Maternal high-fat diet worsens memory deficits in the triple-transgenic (3xTgAD) mouse model of Alzheimer's disease

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Martin, Sarah A L ^a   Jameson, Christine H ^a   Allan, Stuart M ^a   Lawrence, Catherine B ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DISEASE COURSE; EXPERIMENTAL BEHAVIORAL TEST; FAT INTAKE; FEMALE; HIPPOCAMPUS; LACTATION; LIPID DIET; MATERNAL NUTRITION; MOUSE; NERVE CELL; NONHUMAN; PREGNANCY; PROGENY; ANIMAL; DISEASE MODEL; MEMORY DISORDER; PATHOPHYSIOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FEMALE; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; PREGNANCY;

EID: 84903396889     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099226     Document Type: Article

References (60)

1. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, et al. (2011) Alzheimer's disease. Lancet 377: 1019-1031.
2. Lahiri DK, Zawia NH, Greig NH, Sambamurti K, Maloney B (2008) Early-life events may trigger biochemical pathways for Alzheimer's disease: the "LEARn© model. Biogerontology 9: 375-379.
3. Miller DB, O'Callaghan JP (2008) Do early-life insults contribute to the late-life development of Parkinson and Alzheimer diseases? Metabolism 57 Suppl 2: S44-S49.
4. Beydoun MA, Beydoun HA, Wang Y (2008) Obesity and central obesity as risk factors for incident dementia and its subtypes: a systematic review and meta-analysis. Obes Rev 9: 204-218. (Pubitemid 351550691)
5. Fitzpatrick AL, Kuller LH, Lopez OL, Diehr P, O'Meara ES, et al. (2009) Midlife and late-life obesity and the risk of dementia: cardiovascular health study. Arch Neurol 66: 336-342.
6. Profenno LA, Porsteinsson AP, Faraone SV (2010) Meta-analysis of Alzheimer's disease risk with obesity, diabetes, and related disorders. Biol Psychiatry 67: 505-512.
7. Kalmijn S, Launer LJ, Ott A, Witteman JC, Hofman A, et al. (1997) Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann Neurol 42: 776-782. (Pubitemid 27481550)
8. Grant WB (1999) Dietary links to Alzheimer's disease: 1999 update. J Alzheimers Dis 1: 197-201.
9. Luchsinger JA, Tang MX, Shea S, Mayeux R (2002) Caloric intake and the risk of Alzheimer disease. Arch Neurol 59: 1258-1263. (Pubitemid 34856378)
10. Laitinen MH, Ngandu T, Rovio S, Helkala EL, Uusitalo U, et al. (2006) Fat intake at midlife and risk of dementia and Alzheimer's disease: a population-based study. Dement Geriatr Cogn Disord 22: 99-107.
11. Eskelinen MH, Ngandu T, Helkala EL, Tuomilehto J, Nissinen A, et al. (2008) Fat intake at midlife and cognitive impairment later in life: a population-based CAIDE study. Int J Geriatr Psychiatry 23: 741-747.
12. Grant B (1997) Dietary links to Alzheimer's disease. Alzheimer's Disease Review 42-45.
13. Panza F, Solfrizzi V, Colacicco AM, D'Introno A, Capurso C, et al. (2004) Mediterranean diet and cognitive decline. Public Health Nutr 7: 959-963. (Pubitemid 39389283)
14. Ho L, Qin W, Pompl PN, Xiang Z, Wang J, et al. (2004) Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J 18: 902-904.
15. Herculano B, Tamura M, Ohba A, Shimatani M, Kutsuna N,et al. (2013) beta-alanyl-L-histidine rescues cognitive deficits caused by feeding a high fat diet in a transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 33: 983-997.
16. Julien C, Tremblay C, Phivilay A, Berthiaume L, Emond V, et al. (2010) High-fat diet aggravates amyloid-beta and tau pathologies in the 3xTg-AD mouse model. Neurobiol Aging 31: 1516-1531.
17. Maesako M, Uemura K, Kubota M, Kuzuya A, Sasaki K, et al. (2012) Environmental enrichment ameliorated high-fat diet-induced Abeta deposition and memory deficit in APP transgenic mice. Neurobiol Aging 33: 1011-1023.
