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Impact of enriched environment on production of tau, amyloid precursor protein and, amyloid-β peptide in high-fat and high-sucrose-fed rats

Published online by Cambridge University Press:  07 December 2016

Yavuz Selvi*
Affiliation:
Department of Psychiatry, Neuroscience Research Center (SAM) Konya, Selcuk University Medicine Faculty, Konya, Turkey
Hasan Serdar Gergerlioglu
Affiliation:
Department of Psychiatry, Neuroscience Research Center (SAM) Konya, Selcuk University Medicine Faculty, Konya, Turkey
Nursel Akbaba
Affiliation:
Department of Psychiatry, Selcuk University Medicine Faculty, Konya, Turkey
Mehmet Oz
Affiliation:
Department of Physiology, Bozok University Medicine Faculty, Yozgat, Turkey
Ali Kandeger
Affiliation:
Department of Psychiatry, Selcuk University Medicine Faculty, Konya, Turkey
Enver Ahmet Demir
Affiliation:
Department of Physiology, Mustafa Kemal University Medicine Faculty, Hatay, Turkey
Fatma Humeyra Yerlikaya
Affiliation:
Department of Biochemistry, Necmettin Erbakan University Medicine Faculty, Konya, Turkey
Kismet Esra Nurullahoglu-Atalik
Affiliation:
Department of Pharmacology, Necmettin Erbakan University Medicine Faculty, Konya, Turkey
*
Yavuz Selvi, Associate Professor of Psychiatry, Department of Psychiatry, Neuroscience Research Center (SAM) Konya, Selcuk University Medicine Faculty, Konya, Turkey. Tel: +900 332 224 4563; Fax: +900 332 241 6065; E-mail: dryavuzselvi@yahoo.com

Abstract

Objective

The Western-type diet is associated with an elevated risk of Alzheimer’s disease and other milder forms of cognitive impairment. The aim of the present study was to investigate the effects of the environmental enrichment on amyloid and tau pathology in high-fat and high-sucrose-fed rats.

Methods

In total, 40 adult male rats were categorised into two main groups according to their housing conditions: enriched environment (EE, n=16) and standard housing condition (n=24). The groups were further divided into five subgroups that received standard diet, high-fat diet, and high-sucrose diet. We performed the analysis of amyloid β-peptide (Aβ) (1–40), Aβ(1–42), amyloid precursor protein (APP), and tau levels in the hippocampus of rats that were maintained under standard housing conditions or exposed to an EE.

Results

The EE decreased the Aβ(1–40), Aβ(1–42), APP, and tau levels in high-fat and high-sucrose-fed rats.

Conclusion

This observation shows that EE may rescue diet-induced amyloid and tau pathology.

Type
Original Articles
Copyright
© Scandinavian College of Neuropsychopharmacology 2016 

