Cognitive and Physical Activity Differently Modulate Disease Progression in the Amyloid Precursor Protein (APP)-23 Model of Alzheimer's Disease

Biological Psychiatry

Volumn 60, Issue 12, 2006, Pages 1314-1323

  Wolf, Susanne A ^a   Kronenberg, Golo ^a   Lehmann, Kathrin ^a   Blankenship, Aaron ^a   Overall, Rupert ^a   Staufenbiel, Matthias ^b   Kempermann, Gerd ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Adult neurogenesis; enriched environment; mouse; neurotrophin; stem cell; water maze

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NEUROTROPHIN 3;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; EXERCISE; FEMALE; FITNESS; HIPPOCAMPUS; LEARNING; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; UPREGULATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL COUNT; CEREBRAL CORTEX; COGNITION; DISEASE PROGRESSION; ENVIRONMENT; FEMALE; FIBROBLAST GROWTH FACTOR 2; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR I; MAZE LEARNING; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; NERVE GROWTH FACTOR; NEUROTROPHIN 3; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33751550928     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2006.04.004     Document Type: Article

References (91)

1. Adlard P.A., Perreau V.M., and Cotman C.W. The exercise-induced expression of BDNF within the hippocampus varies across life-span. Neurobiol Aging 26 (2005) 511-520
2. Adlard P.A., Perreau V.M., Pop V., and Cotman C.W. Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J Neurosci 25 (2005) 4217-4221
3. Aguado-Llera D., Arilla-Ferreiro E., Campos-Barros A., Puebla-Jimenez L., and Barrios V. Protective effects of insulin-like growth factor-I on the somatostatinergic system in the temporal cortex of beta-amyloid-treated rats. J Neurochem 92 (2005) 607-615
4. 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 (2004) 1751-1754
5. Benraiss A., Chmielnicki E., Lerner K., Roh D., and Goldman S.A. Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J Neurosci 21 (2001) 6718-6731
6. Blanchard R.J., Wall P.M., and Blanchard D.C. Problems in the study of rodent aggression. Horm Behavior 44 (2003) 161-170
7. Bondolfi L., Calhoun M., Ermini F., Kuhn H.G., Wiederhold K.H., Walker L., et al. Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J Neurosci 22 (2002) 515-522
8. Borchelt D.R., Ratovitski T., van Lare J., Lee M.K., Gonzales V., Jenkins N.A., et al. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19 (1997) 939-945
9. Brandt M.D., Jessberger S., Steiner B., Kronenberg G., Reuter K., Bick-Sander A., et al. Transient calretinin-expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 24 (2003) 603-613
10. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., and Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467 (2003) 1-10
11. Caille I., Allinquant B., Dupont E., Bouillot C., Langer A., Muller U., and Prochiantz A. Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 131 (2004) 2173-2181
12. Calhoun M.E., Wiederhold K.H., Abramowski D., Phinney A.L., Probst A., Sturchler-Pierrat C., et al. Neuron loss in APP transgenic mice. Nature 395 (1998) 755-756
13. Cao L., Jiao X., Zuzga D.S., Liu Y., Fong D.M., Young D., and During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36 (2004) 827-835
14. Carro E., and Torres-Aleman I. The role of insulin and insulin-like growth factor I in the molecular and cellular mechanisms underlying the pathology of Alzheimer's disease. Eur J Pharmacol 490 (2004) 127-133
15. Carro E., Trejo J.L., Busiguina S., and Torres-Aleman I. Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. J Neurosci 21 (2001) 5678-5684
16. Colcombe S.J., Kramer A.F., Erickson K.I., Scalf P., McAuley E., Cohen N.J., et al. Cardiovascular fitness, cortical plasticity, and aging. Proc Natl Acad Sci U S A 101 (2004) 3316-3321
17. Colcombe S.J., Kramer A.F., McAuley E., Erickson K.I., and Scalf P. Neurocognitive aging and cardiovascular fitness: recent findings and future directions. J Mol Neurosci 24 (2004) 9-14
18. Conti L., and Cattaneo E. Controlling neural stem cell division within the adult subventricular zone: an APPealing job. Trends Neurosci 28 (2005) 57-59
19. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21 (2005) 1-14