18. Pedrini S, Thomas C, Brautigam H, Schmeidler J, Ho L, et al. (2009) Dietary composition modulates brain mass and solubilizable Abeta levels in a mouse model of aggressive Alzheimer's amyloid pathology. Mol Neurodegener 4: 40.
19. Phivilay A, Julien C, Tremblay C, Berthiaume L, Julien P, et al. (2009) High dietary consumption of trans fatty acids decreases brain docosahexaenoic acid but does not alter amyloid-beta and tau pathologies in the 3xTg-AD model of Alzheimer's disease. Neuroscience 159: 296-307.
20. Knight EM, Martins IVA, Gumusgoz S, Allan SM, Lawrence CB (2014) High-fat diet-induced memory impairment in 3xTgAD mice is independent of changes in amyloid and tau pathology. Neurobiol Aging DOI, 10.1016.
21. Breteler MM (2001) Early life circumstances and late life Alzheimer's disease. Epidemiology 12: 378-379.
22. Whalley LJ, Dick FD, McNeill G (2006) A life-course approach to the aetiology of late-onset dementias. Lancet Neurol 5: 87-96. (Pubitemid 41790699)
23. Kajantie E (2008) Early-life events. Effects on aging. Hormones (Athens) 7: 101-113.
24. Ross MG, Desai M, Khorram O, McKnight RA, Lane RH, et al. (2007) Gestational programming of offspring obesity: a potential contributor to Alzheimer's disease. Curr Alzheimer Res 4: 213-217. (Pubitemid 46557510)
25. Gustafson D (2008) A life course of adiposity and dementia. Eur J Pharmacol 585: 163-175.
26. Barker DJ, Osmond C (1986) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1: 1077-1081. (Pubitemid 16106274)
27. Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60: 5-20. (Pubitemid 34123501)
28. Cottrell EC, Ozanne SE (2008) Early life programming of obesity and metabolic disease. Physiol Behav 94: 17-28. (Pubitemid 351503588)
29. McMillen IC, Adam CL, Muhlhausler BS (2005) Early origins of obesity: programming the appetite regulatory system. J Physiol 565: 9-17. (Pubitemid 40723686)
30. Freeman DJ (2010) Effects of maternal obesity on fetal growth and body composition: implications for programming and future health. Semin Fetal Neonatal Med 15: 113-118.
31. Herring A, Donath A, Yarmolenko M, Uslar E, Conzen C, et al. (2012) Exercise during pregnancy mitigates Alzheimer-like pathology in mouse offspring. FASEB J 26: 117-128.
32. Rodriguez A, Miettunen J, Henriksen TB, Olsen J, Obel C, et al. (2008) Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. Int J Obes (Lond) 32: 550-557. (Pubitemid 351414811)
33. Rodriguez A (2010) Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children. J Child Psychol Psychiatry 51: 134-143.
34. Naef L, Srivastava L, Gratton A, Hendrickson H, Owens SM, et al. (2008) Maternal high fat diet during the perinatal period alters mesocorticolimbic dopamine in the adult rat offspring: reduction in the behavioral responses to repeated amphetamine administration. Psychopharmacology (Berl) 197: 83-94.
35. Raygada M, Cho E, Hilakivi-Clarke L (1998) High maternal intake of polyunsaturated fatty acids during pregnancy in mice alters offsprings' aggressive behavior, immobility in the swim test, locomotor activity and brain protein kinase C activity. J Nutr 128: 2505-2511. (Pubitemid 29013002)
36. Sullivan EL, Grayson B, Takahashi D, Robertson N, Maier A, et al. (2010) Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring. J Neurosci 30: 3826-3830.
37. Jones KL, Will MJ, Hecht PM, Parker CL, Beversdorf DQ (2013) Maternal diet rich in omega-6 polyunsaturated fatty acids during gestation and lactation produces autistic-like sociability deficits in adult offspring. Behav Brain Res 238: 193-199.
38. Tozuka Y, Kumon M, Wada E, Onodera M, Mochizuki H, et al. (2010) Maternal obesity impairs hippocampal BDNF production and spatial learning performance in young mouse offspring. Neurochem Int 57: 235-247.
