Vascular pathology of 20-month-old hypercholesterolemia mice in comparison to triple-transgenic and APPSwDI Alzheimer's disease mouse models

Molecular and Cellular Neuroscience

Volumn 63, Issue , 2014, Pages 83-95

  Hohsfield, Lindsay A ^a   Daschil, Nina ^a   Orädd, Greger ^b   Strömberg, Ingrid ^b   Humpel, Christian ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Alzheimer's disease; Cholesterol; Hypercholesterolemia; Learning; Memory; MRI; Neuroinflammation; Tau; Vascular pathology; Amyloid

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; COLLAGEN TYPE 4; CORTICOSTERONE; GLIAL FIBRILLARY ACIDIC PROTEIN; AMYLOID PRECURSOR PROTEIN; CHOLESTEROL; PRESENILIN 1; PRESENILIN 1, MOUSE; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN VENTRICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; GENOTYPE; HIPPOCAMPUS; HYPERCHOLESTEROLEMIA; LEARNING; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; SPATIAL MEMORY; STRESS; TRANSGENIC MOUSE; VASCULAR DISEASE; WORKING MEMORY; ADVERSE EFFECTS; ANIMAL; BLOOD; C57BL MOUSE; DRUG EFFECTS; GENETICS; GLIA; LIPID DIET; PATHOLOGY; VASCULARIZATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BLOOD-BRAIN BARRIER; CEREBRAL VENTRICLES; CHOLESTEROL; COGNITION; CORTICOSTERONE; DIET, HIGH-FAT; HYPERCHOLESTEROLEMIA; MICE; MICE, INBRED C57BL; NEUROGLIA; PRESENILIN-1; TAU PROTEINS;

EID: 84910154959     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.10.006     Document Type: Article

References (64)

1. Arganda-Carreras I., Fernandez-Gonzalez R., Munoz-Barrutia A., Ortiz-De-Solorzano C. 3D reconstruction of histological sections: application to mammary gland tissue. Microsc. Res. Tech. 2010, 73:1019-1029.
2. Beckmann N., Gerard C., Abramowski D., Cannet C., Staufenbiel M. Noninvasive magnetic resonance imaging detection of cerebral amyloid angiopathy-related microvascular alterations using superparamagnetic iron oxide particles in APP transgenic mouse models of Alzheimer's disease: application to passive Abeta immunotherapy. J. Neurosci. Off. J. Soc. Neurosci. 2011, 31:1023-1031.
3. Bedrosian T.A., Herring K.L., Weil Z.M., Nelson R.J. Altered temporal patterns of anxiety in aged and amyloid precursor protein (APP) transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11686-11691.
4. Beel A.J., Sakakura M., Barrett P.J., Sanders C.R. Direct binding of cholesterol to the amyloid precursor protein: an important interaction in lipid-Alzheimer's disease relationships?. Biochim. Biophys. Acta 2010, 1801:975-982.
5. Bertram L., Lill C.M., Tanzi R.E. The genetics of Alzheimer disease: back to the future. Neuron 2010, 68:270-281.
6. Billings L.M., Oddo S., Green K.N., McGaugh J.L., LaFerla F.M. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 2005, 45:675-688.
7. Bourasset F., Ouellet M., Tremblay C., Julien C., Do T.M., Oddo S., LaFerla F., Calon F. Reduction of the cerebrovascular volume in a transgenic mouse model of Alzheimer's disease. Neuropharmacology 2009, 56:808-813.
8. Bu G. Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat. Rev. Neurosci. 2009, 10:333-344.
9. Chen C.C., Tung Y.Y., Chang C. A lifespan MRI evaluation of ventricular enlargement in normal aging mice. Neurobiol. Aging 2011, 32:2299-2307.
10. Darwish D.S., Wang D., Konat G.W., Schreurs B.G. Dietary cholesterol impairs memory and memory increases brain cholesterol and sulfatide levels. Behav. Neurosci. 2010, 124:115-123.
11. Davis J., Xu F., Deane R., Romanov G., Previti M.L., Zeigler K., Zlokovic B.V., Van Nostrand W.E. Early-onset and robust cerebral microvascular accumulation of amyloid beta-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid beta-protein precursor. J. Biol. Chem. 2004, 279:20296-20306.
12. de la Torre J.C. Vascular risk factors: a ticking time bomb to Alzheimer's disease. Am. J. Alzheimers Dis. Other Demen. 2013, 28:551-559.
13. De Reuck J., Deramecourt V., Cordonnier C., Leys D., Pasquier F., Maurage C.A. Prevalence of small cerebral bleeds in patients with a neurodegenerative dementia: a neuropathological study. J. Neurol. Sci. 2011, 300:63-66.
14. Deci S., Lemieux S.K., Smith-Bell C.A., Sparks D.L., Schreurs B.G. Cholesterol increases ventricular volume in a rabbit model of Alzheimer's disease. J. Alzheimers Dis. 2012, 29:283-292.
15. Di Paolo G., Kim T.W. Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat. Rev. Neurosci. 2011, 12:284-296.
16. Filiano A.J., Tucholski J., Dolan P.J., Colak G., Johnson G.V. Transglutaminase 2 protects against ischemic stroke. Neurobiol. Dis. 2010, 39:334-343.
17. Gama Sosa M.A., Gasperi R.D., Rocher A.B., Wang A.C., Janssen W.G., Flores T., Perez G.M., Schmeidler J., Dickstein D.L., Hof P.R., et al. Age-related vascular pathology in transgenic mice expressing presenilin 1-associated familial Alzheimer's disease mutations. Am. J. Pathol. 2010, 176:353-368.
18. Gamba P., Testa G., Sottero B., Gargiulo S., Poli G., Leonarduzzi G. The link between altered cholesterol metabolism and Alzheimer's disease. Ann. N. Y. Acad. Sci. 2012, 1259:54-64.
19. Ghribi O. Potential mechanisms linking cholesterol to Alzheimer's disease-like pathology in rabbit brain, hippocampal organotypic slices, and skeletal muscle. J. Alzheimers Dis. 2008, 15:673-684.
20. Ghribi O., Golovko M.Y., Larsen B., Schrag M., Murphy E.J. Deposition of iron and beta-amyloid plaques is associated with cortical cellular damage in rabbits fed with long-term cholesterol-enriched diets. J. Neurochem. 2006, 99:438-449.
21. Goymann W., Möstl E., Gwinner E., Karasov W.H. Corticosterone metabolites can be measured noninvasively in excreta of European stonechats (Saxicola torquata rubicola). Auk 2002, 119:1167-1173.
22. Grammas P., Martinez J., Sanchez A., Yin X., Riley J., Gay D., Desobry K., Tripathy D., Luo J., Evola M., et al. A new paradigm for the treatment of Alzheimer's disease: targeting vascular activation. J. Alzheimers Dis. 2014, 40:619-630.
23. Granholm A.C., Bimonte-Nelson H.A., Moore A.B., Nelson M.E., 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. 2008, 14:133-145.
24. Grinberg L.T., Thal D.R. Vascular pathology in the aged human brain. Acta Neuropathol. 2010, 119:277-290.
25. Haag M.D., Hofman A., Koudstaal P.J., Stricker B.H., Breteler M.M. Statins are associated with a reduced risk of Alzheimer disease regardless of lipophilicity. The Rotterdam Study. J. Neurol. Neurosurg. Psychiatry 2009, 80:13-17.
26. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
27. Herzig M.C., Winkler D.T., Burgermeister P., Pfeifer M., Kohler E., Schmidt S.D., Danner S., Abramowski D., Sturchler-Pierrat C., Burki K., et al. Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis. Nat. Neurosci. 2004, 7:954-960.
28. Hirata-Fukae C., Li H.F., Hoe H.S., Gray A.J., Minami S.S., Hamada K., Niikura T., Hua F., Tsukagoshi-Nagai H., Horikoshi-Sakuraba Y., et al. Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model. Brain Res. 2008, 1216:92-103.
