dCREB2-mediated enhancement of memory formation

Journal of Neuroscience

Volumn 33, Issue 17, 2013, Pages 7475-7487

  Tubon, Thomas C ^a,d   Zhang, Jiabin ^a   Friedman, Eugenia L ^a   Jin, Haining ^b   Gonzales, Erin D ^a   Zhou, Hong ^a   Drier, Diana ^c   Gerstner, Jason R ^e   Paulson, Emily A ^a   Fropf, Robin ^a   Yin, Jerry C P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Health   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d Madison College   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; COMPLEMENTARY DNA; LUCIFERASE;

ARTICLE; DROSOPHILA; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; HEAT SHOCK; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MEMORY; NUCLEOTIDE SEQUENCE; OLFACTORY MEMORY; PHYLOGENETIC TREE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING;

EID: 84876547213     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4387-12.2013     Document Type: Article

References (73)

1. Ahmed T, Frey JU (2005) Plasticity-specific phosphorylation of CaMKII, MAP-kinases and CREB during late-LTP in rat hippocampal slices in vitro. Neuropharmacology 49:477-492. CrossRef Medline
2. Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121-145. CrossRef Medline
3. Alzoubi KH, Alkadhi KA (2007) A critical role of CREB in the impairment of late-phase LTP by adult onset hypothyroidism. Exp Neurol 203:63-71. CrossRef Medline
4. 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. CrossRef Medline
5. Barco A, Patterson SL, Alarcon JM, Gromova P, Mata-Roig M, Morozov A, Kandel ER (2005) Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48:123-137. CrossRef Medline
6. 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. CrossRef Medline
7. Belvin MP, Zhou H, Yin JC (1999) The Drosophila dCREB2 gene affects the circadian clock. Neuron 22:777-787. CrossRef Medline
8. Benito E, Barco A (2010) CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33: 230-240. CrossRef Medline
9. Blendy JA, Kaestner KH, Schmid W, Gass P, Schutz G (1996) Targeting of the CREB gene leads to upregulation of a novel CREB mRNA isoform. EMBO J 15:1098-1106. Medline
10. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc Lond B Biol Sci 358:805-814. CrossRef Medline
11. Brightwell JJ, Smith CA, Countryman RA, Neve RL, Colombo PJ (2005) Hippocampal overexpression of mutant CREB blocks long-term, but not short-term memory for a socially transmitted food preference. Learn Mem 12:12-17. CrossRef Medline
12. Brightwell JJ, Smith CA, Neve RL, Colombo PJ (2007) Long-term memory for place learingin is facilitated by expression of cAMP responsive element-binding protein in the dorsal hippocampus. Learn Mem 14:195-199. CrossRef Medline
13. Cao G, Nitabach MN (2008) Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J Neurosci 28: 6493-6501. CrossRef Medline
14. Cao JL, Vialou VF, Lobo MK, Robison AJ, Neve RL, Cooper DC, Nestler EJ, Han MH (2010) Essential role of the cAMP-cAMP response-element binding protein pathway in opiate-induced homeostatic adaptations of locus coeruleus neurons. Proc Natl Acad Sci U S A 107:17011-17016. CrossRef Medline
15. Chaudhury D, Wang LM, Colwell CS (2005) Circadian regulation of hippocampal long-term potentiation. J Biol Rhythms 20:225-236. CrossRef Medline
16. 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. CrossRef Medline
17. Dash PK, Hochner B, Kandel ER (1990) Injection of the cAMP-responsive element binding protein into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718-721. CrossRef Medline
18. Davis GW, Schuster CM, Goodman CS (1996) Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17:669-679. CrossRef Medline
19. Delmas V, Laoide BM, Masquilier D, de Groot RP, Foulkes NS, Sassone-Corsi P (1992) Alternative usage of initiation codons in mRNA encoding the cAMP-responsive-element modulator generates regulators with opposite functions. Proc Natl Acad Sci U S A 89:4226-4230. CrossRef Medline
20. Demczuk S, Harbers M, Vennström B (1993) Identification and analysis of all components of a gel retardation assay by combination with immunoblotting. Proc Natl Acad Sci U S A 90:2574-2578. CrossRef Medline
21. 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. Medline
22. 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. CrossRef Medline