20. Del Ser T., Hachinski V., Merskey H., and Munoz D.G. An autopsy-verified study of the effect of education on degenerative dementia. Brain 122 Pt 12 (1999) 2309-2319
21. Dobrossy M.D., Drapeau E., Aurousseau C., Le Moal M., Piazza P.V., and Abrous D.N. Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 8 (2003) 974-982
22. Dumont M., Strazielle C., Staufenbiel M., and Lalonde R. Spatial learning and exploration of environmental stimuli in 24-month-old female APP23 transgenic mice with the Swedish mutation. Brain Res 1024 (2004) 113-121
23. Ehninger D., and Kempermann G. Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex 13 (2003) 845-851
24. Ehninger D., and Kempermann G. Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity. Genes Brain Behav 5 (2006) 29-39
25. Fabel K., Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., et al. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18 (2003) 2803-2812
26. Falkenberg T., Mohammed A.K., Henriksson B., Persson H., Winblad B., and Lindefors N. Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett 138 (1992) 153-156
27. Farmer J., Zhao X., van Praag H., Wodtke K., Gage F.H., and Christie B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 124 (2004) 71-79
28. Fratiglioni L., Paillard-Borg S., and WinbladB. An active and socially integrated lifestyle in late life might protect against dementia. Lancet Neurol 3 (2004) 343-353
29. Friedland R.P., Fritsch T., Smyth K.A., Koss E., Lerner A.J., Chen C.H., et al. Patients with Alzheimer's disease have reduced activities in midlife compared with healthy control-group members. Proc Natl Acad Sci U S A 98 (2001) 3440-3445
30. Gomez-Pinilla F., Dao L., and So V. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res 764 (1997) 1-8
31. Gould E., Beylin A., Tanapat P., Reeves A., and Shors T.J. Learning enhances adult neurogenesis in the hippoampal formation. Nat Neurosci 2 (1999) 260-265
32. Griesbach G.S., Hovda D.A., Molteni R., Wu A., and Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience 125 (2004) 129-139
33. Haughey N.J., Liu D., Nath A., Borchard A.C., and Mattson M.P. Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neuromolecular Med 1 (2002) 125-135
34. Haughey N.J., Nath A., Chan S.L., Borchard A.C., Rao M.S., and Mattson M.P. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J Neurochem 83 (2002) 1509-1524
35. Ickes B.R., Pham T.M., Sanders L.A., Albeck D.S., Mohammed A.H., and Granholm A.C. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164 (2000) 45-52
36. Jankowsky J.L., Savonenko A., Schilling G., Wang J., Xu G., and Borchelt D.R. Transgenic mouse models of neurodegenerative disease: opportunities for therapeutic development. Curr Neurol Neurosci Rep 2 (2002) 457-464
37. 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 (2003) 1220-1227
38. Jessberger S., Römer B., Babu H., and Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 196 (2005) 342-351
39. Jin K., Galvan V., Xie L., Mao X.O., Gorostiza O.F., Bredesen D.E., and Greenberg D.A. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc Natl Acad Sci U S A 101 (2004) 13363-13367
40. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., and Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 101 (2004) 343-347
41. Katzman R. Education and the prevalence of dementia and Alzheimer's disease. Neurology 43 (1993) 13-20
42. Kawas C.H., Clark C.M., Farlow M.R., Knopman D.S., Marson D., Morris J.C., et al. Clinical trials in Alzheimer disease: debate on the use of placebo controls. Alzheimer Dis Assoc Disord 13 (1999) 124-129
43. Kelly P.H., Bondolfi L., Hunziker D., Schlecht H.P., Carver K., Maguire E., et al. Progressive age-related impairment of cognitive behavior in APP23 transgenic mice. Neurobiol Aging 24 (2003) 365-378
44. Kempermann G., Gast D., and Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52 (2002) 135-143
45. Kempermann G., Jessberger S., Steiner B., and Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27 (2004) 447-452
46. Kempermann G., Kuhn H.G., and Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386 (1997) 493-495
47. Kempermann G., Kuhn H.G., and Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18 (1998) 3206-3212
48. Kronenberg G, Bick-Sander A, Bunk E, Wolf C, Ehninger D, Kempermann G (2005): Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol Aging (Epub ahead of print).
