Dysregulation of memory-related proteins in the hipppocampus of aged rats and their relation with cognitive impairment

Hippocampus

Volumn 15, Issue 8, 2005, Pages 1041-1049

  Monti, Barbara ^a   Berteotti, Chiara ^a   Constestabile, Antonio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Aging; Arc; cAMP response element binding protein; CREB; Memory; Rat hippocampus

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN PROTEIN; CALCINEURIN; CCAAT ENHANCER BINDING PROTEIN BETA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; NEUROTROPHIN 4; PHOSPHOPROTEIN PHOSPHATASE;

ADOLESCENT; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEAR; HIPPOCAMPUS; LEARNING TEST; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; RAT STRAIN; UPREGULATION; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCINEURIN; CCAAT-ENHANCER-BINDING PROTEIN-BETA; COGNITION DISORDERS; CONDITIONING (PSYCHOLOGY); CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYTOSKELETAL PROTEINS; DATA INTERPRETATION, STATISTICAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEAR; HIPPOCAMPUS; LEARNING; MALE; MEMORY DISORDERS; NERVE TISSUE PROTEINS; PHOSPHORYLATION; RATS; RATS, WISTAR;

EID: 30344438257     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.20099     Document Type: Article

References (76)

1. Alberini CM, Ghirardi M, Metz R, Kandel ER. 1994. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099-1114.
2. Alonso M, Vianna MR, Depino AM, Mello E, Souza T, Pereira P, Szapiro G, Viola H, Pitossi F, Izquierdo I, Medina JH. 2002. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12:551-560.
3. Athos J, Impey S, Pineda VV, Chen X, Storm DR. 2002. Hippocampal CRE-mediated gene expression is required for contextual memory formation. Nat Neurosci 5:1119-1120.
4. Barnes CA. 1979. Memory deficits associated with senescence: neurophysiological and behavioural study in the rat. J Comp Physiol Psychol 93:74-104.
5. Bito H, Deisseroth K, Tsien RW. 1996. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
6. Blanchard RJ, Blanchard DC. 1969a. Crouching as an index of fear. J Comp Physiol Psychol 67:370-375.
7. Blanchard RJ, Blanchard DC. 1969b. Passive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol 67:129-135.
8. Blanchard RJ, Fukunaga KK, Blanchard DC. 1976. Environmental control of defensive reactions to footshock. Bull Psychonomic Soc 8:129-130.
9. Brightwell JJ, Gallagher M, Colombo PJ. 2004. Hippocampal CREB1 but not CREB2 is decreased in aged rats with spatial memory impairments. Neurobiol Learn Mem 81:19-26.
10. Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35:625-641.
11. 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.
12. Erickson CA, Barnes CA. 2003. The neurobiology of memory changes in normal aging. Exp Gerontol 38:61-69.
13. Fanselow MS. 1986. Associative vs topographical accounts of the immediate shock freezing deficit in rats: implications for the response selection rules governing species specific defensive reactions. Learn Motiv 17:16-39.
14. Fanselow MS. 1990. Factors governing one trial contextual conditioning. Anim Learn Behav 18:264-270.
15. Fanselow MS. 2000. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110:73-81.
16. Foster TC. 1999. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Brain Res Rev 30:236-249.
17. 2+ dysregulation with brain aging. J Neurosci 21:4066-4073.
18. Gallagher M, Rapp PR. 1997. The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 48:339-370.
19. Gong B, Vitolo OV, Trinchese F, Liu S, Shelanski M, Arancio O. 2004. Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J Clin Invest 114:1624-1634.
20. Guzowski JF, McGaugh JL. 1997. Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc Natl Acad Sci USA 94:2693-2698.
21. Guzowski JF, Setlow B, Wagner EK, McGaugh JL. 2001. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21:5089-5098.
22. Hall J, Thomas KL, Everitt BJ. 2000. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3:533-535.
23. Hawkins RD, Son H, Arancio O. 1998. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118:155-172.
24. Holland PC, Bouton ME. 1999. Hippocampus and context in classical conditioning. Curr Opin Neurobiol 2:195-202.
25. Houston FP, Stevenson GD, McNaughton BL, Barnes CA. 1999. Effects of age on the generalization and incubation of memory in the F344 rat. Learn Mem 6:111-119.
26. Ikegami S, Inokuchi K. 2002. Antisense DNA against calcineurin facilitates memory in contextual fear conditioning by lowering the threshold for hippocampal long-term potentiation induction. Neuroscience 98:637-646.
27. 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.
28. Karege F, Lambercy C, Schwald M, Steimer T, Cisse M. 2001a. Differential changes of cAMP-dependent protein kinase activity and 3H-cAMP binding sites in rat hippocampus during maturation and aging. Neurosci Lett 315:89-92.
29. Karege F, Schwald M, Lambercy C, Murama JJ, Cisse M, Malafosse A. 2001b. A non-radioactive assay for the cAMP-dependent protein kinase activity in rat brain homogenates and age-related changes in hippocampus and cortex. Brain Res 903:86-93.
30. Kausler DH. 1994. Learning and memory in normal aging. San Diego, CA: Academic Press.
31. Kim JJ, Fanselow MS. 1992. Modality-specific retrograde amnesia of fear. Science 256:675-677.
32. Knierim JJ. 2003. Hippocampus and memory. Can we have our place and fear it too? Neuron 37:372-376.
33. Kuo SP, Parfitt KD. 2004. Changes with aging in forskolin-stimulated and basal cyclic AMP in the hippocampus. Society for Neuroscience, Abstract, Program No. 905.5. 2004.
34. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl D. 1995. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 92:5734-5738.
35. Lowry OH, Rosenbrough RJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.
36. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF. 1995. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14:433-445.
37. Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose AM, Weitlauf C, Kandel ER, Winder DG, Mansuy IM. 2001. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 104:675-686.
38. Mansuy IM, Mayford M, Jacob B, Kandel ER, Bach ME. 1998. Restricted and regulated overexpression reveals calcineurin as a key component in the transition from short-term to long-term memory. Cell 92:39-49.
39. Moita MA, Rosis S, Zhou Y, Ledoux SE, Blair HT. 2003. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37: 685-687.
40. Montag-Sallaz M, Montag D. 2003. Learning-induced arg 3.1/arc mRNA expression in the mouse brain. Learn Mem 10:99-107.
41. Monti B, Berteotti C, Contestabile A. 2005. Subchronic Rolipram delivery activates hippocampal CREB and Arc, enhances retention and slows down extinction of conditioned fear memory. Neuropsychopharmacology, in press.
42. Monti B, Contestabile A. 2003. Effect of aging and dietary restriction on DNA fragmentation and caspase activity in the rat spinal cord. Brain Res 992:137-141.
43. Monti B, Virgili M, Contestabile A. 2003. Alterations of markers related to synaptic function in aging rat brain, in normal conditions or under conditions of long-term dietary manipulation. Neurochem Int 44:579-584.
44. Morris RG. 1989. Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J Neurosci 9:3040-3057.
45. Necchi D, Virgili M, Monti B, Contestabile A, Scherini E. 2002. Regional alterations of the NO/NOS system in the aging brain: a biochemical, histochemical and immunochemical study in the rat. Brain Res 933:31-41.
46. Obrietan K, Hoyt KR. 2004. CRE-dependent transcription is increased in Hunghtington's disease transgenic mice. J Neurosci 24:791-796.
47. Oler JA, Markus EJ. 1998. Age-related deficits on the radial maze and in fear conditioning: hippocampal processing and consolidation. Hippocampus 8:402-415.
48. Phillips RG, LeDoux JE. 1994. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn Mem 1:34-44.
49. Pinaud R, Penner MR, Robertson HA, Currie RW. 2001. Upregulation of the immediate early gene arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Brain Res Mol Brain Res 91:50-56.
