Hippocampal CREB1 but not CREB2 is decreased in aged rats with spatial memory impairments

Neurobiology of Learning and Memory

Volumn 81, Issue 1, 2004, Pages 19-26

  Brightwell, J J ^a   Gallagher, M ^c   Colombo, P J ^a,b  

^a TULANE UNIVERSITY   (United States)

^b Tulane University   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Aging; CREB; Memory; Morris water maze; Transcription factor

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; ACTIVATING TRANSCRIPTION FACTOR 4; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ISOPROTEIN; UNCLASSIFIED DRUG;

AGED; AGING; ANALYTIC METHOD; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HOMOGENATE; CONTROLLED STUDY; DATA ANALYSIS; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MEMORY DISORDER; NONHUMAN; PROTEIN EXPRESSION; RAT; RAT STRAIN; REGULATORY MECHANISM; SPATIAL MEMORY; STATISTICAL SIGNIFICANCE; WESTERN BLOTTING;

EID: 0345118873     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2003.08.001     Document Type: Article

References (49)

1. Asanuma M., Nishibayashi S., Iwata E., Kondo Y., Nakanishi T., Vargas M.G., Ogawa N. Alterations of cAMP response-element binding activity in the aged rat brain in response to administration of rolipram, a cAMP-specific phosphodiesterase inhibitor. Brain Research Molecular Brain Research. 41:1996;210-215.
2. Bach M.E., Barad M., Son H., Zhuo M., Lu Y.F., Shih R., Mansuy I., Hawkins R.D., Kandel E.R. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP-signaling pathway. Proceedings of the National Academy of Sciences USA. 96:1999;5280-5285.
3. Barnes C.A. Memory deficits associated with senescence: Neuro-physiological and behavioral study in the rat. Journal of Comparative Physiology and Psychology. 93:1979;74-104.
4. Barnes C.A. Aging and the physiology of memory. Neurobiology of Aging. 9:1988;563-568.
5. Bartsch D., Ghirardi M., Skehel P.A., Karl K.A., Herder S.P., Chen M., Bailey C.H., Kandel E.R. Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change. Cell. 83:1995;979-992.
6. Blendy J.A., Kaestner K.H., Schmid W., Gass P., Schütz G. Targeting of the CREB gene leads to up-regulation of a novel CREB mRNA isoform. EMBO Journal. 15:1996;1098-1106.
7. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
8. Bourtchuladze R., Frenguelli B., Blendy J., Cioffi D., Schutz G., Silva A.J. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell. 79:1994;59-68.
9. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 72:1976;248-254. doi:10.1006/abio.1976.9999.
10. Carew T.J. Molecular enhancement of memory. Neuron. 16:1996;5-8.
11. Colombo P.J., Gallagher M. Individual differences in spatial memory among aged rats are related to hippocampal PKCgamma immunoreactivity. Hippocampus. 12:2002;285-289.
12. Colombo P.J., Wetsel W.C., Gallagher M. Spatial memory is related to hippocampal subcellular concentrations of calcium-dependent protein kinase C isoforms in young and aged rats. Proceedings of the National Academy of Sciences USA. 94:1997;14195-14199.
13. Dash P.K., Hochner B., Kandel E.R. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature. 345:1990;718-721.
14. Davis H.P., Squire L.R. Protein synthesis and memory. Psychological Bulletin. 96:1984;518-559.
15. de Toledo-Morrell L., Geinisman Y., Morrell F. Age-dependent alterations in hippocampal synaptic plasticity: Relation to memory disorders. Neurobiology of Aging. 9:1988;581-590.
16. Foster T.C. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Research Brain Research Reviews. 30:1999;236-249.
17. 2+ dysregulation with brain aging. Journal of Neuroscience. 21:2001;4066-4073.
18. Gallagher M., Burwell R.D., Buchinal M. Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behavioral Neuroscience. 107:1993;618-626.
19. Gallagher M., Pelleymounter M.A. Spatial learning deficits in old rats: A model for memory decline in the aged. Neurobiology of Aging. 9:1988;549-556.
20. Gass P., Wolfer D.P., Balschun D., Rudolph D., Frey U., Lipp H.-P., Schütz G. Deficits in memory tasks of mice with CREB mutations depend on gene dosage. Learning and Memory. 5:1998;274-288.
21. 3H]dopa in various regions of the brain. Journal of Neurochemistry. 13:1966;655-669.
22. Goldspink D.F. Protein turnover and growth of the aged rat brain from the foetus to old age. Journal of Neurochemistry. 50:1988;1364-1368.
23. Gonzalez G.A., Yamamoto K.K., Fischer W.H., Karr D., Menzel P., Biggs W., Vale W.W., Montminy M.R. A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature. 337:1989;749-752.
24. Graves L., Dalvi A., Lucki I., Blendy J.A., Abel T. Behavioral analysis of CREB. αΔ mutation on a B6/129 F1 hybrid background Hippocampus. 12:2002;18-26.
25. Guzowski J.F., McGaugh J.L. Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proceedings of the National Academy of Sciences USA. 94:1997;2693-2698.
26. Hai T., Hartman M.G. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: Activation transcription factor proteins and homeostasis. Gene. 273:2001;1-11.
27. Hoeffler J.P., Meyer T.E., Yun Y., Jameson J.L., Habener J.F. Cyclic AMP-responsive DNA-binding protein: Structure based on a cloned placental cDNA. Science. 242:1988;1430-1433.
28. Impey S., Mark M., Villacres E.C., Poser S., Chavkin C., Storm D.R. Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron. 16:1996;973-982.
29. Impey S., Smith D.M., Obrietan K., Donahue R., Wade C., Storm D.R. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nature Neuroscience. 1:1998;595-601.
30. Jiang C.H., Tsien J.Z., Schultz P.G., Hu Y. The effects of aging on gene expression in the hypothalamus and cortex of mice. Proceedings of the National Academy of Sciences USA. 98:2001;1930-1934.
31. Josselyn S.A., Shi C., Carlezon W.A. Jr., Neve R.L., Nestler E.J., Davis M. Long-term memory is facilitated by cAMP-response element binding protein overexpression in the amygdala. Journal of Neuroscience. 21:2001;2404-2412.
32. Karpinski B.A., Morle G.D., Huggenvik J., Uhler M.D., Leiden J.M. Molecular cloning of human CREB-2: An ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element. Proceedings of the National Academy of Sciences USA. 89:1992;4820-4824.
33. Kelly A., Mullany P.M., Lynch M.A. Protein synthesis in entorhinal cortex and long-term potentiation in dentate gyrus. Hippocampus. 10:2000;431-437.
34. Krug M., Lossner B., Ott T. Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Research Bulletin. 13:1984;39-42.
35. Lanahan A., Lyford G., Stevenson G.S., Worley P.F., Barnes C.A. Selective alteration of long-term potentiation-induced transcriptional response in hippocampus of aged, memory-impaired rats. Journal of Neuroscience. 17:1997;2876-2885.
36. Landfield P.W., McGaugh J.L., Lynch G. Impaired synaptic potentiation processes in the hippocampus of aged, memory-deficient rat. Brain Research. 32:1978;523-533.
37. Liang G., Hai T. Characterization of human activating transcription factor 4, a transcriptional activator that interacts with multiple domains of cAMP-responsive element-binding protein (CREB)-binding protein (CBP). Journal of Biological Chemistry. 272:1997;24088-24095.
38. Malinow R., Mainen Z.F., Hayashi Y. LTP: From silence to four lane traffic. Current Opinion in Neurobiology. 10:2000;352-357.
39. Milner B. Disorders of learning and memory after temporal lobe lesion in man. Clinical Neurosurgery. 19:1972;421-446.
40. Montarolo P.G., Goelet P., Castelluci V.F., Morgan J., Kandel E.R., Schacher S. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science. 234:1986;1249-1254.
41. Nicolle M.M., Colombo P.J., Gallagher M., McKinney M. Metabotropic glutamate receptor-mediated hippocampal phosphoinositide turnover is blunted in spatial learning-impaired aged rats. Journal of Neuroscience. 19:1999;9604-9610.
42. Schoch S., Cibelli G., Magin A., Steinmuller L., Thiel G. Modular structure of cAMP response element binding protein 2 (CREB2). Neurochemistry International. 38:2001;601-608.
43. Schulz S., Siemer H., Krug M., Höllt V. Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo. Journal of Neuroscience. 19:1999;5683-5692.
44. Toni N., Buchs P.A., Nikonenko I., Povilaitite P., Parisi L., Muller D. Remodeling of synaptic membranes after induction of long-term potentiation. Journal of Neuroscience. 21:2001;6245-6251.
45. Vallejo M., Ron D., Miller C.P., Habener J.F. C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proceedings of the National Academy of Sciences USA. 90:1993;4679-4683.
46. Walton M., Young D., Sirimanne E., Dodd J., Christie D., Williams C., Gluckman P., Dragunow M. The role of the cyclic AMP-responsive element binding protein (CREB) in hypoxic-ischemic brain damage and repair. Brain Research Molecular Brain Research. 43:1996;21-29.
47. Winocur G. A neuropsychological analysis of memory loss with age. Neurobiology of Aging. 9:1988;487-494.
48. Yau J.L.W., Olsson T., Morris R.G.M., Noble J., Seckl J.R. Decreased NGFI-A gene expression in the hippocampus of cognitively impaired aged rats. Molecular Brain Research. 42:1996;354-357.
49. Yin J.C.P., Wallach J.S., Del Vecchio M., Wilder E.L., Zhou H., Quinn W.G., Tully T. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell. 79:1994;58-59.