23. Ejima A, Griffith LC (2011) Assay for courtship suppression in Drosophila. Cold Spring Harb Protoc 2011(2):pdb.prot5575. CrossRef Medline
24. Fernandez RI, Lyons LC, Levenson J, Khabour O, Eskin A (2003) Circadian modulation of long-term sensitization in Aplysia. Proc Natl Acad Sci U S A 100:14415-14420. CrossRef Medline
25. Gonzalez GA, Yamamoto KK, Fischer WH, Karr D, Menzel P, Biggs W 3rd, Vale WW, Montminy MR (1989) A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature 337:749-752. CrossRef Medline
26. Goren I, Tavor E, Goldblum A, Honigman A (2001) Two cysteine residues in the DNA-binding domain of CREB control binding to CRE and CREBmediated gene expression. J Mol Biol 313:695-709. CrossRef Medline
27. Guzowski JF, McGaugh JL (1997) Antisense oligodeoxynucleotidemediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc Natl Acad Sci U S A 94:2693-2698. CrossRef Medline
28. 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. CrossRef Medline
29. Han JH, Yiu AP, Cole CJ, Hsiang HL, Neve RL, Josselyn SA (2008) Increasing CREB in the auditory thalamus enhances memory and generalization of auditory conditioned fear. Learn Mem 15:443-453. CrossRef Medline
30. Han MH, Bolaños CA, Green TA, Olson VG, Neve RL, Liu RJ, Aghajanian GK, Nestler EJ (2006) Role of cAMP response element-binding protein in the rat locus ceruleus: regulation of neuronal activity and opiate withdrawal behaviors. J Neurosci 26:4624-4629. CrossRef Medline
31. Hendricks JC, Williams JA, Panckeri K, Kirk D, Tello M, Yin JC, Sehgal A (2001) A non-circadian role for cAMP signaling and CREB activity in Drosophila rest homeostasis. Nat Neurosci 4:1108-1115. CrossRef Medline
32. Horiuchi J, Jiang W, Zhou H, Wu P, Yin JC (2004) Phosphorylation of conserved casein kinase sites regulates cAMP-response element-binding protein DNA binding in Drosophila. J Biol Chem 279:12117-12125. Medline
33. Hotte M, Thuault S, Dineley KT, Hemmings HC Jr, Nairn AC, Jay TM (2007) Phosphorylation of CREB and DARPP-32 during late LTP at hippocampal to prefrontal cortex synapses in vivo. Synapse 61:24-28. CrossRef Medline
34. Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR (1998) Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595-601. CrossRef Medline
35. Izquierdo LA, Barros DM, Vianna MR, Coitinho A, DeDavid e Silva T, Choi H, Moletta B, Medina JH, Izquierdo I (2002) Molecular pharmacological dissection of short- and long-term memory. Cell Mol Neurobiol 22: 269-287. CrossRef Medline
36. Jasnow AM, Shi C, Israel JE, Davis M, Huhman KL (2005) Memory of social defeat is facilitated by cAMP-response element-binding protein overexpression in the amygdala. Behav Neurosci 119:1125-1130. CrossRef Medline
37. Josselyn SA, Nguyen PV (2005) CREB, synapses and memory disorders: past progress and future challenges. Curr Drug Targets CNS Neurol Disord 4:481-497. CrossRef Medline
38. 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. Medline
39. Josselyn SA, Kida S, Silva AJ (2004) Inducible repression of CREB function disrupts amygdala-dependent memory. Neurobiol Learn Mem 82:159-163. CrossRef Medline
40. Kida S, Josselyn SA, Peña de Ortiz S, Kogan JH, Chevere I, Masushige S, Silva AJ (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348-355. CrossRef Medline
41. Ko GY, Shi L, Ko ML (2009) Circadian regulation of ion channels and their functions. J Neurochem 110:1150-1169. CrossRef Medline
42. Lamarre-Vincent N, Hsieh-Wilson LC (2003) Dynamic glycosylation of the transcription factor CREB: a potential role in gene regulation. J AmChem Soc 125:6612-6613. CrossRef Medline
43. Lamprecht R, Hazvi S, Dudai Y (1997) cAMP response element-binding protein in the amygdala is required for long- but not short-term conditioned taste aversion memory. J Neurosci 17:8443-8450. Medline
44. Leutgeb JK, Frey JU, Behnisch T (2005) Single cell analysis of activitydependent cyclic AMP-responsive element-binding protein phosphorylation during long-lasting long-term potentiation in area CA1 of mature rat hippocampal-organotypic cultures. Neuroscience 131:601-610. CrossRef Medline
45. Liu RY, Cleary LJ, Byrne JH (2011) The requirement for enhanced CREB1 expression in consolidation of long-term synaptic facilitation and longterm excitability in sensory neurons of Aplysia. J Neurosci 31:6871-6879. CrossRef Medline
46. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623. CrossRef Medline
47. 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. CrossRef Medline
48. Lyons LC, Rawashdeh O, Katzoff A, Susswein AJ, Eskin A (2005) Circadian modulation of complex learning in diurnal and nocturnal Aplysia. Proc Natl Acad Sci U S A 102:12589-12594. CrossRef Medline
49. 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. CrossRef Medline
50. Miyamoto E (2006) Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100:433-442. CrossRef Medline
51. Mouravlev A, Dunning J, Young D, During MJ (2006) Somatic gene transfer of cAMP response element-binding protein attenuates memory impairment in aging rats. Proc Natl Acad Sci U S A 103:4705-4710. CrossRef Medline
52. 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. CrossRef
53. Philips GT, Tzvetkova EI, Carew TJ (2007) Transient mitogen-activated protein kinase activation is confined to a narrow temporal window required for the induction of two-trial long-term memory in Aplysia. J Neurosci 27:13701-13705. CrossRef Medline
54. Riccio A, Alvania RS, Lonze BE, Ramanan N, Kim T, Huang Y, Dawson TM, Snyder SH, Ginty DD (2006) A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol Cell 21:283-294. CrossRef Medline
55. 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. CrossRef Medline
56. Sakai T, Tamura T, Kitamoto T, Kidokoro Y (2004) A clock gene, period, plays a key role in long-term memory formation in Drosophila. Proc Natl Acad Sci U S A 101:16058-16063. CrossRef Medline
57. Schulz S, Siemer H, Krug M, Höllt V (1999) Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during longterm potentiation in the rat dentate gyrus in vivo. J Neurosci 19:5683-5692. Medline
58. 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. CrossRef Medline
59. Siegel RW, Hall JC (1979) Conditioned responses in courship behavior of normal and mutant Drosophila. Proc Natl Acad Sci U S A 76:3430-3434. Medline
60. Suzuki A, Fukushima H, Mukawa T, Toyoda H, Wu LJ, Zhao MG, Xu H, Shang Y, Endoh K, Iwamoto T, Mamiya N, Okano E, Hasegawa S, Mercaldo V, Zhang Y, Maeda R, Ohta M, Josselyn SA, Zhuo M, Kida S (2011) Upregulation of CREB-mediated transcription enhances both short- and long-term memory. J Neurosci 31:8786-8802. CrossRef Medline
61. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709-726. CrossRef Medline
62. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263-277. CrossRef Medline
63. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35-47. CrossRef Medline
64. Viosca J, Lopez de Armentia M, Jancic D, Barco A (2009) Enhanced CREBdependent 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. Medline
65. Wagatsuma A, Azami S, Sakura M, Hatakeyama D, Aonuma H, Ito E (2006) De Novo synthesis of CREB in a presynaptic neuron is required for synaptic enhancement involved in memory consolidation. J Neurosci Res 84:954-960. CrossRef Medline
66. Wallace DL, Han MH, Graham DL, Green TA, Vialou V, Iñiguez SD, Cao JL, Kirk A, Chakravarty S, Kumar A, Krishnan V, Neve RL, Cooper DC, Bolaños CA, Barrot M, McClung CA, Nestler EJ (2009) CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12:200-209. CrossRef Medline
67. Warburton EC, Glover CP, Massey PV, Wan H, Johnson B, Bienemann A, Deuschle U, Kew JN, Aggleton JP, Bashir ZI, Uney J, Brown MW (2005) cAMP responsive element-binding protein phosphorylation is necessary for perirhinal long-term potentiation and recognition memory. J Neurosci 25:6296-6303. CrossRef Medline
68. Yin JC, Tully T (1996) CREB and the formation of long-term memory. Curr Opin Neurobiol 6:264-268. CrossRef Medline
69. 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. CrossRef Medline
70. Yin JC, Del Vecchio M, Zhou H, Tully T (1995a) CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances longterm memory in Drosophila. Cell 81:107-115. CrossRef Medline
71. 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 15:5123-5130. Medline
72. Zhang JJ, Okutani F, Inoue S, Kaba H (2003) Activation of the cyclic AMP response element-binding protein signaling pathway in the olfactory bulb is required for the acquisition of olfactory aversive learning in young rats. Neuroscience 117:707-713. CrossRef Medline
73. 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. CrossRef Medline