Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo

Journal of Neuroscience

Volumn 19, Issue 13, 1999, Pages 5683-5692

  Schulz, Stefan ^a   Siemer, Helge ^a   Krug, Manfred ^a   Höllt, Volker ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Antibodies; CREB; Hippocampus; Immunocytochemistry; LTP; Phosphorylation

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; GENE EXPRESSION REGULATION; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; LONG TERM MEMORY; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RAT; RNA TRANSCRIPTION; SHORT TERM MEMORY; SYNAPTIC TRANSMISSION;

EID: 0033168788     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-13-05683.1999     Document Type: Article

References (41)

1. Abel T, Kandel ER (1998) Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Res Rev 26:360-378.
2. Adams JC (1992) Biotin amplification of biotin and horseradish peroxidase signals in histochemical stains. J Histochem Cytochem 40:1457-1463.
3. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
4. Bailey CH, Bartsch D, Kandel ER (1996) Towards a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93:13445-13452.
5. Bailey CH, Kaang BK, Chen M, Martin KC, Lim CS, Casadio A, Kandel ER (1997) Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron 18:913-924.
6. 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.
7. 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.
8. Barzilai A, Kennedy TE, Sweatt JD, Kandel ER (1989) 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2:1577-1586.
9. Berger TW, Yeckel MF, Thiels E (1997) Network determinants of hippocampal synaptic plasticity. In: Long-term potentiation, Vol 3 (Baudry M, Davis JL, eds), pp 233-267. Cambridge, MA: MIT.
10. 2+-and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
11. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
12. Bourtchuladze R, Frenguelli B, Blendy J, Cioffy 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.
13. Collingridge GL, Bliss TVP (1995) Memories of NMDA receptors and LTP. Trends Neurosci 18:54-56.
14. 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 354:718-721.
15. 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.
16. Frank DA, Greenberg ME (1994) CREB: a mediator of long-term memory from mollusks to mammals. Cell 79:5-8.
17. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP stimulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
18. Ginty DD, Bonni A, Greenberg ME (1994) Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77:713-725.
19. Hagiwara M, Brindle P, Harootunian A, Armstrong R, Rivier J, Vale W, Tsien R, Montminy MR (1993) Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol Cell Biol 13:4852-4859.
20. Hevroni D, Rattner A, Bundman M, Lederfein D, Gabarah A, Mangelus M, Silverman MA, Kedar H, Naor C, Kornuc M, Hanoch T, Seger R, Theill LE, Nedivi E, Richter-Levin G, Citri Y (3998) Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. J Mol Neurosci 10:75-98.
21. Huang YY, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of the hippocampus requires repeated tetanization. Learn Mem 1:74-82.
22. Hughes P, Dragunow M (1995) Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol Rev 47:133-178.
23. Impey S, Mark M, Villacres EC, 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 16:973-982.
24. Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR (1998a) Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595-601.
25. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
26. Ito I, Hidaka H, Sugiama H (1991) Effects of KN-62, a specific inhibitor of calcium/calmodulin-dependent protein kinase II, on long-term potentiation in the rat hippocampus. Neurosci Lett 121:119-121.
27. Krug M, Lössner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39-42.
28. Matthies H (1989) In search of cellular mechanisms of memory. Prog Neurobiol 32:277-349.
29. Matthies H, Frey U, Reymann K, Krug M, Jork R, Schroeder H (1990) Multiple mechanisms and multiple stages of LTP. In: Excitatory amino acids and neuronal plasticity (Ben Ari Y, ed), pp 359-368. New York: Plenum.
30. Matthies Jr H, Reymann KG (1993) Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation. NeuroReport 4:712-714.
31. Matthies H, Schulz S, Höllt V, Krug M (1997a) Inhibition by compactin demonstrates a requirement of isoprenoid intermediates in hippocampal LTP. Neuroscience 79:341-346.
32. Matthies H, Schulz S, Thiemann W, Siemer H, Schmidt H, Krug M, Höllt V (1997b) Design of a multiple slice interface chamber and application for resolving the temporal pattern of CREB phosphorylation in hippocampal long-term potentiation. J Neurosci Methods 78:173-179.
33. Nicoll RA, Malenka RC (1995) Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115-117.
34. Otani S, Ben Ari Y (1993) Biochemical correlates of long-term potentiation in hippocampal synapses. Int Rev Neurobiol 35:1-41.
35. Paxinos G, Watson C (1983) The rat brain in stereotaxic coordinates. New York: Academic.
36. Schulz S, Höllt V (1998) Opioid withdrawal activates MAP kinase in locus coeruleus neurons in morphine-dependent rats in vivo. Eur J Neurosci 10:1196-1201.
37. 2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252:427-430.
38. Stevens CF (1994) CREB and memory consolidation. Neuron 13:769-770.
39. 2+/calmodulin-dependent protein kinases type II and IV involves phosphorylation of a site that negatively regulates activity. Genes Dev 8:2527-2539.
40. 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.
41. 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 81:107-115.