The effect of a high-fat diet on brain plasticity, inflammation and cognition in female ApoE4-knockin and ApoE-knockout mice

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Janssen, Carola I F ^a   Jansen, Diane ^a   Mutsaers, Martina P C ^a   Dederen, Pieter J W C ^a   Geenen, Bram ^a   Mulder, Monique T ^b   Kiliaan Kiliaan, Amanda J ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E4; CD68 ANTIGEN; CD68 ANTIGEN, HUMAN; DIFFERENTIATION ANTIGEN; DLGH4 PROTEIN, MOUSE; DOUBLECORTIN PROTEIN; GLUCOSE TRANSPORTER 1; GUANYLATE KINASE; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE; SLC2A1 PROTEIN, MOUSE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL CA1 REGION; LIPID DIET; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; SPATIAL LEARNING; SPATIAL MEMORY; ANIMAL; BODY WEIGHT; BRAIN; DEFICIENCY; DENTATE GYRUS; GENE TARGETING; HUMAN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KNOCKOUT MOUSE; MAZE TEST; METABOLISM; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; APOLIPOPROTEIN E4; BODY WEIGHT; BRAIN; COGNITION; DENTATE GYRUS; DIET, HIGH-FAT; FEMALE; GENE KNOCK-IN TECHNIQUES; GLUCOSE TRANSPORTER TYPE 1; GUANYLATE KINASES; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MAZE LEARNING; MEMBRANE PROTEINS; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURONAL PLASTICITY; NEUROPEPTIDES; ORGAN SIZE;

EID: 84969522838     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155307     Document Type: Article

References (55)

1. Knouff C, Hinsdale ME, Mezdour H, Altenburg MK, Watanabe M, Quarfordt SH, et al. (1999) Apo E structure determines VLDL clearance and atherosclerosis risk in mice. J Clin Invest 103: 1579-1586. PMID: 10359567
2. Stojakovic T, Scharnagl H, Marz W (2004) ApoE: crossroads between Alzheimer's disease and atherosclerosis. Semin Vasc Med 4: 279-285. PMID: 15630629
3. Kim J, Basak JM, Holtzman DM (2009) The role of apolipoprotein E in Alzheimer's disease. Neuron 63: 287-303. doi: 10.1016/j.neuron.2009.06.026 PMID: 19679070
4. Tanzi RE, Bertram L (2001) New frontiers in Alzheimer's disease genetics. Neuron 32: 181-184. PMID: 11683989
5. Spinney L (2014) Alzheimer's disease: The forgetting gene. Nature 510: 26-28. doi: 10.1038/510026a PMID: 24899289
6. Mahley RW, Huang Y, Weisgraber KH (2006) Putting cholesterol in its place: apoE and reverse cholesterol transport. J Clin Invest 116: 1226-1229. PMID: 16670767
7. de la Torre JC (2004) Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 3: 184-190. PMID: 14980533
8. Grammas P, Yamada M, Zlokovic B (2002) The cerebromicrovasculature: a key player in the pathogenesis of Alzheimer's disease. J Alzheimers Dis 4: 217-223. PMID: 12226540
9. Kalaria RN, Akinyemi R, Ihara M (2012) Does vascular pathology contribute to Alzheimer changes? J Neurol Sci 322: 141-147. doi: 10.1016/j.jns.2012.07.032 PMID: 22884479
10. Skoog I, Gustafson D (2006) Update on hypertension and Alzheimer's disease. Neurol Res 28: 605-611. PMID: 16945211
11. de la Torre JC (2012) A turning point for Alzheimer's disease? Biofactors 38: 78-83. doi: 10.1002/biof.200 PMID: 22422426
12. Muller M, Tang MX, Schupf N, Manly JJ, Mayeux R, Luchsinger JA (2007) Metabolic syndrome and dementia risk in a multiethnic elderly cohort. Dement Geriatr Cogn Disord 24: 185-192. PMID: 17641531
13. Thambisetty M, Beason-Held L, An Y, Kraut MA, Resnick SM APOE epsilon4 genotype and longitudinal changes in cerebral blood flow in normal aging. Arch Neurol 67: 93-98. doi: 10.1001/archneurol.2009.913 PMID: 20065135
14. Birdsill AC, Carlsson CM, Willette AA, Okonkwo OC, Johnson SC, Xu G, et al. (2013) Low cerebral blood flow is associated with lower memory function in metabolic syndrome. Obesity (Silver Spring) 21: 1313-1320.
