Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms

Neurobiology of Aging

Volumn 28, Issue 6, 2007, Pages 831-844

  Costa, David A ^a,b   Cracchiolo, Jennifer R ^a,c   Bachstetter, Adam D ^a,d   Hughes, Tiffany F ^a,b   Bales, Kelly R ^e   Paul, Steven M ^e   Mervis, Ronald F ^c,d   Arendash, Gary W ^a,c   Potter, Huntington ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d Neurostructural Research Labs   (United States)

^e ELI LILLY AND COMPANY   (United States)

Author keywords

Alzheimer's disease; Amyloid; Environmental enrichment; Microarray

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; MUTANT PROTEIN; PRESENILIN 1;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITE; ENVIRONMENTAL ENRICHMENT; FEMALE; HIPPOCAMPUS; HOUSING; MALE; MICROARRAY ANALYSIS; MOUSE; MOUSE STRAIN; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 34247209601     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2006.04.009     Document Type: Article

References (72)

1. Amada N., Aihara K., Ravid R., and Horie M. Reduction of NR1 and phosphorylated Ca2+/calmodulin-dependent protein kinase II levels in Alzheimer's disease. Neuroreport 16 16 (2005) 1809-1813
2. Arendash G.W., Garcia M.F., Costa D.A., Cracchiolo J.R., Wefes I.M., and Potter H. Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. Neuroreport 15 11 (2004) 1751-1754
3. Arendash G.W., Gordon M.N., Diamond D.M., Austin L.A., Hatcher J.M., Jantzen P., et al. Behavioral assessment of Alzheimer's transgenic mice following long-term Abeta vaccination: task specificity and correlations between Abeta deposition and spatial memory. DNA Cell Biol 20 11 (2001) 737-744
4. Arendash G.W., King D.L., Gordon M.N., Morgan D., Hatcher J.M., Hope C.E., et al. Progressive, age-related behavioral impairments in transgenic mice carrying both mutant amyloid precursor protein and presenilin-1 transgenes. Brain Res 891 1-2 (2001) 42-53
5. Arendash G.W., Lewis J., Leighty R.E., McGowan E., Cracchiolo J.R., Hutton M., et al. Multi-metric behavioral comparison of APPsw and P301L models for Alzheimer's disease: linkage of poorer cognitive performance to tau pathology in forebrain. Brain Res 1012 1-2 (2004) 29-41
6. Barad M., Bourtchouladze R., Winder D.G., Golan H., and Kandel E. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci USA 95 25 (1998) 15020-15025
7. Bourtchouladze R., Lidge R., Catapano R., Stanley J., Gossweiler S., Romashko D., et al. A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proc Natl Acad Sci USA 100 18 (2003) 10518-10522
8. Cappai R., Mok S.S., Galatis D., Tucker D.F., Henry A., Beyreuther K., et al. Recombinant human amyloid precursor-like protein 2 (APLP2) expressed in the yeast Pichia pastoris can stimulate neurite outgrowth. FEBS Lett 442 1 (1999) 95-98
9. Castagne V., Lefevre K., and Clarke P.G. Dual role of the NF-kappaB transcription factor in the death of immature neurons. Neuroscience 108 3 (2001) 517-526
10. Chikahisa S., Sei H., Morishima M., Sano A., Kitaoka K., Nakaya Y., et al. Exposure to music in the perinatal period enhances learning performance and alters BDNF/TrkB signaling in mice as adults. Behav Brain Res 169 2 (2006) 312-319
11. Comery T.A., Shah R., and Greenough W.T. Differential rearing alters spine density on medium-sized spiny neurons in the rat corpus striatum: evidence for association of morphological plasticity with early response gene expression. Neurobiol Learn Mem 63 3 (1995) 217-219
12. Costa D.A., Nilsson L.N., Bales K.R., Paul S.M., and Potter H. Apolipoprotein is required for the formation of filamentous amyloid, but not for amorphous Abeta deposition, in an AbetaPP/PS double transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 6 5 (2004) 509-514
