Detrimental effects of a high fat/high cholesterol diet on memory and hippocampal markers in aged rats

Behavioural Brain Research

Volumn 312, Issue , 2016, Pages 294-304

  Ledreux, Aurélie ^a   Wang, Xiuzhe ^b,c   Schultzberg, Marianne ^b   Granholm, Ann Charlotte ^a   Freeman, Linnea R ^a,d  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d FURMAN UNIVERSITY   (United States)

Author keywords

Aging; Cognition; Hippocampus; Spatial memory; Tau phosphorylation

Indexed keywords

TAU PROTEIN; CALBINDIN 1; CHOLESTEROL; MAPT PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, RAT;

AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CHOLESTEROL DIET; COGNITION; COGNITIVE DEFECT; COGNITIVE FUNCTION TEST; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; LIPID DIET; MALE; MEMORY; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIAL ARM MAZE TEST; RAT; SPATIAL MEMORY; TASK PERFORMANCE; TISSUE DISTRIBUTION; TISSUE STRUCTURE; WESTERN BLOTTING; WORKING MEMORY; ANIMAL; ENCEPHALITIS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PYRAMIDAL NERVE CELL; SHORT TERM MEMORY;

AGING; ANIMALS; CALBINDIN 1; CHOLESTEROL; DIET, HIGH-FAT; ENCEPHALITIS; HIPPOCAMPUS; MALE; MEMORY, SHORT-TERM; MICROGLIA; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHORYLATION; PYRAMIDAL CELLS; RATS; SPATIAL MEMORY; TAU PROTEINS;

EID: 84977083346     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.06.012     Document Type: Article

References (80)

