Scholar
  77. 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 27:13909–13918PubMedCrossRefGoogle Scholar
  78. 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 278:15727–15734PubMedCrossRefGoogle Scholar
  79. 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 26:8662–8671PubMedCrossRefGoogle Scholar
  80. 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 45:741–752PubMedCrossRefGoogle Scholar
  81. 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 91:927–938PubMedCrossRefGoogle Scholar
  82. Mayr B, Montminy M (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2:599–609PubMedCrossRefGoogle Scholar
  83. Montminy M (1997) Transcriptional regulation by cyclic AMP. Annu Rev Biochem 2:599–609Google Scholar
  84. Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801PubMedCrossRefGoogle Scholar
  85. Perazzona B, Isabel G, Preat T, Davis RL (2004) The role of cAMP response element-binding protein in Drosophila long-term memory. J Neurosci 24:8823–8828PubMedCrossRefGoogle Scholar
  86. 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 19:228–234PubMedCrossRefGoogle Scholar
  87. 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 8:253–261PubMedPubMedCentralCrossRefGoogle Scholar
  88. 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 105:15593–15598PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 102:13915–13920PubMedPubMedCentralCrossRefGoogle Scholar
  90. Salinas JA, Gold PE (2005) Glucose regulation of memory for reward reduction in young and aged rats. Neurobiol Aging 26:45–52PubMedCrossRefGoogle Scholar
  91. 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 7:209PubMedPubMedCentralCrossRefGoogle Scholar
  92. Sassone-Corsi P (2012) The cyclic AMP pathway. Cold Spring Har Perspect Biol 4:a011148Google Scholar
  93. Scott R, Bourtchuladze R, Gossweiler S, Dubnau J, Tully T (2002) CREB and the discovery of cognitive enhancers. J Mol Neurosci 19:171–177PubMedCrossRefGoogle Scholar
  94. 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 32:17857–17868PubMedCrossRefGoogle Scholar
  95. 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 282:6283–6291PubMedCrossRefGoogle Scholar
  96. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Shaywitz AJ, Greenberg ME (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821–861PubMedCrossRefGoogle Scholar
  98. 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 107:219–229PubMedCrossRefGoogle Scholar
  99. Sheng M, Thompson MA, Greenberg ME (1991) CREB: a Ca2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252:1427–1430PubMedCrossRefGoogle Scholar
  100. 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–D693PubMedGoogle Scholar
  101. Stern SA, Alberini CM (2013) Mechanisms of memory enhancement. Wiley Interdiscip Rev Syst Biol Med 5:37–53PubMedCrossRefGoogle Scholar
  102. 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 21:556–563PubMedPubMedCentralCrossRefGoogle Scholar
  103. 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 8:2527–2539PubMedCrossRefGoogle Scholar
  104. 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.Google Scholar
  105. 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 31:8786–8802PubMedCrossRefGoogle Scholar
  106. 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:e50121PubMedPubMedCentralCrossRefGoogle Scholar
  107. 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 CrossRefGoogle Scholar
  108. 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 33:7475–7487PubMedPubMedCentralCrossRefGoogle Scholar
  109. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35–47PubMedCrossRefGoogle Scholar
  110. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590PubMedCrossRefGoogle Scholar
  111. 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 27:6128–6140PubMedPubMedCentralCrossRefGoogle Scholar
  112. 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 16:193–197PubMedCrossRefGoogle Scholar
  113. Wen AY, Sakamoto KM, Miller LS (2010) The role of the transcription factor CREB in immune function. J Immunol 185:6413–6419PubMedCrossRefGoogle Scholar
  114. 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 98:11024–11031PubMedPubMedCentralCrossRefGoogle Scholar
  115. 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 73:649–658PubMedCrossRefGoogle Scholar
  116. 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 276:1735–1741PubMedCrossRefGoogle Scholar
  117. 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 10:1578–1586PubMedPubMedCentralCrossRefGoogle Scholar
  118. 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 16:161–174PubMedCrossRefGoogle Scholar
  119. 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 79:49–58PubMedCrossRefGoogle Scholar
  120. 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 81:107–115PubMedCrossRefGoogle Scholar
  121. 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 15:123–130CrossRefGoogle Scholar
  122. 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 83:722–735PubMedCrossRefGoogle Scholar
  123. 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 52:845–855PubMedPubMedCentralCrossRefGoogle Scholar
  124. 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 102:4459–4464PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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 118:80–88PubMedCrossRefGoogle Scholar
  126. 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 12:1438–1443PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Anne Tanenhaus
    • 1
    Email author
  • Jiabin Zhang
    • 2
  • Jerry C. P. Yin
    • 3
  1. 1.Department of EmbryologyCarnegie Institution for ScienceBaltimoreUSA
  2. 2.Department of Molecular Pharmacology and Experimental TherapeuticsMayo ClinicRochesterUSA
  3. 3.Laboratory of GeneticsUniversity of Wisconsin, MadisonMadisonUSA

Personalised recommendations