39. Rodriguez JS, Rodriguez-Gonzalez GL, Reyes-Castro LA, Ibanez C, Ramirez A, et al. (2012) Maternal obesity in the rat programs male offspring exploratory, learning and motivation behavior: prevention by dietary intervention pre-gestation or in gestation. Int J Dev Neurosci 30: 75-81.
40. Peleg-Raibstein D, Luca E, Wolfrum C (2012) Maternal high-fat diet in mice programs emotional behavior in adulthood. Behav Brain Res 233: 398-404.
41. Yu H, Bi Y, Ma W, He L, Yuan L, et al. (2010) Long-term effects of high lipid and high energy diet on serum lipid, brain fatty acid composition, and memory and learning ability in mice. Int J Dev Neurosci 28: 271-276.
42. White CL, Pistell PJ, Purpera MN, Gupta S, Fernandez-Kim SO, et al. (2009) Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiol Dis 35: 3-13.
43. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, et al. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421. (Pubitemid 36937044)
44. Hiramatsu M, Sasaki M, Nabeshima T, Kameyama T (1997) Effects of dynorphin A (1-13) on carbon monoxide-induced delayed amnesia in mice. Pharmacol Biochem Behav 56: 73-79. (Pubitemid 27016108)
45. Wall PM, Messier C (2002) Infralimbic kappa opioid and muscarinic M1 receptor interactions in the concurrent modulation of anxiety and memory. Psychopharmacology (Berl) 160: 233-244. (Pubitemid 34230675)
46. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1: 848-858.
47. Paxinos G and Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordintes. Academic Press.
48. Ainge H, Thompson C, Ozanne SE, Rooney KB (2011) A systematic review on animal models of maternal high fat feeding and offspring glycaemic control. Int J Obes (Lond) 35: 325-335.
49. Li M, Sloboda DM, Vickers MH (2011) Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp Diabetes Res 2011: 592408.
50. Knight EM, Verkhratsky A, Luckman SM, Allan SM, Lawrence CB (2012) Hypermetabolism in a triple-transgenic mouse model of Alzheimer's disease. Neurobiol Aging 33: 187-193.
51. Adebakin A, Bradley J, Gumusgoz S, Waters EJ, Lawrence CB (2012) Impaired satiation and increased feeding behaviour in the triple-transgenic Alzheimer's disease mouse model. PLoS One 7: e45179.
52. Liang C, Oest ME, Prater MR (2009) Intrauterine exposure to high saturated fat diet elevates risk of adult-onset chronic diseases in C57BL/6 mice. Birth Defects Res B Dev Reprod Toxicol 86: 377-384.
53. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, et al. (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51: 383-392. (Pubitemid 351159954)
54. Polidori MC, Pientka L, Mecocci P (2012) A review of the major vascular risk factors related to Alzheimer's disease. J Alzheimers Dis 32: 521-530.
55. Bilbo SD, Tsang V (2010) Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J 24: 2104-2115.
56. Tozuka Y, Wada E, Wada K (2009) Diet-induced obesity in female mice leads to peroxidized lipid accumulations and impairment of hippocampal neurogenesis during the early life of their offspring. FASEB J 23: 1920-1934.
57. Rahman A, Akterin S, Flores-Morales A, Crisby M, Kivipelto M, et al. (2005) High cholesterol diet induces tau hyperphosphorylation in apolipoprotein E deficient mice. FEBS Lett 579: 6411-6416. (Pubitemid 41612160)
58. Leboucher A, Laurent C, Fernandez-Gomez FJ, Burnouf S, Troquier L, et al. (2013) Detrimental effects of diet-induced obesity on tau pathology are independent of insulin resistance in tau transgenic mice. Diabetes 62: 1681-1688.
59. Park SH, Kim JH, Choi KH, Jang YJ, Bae SS, et al. (2013) Hypercholesterolemia accelerates amyloid beta-induced cognitive deficits. Int J Mol Med 31: 577-582.
60. Patil S, Chan C (2005) Palmitic and stearic fatty acids induce Alzheimer-like hyperphosphorylation of tau in primary rat cortical neurons. Neurosci Lett 384: 288-293. (Pubitemid 40836016)