49. Kronenberg G., Reuter K., Steiner B., Brandt M.D., Jessberger S., Yamaguchi M., and Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 467 (2003) 455-463
50. Krucker T., Schuler A., Meyer E.P., Staufenbiel M., and Beckmann N. Magnetic resonance angiography and vascular corrosion casting as tools in biomedical research: application to transgenic mice modeling Alzheimer's disease. Neurol Res 26 (2004) 507-516
51. Lackey B.R., Gray S.L., and Henricks D.M. Actions and interactions of the IGF system in Alzheimer's disease: review and hypotheses. Growth Horm IGF Res 10 (2000) 1-13
52. Lalonde R., Dumont M., Staufenbiel M., Sturchler-Pierrat C., and Strazielle C. Spatial learning, exploration, anxiety, and motor coordination in female APP23 transgenic mice with the Swedish mutation. Brain Res 956 (2002) 36-44
53. Larsson E., Nanobashvili A., Kokaia Z., and Lindvall O. Evidence for neuroprotective effects of endogenous brain-derived neurotrophic factor after global forebrain ischemia in rats. J Cereb Blood Flow Metab 19 (1999) 1220-1228
54. 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 (2005) 701-713
55. Letenneur L., Gilleron V., Commenges D., Helmer C., Orgogozo J.M., and Dartigues J.F. Are sex and educational level independent predictors of dementia and Alzheimer's disease? Incidence data from the PAQUID project. J Neurol Neurosurg Psychiatry 66 (1999) 177-183
56. Lichtenwalner R.J., Forbes M.E., Bennett S.A., Lynch C.D., Sonntag W.E., and Riddle D.R. Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107 (2001) 603-613
57. Lytle M.E., Vander Bilt J., Pandav R.S., Dodge H.H., and Ganguli M. Exercise level and cognitive decline: the MoVIES project. Alzheimer Dis Assoc Disord 18 (2004) 57-64
58. Moceri V.M., Kukull W.A., Emanuel I., van Belle G., and Larson E.B. Early-life risk factors and the development of Alzheimer's disease. Neurology 54 (2000) 415-420
59. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11 (1984) 47-60
60. Mortimer J.A. Brain reserve and the clinical expression of Alzheimer's disease. Geriatrics 52 Suppl 2 (1997) S50-S53
61. Neeper S.A., Gomez-Pinilla F., Choi J., and Cotman C. Exercise and brain neurotrophins. Nature 373 (1995) 109
62. Niikura T., Hashimoto Y., Okamoto T., Abe Y., Yasukawa T., Kawasumi M., et al. Insulin-like growth factor I (IGF-I) protects cells from apoptosis by Alzheimer's V642I mutant amyloid precursor protein through IGF-I receptor in an IGF-binding protein-sensitive manner. J Neurosci 21 (2001) 1902-1910
63. Pham T.M., Ickes B., Albeck D., Soderstrom S., Granholm A.C., and Mohammed A.H. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94 (1999) 279-286
64. Pham T.M., Soderstrom S., Winblad B., and Mohammed A.H. Effects of environmental enrichment on cognitive function and hippocampal NGF in the nonhandled rats. Behav Brain Res 103 (1999) 63-70
65. Price D.L., Tanzi R.E., Borchelt D.R., and Sisodia S.S. Alzheimer's disease: genetic studies and transgenic models. Annu Rev Genet 32 (1998) 461-493
66. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19 (2004) 234-246
67. Roses A.D. Alzheimer diseases: a model of gene mutations and susceptibility polymorphisms for complex psychiatric diseases. Am J Med Genet 81 (1998) 49-57
68. Rozen S., and Skaletsky H.J. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S., and Misener S. (Eds). Bioinformatics Methods and Protocols: Methods in Molecular Biology (2000), Humana Press, Totowa, NJ 365-386. http://fokker.wi.mit.edu/primer3 source code available at http://fokker.wi.mit.edu/primer3
69. Rozmahel R., Huang J., Chen F., Liang Y., Nguyen V., Ikeda M., et al. Normal brain development in PS1 hypomorphic mice with markedly reduced gamma-secretase cleavage of betaAPP. Neurobiol Aging 23 (2002) 187-194
