Liver X receptor agonist treatment ameliorates amyloid pathology and memory deficits caused by high-fat diet in APP23 mice

Journal of Neuroscience

Volumn 30, Issue 20, 2010, Pages 6862-6872

  Fitz, Nicholas F ^a   Cronican, Andrea ^a   Pham, Tam ^a   Fogg, Allison ^a   Fauq, Abdul H ^b   Chapman, Robert ^b   Lefterov, Iliya ^a   Koldamova, Radosveta ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; LIVER X RECEPTOR AGONIST; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; OLIGOMER;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BEHAVIOR; BIOCHEMISTRY; C57BL 6 MOUSE; CHOLESTEROL DIET; CLINICAL EVALUATION; COGNITION; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE EXACERBATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTERSTITIAL FLUID; LIPID DIET; MAZE TEST; MEMORY DISORDER; MENTAL DETERIORATION; MICRODIALYSIS; MICROGLIA; MORPHOLOGY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; WESTERN BLOTTING;

AGE FACTORS; AMYLOID; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA, CONDITIONED; DIETARY FATS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; HUMANS; HYDROCARBONS, FLUORINATED; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRODIALYSIS; MICROGLIA; MUTATION; ORPHAN NUCLEAR RECEPTORS; PEPTIDE FRAGMENTS; RETENTION (PSYCHOLOGY); RNA, MESSENGER; SULFONAMIDES;

EID: 77952630395     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1051-10.2010     Document Type: Article

References (39)