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References

1. Whitmer, RA, Gunderson, EP, Barrett-Connor, E, Quesenberry, CP Jr, Yaffe, K. Obesity in middle age and future risk of dementia: a 27 year longitudinal population based study. BMJ 2005;330:1360.CrossRefGoogle ScholarPubMed
2. Berrino, F. [Western diet and Alzheimer’s disease]. Epidemiol Prev 2001;26:107115.Google Scholar
3. Morris, M, Evans, D, Bienias, J, Tangney, C, Wilson, R. Dietary fat intake and 6-year cognitive change in an older biracial community population. Neurology 2004;62:15731579.CrossRefGoogle Scholar
4. Kanoski, SE, Davidson, TL. Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiol Behav 2011;103:5968.CrossRefGoogle ScholarPubMed
5. Cordner, ZA, Tamashiro, KL. Effects of high-fat diet exposure on learning & memory. Physiol Behav 2015;152:363371.CrossRefGoogle ScholarPubMed
6. Luchsinger, JA, Tang, M-X, Shea, S, Mayeux, R. Caloric intake and the risk of Alzheimer disease. Arch Neurol 2002;59:12581263.CrossRefGoogle ScholarPubMed
7. Profenno, LA, Porsteinsson, AP, Faraone, SV. Meta-analysis of Alzheimer’s disease risk with obesity, diabetes, and related disorders. Biol Psychiatry 2010;67:505512.CrossRefGoogle ScholarPubMed
8. Martin, SA, Jameson, CH, Allan, SM, Lawrence, CB. Maternal high-fat diet worsens memory deficits in the triple-transgenic (3xTgAD) mouse model of Alzheimer’s disease. PLoS One. 2014;9:e99226.CrossRefGoogle ScholarPubMed
9. Panza, F, Solfrizzi, V, Colacicco, A et al. Mediterranean diet and cognitive decline. Public Health Nutr 2004;7:959963.CrossRefGoogle ScholarPubMed
10. Vandal, M, White, PJ, Tremblay, C et al. Insulin reverses the high-fat diet–induced increase in brain Aβ and improves memory in an animal model of Alzheimer disease. Diabetes. 2014;63:42914301.CrossRefGoogle Scholar
11. Takalo, M, Haapasalo, A, Martiskainen, H et al. High-fat diet increases tau expression in the brain of T2DM and AD mice independently of peripheral metabolic status. J Nutr Biochem 2014;25:634641.CrossRefGoogle Scholar
12. Julien, C, Tremblay, C, Phivilay, A et al. High-fat diet aggravates amyloid-beta and tau pathologies in the 3xTg-AD mouse model. Neurobiol Aging 2010;31:15161531.CrossRefGoogle ScholarPubMed
13. Cao, D, Lu, H, Lewis, TL, Li, L. Intake of sucrose-sweetened water induces insulin resistance and exacerbates memory deficits and amyloidosis in a transgenic mouse model of Alzheimer disease. J Biol Chem 2007;282:3627536282.CrossRefGoogle Scholar
14. Van Praag, H, Kempermann, G, Gage, FH. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000;1:191198.CrossRefGoogle ScholarPubMed
15. Faverjon, S, Silveira, D, Fu, D et al. Beneficial effects of enriched environment following status epilepticus in immature rats. Neurology 2002;59:13561364.CrossRefGoogle ScholarPubMed
16. Dahlqvist, P, Rönnbäck, A, Bergström, SA, Söderström, I, Olsson, T. Environmental enrichment reverses learning impairment in the Morris water maze after focal cerebral ischemia in rats. Eur J Neurosci 2004;19:22882298.CrossRefGoogle ScholarPubMed
17. Gobbo, O, O’Mara, S. Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav Brain Res 2004;152:231241.CrossRefGoogle ScholarPubMed
18. Jankowsky, JL, Melnikova, T, Fadale, DJ et al. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer’s disease. J Neurosci 2005;25:52175224.CrossRefGoogle Scholar