70. Sapolsky R.M. The physiology of dominance in stable versus unstable social hierarchies. In: Mason W., and Mendoza S. (Eds). Primate social conflict (1993), SUNY Press, New York 171
71. Schanzer A., Wachs F.P., Wilhelm D., Acker T., Cooper-Kuhn C., Beck H., et al. Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol 14 (2004) 237-248
72. Selkoe D.J. The genetics and molecular pathology of Alzheimer's disease: roles of amyloid and the presenilins. Neurol Clin 18 (2000) 903-922
73. Smith M.A., Makino S., Kvetnansky R., and Post R.M. Effects of stress on neurotrophic factor expression in the rat brain. Ann N Y Acad Sci 771 (1995) 234-239
74. 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 (1996) 528-532
75. Solerte S.B., Ferrari E., Cuzzoni G., Locatelli E., Giustina A., Zamboni M., et al. Decreased release of the angiogenic peptide vascular endothelial growth factor in Alzheimer's disease: recovering effect with insulin and DHEA sulfate. Dement Geriatr Cogn Disord 19 (2005) 1-10
76. Staff R.T., Murray A.D., Deary I.J., and Whalley L.J. What provides cerebral reserve?. Brain 127 (2004) 1191-1199
77. Steiner B., Kronenberg G., Jessberger S., Brandt M.D., Reuter K., and Kempermann G. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46 (2004) 41-52
78. Sturchler-Pierrat C., Abramowski D., Duke M., Wiederhold K.H., Mistl C., Rothacher S., et al. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci U S A 94 (1997) 13287-13292
79. Teather L.A., Magnusson J.E., Chow C.M., and Wurtman R.J. Environmental conditions influence hippocampus-dependent behaviours and brain levels of amyloid precursor protein in rats. Eur J Neurosci 16 (2002) 2405-2415
80. Torasdotter M., Metsis M., Henriksson B.G., Winblad B., and Mohammed A.H. Environmental enrichment results in higher levels of nerve growth factor mRNA in the rat visual cortex and hippocampus. Behav Brain Res 93 (1998) 83-90
81. Trejo J.L., Carro E., and Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 21 (2001) 1628-1634
82. Van Dam D., D'Hooge R., Staufenbiel M., Van Ginneken C., Van Meir F., and De Deyn P.P. Age-dependent cognitive decline in the APP23 model precedes amyloid deposition. Eur J Neurosci 17 (2003) 388-396
83. van Praag H., Kempermann G., and Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2 (1999) 266-270
84. van Praag H., Shubert T., Zhao C., and Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25 (2005) 8680-8685
85. Wang J., Tanila H., Puolivali J., Kadish I., and van Groen T. Gender differences in the amount and deposition of amyloidbeta in APPswe and PS1 double transgenic mice. Neurobiol Dis 14 (2004) 318-327
86. Wang R., Dineley K.T., Sweatt J.D., and Zheng H. Presenilin 1 familial Alzheimer's disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience 126 (2004) 305-312
87. Wen P.H., Hof P.R., Chen X., Gluck K., Austin G., Younkin S.G., et al. The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp Neurol 188 (2004) 224-237
88. Will B.E., Rosenzweig M.R., Bennett E.L., Hebert M., and Morimoto H. Relatively brief environmental enrichment aids recovery of learning capacity and alters brain measures after postweaning brain lesions in rats. J Comp Physiol Psychol 91 (1977) 33-50
89. Wilson R.S., Mendes De Leon C.F., Barnes L.L., Schneider J.A., Bienias J.L., Evans D.A., and Bennett D.A. Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA 287 (2002) 742-748
90. Yang S.P., Bae D.G., Kang H.J., Gwag B.J., Gho Y.S., and Chae C.B. Co-accumulation of vascular endothelial growth factor with beta-amyloid in the brain of patients with Alzheimer's disease. Neurobiol Aging 25 (2004) 283-290
91. 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 (1999) 448-453