1. [1] Flegal, K.M., Carroll, M.D., Kit, B.K., Ogden, C.L., Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA 307 (2012), 491–497.
2. [2] Must, A., Spadano, J., Coakley, E.H., Field, A.E., Colditz, G., Dietz, W.H., The disease burden associated with overweight and obesity. JAMA 282 (1999), 1523–1529.
3. [3] Guh, D.P., Zhang, W., Bansback, N., Amasi, Z., Birmingham, C.L., Anis, A.H., The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health, 9, 2009, 88.
4. [4] Kivipelto, M., Ngandu, T., Fratiglioni, L., Obesity and vascular risk factors at midlife and the risk of dementia and Alzheimer disease. Arch. Neurol. 62 (2005), 1556–1560.
5. [5] Umegaki, H., Neurodegeneration in diabetes mellitus. Adv. Exp. Med. Biol. 724 (2012), 258–265.
6. [6] Whitmer, R.A., Gustafson, D.R., Barrett-Connor, E., Haan, M.N., Gunderson, E.P., Yaffe, K., Central obesity and increased risk of dementia more than three decades later. Neurology 71 (2008), 1057–1064.
7. [7] Craft, S., The role of metabolic disorders in Alzheimer disease and vascular dementia. Arch. Neurol. 66 (2009), 300–305.
8. [8] Craft, S., Watson, G.S., Insulin and neurodegenerative disease: shared and specified mechanisms. Lancet Neurol. 3 (2004), 169–178.
9. [9] Parrott, M.D., Greenwood, C.E., Dietary influences on cognitive function with aging: from high-fat diets to healthful eating. Ann. N. Y. Acad. Sci. 1114 (2007), 389–397.
10. [10] Morris, M.C., Evans, D.A., Bienas, J.L., Tangney, C.C., Wilson, R.S., Dietary fat intake and 6-year cognitive change in an older biracial community population. Neurology 62 (2004), 1573–1579.
11. [11] Baran, S., Campbell, A., Kleen, J., Foltz, C., Wright, R., Diamond, D., Conrad, C.D., Combination of high fat diet and chronic stress retracts hippocampal dendrites. Neuroreport 16 (2005), 39–43.
12. [12] Granholm, A.C., Bimonte-Nelson, H.A., Moore, A., Nelson, M., Freeman, L.R., Sambamurti, K., Effects of a saturated fat and high cholesterol diet on memory and hippocampal morphology in the middle-aged rat. J. Alzheimers Dis. 14 (2008), 133–145.
13. [13] Winocur, G., Greenwood, C.E., The effects of high fat diets and environmental influences on cognitive performance in rats. Behav. Brain Res. 101 (1999), 153–161.
14. [14] Winocur, G., Greenwood, C.E., Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol. Aging 26:Suppl. 1 (2005), 46–49.
15. [15] Mielke, J.G., Nicolitch, K., Avellaneda, V., Earlam, K., Ahuja, T., Mealing, G., Messier, C., Longitudinal study of the effects of a high-fat diet on glucose regulation, hippocampal function, and cerebral insulin sensitivity in C57BL/6 mice. Behav. Brain Res. 175 (2006), 374–382.
16. [16] Freeman, L.R., Haley-Zitlin, V., Rosenberger, D.S., Granholm, A.C., Damaging effects of a high-fat diet to the brain and cognition: a review of proposed mechanisms. Nutr. Neurosci. 17 (2014), 241–251.
17. [17] Morrison, C.D., Pistell, P.J., Ingram, D.K., Johnson, W.D., Liu, Y., Fernandez-Kim, S.O., White, C.L., Purpera, M.N., Uranga, R.M., Bruce-Keller, A.J., Keller, J.N., High fat diet increases hippocampal oxidative stress and cognitive impairment in aged mice: implications for decreased Nrf2 signaling. J. Neurochem. 114 (2010), 1581–1589.
18. [18] Pistell, P.J., Morrison, C.D., Gupta, S., Knight, A.G., Keller, J.N., Ingram, D.K., Bruce-Keller, A.J., Cognitive impairment following high fat diet consumption is associated with brain inflammation. J. Neuroimmunol. 219 (2010), 25–32.
19. [19] Zhang, X., Dong, F., Ren, J., Driscoll, M., Culver, B., High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp. Neurol. 191 (2005), 318–325.
20. [20] Freeman, L.R., Haley-Zitlin, V., Stevens, C., Granholm, A.C., Diet-induced effects on neuronal and glial elements in the middle-aged rat hippocampus. Nutr. Neurosci. 14 (2011), 32–44.
21. [21] Freeman, L.R., Granholm, A.C., Vascular changes in rat hippocampus following a high saturated fat and cholesterol diet. J. Cereb. Blood Flow Metab. 32 (2012), 643–653.
22. [22] Morris, M.C., Tangney, C.C., Dietary fat composition and dementia risk. Neurobiol. Aging 35:Suppl. 2 (2014), S59–S64.
23. [23] Kalmijn, S., Launer, L., Ott, A., Witteman, J., Hofman, A., Breteler, M., Dietary fat intake and the risk of incident dementia in the Rotterdam study. Ann. Neurol. 42 (1997), 776–782.
24. [24] Morris, M.C., Evans, D.A., Bienias, J.L., Tangney, C.C., Bennett, D.A., Aggarwal, N., Schneider, J., Wilson, R.S., Dietary fats and the risk of incident Alzheimer disease. Arch. Neurol. 60 (2003), 194–200.
25. [25] Eskelinen, M.H., Ngandu, T., Helkala, E.L., Tuomilehto, J., Nissinen, A., Soininen, H., Kivipelto, M., Fat intake at midlife and cognitive impairment later in life: a population-based CAIDE study. Int. J. Geriatr. Psychiatry 23 (2008), 741–747.
26. [26] Okereke, O.I., Rosner, B.A., Kim, D.H., Kang, J.H., Cook, N.R., Manson, J.E., Buring, J.E., Willett, W.C., Grodstein, F., Dietary fat types and 4-year cognitive change in community-dwelling older women. Ann. Neurol. 72 (2012), 124–134.
27. [27] Bayer-Carter, J.L., Green, P.S., Montine, T.J., VanFossen, B., Baker, L.D., Watson, G.S., Bonner, L.M., Callaghan, M., Leverenz, J.B., Walter, B.K., Tsai, E., Plymate, S.R., Postupna, N., Wilkinson, C.W., Zhang, J., Lampe, J., Kahn, S.E., Craft, S., Diet intervention and cerebrospinal fluid biomarkers in amnestic mild cognitive impairment. Arch. Neurol. 68 (2011), 743–762.
28. [28] Levin-Allerhand, J., Lominska, C., Smith, J., Increased amyloid-levels in APPSWE transgenic mice treated chronically with a physiological high-fat high-cholesterol diet. J. Nutr. Health Aging 6 (2002), 315–319.
29. [29] Hooijmans, C.R., Van der Zee, C.E., Dederen, P.J., Brouwer, K.M., Reijmer, Y.D., van Groen, T., Broersen, L.M., Lütjohann, D., Heerschap, A., Kiliaan, A.J., DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPswe/PS1dE9 mice. Neurobiol. Dis. 33 (2009), 482–498.
30. [30] Zhang, L., Dasuri, K., Fernandez-Kim, S.O., Bruce-Keller, A.J., Freeman, L.R., Pepping, J.K., Beckett, T.L., Murphy, M.P., Keller, J.N., Prolonged diet induced obesity has minimal effects towards brain pathology in mouse model of cerebral amyloid angiopathy: implications for studying obesity-brain interactions in mice. Biochim. Biophys. Acta 1832 (2013), 1456–1462.
31. [31] Leboucher, A., Laurent, C., Fernandez-Gomez, F.-J., Burnouf, S., Troquier, L., Eddarkaoui, S., Demeyer, D., Caillierez, R., Zommer, N., Vallez, E., Bantubungi, K., Breton, C., Pigny, P., Buée-Scherrer, V., Staels, B., Hamdane, M., Tailleux, A., Buée, L., Blum, D., Detrimental effects of diet-Induced obesity on t pathology are independent of insulin resistance in t transgenic mice. Diabetes 2 (2013), 1681–1693.
32. [32] Koga, S., Kojima, A., Kuwabara, S., Yoshiyama, Y., Immunohistochemical analysis of tau phosphorylation and astroglial activation with enhanced leptin receptor expression in diet-induced obesity mouse hippocampus. Neurosci. Lett. 571 (2014), 11–16.
33. [33] Bimonte-Nelson, H., Singleton, R., Hunter, C., Price, K., Moore, A., Granholm, A.C., Ovarian hormones and cognition in the aged female rat: I. Long-term but not short term, ovariectomy enhances spatial performance. Behav. Neurosci. 117 (2003), 1395–1406.
34. [34] French, K., Bimonte-Nelson, H.A., Granholm, A.C., Galantamine effects on memory, spatial cue utilization, and neurotrophic factors in gaed female rats. Cell Transplant. 16 (2007), 197–205.
35. [35] Jarrard, L.E., Okaichi, H., Steward, O., Goldschmidt, R.B., On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. Behav. Neurosci. 98 (1984), 946–954.
36. [36] M'Harzi, M., Jarrard, L., Strategy selection in a task with spatial and nonspatial components: effects of fimbria-fornix lesions in rats. Behav. Neural Biol. 58 (1992), 171–179.
37. [37] Hunter, C., Bimonte, H.A., Granholm, A.C., Behavioral comparison of 4 and 6-month old Ts65Dn mice: age-related impairments in working and reference memory. Behav. Brain Res. 138 (2003), 121–131.
38. [38] Backman, C., Rose, G., Hoffer, B., Henry, M., Bartus, R., Friden, P., Granholm, A.C., Systemic administration of a nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J. Neurosci. 16 (1996), 5437–5442.
39. [39] Granholm, A.C., Sanders, L., Seo, H., Lin, L., Ford, K., Isacson, O., Estrogen alters amyloid precursor protein as well as dendritic and cholinergic markers in a mouse model of Down syndrome. Hippocampus 13 (2003), 905–914.
40. [40] Lockrow, J., Prakasam, A., Huang, P., Bimonte-Nelson, H.A., Sambamurti, K., Granholm, A.C., Cholinergic degeneration and memory loss delayed by vitamin E in a Down syndrome mouse model. Exp. Neurol. 216 (2008), 278–289.
41. [41] Willis, L., Small, B.J., Bickford, P.C., Umphlet, C., Moore, A., Granholm, A.C., Dietary blueberry supplementation affects growth but not vascularization of neural transplants. J. Cereb. Blood Flow Metab. 28 (2008), 1150–1164.
42. [42] Gundersen, H., Bagger, P., Bendtsen, T., Evans, S., Korbo, L., Marcussen, N., Moller, A., Nielsen, K., Nyengaard, J.R., Pakkenberg, B., et al. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96 (1988), 857–881.
43. [43] Sarlus, H., Hoglund, C., Karshikoff, B., Wang, X., Lekander, M., Schultzberg, M., Oprica, M., Allergy influences the inflammatory status of the brain and enhances tau-phosphorylation. J. Cell. Mol. Med. 16 (2012), 2401–2412.
44. [44] Chard, P.S., Jordan, J., Marcuccilli, C., Miller, R., Leiden, J., Roos, R., Ghadge, G.D., Regulation of excitatory transmission at hippocampal synapses by cabindin D28k. PNAS 92 (1995), 5144–5148.
45. [45] Westerink, R.H., Beekwilder, J.P., Wadman, W.J., Differential alterations of synaptic plasticity in dentate gyrus and CA1 hippocampal area of Calbindin-D28K knockout mice. Brain Res. 1450 (2012), 1–10.
46. [46] Krzywkowski, P., Potier, B., Billard, J., Dutar, P., Lamour, Y., Synaptic mechanisms and calcium binding proteins in the aged rat brain. Life Sci. 59 (1996), 421–428.
47. 2+ binding proteins during rat brain ageing: loss of calbindin and calretinin in the hippocampus with no change in the cerebellum. Eur. J. Neurosci. 6 (1994), 1491–1499.
48. [48] Fifre, A., Sponne, I., Koziel, V., Kriem, B., Yen Potin, F.T., Bihain, B.E., Olivier, J.L., Oster, T., Pillot, T., Microtubule-associated protein MAP1A MAP1B, and MAP2 proteolysis during soluble amyloid beta-peptide-induced neuronal apoptosis. Synergistic involvement of calpain and caspase-3. J. Biol. Chem. 281 (2006), 229–240.
49. [49] Takahashi, R.H., Capetillo-Zarate, E., Lin, M.T., Milner, T.A., Gouras, G.K., Accumulation of intraneuronal beta-amyloid 42 peptides is associated with early changes in microtubule-associated protein 2 in neurites and synapses. PLoS One, 8, 2013, e51965.
50. [50] Salimi, K., Humpel, C., Down-regulation of complement receptor 3 and major histocompatibility complex I and II antigen-like immonureactivity accompanies ramification in isolated rat microglia. Brain Res. 946 (2002), 283–289.
51. [51] Sheffield, L., Berman, N., Microglial expression of MHC class II increases in normal aging of nonhuman priamtes. Neurobiol. Aging 19 (1998), 47–55.
52. [52] Luo, X.-G., Ding, J.-Q., Chen, S.-D., Microglia in the aging brain: relevance to neurodegeneration. Mol Neurodegeneration 5 (2010), 12–20.
53. [53] Augustinack, J.C., Schneider, A., Mandelkow, E.-M., Hyman, B.T., Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. (Berl.) 103 (2001), 26–35.
54. [54] Bimonte, H.A., Nelson, M.E., Granholm, A.C., Age-related deficits as working memory load increases: relationships with growth factors. Neurobiol. Aging 24 (2003), 37–48.
55. [55] Sharma, S., Rakoczy, S., Brown-Borg, H., Assessment of spatial memory in mice. Life Sci. 87 (2010), 521–536.
56. [56] Veng, L., Granholm, A.C., Rose, G.M., Age-related sex differences in spatial learning and basal forebrain cholinergic neurons in F344 rats. Physiol. Behav. 80 (2003), 27–36.
57. [57] Shukitt-Hale, B., McEwen, J.J., Szprengiel, A., Joseph, J.A., Effect of age on the radial arm water maze – a test of spatial learning and memory. Neurobiol. Aging 25 (2004), 223–229.
58. [58] Boitard, C., Cavaroc, A., Sauvant, J., Aubert, A., Castanon, N., Laye, S., Ferreira, G., Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain Behav. Immun. 40 (2014), 9–17.
59. [59] Kanoski, S.E., Davidson, T.L., Different patterns of memory impairments accompany short- and longer-term maintenance on a high-energy diet. J. Exp. Psychol. Anim. Behav. Process. 36 (2010), 313–319.
60. [60] Camer, D., Yu, Y., Szabo, A., Fernandez, F., Dinh, C.H., Huang, X.F., Bardoxolone methyl prevents high-fat diet-induced alterations in prefrontal cortex signalling molecules involved in recognition memory. Prog. Neuropsychopharmacol. Biol. Psychiatry 59 (2015), 68–75.