19. Gergerlioglu, HS, Oz, M, Demir, EA, Nurullahoglu-Atalik, KE, Yerlikaya, FH. Environmental enrichment reverses cognitive impairments provoked by Western diet in rats: role of corticosteroid receptors. Life Sci 2016;148:279285.CrossRefGoogle ScholarPubMed
20. Wilson, R, Bennett, D, Bienias, J et al. Cognitive activity and incident AD in a population-based sample of older persons. Neurology 2002;59:19101914.CrossRefGoogle Scholar
21. Colcombe, SJ, Kramer, AF, McAuley, E, Erickson, KI, Scalf, P. Neurocognitive aging and cardiovascular fitness. J Mol Neurosci 2004;24:914.CrossRefGoogle ScholarPubMed
22. Friedland, RP, Fritsch, T, Smyth, KA et al. Patients with Alzheimer’s disease have reduced activities in midlife compared with healthy control-group members. Proc Natl Acad Sci 2001;98:34403445.CrossRefGoogle ScholarPubMed
23. Hu, Y-S, Xu, P, Pigino, G, Brady, ST, Larson, J, Lazarov, O. Complex environment experience rescues impaired neurogenesis, enhances synaptic plasticity, and attenuates neuropathology in familial Alzheimer’s disease-linked APPswe/PS1ΔE9 mice. FASEB Journal 2010;24:16671681.CrossRefGoogle ScholarPubMed
24. Beauquis, J, Pavía, P, Pomilio, C et al. Environmental enrichment prevents astroglial pathological changes in the hippocampus of APP transgenic mice, model of Alzheimer’s disease. Exp Neurol 2013;239:2837.CrossRefGoogle ScholarPubMed
25. Gerenu, G, Dobarro, M, Ramirez, MJ, Gil-Bea, FJ. Early cognitive stimulation compensates for memory and pathological changes in Tg2576 mice. Biochim Biophys Acta 2013;1832:837847.CrossRefGoogle ScholarPubMed
26. Maesako, M, Uemura, K, Kubota, M et al. Environmental enrichment ameliorated high-fat diet-induced Aβ deposition and memory deficit in APP transgenic mice. Neurobiol Aging 2012;33:1011. e11e23.CrossRefGoogle ScholarPubMed
27. Costa, DA, Cracchiolo, JR, Bachstetter, AD et al. Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol Aging 2007;28:831844.CrossRefGoogle ScholarPubMed
28. Ghribi, O, Larsen, B, Schrag, M, Herman, MM. High cholesterol content in neurons increases BACE, β-amyloid, and phosphorylated tau levels in rabbit hippocampus. Exp Neurol 2006;200:460467.CrossRefGoogle ScholarPubMed
29. Hooijmans, C, Rutters, F, Dederen, P et al. Changes in cerebral blood volume and amyloid pathology in aged Alzheimer APP/PS1 mice on a docosahexaenoic acid (DHA) diet or cholesterol enriched Typical Western Diet (TWD). Neurobiol Dis 2007;28:1629.CrossRefGoogle ScholarPubMed
30. Herring, A, Lewejohann, L, Panzer, A-L et al. Preventive and therapeutic types of environmental enrichment counteract beta amyloid pathology by different molecular mechanisms. Neurobiol Dis 2011;42:530538.CrossRefGoogle ScholarPubMed
31. Patel, NV, Gordon, MN, Connor, KE et al. Caloric restriction attenuates Aβ-deposition in Alzheimer transgenic models. Neurobiol Aging 2005;26:9951000.CrossRefGoogle ScholarPubMed
32. Ballatore, C, Lee, VM-Y, Trojanowski, JQ. Tau-mediated neurodegeneration in Alzheimer’s disease and related disorders. Nat Rev Neurosci 2007;8:663672.CrossRefGoogle ScholarPubMed
33. Oakley, H, Cole, SL, Logan, S et al. Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: potential factors in amyloid plaque formation. J Neurosci 2006;26:1012910140.CrossRefGoogle ScholarPubMed
34. Haass, C, Selkoe, DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid β-peptide. Nat Rev Mol Cell Biol 2007;8:101112.CrossRefGoogle ScholarPubMed
35. Gouras, GK, Tampellini, D, Takahashi, RH, Capetillo-Zarate, E. Intraneuronal β-amyloid accumulation and synapse pathology in Alzheimer’s disease. Acta Neuropathol 2010;119:523541.CrossRefGoogle ScholarPubMed
