Skip to main content
×
×
Home

Differential effects of dietary fatty acids on the cerebral distribution of plasma-derived apo B lipoproteins with amyloid-β

  • Ryusuke Takechi (a1) (a2) (a3), Susan Galloway (a1) (a2) (a3), Menuka M. S. Pallebage-Gamarallage (a1) (a2) (a3), Cheryl L. Wellington (a4), Russell D. Johnsen (a5) (a6), Satvinder S. Dhaliwal (a1) (a2) (a3) and John C. L. Mamo (a1) (a2) (a3)...
Abstract

Some dietary fats are a risk factor for Alzheimer's disease (AD) but the mechanisms for this association are presently unknown. In the present study we showed in wild-type mice that chronic ingestion of SFA results in blood–brain barrier (BBB) dysfunction and significant delivery into the brain of plasma proteins, including apo B lipoproteins that are endogenously enriched in amyloid-β (Aβ). Conversely, the plasma concentration of S100B was used as a marker of brain-to-blood leakage and was found to be increased two-fold because of SFA feeding. Consistent with a deterioration in BBB integrity in SFA-fed mice was a diminished cerebrovascular expression of occludin, an endothelial tight junction protein. In contrast to SFA-fed mice, chronic ingestion of MUFA or PUFA had no detrimental effect on BBB integrity. Utilising highly sensitive three-dimensional immunomicroscopy, we also showed that the cerebral distribution and co-localisation of Aβ with apo B lipoproteins in SFA-fed mice are similar to those found in amyloid precursor protein/presenilin-1 (APP/PS1) amyloid transgenic mice, an established murine model of AD. Moreover, there was a strong positive association of plasma-derived apo B lipoproteins with cerebral Aβ deposits. Collectively, the findings of the present study provide a plausible explanation of how dietary fats may influence AD risk. Ingestion of SFA could enhance peripheral delivery to the brain of circulating lipoprotein–Aβ and exacerbate the amyloidogenic cascade.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Differential effects of dietary fatty acids on the cerebral distribution of plasma-derived apo B lipoproteins with amyloid-β
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Differential effects of dietary fatty acids on the cerebral distribution of plasma-derived apo B lipoproteins with amyloid-β
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Differential effects of dietary fatty acids on the cerebral distribution of plasma-derived apo B lipoproteins with amyloid-β
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Professor John Mamo, fax +61 8 92662958, email J.Mamo@Curtin.edu.au
References
Hide All
1Pasinetti, GM & Eberstein, JA (2008) Metabolic syndrome and the role of dietary lifestyles in Alzheimer's disease. J Neurochem 106, 15031514.
2Kalmijn, S (2000) Fatty acid intake and the risk of dementia and cognitive decline: a review of clinical and epidemiological studies. J Nutr Health Aging 4, 202207.
3Petot, GJ & Friedland, RP (2004) Lipids, diet and Alzheimer's disease: an extended summary. J Neurol Sci 226, 3133.
4Sparks, DL, Scheff, SW, Hunsaker, JC III, et al. (1994) Induction of Alzheimer-like β-amyloid immunoreactivity in the brains of rabbits with dietary cholesterol. Exp Neurol 126, 8894.
5Refolo, LM, Malester, B, LaFrancois, J, et al. (2000) Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol Dis 7, 321331.
6Ellis, RJ, Olichney, JM, Thal, LJ, et al. (1996) Cerebral amyloid angiopathy in the brains of patients with Alzheimer's disease: the CERAD experience, Part XV. Neurology 46, 15921596.
7Kalaria, RN (1992) The blood–brain barrier and cerebral microcirculation in Alzheimer disease. Cerebrovasc Brain Metab Rev 4, 226260.
8Wisniewski, HM, Vorbrodt, AW & Wegiel, J (1997) Amyloid angiopathy and blood–brain barrier changes in Alzheimer's disease. Ann NY Acad Sci 826, 161172.
9Cullern, KM (1997) Perivascular astrocytes within Alzheimer's disease plaques. Neuroreport 8, 19611966.
10Itagaki, S, McGeer, PL, Akiyama, H, et al. (1989) Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol 24, 173182.
11Hachinski, V & Munoz, DG (1997) Cerebrovascular pathology in Alzheimer's disease: cause, effect or epiphenomenon? Ann N Y Acad Sci 826, 16.
12Joachim, CL, Duffy, LK, Morris, JH, et al. (1988) Protein chemical and immunocytochemical studies of meningovascular β-amyloid protein in Alzheimer's disease and normal aging. Brain Res 474, 100111.
13Deane, R, Sagare, A, Hamm, K, et al. (2005) IgG-assisted age-dependent clearance of Alzheimer's amyloid β peptide by the blood–brain barrier neonatal Fc receptor. J Neurosci 25, 1149511503.