50. Quinn JJ, Oommen SS, Morrison GE, Fanselow MS. 2002. Post-training excitotoxic lesions of the dorsal hippocampus attenuate forward trace, backward trace, and delay fear conditioning in a temporally specific manner. Hippocampus 12:495-504.
51. Rogelj B, Hartmann CE, Yeo CH, Hunt SP, Giese KP. 2003. Contextual fear conditioning regulates the expression of brain-specific small nucleolar RNAs in hippocampus. Eur J Neurosci 18:3089-3096.
52. Rosenzweig ES, Barnes CA. 2003. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69:143-179.
53. Rudy JW, O'Reilly RC. 2001. Conjunctive representations, the hippocampus, and contextual fear conditioning. Cogn Affect Behav Neurosci 1:66-82.
54. Sanders MJ, Wiltgen BJ, Fanselow MS. 2003. The place of the hippocampus in fear conditioning. Eur J Pharmacol 463:217-223.
55. Schaaf MJ, Workel JO, Lesscher HM, Vreugdenhil E, Oitzl MS, de Kloet ER. 2001. Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Res 915:227-233.
56. 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.
57. Silva AJ, Kogan JH, Frankland PW, Kida S. 1998. CREB and memory. Annu Rev Neurosci 21:127-148.
58. Tanila H, Shapiro M, Gallagher M, Eichenbaum H. 1997. Brain aging: changes in the nature of information coding by the hippocampus. J Neurosci 17:5155-5166.
59. Taubenfeld SM, Wiig KA, Bear MF, Alberini CM. 1999. A molecular correlate of memory and amnesia in the hippocampus. Nat Neurosci 2:309-310.
60. Taubenfeld SM, Milekic MH, Monti B, Alberini CM. 2001a. The consolidation of new but not reactivated memory requires hippocampal C/EBPβ Nat Neurosci 4:813-818.
61. Taubenfeld SM, Wiig KA, Monti B, Dolan B, Pollonini G, Alberini CM. 2001b. Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein [β] and [δ] co-localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J Neurosci 21:84-91.
62. Teyler TJ, Discenna P. 1984. Long-term potentiation as a candidate mnemonic device. Brain Res 319:15-28.
63. Tully T. 1991. Genetic dissection of learning and memory in Drosophila melanogaster. In: Madden J, editor. Neurobiology of learning, emotion and affect. New York: Raven. p 30-66.
64. Tully T, Bourtchouladze R, Scott R, Tallman J. 2003. Targeting the CREB pathway for memory enhances. Nat Rev Drug Discov 2:267-277.
65. Virgili M, Monti B, Polazzi E, Angiolini G, Contestabile A. 2001a. Topography of neurochemical alterations in the CNS of aged rats. Int J Dev Neurosci 19:109-116.
66. Virgili M, Necchi D, Scherini E, Contestabile A. 2001b. Increase of the ornithine decarboxylase/polyamine system and transglutaminase upregulation in the spinal cord of aged rats. Neurosci Lett 309: 62-66.
67. 2+ and cAMP requires protein kinase A, mitogen-activated protein kinase/extracellular regulated kinase activation. J Neurosci 21:5484-5493.
68. Ward MT, Oler JA, Markus EJ. 1999. Hippocampal dysfunction during aging I: deficits in memory consolidation. Neurobiol Aging 20:363-372.
69. 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 USA 98:11024-11031.
70. Westbrook RF, Good AJ, Kiernan MJ. 1994. Effects of the interval between exposure to a novel environment and the occurrence of shock on the freezing responses of rats. Q J Exp Psychol B 47:427-446.
71. Winder DG, Sweatt JD. 2001. Roles of serine/threonine phosphatase in hippocampal synaptic plasticity. Nat Rev Neurosci 2:461-474.
72. Woolf NJ, Zinnerman MD, Johnson GV. 1999. Hippocampal microtubule-associated protein-2 alterations with contextual memory. Brain Res 821:241-249.
73. Woolf NJ, Milov AM, Schweitzer ES, Roghani A. 2001. Elevation of nerve growth factor and antisense knockdown of TrkA receptor during contextual memory consolidation. J Neurosci 21:1047-1055.
74. Xie CW, Sayah D, Chen QS, Wei WZ, Smith D, Liu X. 2000. Deficient long-term memory and long-lasting long-term potentiation in mice with a targeted deletion of neurotrophin-4 gene. Proc Natl Acad Sci USA 97:8116-8121.
75. Yamada K, Mizuno M, Nabeshima T. 2002. Role for brain-derived neurotrophic factor in learning and memory. Life Sci 70:735-744.
76. Ying SW, Futter M, Rosenblum K, Webber MJ, Hunt SP, Bliss TV, Bramham CR. 2002. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22:1532-1540.