36. Kowall, N, McKee, A, Yankner, B, Beal, M. In vivo neurotoxicity of beta-amyloid [β (1–40)] and the β (25–35) fragment. Neurobiol Aging 1992;13:537542.CrossRefGoogle ScholarPubMed
37. Lee, J, Retamal, C, Cuitiño, L et al. Adaptor protein sorting nexin 17 regulates amyloid precursor protein trafficking and processing in the early endosomes. J Biol Chem 2008;283:1150111508.CrossRefGoogle ScholarPubMed
38. Masters, CL, Simms, G, Weinman, NA, Multhaup, G, McDonald, BL, Beyreuther, K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci 1985;82:42454249.CrossRefGoogle ScholarPubMed
39. Duyckaerts, C, Delatour, B, Potier, M-C. Classification and basic pathology of Alzheimer disease. Acta Neuropathol 2009;118:536.CrossRefGoogle ScholarPubMed
40. Bloom, GS. Amyloid-β and tau: the trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol 2014;71:505508.CrossRefGoogle ScholarPubMed
41. Nisbet, RM, Polanco, J-C, Ittner, LM, Götz, J. Tau aggregation and its interplay with amyloid-β. Acta Neuropathol 2015;129:207220.CrossRefGoogle ScholarPubMed
42. Zhang, L, Zhang, J, Sun, H, Zhu, H, Liu, H, Yang, Y. An enriched environment elevates corticosteroid receptor levels in the hippocampus and restores cognitive function in a rat model of chronic cerebral hypoperfusion. Pharmacol Biochem Behav 2013;103:693700.CrossRefGoogle Scholar
43. Lazarov, O, Robinson, J, Tang, Y-P et al. Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell 2005;120:701713.CrossRefGoogle ScholarPubMed
44. Mainardi, M, Di Garbo, A, Caleo, M, Berardi, N, Sale, A, Maffei, L. Environmental enrichment strengthens corticocortical interactions and reduces amyloid-β oligomers in aged mice. Front Aging Neurosci 2014;6:111.CrossRefGoogle ScholarPubMed
45. Orr, ME, Salinas, A, Buffenstein, R, Oddo, S. Mammalian target of rapamycin hyperactivity mediates the detrimental effects of a high sucrose diet on Alzheimer’s disease pathology. Neurobiol Aging 2014;35:12331242.CrossRefGoogle ScholarPubMed
46. Ho, L, Qin, W, Pompl, PN et al. Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer’s disease. FASEB J 2004;18:902904.CrossRefGoogle Scholar
47. Howland, DS, Trusko, SP, Savage, MJ et al. Modulation of secreted β-amyloid precursor protein and amyloid β-peptide in brain by cholesterol. J Biol Chem 1998;273:1657616582.CrossRefGoogle ScholarPubMed
48. O’Brien, RJ, Wong, PC. Amyloid precursor protein processing and Alzheimer’s disease. Ann Rev Neurosci 2011;34:185.CrossRefGoogle ScholarPubMed
49. Ehehalt, R, Keller, P, Haass, C, Thiele, C, Simons, K. Amyloidogenic processing of the Alzheimer β-amyloid precursor protein depends on lipid rafts. J Cell Biol 2003;160:113123.CrossRefGoogle ScholarPubMed
50. Thirumangalakudi, L, Prakasam, A, Zhang, R et al. High cholesterol‐induced neuroinflammation and amyloid precursor protein processing correlate with loss of working memory in mice. J Neurochem 2008;106:475485.CrossRefGoogle ScholarPubMed
51. Phivilay, A, Julien, C, Tremblay, C et al. High dietary consumption of trans fatty acids decreases brain docosahexaenoic acid but does not alter amyloid-β and tau pathologies in the 3xTg-AD model of Alzheimer’s disease. Neuroscience 2009;159:296307.CrossRefGoogle Scholar
52. Knight, EM, Martins, IV, Gümüsgöz, S, Allan, SM, Lawrence, CB. High-fat diet-induced memory impairment in triple-transgenic Alzheimer’s disease (3xTgAD) mice is independent of changes in amyloid and tau pathology. Neurobiol Aging 2014;35:18211832.CrossRefGoogle ScholarPubMed