13. Cotman C.W. The role of neurotrophins in brain aging: a perspective in honor of Regino Perez-Polo. Neurochem Res 30 6-7 (2005) 877-881
14. Dobrogowska D.H., and Vorbrodt A.W. Immunogold localization of tight junctional proteins in normal and osmotically-affected rat blood-brain barrier. J Mol Histol 35 5 (2004) 529-539
15. Dodart J.C., Bales K.R., Johnstone E.M., Little S.P., and Paul S.M. Apolipoprotein E alters the processing of the beta-amyloid precursor protein in APP(V717F) transgenic mice. Brain Res 955 1-2 (2002) 191-199
16. Duff K., Eckman C., Zehr C., Yu X., Prada C.M., Perez-tur J., et al. Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1. Nature 383 6602 (1996) 710-713
17. Frankland P.W., O'Brien C., Ohno M., Kirkwood A., and Silva A.J. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411 6835 (2001) 309-313
18. Frick K.M., and Fernandez S.M. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol Aging 24 4 (2003) 615-626
19. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., et al. Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373 6514 (1995) 523-527
20. Glazewski S., Chen C.M., Silva A., and Fox K. Requirement for alpha-CaMKII in experience-dependent plasticity of the barrel cortex. Science 272 5260 (1996) 421-423
21. Glazewski S., Giese K.P., Silva A., and Fox K. The role of alpha-CaMKII autophosphorylation in neocortical experience-dependent plasticity. Nat Neurosci 3 9 (2000) 911-918
22. Globus A., Rosenzweig M.R., Bennett E.L., and Diamond M.C. Effects of differential experience on dendritic spine counts in rat cerebral cortex. J Comp Physiol Psychol 82 2 (1973) 175-181
23. Gong B., Vitolo O.V., Trinchese F., Liu S., Shelanski M., and Arancio O. Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J Clin Invest 114 11 (2004) 1624-1634
24. Gordon M.N., King D.L., Diamond D.M., Jantzen P.T., Boyett K.V., Hope C.E., et al. Correlation between cognitive deficits and Abeta deposits in transgenic APP + PS1 mice. Neurobiol Aging 22 3 (2001) 377-385
25. Honer W.G. Pathology of presynaptic proteins in Alzheimer's disease: more than simple loss of terminals. Neurobiol Aging 24 8 (2003) 1047-1062
26. Huber J.D., Egleton R.D., and Davis T.P. Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24 12 (2001) 719-725
27. Hughes P., and Dragunow M. Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol Rev 47 1 (1995) 133-178
28. Inayama M., Nishioka Y., Azuma M., Muto S., Aono Y., Makino H., et al. A novel I{kappa}B kinase-{beta} inhibitor ameliorates bleomycin-induced pulmonary fibrosis in mice. Am J Respir Crit Care Med 173 9 (2006) 1016-1022
29. Jankowsky J.L., Melnikova T., Fadale D.J., Xu G.M., Slunt H.H., Gonzales V., et al. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J Neurosci 25 21 (2005) 5217-5224
30. Jankowsky J.L., Xu G., Fromholt D., Gonzales V., and Borchelt D.R. Environmental enrichment exacerbates amyloid plaque formation in a transgenic mouse model of Alzheimer disease. J Neuropathol Exp Neurol 62 12 (2003) 1220-1227
31. Jensen M.T., Mottin M.D., Cracchiolo J.R., Leighty R.E., and Arendash G.W. Lifelong immunization with human beta-amyloid (1-42) protects Alzheimer's transgenic mice against cognitive impairment throughout aging. Neuroscience 130 3 (2005) 667-684
32. Koponen E., Voikar V., Riekki R., Saarelainen T., Rauramaa T., Rauvala H., et al. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLCgamma pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci 26 1 (2004) 166-181
33. Lazarov O., Robinson J., Tang Y.P., Hairston I.S., Korade-Mirnics Z., Lee V.M., et al. Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120 5 (2005) 701-713
34. Leighty R.E., Nilsson L.N., Potter H., Costa D.A., Low M.A., Bales K.R., et al. Use of multimetric statistical analysis to characterize and discriminate between the performance of four Alzheimer's transgenic mouse lines differing in Abeta deposition. Behav Brain Res 153 1 (2004) 107-121
35. Limback-Stokin K., Korzus E., Nagaoka-Yasuda R., and Mayford M. Nuclear calcium/calmodulin regulates memory consolidation. J Neurosci 24 48 (2004) 10858-10867
36. Loewenstein D.A., Acevedo A., Czaja S.J., and Duara R. Cognitive rehabilitation of mildly impaired Alzheimer disease patients on cholinesterase inhibitors. Am J Geriatr Psychiatry 12 4 (2004) 395-402
37. MacIntyre A., Hammond C.J., Little C.S., Appelt D.M., and Balin B.J. Chlamydia pneumoniae infection alters the junctional complex proteins of human brain microvascular endothelial cells. FEMS Microbiol Lett 217 2 (2002) 167-172
38. Malinow R., Schulman H., and Tsien R.W. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245 4920 (1989) 862-866
39. Navakkode S., Sajikumar S., and Frey J.U. The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. J Neurosci 24 35 (2004) 7740-7744
40. Nilsson L.N., Arendash G.W., Leighty R.E., Costa D.A., Low M.A., Garcia M.F., et al. Cognitive impairment in PDAPP mice depends on ApoE and ACT-catalyzed amyloid formation. Neurobiol Aging 25 9 (2004) 1153-1167
41. Ognibene E., Middei S., Daniele S., Adriani W., Ghirardi O., Caprioli A., et al. Aspects of spatial memory and behavioral disinhibition in Tg2576 transgenic mice as a model of Alzheimer's disease. Behav Brain Res 156 2 (2005) 225-232
42. Park H., Lee J.A., Lee C., Kim M.J., Chang D.J., Kim H., et al. An Aplysia type 4 phosphodiesterase homolog localizes at the presynaptic terminals of Aplysia neuron and regulates synaptic facilitation. J Neurosci 25 39 (2005) 9037-9045
43. Pinaud R., Penner M.R., Robertson H.A., and Currie R.W. 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 1-2 (2001) 50-56
44. Potter H., Wefes I.M., and Nilsson L.N. The inflammation-induced pathological chaperones ACT and apo-E are necessary catalysts of Alzheimer amyloid formation. Neurobiol Aging 22 6 (2001) 923-930
45. Ramirez-Amaya V., Escobar M.L., Chao V., and Bermudez-Rattoni F. Synaptogenesis of mossy fibers induced by spatial water maze overtraining. Hippocampus 9 6 (1999) 631-636
46. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., et al. Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci USA 97 23 (2000) 12880-12884
47. Riley K.P., Snowdon D.A., Desrosiers M.F., and Markesbery W.R. Early life linguistic ability, late life cognitive function, and neuropathology: findings from the Nun Study. Neurobiol Aging 26 3 (2005) 341-347
48. Schwarzman A.L., Gregori L., Vitek M.P., Lyubski S., Strittmatter W.J., Enghilde J.J., et al. Transthyretin sequesters amyloid beta protein and prevents amyloid formation. Proc Natl Acad Sci USA 91 18 (1994) 8368-8372
49. Serot J.M., Christmann D., Dubost T., and Couturier M. Cerebrospinal fluid transthyretin: aging and late onset Alzheimer's disease. J Neurol Neurosurg Psychiatry 63 4 (1997) 506-508
50. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87 4 (1953) 387-406
51. Silva A.J., Paylor R., Wehner J.M., and Tonegawa S. Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257 5067 (1992) 206-211
52. Silva A.J., Wang Y., Paylor R., Wehner J.M., Stevens C.F., and Tonegawa S. Alpha calcium/calmodulin kinase II mutant mice: deficient long-term potentiation and impaired spatial learning. Cold Spring Harb Symp Quant Biol 57 (1992) 527-539
53. Snowdon D.A., Kemper S.J., Mortimer J.A., Greiner L.H., Wekstein D.R., and Markesbery W.R. Linguistic ability in early life and cognitive function and Alzheimer's disease in late life. Findings from the Nun Study. JAMA 275 7 (1996) 528-532
54. Stein T.D., Anders N.J., DeCarli C., Chan S.L., Mattson M.P., and Johnson J.A. Neutralization of transthyretin reverses the neuroprotective effects of secreted amyloid precursor protein (APP) in APPSW mice resulting in tau phosphorylation and loss of hippocampal neurons: support for the amyloid hypothesis. J Neurosci 24 35 (2004) 7707-7717
55. Stein T.D., and Johnson J.A. Lack of neurodegeneration in transgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J Neurosci 22 17 (2002) 7380-7388
56. Stern Y., Gurland B., Tatemichi T.K., Tang M.X., Wilder D., and Mayeux R. Influence of education and occupation on the incidence of Alzheimer's disease. JAMA 271 13 (1994) 1004-1010
57. Sung S., Yang H., Uryu K., Lee E.B., Zhao L., Shineman D., et al. Modulation of nuclear factor-kappa B activity by indomethacin influences A beta levels but not A beta precursor protein metabolism in a model of Alzheimer's disease. Am J Pathol 165 6 (2004) 2197-2206
58. Tanzi R.E., Gusella J.F., Watkins P.C., Bruns G.A., St George-Hyslop P., Van Keuren M.L., et al. Amyloid beta protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer locus. Science 235 4791 (1987) 880-884
59. Tsuzuki K., Fukatsu R., Hayashi Y., Yoshida T., Sasaki N., Takamaru Y., et al. Amyloid beta protein and transthyretin, sequestrating protein colocalize in normal human kidney. Neurosci Lett 222 3 (1997) 163-166
60. Tsuzuki K., Fukatsu R., Yamaguchi H., Tateno M., Imai K., Fujii N., et al. Transthyretin binds amyloid beta peptides. Abeta1-42 and Abeta1-40 to form complex in the autopsied human kidney-possible role of transthyretin for abeta sequestration. Neurosci Lett 281 2-3 (2000) 171-174
61. Turner C.A., Lewis M.H., and King M.A. Environmental enrichment: effects on stereotyped behavior and dendritic morphology. Dev Psychobiol 43 1 (2003) 20-27
62. Ujiie M., Dickstein D.L., Carlow D.A., and Jefferies W.A. Blood-brain barrier permeability precedes senile plaque formation in an Alzheimer disease model. Microcirculation 10 6 (2003) 463-470
63. Valverde F. The rapid Golgi technique for staining CNS neurons: light microscopy. Neurosci Protocols 1 (1993) 1-9
64. Van Gelder R.N., von Zastrow M.E., Yool A., Dement W.C., Barchas J.D., and Eberwine J.H. Amplified RNA synthesized from limited quantities of heterogeneous cDNA. Proc Natl Acad Sci USA 87 5 (1990) 1663-1667
65. Viatour P., Merville M.P., Bours V., and Chariot A. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 30 1 (2005) 43-52
66. Wang P., Yang G., Mosier D.R., Chang P., Zaidi T., Gong Y.D., et al. Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-Like protein 2. J Neurosci 25 5 (2005) 1219-1225
67. Warrington J.A., Nair A., Mahadevappa M., and Tsyganskaya M. Comparison of human adult and fetal expression and identification of 535 housekeeping/maintenance genes. Physiol Genom 2 3 (2000) 143-147
68. Wilson R.S., Mendes De Leon C.F., Barnes L.L., Schneider J.A., Bienias J.L., Evans D.A., et al. Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA 287 6 (2002) 742-748
69. Yao P.J., Zhu M., Pyun E.I., Brooks A.I., Therianos S., Meyers V.E., et al. Defects in expression of genes related to synaptic vesicle trafficking in frontal cortex of Alzheimer's disease. Neurobiol Dis 12 2 (2003) 97-109
70. Young D., Lawlor P.A., Leone P., Dragunow M., and During M.J. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med 5 4 (1999) 448-453
71. Zhang H.T., Zhao Y., Huang Y., Dorairaj N.R., Chandler L.J., and O'Donnell J.M. Inhibition of the phosphodiesterase 4 (PDE4) enzyme reverses memory deficits produced by infusion of the MEK inhibitor U0126 into the CA1 subregion of the rat hippocampus. Neuropsychopharmacology 29 8 (2004) 1432-1439
72. Zou J.Y., and Crews F.T. TNF alpha potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: neuroprotection by NF kappa B inhibition. Brain Res 1034 1-2 (2005) 11-24