14Mackic, JB, Bading, J, Ghiso, J, et al. (2002) Circulating amyloid-β peptide crosses the blood–brain barrier in aged monkeys and contributes to Alzheimer's disease lesions. Vascul Pharmacol 38, 303313.
15Crossgrove, JS, Li, GJ & Zheng, W (2005) The choroid plexus removes β-amyloid from brain cerebrospinal fluid. Exp Biol Med 230, 771776.
16Donahue, JE, Flaherty, SL, Johanson, CE, et al. (2006) RAGE, LRP-1, and amyloid-β protein in Alzheimer's disease. Acta Neuropathol 112, 405415.
17Galloway, S, Jian, L, Johnsen, R, et al. (2007) β-Amyloid or its precursor protein is found in epithelial cells of the small intestine and is stimulated by high-fat feeding. J Nutr Biochem 18, 279284.
18Takechi, R, Galloway, S, Pallebage-Gamarallage, MMS, et al. (2008) Chylomicron amyloid-β in the aetiology of Alzheimer's disease. Atheroscler Supp 9, 1925.
19Koudinov, AR & Koudinova, NV (1997) Alzheimer's soluble amyloid β protein is secreted by HepG2 cells as an apolipoprotein. Cell Biol Int 21, 265271.
20James, AP, Pal, S, Gennat, HC, et al. (2003) The incorporation and metabolism of amyloid-β into chylomicron-like lipid emulsions. J Alzeimers Dis 5, 179188.
21Mamo, JC, Jian, L, James, AP, et al. (2008) Plasma lipoprotein β-amyloid in subjects with Alzheimer's disease or mild cognitive impairment. Ann Clin Biochem 45, 395403.
22Smith, D, Watts, GF, Dane-Stewart, C, et al. (1999) Post-prandial chylomicron response can be predicted by a single measurement of plasma apolipoprotein B48 in the fasting state. Eur J Clin Invest 29, 204209.
23Boyt, AA, Taddei, TK, Hallmayer, J, et al. (2000) The effect of insulin and glucose on the plasma concentration of Alzheimer's amyloid precursor protein. Neuroscience 95, 727734.
24LaRue, B, Hogg, E, Sagare, A, et al. (2004) Method for measurement of the blood–brain barrier permeability in the perfused mouse brain: application to amyloid-β peptide in wild type and Alzheimer's Tg2576 mice. J Neurosci Methods 138, 233242.
25Burgess, BL, McIsaac, SA, Naus, KE, et al. (2006) Elevated plasma triglyceride levels precede amyloid deposition in Alzheimer's disease mouse models with abundant A β in plasma. Neurobiol Dis 24, 114127.
26Arendash, GW, Su, GC, Crawford, FC, et al. (1999) Intravascular β-amyloid infusion increases blood pressure: implications for a vasoactive role of β-amyloid in the pathogenesis of Alzheimer's disease. Neurosci Lett 268, 1720.
27Maness, LM, Banks, WA, Podlisny, MB, et al. (1994) Passage of human amyloid β-protein 1-40 across the murine blood–brain barrier. Life Sci 55, 16431650.
28Thomas, T, McLendon, C, Sutton, ET, et al. (1997) Cerebrovascualr endothelial dysfunction mediated by β-amyloid. Neuroreport 8, 13871391.
29Natah, SS, Mouihate, A, Pittman, QJ, et al. (2005) Disruption of the blood–brain barrier during TNBS colitis. Neurogastroenterol Motil 17, 433446.
30Kay, AD, Day, SP, Nicoll, JA, et al. (2003) Remodelling of cerebrospinal fluid lipoproteins after subarachnoid hemorrhage. Atherosclerosis 170, 141146.
31Takechi, R, Galloway, S, Pallebage-Gamarallage, MM, et al. (2008) Three-dimensional immunofluorescent double labelling using polyclonal antibodies derived from the same species: enterocytic colocalization of chylomicrons with Golgi apparatus. Histochem Cell Biol 129, 779784.
32Kleindienst, A, Hesse, F, Bullock, MR, et al. (2007) The neurotrophic protein S100B: value as a marker of brain damage and possible therapeutic implications. Prog Brain Res 161, 317325.
33Yang, Q, Hou, X, Hamberger, A, et al. (1995) S-100 β immunoreactivity in neurons of the rat peripheral sensory ganglia. Neuroreport 6, 20052009.
34Kawai, M, Kalaria, RN, Harik, SI, et al. (1990) The relationship of amyloid plaques to cerebral capillaries in Alzheimer's disease. Am J Pathol 137, 14351446.
35Yanagisawa, K, McLaurin, J, Michikawa, M, et al. (1997) Amyloid β-protein (A β) associated with lipid molecules: immunoreactivity distinct from that of soluble A β. FEBS Lett 420, 4346.
36James, AP & Mamo, JC (2005) The immunodetection of lipoprotein-bound amyloid-β is attenuated because of the presence of lipids. Ann Clin Biochem 42, 7072.