53. Julien, C, Tremblay, C, Bendjelloul, F et al. Decreased drebrin mRNA expression in Alzheimer disease: correlation with tau pathology. J Neurosci Res 2008;86:22922302.CrossRefGoogle ScholarPubMed
54. Ma, Q-L, Yang, F, Rosario, ER et al. β-amyloid oligomers induce phosphorylation of tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling: suppression by omega-3 fatty acids and curcumin. J Neurosci 2009;29:90789089.CrossRefGoogle ScholarPubMed
55. Biessels, GJ, Staekenborg, S, Brunner, E, Brayne, C, Scheltens, P. Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol 2006;5:6474.CrossRefGoogle ScholarPubMed
56. Bitel, C, Kasinathan, C, Kaswala, R, Klein, W, Frederikse, P. Amyloid-β and tau pathology of Alzheimer’s disease induced by diabetes in an animal model. J Alzheimers Dis 2012;32:291305.CrossRefGoogle Scholar
57. Li, Z-G, Zhang, W, Sima, AA. Alzheimer-like changes in rat models of spontaneous diabetes. Diabetes 2007;56:18171824.CrossRefGoogle ScholarPubMed
58. Craft, S. Insulin resistance and Alzheimer’s disease pathogenesis: potential mechanisms and implications for treatment. Curr Alzheimer Res 2007;4:147152.CrossRefGoogle ScholarPubMed
59. Gasparini, L, Gouras, GK, Wang, R et al. Stimulation of β-amyloid precursor protein trafficking by insulin reduces intraneuronal β-amyloid and requires mitogen-activated protein kinase signaling. J Neurosci 2001;21:25612570.CrossRefGoogle ScholarPubMed
60. Greenwood, CE, Winocur, G. High-fat diets, insulin resistance and declining cognitive function. Neurobiol Aging 2005;26:4245.CrossRefGoogle ScholarPubMed
61. Pasinetti, GM, Eberstein, JA. Metabolic syndrome and the role of dietary lifestyles in Alzheimer’s disease. J Neurochem 2008;106:15031514.CrossRefGoogle ScholarPubMed
62. Eskelinen, MH, Ngandu, T, Helkala, EL et al. Fat intake at midlife and cognitive impairment later in life: a population‐based CAIDE study. Int J Geriatr Psychiatry 2008;23:741747.CrossRefGoogle ScholarPubMed
63. Maesako, M, Uemura, K, Iwata, A et al. Continuation of exercise is necessary to inhibit high fat diet-induced β-amyloid deposition and memory deficit in amyloid precursor protein transgenic mice. PLoS One. 2013;8:e72796.CrossRefGoogle ScholarPubMed
64. Fischer, A. Environmental enrichment as a method to improve cognitive function. What can we learn from animal models? Neuroimage 2016;131:4247.CrossRefGoogle ScholarPubMed
65. Krech, D, Rosenzweig, MR, Bennett, EL. Relations between brain chemistry and problem-solving among rats raised in enriched and impoverished environments. J Comp Physiol Psychol 1962;55:801.CrossRefGoogle ScholarPubMed
66. Yuede, CM, Zimmerman, SD, Dong, H et al. Effects of voluntary and forced exercise on plaque deposition, hippocampal volume, and behavior in the Tg2576 mouse model of Alzheimer’s disease. Neurobiol Dis 2009;35:426432.CrossRefGoogle ScholarPubMed
67. Cao, L, Choi, EY, Liu, X et al. White to brown fat phenotypic switch induced by genetic and environmental activation of a hypothalamic-adipocyte axis. Cell Metab 2011;14:324338.CrossRefGoogle Scholar
68. Windisch, M. Why did animal models fail to show the right way to Alzheimer Therapy? Neurobiol Aging 2014;35:S25S26.CrossRefGoogle Scholar
69. Elder, GA, Gama Sosa, MA, De Gasperi, R. Transgenic mouse models of Alzheimer’s disease. Mt Sinai J Med 2010;77:6981.CrossRefGoogle ScholarPubMed