15. Zerbi V, Wiesmann M, Emmerzaal TL, Jansen D, Van Beek M, Mutsaers MPC, et al. (2014) Resting-State Functional Connectivity Changes in Aging apoE4 and apoE-KO Mice. J Neurosci 34: 13963-13975. doi: 10.1523/JNEUROSCI.0684-14.2014 PMID: 25319693
16. Rapp A, Gmeiner B, Huttinger M (2006) Implication of apoE isoforms in cholesterol metabolism by primary rat hippocampal neurons and astrocytes. Biochimie 88: 473-483. PMID: 16376010
17. Michikawa M, Fan QW, Isobe I, Yanagisawa K (2000) Apolipoprotein E exhibits isoform-specific promotion of lipid efflux from astrocytes and neurons in culture. J Neurochem 74: 1008-1016. PMID: 10693931
18. Jansen PJ, Lutjohann D, Thelen KM, von Bergmann K, van Leuven F, Ramaekers FCS, et al. (2009) Absence of ApoE upregulates murine brain ApoD and ABCA1 levels, but does not affect brain sterol levels, while human ApoE3 and human ApoE4 upregulate brain cholesterol precursor levels. J Alzheimers Dis 18: 319-329. doi: 10.3233/JAD-2009-1150 PMID: 19584433
19. Jansen D, Zerbi V, Janssen CI, van Rooij D, Zinnhardt B, Dederen PJ, et al. (2014) Impact of a multi-nutrient diet on cognition, brain metabolism, hemodynamics, and plasticity in apoE4 carrier and apoE knockout mice. Brain Struct Funct 219: 1841-1868. doi: 10.1007/s00429-013-0606-7 PMID: 23832599
20. Libby P, Lichtman AH, Hansson GK (2013) Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 38: 1092-1104. doi: 10.1016/j.immuni.2013.06.009 PMID: 23809160
21. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N (1992) Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci U S A 89: 4471-4475. PMID: 1584779
22. Rijpma A, Jansen D, Arnoldussen IAC, Fang XT, Wiesmann M, Mutsaers MPC, et al. (2013) Sex Differences in Presynaptic Density and Neurogenesis in Middle-Aged ApoE4 and ApoE Knockout Mice. Journal of Neurodegenerative Diseases: 9.
23. Levi O, Michaelson DM (2007) Environmental enrichment stimulates neurogenesis in apolipoprotein E3 and neuronal apoptosis in apolipoprotein E4 transgenic mice. J Neurochem 100: 202-210. PMID: 17074063
24. Kim S, Kim MJ, Kim S, Kang HS, Lim SW, Myung W, et al. (2015) Gender differences in risk factors for transition from mild cognitive impairment to Alzheimer's disease: A CREDOS study. Compr Psychiatry 62: 114-122. doi: 10.1016/j.comppsych.2015.07.002 PMID: 26343475
25. Damoiseaux JS, Seeley WW, Zhou J, Shirer WR, Coppola G, Karydas A, et al. (2012) Gender modulates the APOE epsilon4 effect in healthy older adults: convergent evidence from functional brain connectivity and spinal fluid tau levels. J Neurosci 32: 8254-8262. doi: 10.1523/JNEUROSCI.0305-12.2012 PMID: 22699906
26. Beydoun MA, Boueiz A, Abougergi MS, Kitner-Triolo MH, Beydoun HA, Resnick SM, et al. (2012) Sex differences in the association of the apolipoprotein E epsilon 4 allele with incidence of dementia, cognitive impairment, and decline. Neurobiol Aging 33: 720-731 e724. doi: 10.1016/j.neurobiolaging.2010.05.017 PMID: 20619505
27. Fleisher A, Grundman M, Jack CR Jr., Petersen RC, Taylor C, Kim HT, et al. (2005) Sex, apolipoprotein E epsilon 4 status, and hippocampal volume in mild cognitive impairment. Arch Neurol 62: 953-957. PMID: 15956166
28. Shi L, Du X, Zhou H, Tao C, Liu Y, Meng F, et al. (2014) Cumulative effects of the ApoE genotype and gender on the synaptic proteome and oxidative stress in the mouse brain. Int J Neuropsychopharmacol 17: 1863-1879. doi: 10.1017/S1461145714000601 PMID: 24810422
29. Jankowsky JL, Slunt HH, Gonzales V, Jenkins NA, Copeland NG, Borchelt DR (2004) APP processing and amyloid deposition in mice haplo-insufficient for presenilin 1. Neurobiol Aging 25: 885-892. PMID: 15212842
30. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, Borchelt DR (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 17: 157-165. PMID: 11337275
31. Mulder M, Blokland A, van den Berg DJ, Schulten H, Bakker AH, Terwel D, et al. (2001) Apolipoprotein E protects against neuropathology induced by a high-fat diet and maintains the integrity of the blood-brain barrier during aging. Lab Invest 81: 953-960. PMID: 11454984
32. Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
33. Champagne D, Dupuy JB, Rochford J, Poirier J (2002) Apolipoprotein E knockout mice display procedural deficits in the Morris water maze: analysis of learning strategies in three versions of the task. Neuroscience 114: 641-654. PMID: 12220566
34. Grootendorst J, Kempes MM, Lucassen PJ, Dalm S, de Kloet ER, Oitzl MS (2002) Differential effect of corticosterone on spatial learning abilities in apolipoprotein E knockout and C57BL/6J mice. Brain Res 953: 281-285. PMID: 12384263
35. Oitzl MS, Mulder M, Lucassen PJ, Havekes LM, Grootendorst J, de Kloet ER (1997) Severe learning deficits in apolipoprotein E-knockout mice in a water maze task. Brain Res 752: 189-196. PMID: 9106456
36. Grootendorst J, de Kloet ER, Dalm S, Oitzl MS (2001) Reversal of cognitive deficit of apolipoprotein E knockout mice after repeated exposure to a common environmental experience. Neuroscience 108: 237-247. PMID: 11734357
37. Grootendorst J, Enthoven L, Dalm S, de Kloet ER, Oitzl MS (2004) Increased corticosterone secretion and early-onset of cognitive decline in female apolipoprotein E-knockout mice. Behav Brain Res 148: 167-177. PMID: 14684257
38. Yin J, Turner GH, Coons SW, Maalouf M, Reiman EM, Shi J (2014) Association of amyloid burden, brain atrophy and memory deficits in aged apolipoprotein epsilon4 mice. Curr Alzheimer Res 11: 283-290. PMID: 24694076
39. Raber J, Wong D, Buttini M, Orth M, Bellosta S, Pitas RE, et al. (1998) Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc Natl Acad Sci U S A 95: 10914-10919. PMID: 9724804
40. Bour A, Grootendorst J, Vogel E, Kelche C, Dodart JC, Bales K, et al. (2008) Middle-aged human apoE4 targeted-replacement mice show retention deficits on a wide range of spatial memory tasks. Behav Brain Res 193: 174-182. doi: 10.1016/j.bbr.2008.05.008 PMID: 18572260