1. Cirrito JR, May PC, O'Dell MA, Taylor JW, Parsadanian M, Cramer JW, Audia JE, Nissen JS, Bales KR, Paul SM, DeMattos RB, Holtzman DM (2003) In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and halflife. J Neurosci 23:8844-8853.
2. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-VanceMA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921-923.
3. Cronican AA, Fitz NF, Pham T, Fogg A, Kifer B, Koldamova R, Lefterov I (2010) Proton pump inhibitor lansoprazole is a nuclear liver X receptor agonist. Biochem Pharmacol 79:1310-1316.
4. George AJ, Holsinger RMD, McLean CA, Laughton KM, Beyreuther K, Evin G, Masters CL, Li QX (2004) APP intracellular domain is increased and soluble A[beta] is reduced with diet-induced hypercholesterolemia in a transgenic mouse model of Alzheimer disease. Neurobiol Dis 16:124-132. (Pubitemid 38569803)
5. Grefhorst A, Elzinga BM, Voshol PJ, Plösch T, Kok T, Bloks VW, van der Sluijs FH, Havekes LM, Romijn JA, Verkade HJ, Kuipers F (2002) Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J Biol Chem 277:34182-34190.
6. Hirsch-Reinshagen V, Maia LF, Burgess BL, Blain JF, Naus KE, McIsaac SA, Parkinson PF, Chan JY, Tansley GH, Hayden MR, Poirier J, Van Nostrand W, Wellington CL (2005) The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. J Biol Chem 280:43243-43256. (Pubitemid 43049291)
7. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, Lamb B, Willson TM, Collins JL, Richardson JC, Smith JD, Comery TA, Riddell D, Holtzman DM, Tontonoz P, Landreth GE (2008) ApoE promotes the proteolytic degradation of Abeta. Neuron 58:681-693. (Pubitemid 351778466)
8. Jick H, Zornberg GL, Jick SS, Seshadri S, Drachman DA (2000) Statins and the risk of dementia. Lancet 356:1627-1631.
9. Kalaany NY, Mangelsdorf DJ (2006) LXRs and FXR: the yin and yang of cholesterol and fat metabolism. Annu Rev Physiol 68:159-191.
10. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489. (Pubitemid 36444329)
11. Kim J, Basak JM, Holtzman DM (2009) The role of apolipoprotein E in Alzheimer's disease. Neuron 63:287-303.
12. Kivipelto M, Helkala EL, Laakso MP, Hänninen T, Hallikainen M, Alhainen K, Soininen H, Tuomilehto J, Nissinen A (2001) Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study. BMJ 322:1447-1451. (Pubitemid 32575406)
13. Kivipelto M, Helkala EL, Laakso MP, Hänninen T, Hallikainen M, Alhainen K, Iivonen S, Mannermaa A, Tuomilehto J, Nissinen A, Soininen H (2002) Apolipoprotein E epsilon4 allele, elevated midlife total cholesterol level, and high midlife systolic blood pressure are independent risk factors for late-life Alzheimer disease. Ann Intern Med 137:149-155. (Pubitemid 34827510)
14. Kivipelto M, Ngandu T, Fratiglioni L, Viitanen M, Kåreholt I, Winblad B, Helkala EL, Tuomilehto J, Soininen H, Nissinen A (2005) Obesity and vascular risk factors at midlife and the risk of dementia and Alzheimer disease. Arch Neurol 62:1556-1560. (Pubitemid 41434560)
15. Koldamova R, Lefterov I (2007) Role of LXR and ABCA1 in the pathogenesis of Alzheimer's disease - implications for a new therapeutic approach. Curr Alzheimer Res 4:171-178. (Pubitemid 46557507)
16. Koldamova R, Staufenbiel M, Lefterov I (2005a) Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. J Biol Chem 280:43224-43235. (Pubitemid 43049289)
17. Koldamova RP, Lefterov IM, Staufenbiel M, Wolfe D, Huang S, Glorioso JC, Walter M, Roth MG, Lazo JS (2005b) The liver X receptor ligand T0901317 decreases amyloid beta production in vitro and in a mouse model of Alzheimer's disease. J Biol Chem 280:4079-4088. (Pubitemid 40288571)
18. Laffitte BA, Repa JJ, Joseph SB, Wilpitz DC, Kast HR, Mangelsdorf DJ, Tontonoz P (2001) LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc Natl Acad Sci U S A 98:507-512.
19. Lefterov I, Bookout A, Wang Z, Staufenbiel M, Mangelsdorf D, Koldamova R (2007) Expression profiling in APP23 mouse brain: inhibition of Abeta amyloidosis and inflammation in response to LXR agonist treatment. Mol Neurodegener 2:20. (Pubitemid 351177401)
20. Lefterov I, Fitz N, Cronican A, Lefterov PI, Staufenbiel M, Koldamova RP (2009) Memory deficits in APP23/Abca1+/- mice correlate with the level of Abeta oligomers. ASN Neuro 1:2.
21. Parrott MD, Greenwood CE (2007) Dietary influences on cognitive function with aging: from high-fat diets to healthful eating. Ann N Y Acad Sci 1114:389-397.
22. Peng D, Hiipakka RA, Xie JT, Reardon CA, Getz GS, Liao S (2010) Differential effects of activation of liver X receptor on plasma lipid homeostasis in wild-type and lipoprotein clearance-deficient mice. Atherosclerosis 208:126-133.
23. Poirier J, Davignon J, Bouthillier D, Kogan S, Bertrand P, Gauthier S (1993) Apolipoprotein E polymorphism and Alzheimer's disease. Lancet 342:697-699.
24. Puglielli L, Tanzi RE, Kovacs DM (2003) Alzheimer's disease: the cholesterol connection. Nat Neurosci 6:345-351.
25. Refolo LM, Pappolla MA, Malester B, LaFrancois J, Bryant-Thomas T, Wang R, Tint GS, Sambamurti K, Duff K (2000) Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol Dis 7:321-331.
26. Refolo LM, Pappolla MA, LaFrancois J, Malester B, Schmidt SD, Thomas-Bryant T, Tint GS, Wang R, Mercken M, Petanceska SS, Duff KE (2001) A cholesterol-lowering drug reduces beta-amyloid pathology in a transgenic mouse model of Alzheimer's disease. Neurobiol Dis 8:890-899. (Pubitemid 33055603)
27. Riddell DR, Zhou H, Comery TA, Kouranova E, Lo CF, Warwick HK, Ring RH, Kirksey Y, Aschmies S, Xu J, Kubek K, Hirst WD, Gonzales C, Chen Y, Murphy E, Leonard S, Vasylyev D, Oganesian A, Martone RL, Pangalos MN, et al. (2007) The LXR agonist TO901317 selectively lowers hippocampal Abeta42 and improves memory in the Tg2576 mouse model of Alzheimer's disease. Mol Cell Neurosci 34:621-628. (Pubitemid 46483091)
28. Scarmeas N, Stern Y, Mayeux R, Luchsinger JA (2006) Mediterranean diet, Alzheimer disease, and vascular mediation. Arch Neurol 63:1709-1717.
29. Shibata N, Glass CK (2009) Regulation of macrophage function in inflammation and atherosclerosis. J Lipid Res 50 Suppl:S277-S281.
30. Simons M, Keller P, De Strooper B, Beyreuther K, Dotti CG, Simons K (1998) Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc Natl Acad Sci U S A 95:6460-6464. (Pubitemid 28249035)
31. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993) Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci U S A 90:1977-1981. (Pubitemid 23069980)
32. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Bürki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci U S A 94:13287-13292. (Pubitemid 27518514)
33. Takechi R, Galloway S, Pallebage-Gamarallage MM, Wellington CL, Johnsen RD, Dhaliwal SS, Mamo JC (2010) Differential effects of dietary fatty acids on the cerebral distribution of plasma-derived apo B lipoproteins with amyloid-beta. Br J Nutr 103:652-662.
34. Thirumangalakudi L, Prakasam A, Zhang R, Bimonte-Nelson H, Sambamurti K, Kindy MS, Bhat NR (2008) High cholesterol-induced neuroinflammation and amyloid precursor protein processing correlate with loss of working memory in mice. J Neurochem 106:475-485.
35. Wahrle SE, Jiang H, Parsadanian M, Legleiter J, Han X, Fryer JD, Kowalewski T, Holtzman DM (2004) ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE. J Biol Chem 279:40987-40993. (Pubitemid 39287699)
36. Wahrle SE, Jiang H, Parsadanian M, Hartman RE, Bales KR, Paul SM, Holtzman DM (2005) Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease. J Biol Chem 280:43236-43242. (Pubitemid 43049290)
37. Zandi PP, Sparks DL, Khachaturian AS, Tschanz J, Norton M, Steinberg M, Welsh-Bohmer KA, Breitner JC (2005) Do statins reduce risk of incident dementia and Alzheimer disease? The Cache County Study. Arch Gen Psychiatry 62:217-224. (Pubitemid 40189139)
38. Zanotti I, Favari E, Sposito AC, Rothblat GH, Bernini F (2004) Pitavastatin increases ABCA1-mediated lipid efflux from Fu5AH rat hepatoma cells. Biochem Biophys Res Commun 321:670-674. (Pubitemid 39118390)
39. Zelcer N, Khanlou N, Clare R, Jiang Q, Reed-Geaghan EG, Landreth GE, Vinters HV, Tontonoz P (2007) Attenuation of neuroinflammation and Alzheimer's disease pathology by liver x receptors. Proc Natl Acad Sci U S A 104:10601-10606. (Pubitemid 47185711)