37Morgan, NG (2009) Fatty acids and β-cell toxicity. Curr Opin Clin Nutr Metab Care 12, 117122.
38Carpentier, AC (2008) Postprandial fatty acid metabolism in the development of lipotoxicity and type 2 diabetes. Diabetes Metab 34, 97107.
39Cnop, M, Igoillo-Esteve, M, Chunha, DA, et al. (2008) An update on lipotoxic endoplasmic reticulum stress in pancreatic β-cells. Biochem Soc Trans 36, 909915.
40Solfrizzi, V, Frisardi, V, Capurso, C, et al. (2009) Dietary fatty acids in dementia and predementia syndromes: epidemiological evidence and possible underlying mechanisms. Ageing Res Rev (epublication ahead of print version 28 July 2009).
41Van oostrom, AJ, Alipour, A, Plokker, TW, et al. (2007) The metabolic syndrome in relation to complement component 3 and postprandial lipemia in patients from an outpatient lipid clinic and healthy volunteers. Atherosclerosis 190, 167173.
42Patil, S, Balu, D, Melrose, J, et al. (2008) Brain region-specificity of palmitic acid-induced abnormalities associated with Alzheimer's disease. BMC Res Notes 1, 20.
43Diakogiannaki, E & Morgan, NG (2008) Differential regulation of the ER stress response by long-chain fatty acids in the pancreatic β-cell. Biochem Soc Trans 36, 959962.
44Unger, RH (1995) Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications. Diabetes 44, 863870.
45Deane, R, Sagare, A, Hamm, K, et al. (2008) ApoE isoform-specific disruption of amyloid β peptide clearance from mouse brain. J Clin Invest 118, 40024013.
46Deane, R, Bell, RD, Sagare, A, et al. (2009) Clearance of amyloid-β peptide across the blood–brain barrier: implication for therapies in Alzheimer's disease. CNS Neurol Disord Drug Targets 8, 1630.
47Namba, Y, Tsuchiya, H & Ikeda, K (1992) Apolipoprotein B immunoreactivity in senile plaque and vascular amyloids and neurofibrillary tangles in the brains of patients with Alzheimer's disease. Neurosci Lett 134, 264266.
48Cole, GM & Ard, MD (2000) Influence of lipoproteins on microglial degradation of Alzheimer's amyloid β-protein. Microsc Res Tech 50, 316324.
49Clifford, PM, Zarrabi, S, Siu, G, et al. (2007) Aβ peptides can enter the brain through a defective blood–brain barrier and bind selectively to neurons. Brain Res 1142, 223236.
50Takechi, R, Galloway, S, Pallebage-Gamarallage, M, et al. (2009) Three-dimensional colocalization analysis of plasma-derived apolipoprotein B with amyloid plaques in APP/PS1 transgenic mice. Histochem Cell Biol 131, 661666.
51Kreuter, J, Hekmatara, T, Dreis, S, et al. (2007) Covalent attachment of apolipoprotein A-I and apolipoprotein B-100 to albumin nanoparticles enables drug transport into the brain. J Control Release 118, 5458.
52Caramelli, P, Nitrini, R, Maranhao, R, et al. (1999) Increased apolipoprotein B serum concentration in Alzheimer's disease. Acta Neurol Scand 100, 6163.
53Mamo, JC, Proctor, SD & Smith, D (1998) Retention of chylomicron remnants by arterial tissue; importance of an efficient clearance mechanism from plasma. Atherosclerosis 141, S63S69.
54Elsegood, CL, Pal, S, Roach, PD, et al. (2001) Binding and uptake of chylomicron remnants by primary and THP-1 human monocyte-derived macrophages: determination of binding proteins. Clin Sci 101, 111119.
55Profenno, LA, Porsteinsson, AP & Faraone, SV (2009) Meta-analysis of Alzheimer's disease risk with obesity, diabetes and related disorders. Biol Psychiatry (epublication ahead of print version 7 April 2009).
56Mamo, JC, Watts, GF, Barrett, PH, et al. (2001) Postprandial dyslipidemia in men with visceral obesity: an effect of reduced LDL receptor expression? Am J Physiol Endocrinol Metab 281, E626E632.
57Nelson, TJ & Alkon, DL (2007) Protection against β-amyloid-induced apoptosis by peptides interacting with β-amyloid. J Biol Chem 282, 3123831249.
58Laitinen, MH, Ngandu, T, Rovio, S, et al. (2006) Fat intake at midlife and risk of dementia and Alzheimer's disease: a population based study. Dement Geriatr Cogn Disord 22, 99107.
59Schaefer, EJ, Bongard, V, Beiser, AS, et al. (2006) Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: the Framingham Heart Study. Arch Neurol 63, 15451550.
60Oksman, M, Iivonen, H, Hogyes, E, et al. (2006) Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on β-amyloid accumulation in APP/PS1 trangenic mice. Neurobiol Dis 23, 563572.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed