Neurobiology of Aging
Volume 29, Issue 10 , Pages 1533-1546 , October 2008

Alteration of CREB phosphorylation and spatial memory deficits in aged 129T2/Sv mice

Received 7 January 2007 ,Revised 12 March 2007 ,Accepted 23 March 2007.

References 

  1. Akirav I, Sandi C, Richter-Levin G. Differential activation of hippocampus and amygdala following spatial learning under stress. Eur. J. Neurosci. 2001;14(4):719–725
  2. Anderson KA, Noeldner PK, Reece K, Wadzinski BE, Means AR. Regulation and function of the calcium/calmodulin-dependent protein kinase IV/protein serine/threonine phosphatase 2A signaling complex. J. Biol. Chem. 2004;279(30):31708–31716
  3. Asanuma M, Nishibayashi S, Iwata E, Kondo Y, Nakanishi T, Vargas MG, et al. Alterations of cAMP response element-binding activity in the aged rat brain in response to administration of rolipram, a cAMP-specific phosphodiesterase inhibitor. Mol. Brain Res. 1996;41(1–2):210–215
  4. Athos J, Impey S, Pineda VV, Chen X, Storm DR. Hippocampal CRE-mediated gene expression is required for contextual memory formation. Nat. Neurosci. 2002;5(11):1119–1120
  5. Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R, et al. 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. Proc. Natl. Acad. Sci. U.S.A. 1999;96(9):5280–5285
  6. Baker JG, Hall IP, Hill SJ. Temporal characteristics of cAMP response element-mediated gene transcription: requirement for sustained cAMP production. Mol. Pharmacol. 2004;65(4):986–998
  7. Barnes CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 1979;93(1):74–104
  8. Barnes CA, McNaughton BL. An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses. Behav. Neurosci. 1985;99(6):1040–1048
  9. Bernabeu R, Bevilaqua L, Ardenghi P, Bromberg E, Schmitz P, Bianchin M, et al. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc. Natl. Acad. Sci. U.S.A. 1997;94(13):7041–7046
  10. Bito H, Deisseroth K, Tsien RW. CREB phosphorylation and dephosphorylation: a Ca2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell. 1996;87(7):1203–1214
  11. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell. 1994;79(1):59–68
  12. Brightwell JJ, Gallagher M, Colombo PJ. Hippocampal CREB1 but not CREB2 is decreased in aged rats with spatial memory impairments. Neurobiol. Learn. Mem. 2004;81(1):19–26
  13. Buhot MC, Wolff M, Savova M, Malleret G, Hen R, Segu L. Protective effect of 5-HT1B receptor gene deletion on the age-related decline in spatial learning abilities in mice. Behav. Brain Res. 2003;142(1–2):135–142
  14. Burke SN, Barnes CA. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 2006;7(1):30–40
  15. Colombo PJ, Brightwell JJ, Countryman RA. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J. Neurosci. 2003;23(8):3547–3554
  16. Deisseroth K, Bito H, Tsien RW. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron. 1996;16(1):89–101
  17. D’Hooge R, De Deyn PP . Applications of the Morris water maze in the study of learning and memory. Brain Res. Rev. 2001;36(1):60–90
  18. Florian C, Mons N, Roullet P. CREB antisense oligodeoxynucleotide administration into the dorsal hippocampal CA3 region impairs long- but not short-term spatial memory in mice. Learn. Mem. 2006;13(4):465–472
  19. Foster TC. Involvement of hippocampal synaptic plasticity in age-related memory decline.. Brain Res. Rev. 1999;30(3):236–249
  20. Foster TC, Sharrow KM, Masse JR, Norris CM, Kumar A. Calcineurin links Ca2+ dysregulation with brain aging. J. Neurosci. 2001;21(11):4066–4073
  21. Frick KM, Baxter MG, Markowska AL, Olton DS, Price DL. Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging. 1995;16(2):149–160
  22. Gallagher M, Rapp PR. The use of animal models to study the effects of aging on cognition. Annu. Rev. Psychol. 1997;48:339–370
  23. Geinisman Y, Detoledo-Morrell L, Morrell F, Heller RE. Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog. Neurobiol. 1995;45(3):223–252
  24. Gilbert PE, Kesner RP, Lee I. Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus. 2001;11(6):626–636
  25. Guzowski JF, McGaugh JL. Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl. Acad. Sci. U.S.A. 1997;94(6):2693–2698
  26. Hardingham GE, Arnold FJ, Bading H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 2001;4(3):261–267
  27. Hardingham GE, Bading H. The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 2003;26(2):81–89
  28. Hattiangady B, Rao MS, Shetty GA, Shetty AK. Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Exp. Neurol. 2005;195(2):353–371
  29. Head E, Mehta R, Hartley J, Kameka M, Cummings BJ, Cotman CW, et al. Spatial learning and memory as a function of age in the dog. Behav. Neurosci. 1995;109(5):851–858
  30. Huang YY, Pittenger C, Kandel ER. A form of long-lasting, learning-related synaptic plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. Proc. Natl. Acad. Sci. U.S.A. 2004;101(3):859–864
  31. Hsu KS, Huang CC, Liang YC, Wu HM, Chen YL, Lo SW, et al. Alterations in the balance of protein kinase and phosphatase activities and age-related impairments of synaptic transmission and long-term potentiation. Hippocampus. 2002;12(6):787–802
  32. Impey S, Mark M, Villacres EC, Poser S, Chavkin C, Storm DR. Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron. 1996;16(5):973–982
  33. Ingram DK, Jucker M. Developing mouse models of aging: a consideration of strain differences in age-related behavioral and neural parameters. Neurobiol. Aging. 1999;20(2):137–145
  34. Izquierdo I, Bevilaqua LR, Rossato JI, Bonini JS, Medina JH, Cammarota M. Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 2006;29(9):496–505
  35. Izquierdo LA, Barros DM, Vianna MR, Coitinho A, deDavid e Silva T, Choi H, et al. Molecular pharmacological dissection of short- and long-term memory. Cell Mol. Neurobiol. 2002;22(3):269–287
  36. Johannessen M, Delghandi MP, Moens U. What turns CREB on?. Cell Signal. 2004;16(11):1211–1227
  37. Josselyn SA, Kida S, Silva AJ. Inducible repression of CREB function disrupts amygdala-dependent memory. Neurobiol. Learn. Mem. 2004;82(2):159–163
  38. Josselyn SA, Shi C, Carlezon WA, Neve RL, Nestler EJ, Davis M. Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J. Neurosci. 2001;21(7):2404–2412
  39. Kudo K, Wati H, Qiao C, Arita J, Kanba S. Age-related disturbance of memory and CREB phosphorylation in CA1 area of hippocampus of rats. Brain Res. 2005;1054(1):30–37
  40. Lamprecht R. CREB: a message to remember. Cell Mol. Life Sci. 1999;55(4):554–563
  41. Lanahan A, Worley P. Immediate-early genes and synaptic function. Neurobiol. Learn. Mem. 1998;70(1–2):37–43
  42. Landfield PW, McGaugh JL, Lynch G. Impaired synaptic potentiation processes in the hippocampus of aged, memory-deficient rats. Brain Res. 1978;150(1):85–101
  43. Lee I, Kesner RP. Differential roles of dorsal hippocampal subregions in spatial working memory with short versus intermediate delay. Behav. Neurosci. 2003;117(5):1044–1053
  44. Lindner MD. Reliability, distribution, and validity of age-related cognitive deficits in the Morris water maze. Neurobiol. Learn. Mem. 1997;68(3):203–220
  45. Liu FC, Graybiel AM. Spatiotemporal dynamics of CREB phosphorylation: transient versus sustained phosphorylation in the developing striatum. Neuron. 1996;17(6):1133–1144
  46. Liu FC, Graybiel AM. Region-dependent dynamics of cAMP response element-binding protein phosphorylation in the basal ganglia. Proc. Natl. Acad. Sci. U.S.A. 1998;95(8):4708–4713
  47. Lonze BE, Ginty DD. Function and regulation of CREB family transcription factors in the nervous system. Neuron. 2002;35(4):605–623
  48. Lynch MA. Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta?. Prog. Neurobiol. 1998;56(5):571–589
  49. Malleret G, Hen R, Guillou JL, Segu L, Buhot MC. 5-HT1B receptor knock-out mice exhibit increased exploratory activity and enhanced spatial memory performance in the Morris water maze. J. Neurosci. 1999;19(14):6157–6168
  50. McGaugh JL. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 2004;27:1–28
  51. McGaugh JL, Cahill L. Interaction of neuromodulatory systems in modulating memory storage. Behav. Brain Res. 1997;83(1–2):31–38
  52. McIntyre CK, Miyashita T, Setlow B, Marjon KD, Steward O, Guzowski JF, et al. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2005;102(30):10718–10723
  53. Miyamoto E. Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J. Pharmacol. Sci. 2006;100(5):433–442
  54. Mizuno M, Yamada K, Maekawa N, Saito K, Seishima M, Nabeshima T. CREB phosphorylation as a molecular marker of memory processing in the hippocampus for spatial learning. Behav. Brain Res. 2002;133(2):135–141
  55. Moncada D, Viola H. Phosphorylation state of CREB in the rat hippocampus: a molecular switch between spatial novelty and spatial familiarity?. Neurobiol. Learn. Mem. 2006;
  56. Mons N, Segu L, Nogues X, Buhot MC. Effects of age and spatial learning on adenylyl cyclase mRNA expression in the mouse hippocampus. Neurobiol. Aging. 2004;25(8):1095–1106
  57. Monti B, Berteotti C, Contestabile A. Dysregulation of memory-related proteins in the hippocampus of aged rats and their relation with cognitive impairment. Hippocampus. 2005;15(8):1041–1049
  58. Mouravlev A, Dunning J, Young D, During MJ. Somatic gene transfer of cAMP response element-binding protein attenuates memory impairment in aging rats. Proc. Natl. Acad. Sci. U.S.A. 2006;103(12):4705–4710
  59. Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S. NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. Neurosci. 2004;5(5):361–372
  60. Packard MG, Cahill L, McGaugh JL. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc. Natl. Acad. Sci. U.S.A. 1994;91(18):8477–8481
  61. Pittenger C, Fasano S, Mazzocchi-Jones D, Dunnett SB, Kandel ER, Brambilla R. Impaired bidirectional synaptic plasticity and procedural memory formation in striatum-specific cAMP response element-binding protein-deficient mice. J. Neurosci. 2006;26(10):2808–2813
  62. Pittenger C, Huang YY, Paletzki RF, Bourtchouladze R, Scanlin H, Vronskaya S, et al. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron. 2002;34(3):447–462
  63. Ramos BP, Birnbaum SG, Lindenmayer I, Newton SS, Duman RS, Arnsten AF. Dysregulation of protein kinase a signaling in the aged prefrontal cortex: new strategy for treating age-related cognitive decline. Neuron. 2003;40(4):835–845
  64. Rapp PR, Kansky MT, Roberts JA. Impaired spatial information processing in aged monkeys with preserved recognition memory. Neuroreport. 1997;8(8):1923–1928
  65. Richter-Levin G, Akirav I. Emotional tagging of memory formation—in the search for neural mechanisms. Brain Res. Rev. 2003;43(3):247–256
  66. Rosenzweig ES, Barnes CA. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol. 2003;69(3):143–179
  67. Schulz S, Siemer H, Krug M, Hollt V. Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo. J. Neurosci. 1999;19(13):5683–5692
  68. Silva AJ, Kogan JH, Frankland PW, Kida S. CREB and memory. Annu. Rev. Neurosci. 1998;21:127–148
  69. Skeberdis VA, Chevaleyre V, Lau CG, Goldberg JH, Pettit DL, Suadicani SO, et al. Protein kinase A regulates calcium permeability of NMDA receptors. Nat. Neurosci. 2006;9(4):501–510
  70. Stanciu M, Radulovic J, Spiess J. Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: relationship to Fos production. Mol. Brain Res. 2001;94(1–2):15–24
  71. Taubenfeld SM, Milekic MH, Monti B, Alberini CM. The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat. Neurosci. 2001;4(8):813–818
  72. Touzani K, Marighetto A, Jaffard R. Fos imaging reveals ageing-related changes in hippocampal response to radial maze discrimination testing in mice. Eur. J. Neurosci. 2003;17(3):628–640
  73. Trifilieff P, Herry C, Vanhoutte P, Caboche J, Desmedt A, Riedel G, et al. Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn. Mem. 2006;13(3):349–358
  74. Tsien JZ, Huerta PT, Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell. 1996;87(7):1327–1338
  75. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, et al. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. U.S.A. 2001;98(20):11024–11031
  76. Wolff M, Savova M, Malleret G, Segu L, Buhot MC. Differential learning abilities of 129T2/Sv and C57BL/6J mice as assessed in three water maze protocols. Behav. Brain Res. 2002;136(2):463–474
  77. Wyss JM, Chambless BD, Kadish I, van Groen T. Age-related decline in water maze learning and memory in rats: strain differences. Neurobiol. Aging. 2000;21(5):671–681

PII: S0197-4580(07)00133-9

doi: 10.1016/j.neurobiolaging.2007.03.023

Neurobiology of Aging
Volume 29, Issue 10 , Pages 1533-1546 , October 2008