Environmental enrichment compensates for the effects of stress on disease progression in Tg2576 mice, an Alzheimer's disease model

Journal of Neurochemistry

Volumn 119, Issue 6, 2011, Pages 1282-1293

  Jeong, Yun Ha ^a,c   Kim, Joon Min ^a   Yoo, Jongman ^a   Lee, Sang Hyung ^b   Kim, Hye Sun ^a   Suh, Yoo Hun ^a  

^a Seoul National University   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; cognitive impairments; environmental enrichment; neurodegenerative disease; stress

Indexed keywords

TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE COURSE; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL FACTOR; FEMALE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STRESS; THERAPY EFFECT;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; CELL MOVEMENT; CORTICOSTERONE; CYCLIN-DEPENDENT KINASE 5; DENTATE GYRUS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENVIRONMENT; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MAZE LEARNING; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEUROPEPTIDES; PEPTIDE FRAGMENTS; PHOSPHOTRANSFERASES; PROLIFERATING CELL NUCLEAR ANTIGEN; STRESS, PSYCHOLOGICAL; TAU PROTEINS;

MUS; MUS MUSCULUS;

EID: 82955193701     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07514.x     Document Type: Article

References (56)

1. Abrous D. N., Koehl M., and, Le Moal M., (2005) Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85, 523-569. (Pubitemid 40404636)
2. Adlard P. A., Perreau V. M., Pop V., and, Cotman C. W., (2005) Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J. Neurosci. 25, 4217-4221. (Pubitemid 40628765)
3. Ambrée O., Leimer U., Herring A., Görtz N., Sachser N., Heneka M. T., Paulus W., and, Keyvani K., (2006) Reduction of amyloid angiopathy and Abeta plaque burden after enriched housing in TgCRND8 mice: involvement of multiple pathways. Am. J. Pathol. 169, 544-552. (Pubitemid 44156313)
4. Arendash G.W., Garcia M. F., Costa D. A., Cracchiolo J. R., Wefes I. M., and, Potter H., (2004) Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. Neuroreport 15, 1751-1754. (Pubitemid 39062588)
5. Azmitia E. C., (2001) Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res. Bull. 56, 413-424. (Pubitemid 34031777)
6. Belz E. E., Kennell J. S., Czambel R. K., Rubin R. T., and, Rhodes M. E., (2003) Environmental enrichment lowers stress-responsive hormones in singly housed male and female rats. Pharmacol. Biochem. Behav. 76, 481-486. (Pubitemid 37487904)
7. Brown J., Cooper-Kuhn C. M., Kempermann G., Van Praag H., Winkler J., Gage F. H., and, Kuhn H. G., (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 17, 2042-2046. (Pubitemid 36713965)
8. Cameron H. A., McEwen B. S., and, Gould E., (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci. 15, 4687-4692.
9. Catania C., Sotiropoulos I., Silva R., Onofri C., Breen K. C., Sousa N., and, Almeida O. F., (2009) The amyloidogenic potential and behavioral correlates of stress. Mol. Psychiatry 14, 95-105.
10. Costa D. A., Cracchiolo J. R., Bachstetter A. D., Hughes T. F., Bales K. R., Paul S. M., Mervis R. F., Arendash G. W., and, Potter H., (2007) Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol. Aging 28, 831-844. (Pubitemid 46613825)
11. Cracchiolo J. R., Mori T., Nazian S. J., Tan J., Potter H., and, Arendash G. W., (2007) Enhanced cognitive activity-over and above social or physical activity-is required to protect Alzheimer's mice against cognitive impairment, reduce Abeta deposition, and increase synaptic immunoreactivity. Neurobiol. Learn. Mem. 88, 277-294. (Pubitemid 47321221)
12. Doetsch F., and, Hen R., (2005) Young and excitable: the function of new neurons in the adult mammalian brain. Curr. Opin. Neurobiol. 15, 121-128. (Pubitemid 40249971)
13. Doetsch F., Caillé I., Lim D. A., García-Verdugo J. M., and, Alvarez-Buylla A., (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716. (Pubitemid 29278045)
14. Dong H., Goico B., Martin M., Csernansky C. A., Bertchume A., and, Csernansky J. G., (2004) Modulation of hippocampal cell proliferation, memory, and amyloid plaque deposition in APPsw (Tg2576) mutant mice by isolation stress. Neuroscience 127, 601-609. (Pubitemid 38993164)