41. Suckow MA, Danneman P, Brayton C (2001) The Laboratory Mouse: CRC Press LLC.
42. Underwood EL, Thompson LT (2016) A High-Fat Diet Causes Impairment in Hippocampal Memory and Sex-Dependent Alterations in Peripheral Metabolism. Neural Plast 2016: 7385314. doi: 10.1155/2016/7385314 PMID: 26819773
43. Nathan BP, Bellosta S, Sanan DA, Weisgraber KH, Mahley RW, Pitas RE (1994) Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science 264: 850-852. PMID: 8171342
44. Raber J (2008) AR, apoE, and cognitive function. Horm Behav 53: 706-715. doi: 10.1016/j.yhbeh.2008.02.012 PMID: 18395206
45. Andrews-Zwilling Y, Bien-Ly N, Xu Q, Li G, Bernardo A, Yoon SY, et al. (2010) Apolipoprotein E4 causes age- and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J Neurosci 30: 13707-13717. doi: 10.1523/JNEUROSCI.4040-10.2010 PMID: 20943911
46. Dorey E, Chang N, Liu QY, Yang Z, Zhang W (2014) Apolipoprotein E, amyloid-beta, and neuroinflammation in Alzheimer's disease. Neurosci Bull 30: 317-330. doi: 10.1007/s12264-013-1422-z PMID: 24652457
47. Ophir G, Amariglio N, Jacob-Hirsch J, Elkon R, Rechavi G, Michaelson DM (2005) Apolipoprotein E4 enhances brain inflammation by modulation of the NF-kappaB signaling cascade. Neurobiol Dis 20: 709-718. PMID: 15979312
48. Bartelt A, Orlando P, Mele C, Ligresti A, Toedter K, Scheja L, et al. (2011) Altered endocannabinoid signalling after a high-fat diet in Apoe(-/-) mice: relevance to adipose tissue inflammation, hepatic steatosis and insulin resistance. Diabetologia 54: 2900-2910. doi: 10.1007/s00125-011-2274-6 PMID: 21847582
49. Ruby MA, Nomura DK, Hudak CS, Mangravite LM, Chiu S, Casida JE, et al. (2008) Overactive endocannabinoid signaling impairs apolipoprotein E-mediated clearance of triglyceride-rich lipoproteins. Proc Natl Acad Sci U S A 105: 14561-14566. doi: 10.1073/pnas.0807232105 PMID: 18794527
50. Arnoldussen IA, Kiliaan AJ, Gustafson DR (2014) Obesity and dementia: adipokines interact with the brain. Eur Neuropsychopharmacol 24: 1982-1999. doi: 10.1016/j.euroneuro.2014.03.002 PMID: 24704273
51. Das UN (2001) Is obesity an inflammatory condition? Nutrition 17: 953-966. PMID: 11744348
52. Dhungana H, Rolova T, Savchenko E, Wojciechowski S, Savolainen K, Ruotsalainen AK, et al. (2013) Western-type diet modulates inflammatory responses and impairs functional outcome following permanent middle cerebral artery occlusion in aged mice expressing the human apolipoprotein E4 allele. J Neuroinflammation 10: 102. doi: 10.1186/1742-2094-10-102 PMID: 23957944
53. Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomez-Pinilla F (2002) A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112: 803-814. PMID: 12088740
54. Levi O, Jongen-Relo AL, Feldon J, Roses AD, Michaelson DM (2003) ApoE4 impairs hippocampal plasticity isoform-specifically and blocks the environmental stimulation of synaptogenesis and memory. Neurobiol Dis 13: 273-282. PMID: 12901842
55. Alata W, Ye Y, St-Amour I, Vandal M, Calon F (2015) Human apolipoprotein E varepsilon4 expression impairs cerebral vascularization and blood-brain barrier function in mice. J Cereb Blood Flow Metab 35: 86-94. doi: 10.1038/jcbfm.2014.172 PMID: 25335802