61. [61] Hoane, M.R., Swan, A.A., Heck, S.E., The effects of a high-fat sucrose diet on functional outcome following cortical contusion injury in the rat. Behav. Brain Res. 223 (2011), 119–124.
62. [62] Goldbart, A.D., Row, B.W., Kheirandish-Gozal, L., Cheng, Y., Brittian, K.R., Gozal, D., High fat/refined carbohydrate diet enhances the susceptibility to spatial learning deficits in rats exposed to intermittent hypoxia. Brain Res. 1090 (2006), 190–196.
63. [63] Hosking, D.E., Nettelbeck, T., Wilson, C., Danthiir, V., Retrospective lifetime dietary patterns predict cognitive performance in community-dwelling older Australians. Br. J. Nutr. 112 (2014), 228–237.
64. [64] Gu, Y., Scarmeas, N., Dietary patterns in Alzheimer's disease and cognitive aging. Curr. Alzheimer Res. 8 (2011), 510–519.
65. [65] Kelly, K.M., Nadon, N.L., Morrison, J.H., Thibault, O., Barnes, C.A., Blalock, E.M., The neurobiology of aging. Epilepsy Res. 68 (2006), S5–S20.
66. [66] Unal-Cevik, I., Kilinc, M., Gursoy-Ozdemir, Y., Gurer, G., Dalkara, T., Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res. 1015 (2004), 169–174.
67. [67] Disterhoft, J.F., Moyer, J.R., Thompson, L.T., The calcium rationale in aging and Alzheimer's disease. Evidence from an animal model of normal aging. Ann. N. Y. Acad. Sci. 747 (1994), 382–406.
68. [68] Khachaturian, Z.S., Calcium, membranes, aging, and Alzheimer's disease. Introduction and overview. Ann. N. Y. Acad. Sci. 568 (1989), 1–4.
69. [69] Thibault, O., Porter, N.M., Chen, K.C., Blalock, E.M., Kaminker, P.G., Clodfelter, G.V., Brewer, L.D., Landfield, P.W., Calcium dysregulation in neuronal aging and Alzheimer's disease: history and new directions. Cell Calcium 24 (1998), 417–433.
70. [70] Hayakawa, N., Kato, H., Araki, T., Age-related changes of astorocytes, oligodendrocytes and microglia in the mouse hippocampal CA1 sector. Mech. Ageing Dev. 128 (2007), 311–316.
71. [71] Niculescu, M.D., Lupu, D.S., High fat diet-induced maternal obesity alters fetal hippocampal development. Int. J. Dev. Neurosci. 27 (2009), 627–633.
72. [72] Calvo-Ochoa, E., Hernandez-Ortega, K., Ferrera, P., Morimoto, S., Arias, C., Short-term high-fat-and-fructose feeding produces insulin signaling alterations accompanied by neurite and synaptic reduction and astroglial activation in the rat hippocampus. J. Cereb. Blood Flow Metab. 34 (2014), 1001–1008.
73. [73] Chang, L., Jones, Y., Ellisman, M.H., Goldstein, L.S., Karin, M., JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev. Cell 4 (2003), 521–533.
74. [74] Vernia, S., Cavanagh-Kyros, J., Garcia-Haro, L., Sabio, G., Barrett, T., Jung, D.Y., Kim, J.K., Xu, J., Shulha, H.P., Garber, M., Gao, G., Davis, R.J., The PPARα-FGF21 hormone axis contributes to metabolic regulation by the hepatic JNK signaling pathway. Cell Metab. 20 (2014), 512–525.
75. [75] Johnson, R.W., Feeding the beast: can microglia in the senescent brain be regulated by diet?. Brain Behav. Immun. 43 (2015), 1–8.
76. [76] Kettenmann, H., Hanisch, U.K., Noda, M., Verkhratsky, A., Physiology of microglia. Physiol. Rev. 91 (2011), 461–553.
77. [77] Freeman, L.R., Small, B.J., Bickford, P.C., Umphlet, C., Granholm, A.C., A high-fat/high-cholesterol diet inhibits growth of fetal hippocampal transplants via increased inflammation. Cell Transplant. 20 (2011), 1499–1514.
78. [78] Nguyen, J.C., Killcross, A.S., Jenkins, T.A., Obesity and cognitive decline: role of inflammation and vascular changes. Front. Neurosci. 8 (2014), 375–383.
79. [79] Spolcova, A., Mikulaskova, B., Krskova, K., Gajdosechova, L., Zorad, S., Olszanecki, R., Suski, M., Bujak-Gizycka, B., Zelezna, B., Maletinska, L., Deficient hippocampal insulin signaling and augmented Tau phosphorylation is related to obesity- and age-induced peripheral insulin resistance: a study in Zucker rats. BMC Neurosci. 15 (2014), 111–118.
80. [80] Takalo, M., Haapasalo, A., Martiskainen, H., Kurkinen, K.M., Koivisto, H., Miettinen, P., Khandelwal, V.K., Kemppainen, S., Kaminska, D., Mäkinen, P., Leinonen, V., Pihlajamäki, J., Soininen, H., Laakso, M., Tanila, H., Hiltunen, M., High-fat diet increases Tau expression in the brain of T2DM and AD mice independently of peripheral metabolic status. J. Nutr. Biochem. 25 (2014), 634–641.