15. Farah V. M., Joaquim L. F., Bernatova I., and, Morris M., (2004) Acute and chronic stress influence blood pressure variability in mice. Physiol. Behav. 83, 135-142. (Pubitemid 39387702)
16. Feng Q., Cheng B., Yang R., Sun F. Y., and, Zhu C. Q., (2005) Dynamic changes of phosphorylated tau in mouse hippocampus after cold water stress. Neurosci. Lett. 388, 13-16. (Pubitemid 41569362)
17. Finkel S. I., (2003) Behavioral and psychologic symptoms of dementia. Clin. Geriatr. Med. 19, 799-824. (Pubitemid 37474160)
18. Flaherty D. B., Soria J. P., Tomasiewicz H. G., and, Wood J. G., (2000) Phosphorylation of human tau protein by microtubule-associated kinases: GSK3beta and cdk5 are key participants. J. Neurosci. Res. 62, 463-472.
19. Francis D. D., Diorio J., Plotsky P. M., and, Meaney M. J., (2002) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 22, 7840-7843. (Pubitemid 35379088)
20. Friedland R. P., Fritsch T., Smyth K. A., Koss E., Lerner A. J., Chen C. H., Petot G. J., and, Debanne S. M., (2001) Patients with Alzheimer's disease have reduced activities in midlife compared with healthy control-group members. Proc. Natl. Acad. Sci. USA 98, 3440-3445. (Pubitemid 32220864)
21. Gould E., McEwen B. S., Tanapat P., Galea L. A., and, Fuchs E., (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17, 2492-2498. (Pubitemid 27137415)
22. Gould E., Beylin A., Tanapat P., Reeves A., and, Shors T. J., (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260-265. (Pubitemid 30491297)
23. Herring A., Ambrée O., Tomm M., Habermann H., Sachser N., Paulus W., and, Keyvani K., (2009) Environmental enrichment enhances cellular plasticity in transgenic mice with Alzheimer-like pathology. Exp. Neurol. 216, 184-192.
24. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F. S., and, Cole G., (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102. (Pubitemid 26332733)
25. Jankowsky J. L., Xu G., Fromholt D., Gonzales V., and, Borchelt D. R., (2003) Environmental enrichment exacerbates amyloid plaque formation in a transgenic mouse model of Alzheimer disease. J. Neuropathol. Exp. Neurol. 62, 1220-1227. (Pubitemid 37494191)
26. Jankowsky J. L., Melnikova T., Fadale D. J., Xu G. M., Slunt H. H., Gonzales V., Younkin L. H., Younkin S. G., Borchelt D. R., and, Savonenko A. V., (2005) Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J. Neurosci. 25, 5217-5224. (Pubitemid 40726973)
27. Jeong Y. H., Park C. H., Yoo J., Shin K. Y., Ahn S. M., Kim H. S., Lee S. H., Emson P. C., and, Suh Y. H., (2006) Chronic stress accelerates learning and memory impairments and increases amyloid deposition in APPV717I-CT100 transgenic mice, an Alzheimer's disease model. FASEB J. 20, 729-731. (Pubitemid 46671196)
28. Kawarabayashi T., Younkin L. H., Saido T. C., Shoji M., Ashe K. H., and, Younkin S. G., (2001) Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J. Neurosci. 21, 372-381. (Pubitemid 32107428)
29. Kempermann G., Wiskott L., and, Gage F. H., (2004) Functional significance of adult neurogenesis. Curr. Opin. Neurobiol. 14, 186-191. (Pubitemid 38479935)
30. Korneyev A. Y., (1998) Stress-induced tau phosphorylation in mouse strains with different brain Erk 1/2 immunoreactivity. Neurochem. Res. 23, 1539-1543. (Pubitemid 28516294)
31. Korneyev A., Binder L., and, Bernardis J., (1995) Rapid reversible phosphorylation of rat brain tau proteins in response to cold water stress. Neurosci. Lett. 191, 19-22.
32. Lazarov O., Robinson J., Tang Y. P., Hairston I. S., Korade-Mirnics Z., Lee V. M., Hersh L. B., Sapolsky R. M., Mirnics K., and, Sisodia S. S., (2005) Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120, 701-703.
33. Lazic S. E., Grote H. E., Blakemore C., Hannan A. J., van Dellen A., Phillips W., and, Barker R. A., (2006) Neurogenesis in the R6/1 transgenic mouse model of Huntington's disease: effects of environmental enrichment. Eur. J. Neurosci. 23, 1829-1838.
34. Lesné S., Koh M. T., Kotilinek L., Kayed R., Glabe C. G., Yang A., Gallagher M., and, Ashe K. H., (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352-357.
35. Loewenstein D. A., Acevedo A., Czaja S. J., and, Duara R., (2004) Cognitive rehabilitation of mildly impaired Alzheimer disease patients on cholinesterase inhibitors. Am. J. Geriatr. Psychiatry 12, 395-402. (Pubitemid 38878859)
36. Lois C., and, Alvarez-Buylla A., (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148. (Pubitemid 24210676)
37. Mattson M. P., (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639. (Pubitemid 39061671)
38. McEwen B. S., (2001) Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann. NY Acad. Sci. 933, 265-277. (Pubitemid 32390122)
39. Mirescu C., Peters J.D., and, Gould E., (2004) Early life experience alters response of adult neurogenesis to stress. Nat. Neurosci. 7, 841-846. (Pubitemid 38989507)
40. Mirmiran M., Van Gool W. A., Van Haaren F., and, Polak C. E., (1986) Environmental influences on brain and behavior in aging and Alzheimer's disease. Prog. Brain Res. 70, 443-459.
41. Mitra R., and, Sapolsky R. M., (2009) Effects of enrichment predominate over those of chronic stress on fear-related behavior in male rats. Stress 12, 305-312.
42. Mohammed A. H., Zhu S. W., Darmopil S., Hjerling-Leffler J., Ernfors P., Winblad B., Diamond M. C., Eriksson P. S., and, Bogdanovic N., (2002) Environmental enrichment and the brain. Prog. Brain Res. 138, 109-133. (Pubitemid 35460911)
43. Morris R., (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60. (Pubitemid 14088970)
44. Papasozomenos S. C., (1996) Heat shock induces rapid dephosphorylation of tau in both female and male rats followed by hyperphosphorylation only in female rats: implications for Alzheimer's disease. J. Neurochem. 66, 1140-1149. (Pubitemid 26065912)
45. van Praag H., Kempermann G., and, Gage F. H., (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270. (Pubitemid 30491298)
46. van Praag H., Kempermann G., and, Gage F. H., (2000) Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1, 191-198.
47. Ritchie K., and, Lovestone S., (2002) The dementias. Lancet 360, 1759-1766. (Pubitemid 35447916)
48. Rochefort C., Gheusi G., Vincent J. D., and, Lledo P. M., (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679-2689. (Pubitemid 37465817)
49. Shapiro L. A., Ng K. L., Zhou Q. Y., and, Ribak C. E., (2007) Olfactory enrichment enhances the survival of newly born cortical neurons in adult mice. Neuroreport 18, 981-985. (Pubitemid 46905169)
50. Wilson R. S., Mendes De Leon C. F., Barnes L. L., Schneider J. A., Bienias J. L., Evans D. A., and, Bennett D. A., (2002) Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA 287, 742-748. (Pubitemid 34250460)
51. Wilson R. S., Evans D. A., Bienias J. L., Mendes de Leon C. F., Schneider J. A., and, Bennett D. A., (2003) Proneness to psychological distress is associated with risk of Alzheimer's disease. Neurology 61, 1479-1485. (Pubitemid 37505565)
52. Wilson R. S., Barnes L. L., Bennett D. A., Li Y., Bienias J. L., Mendes de Leon C. F., and, Evans D. A., (2005) Proneness to psychological distress and risk of Alzheimer disease in a biracial community. Neurology 64, 380-382.
53. Wilson R. S., Arnold S. E., Schneider J. A., Kelly J. F., Tang Y., and, Bennett D. A., (2006) Chronic psychological distress and risk of Alzheimer's disease in old age. Neuroepidemiology 27, 143-153. (Pubitemid 44651434)
54. Wilson R. S., Krueger K. R., Arnold S. E., Schneider J. A., Kelly J. F., Barnes L. L., Tang Y., and, Bennett D. A., (2007) Loneliness and risk of Alzheimer disease. Arch. Gen. Psychiatry 64, 234-240. (Pubitemid 46220781)
55. Wolf S. A., Kronenberg G., Lehmann K., Blankenship A., Overall R., Staufenbiel M., and, Kempermann G., (2006) Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer's disease. Biol. Psychiatry 60, 1314-1323. (Pubitemid 44838527)
56. Zigova T., Pencea V., Wiegand S. J., and, Luskin M. B., (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell. Neurosci. 11, 234-245. (Pubitemid 28361411)