29. Hohsfield L.A., Ehrlich D., Humpel C. Cholesterol diet counteracts repeated anesthesia/infusion-induced cognitive deficits in male Brown Norway rats. Neurobiol. Learn. Mem. 2013, 106C:154-162.
30. Humpel C. Chronic mild cerebrovascular dysfunction as a cause for Alzheimer's disease?. Exp. Gerontol. 2011, 46:225-232.
31. Hunter J.M., Bowers W.J., Maarouf C.L., Mastrangelo M.A., Daugs I.D., Kokjohn T.A., Kalback W.M., Luehrs D.C., Valla J., Beach T.G., et al. Biochemical and morphological characterization of the AbetaPP/PS/tau triple transgenic mouse model and its relevance to sporadic Alzheimer's disease. J. Alzheimers Dis. 2011, 27:361-376.
32. Iadecola C. The pathobiology of vascular dementia. Neuron 2013, 80:844-866.
33. Jones L., Holmans P.A., Hamshere M.L., Harold D., Moskvina V., Ivanov D., Pocklington A., Abraham R., Hollingworth P., Sims R., et al. Genetic evidence implicates the immune system and cholesterol metabolism in the aetiology of Alzheimer's disease. PLoS One 2010, 5:e13950.
34. Knight E.M., Martins I.V., Gumusgoz S., Allan S.M., Lawrence C.B. High-fat diet-induced memory impairment in triple-transgenic Alzheimer's disease (3xTgAD) mice is independent of changes in amyloid and tau pathology. Neurobiol. Aging 2014, 35:1821-1832.
35. Kumar-Singh S., Pirici D., McGowan E., Serneels S., Ceuterick C., Hardy J., Duff K., Dickson D., Van Broeckhoven C. Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls. Am. J. Pathol. 2005, 167:527-543.
36. Lambert J.C., Ibrahim-Verbaas C.A., Harold D., Naj A.C., Sims R., Bellenguez C., Jun G., Destefano A.L., Bis J.C., Beecham G.W., et al. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat. Genet. 2013, 45:1452-1458.
37. Maulik M., Westaway D., Jhamandas J.H., Kar S. Role of cholesterol in APP metabolism and its significance in Alzheimer's disease pathogenesis. Mol. Neurobiol. 2013, 47:37-63.
38. Nestor S.M., Rupsingh R., Borrie M., Smith M., Accomazzi V., Wells J.L., Fogarty J., Bartha R. Ventricular enlargement as a possible measure of Alzheimer's disease progression validated using the Alzheimer's disease neuroimaging initiative database. Brain 2008, 131:2443-2454.
39. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
40. Perez-Garmendia R., Hernandez-Zimbron L.F., Morales M.A., Luna-Munoz J., Mena R., Nava-Catorce M., Acero G., Vasilevko V., Viramontes-Pintos A., Cribbs D.H., et al. Identification of N-terminally truncated pyroglutamate amyloid-beta in cholesterol-enriched diet-fed rabbit and AD brain. J. Alzheimers Dis. 2014, 39:441-455.
41. Petanceska S.S., DeRosa S., Sharma A., Diaz N., Duff K., Tint S.G., Refolo L.M., Pappolla M. Changes in apolipoprotein E expression in response to dietary and pharmacological modulation of cholesterol. J. Mol. Neurosci. 2003, 20:395-406.
42. Philipson O., Lord A., Gumucio A., O'Callaghan P., Lannfelt L., Nilsson L.N. Animal models of amyloid-beta-related pathologies in Alzheimer's disease. FEBS J. 2010, 277:1389-1409.
43. Pirchl M., Ullrich C., Humpel C. Differential effects of short- and long-term hyperhomocysteinaemia on cholinergic neurons, spatial memory and microbleedings in vivo in rats. Eur. J. Neurosci. 2010, 32:1516-1527.
44. Puglielli L., Tanzi R.E., Kovacs D.M. Alzheimer's disease: the cholesterol connection. Nat. Neurosci. 2003, 6:345-351.
45. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362:329-344.
46. Raber J. Role of apolipoprotein E in anxiety. Neural Plast. 2007, 2007:91236.
47. Ramesh B.N., Raichurkar K.P., Shamasundar N.M., Rao T.S., Rao K.S. Abeta(42) induced MRI changes in aged rabbit brain resembles AD brain. Neurochem. Int. 2011, 59:637-642.
48. Refolo L.M., Malester B., LaFrancois J., Bryant-Thomas T., Wang R., Tint G.S., Sambamurti K., Duff K., Pappolla M.A. Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol. Dis. 2000, 7:321-331.
49. Reiss A.B., Voloshyna I. Regulation of cerebral cholesterol metabolism in Alzheimer disease. J. Investig. Med. 2012, 60:576-582.
50. Sagare A.P., Bell R.D., Zlokovic B.V. Neurovascular defects and faulty amyloid-beta vascular clearance in Alzheimer's disease. J. Alzheimers Dis. 2013, 33(Suppl 1):S87-S100.
51. Schreurs B.G. The effects of cholesterol on learning and memory. Neurosci. Biobehav. Rev. 2010, 34:1366-1379.
52. Schreurs B.G., Wang D., Smith-Bell C.A., Burhans L.B., Bell R., Gonzalez-Joekes J. Dietary cholesterol concentration and duration degrade long-term memory of classical conditioning of the rabbit's nictitating membrane response. Int. J. Alzheimers Dis. 2012, 2012:732634.
53. Schreurs B.G., Smith-Bell C.A., Wang D., Burhans L.B. Dietary cholesterol degrades rabbit long term memory for discrimination learning but facilitates acquisition of discrimination reversal. Neurobiol. Learn. Mem. 2013, 106:238-245.
54. Shobab L.A., Hsiung G.Y., Feldman H.H. Cholesterol in Alzheimer's disease. Lancet Neurol. 2005, 4:841-852.
55. Sparks D.L., Kuo Y.M., Roher A., Martin T., Lukas R.J. Alterations of Alzheimer's disease in the cholesterol-fed rabbit, including vascular inflammation. Preliminary observations. Ann. N. Y. Acad. Sci. 2000, 903:335-344.
56. Sterniczuk R., Antle M.C., Laferla F.M., Dyck R.H. Characterization of the 3xTg-AD mouse model of Alzheimer's disease: part 2. Behavioral and cognitive changes. Brain Res. 2010, 1348:149-155.
57. Thirumangalakudi L., Prakasam A., Zhang R., Bimonte-Nelson H., Sambamurti K., Kindy M.S., Bhat N.R. High cholesterol-induced neuroinflammation and amyloid precursor protein processing correlate with loss of working memory in mice. J. Neurochem. 2008, 106:475-485.
58. Ullrich C., Pirchl M., Humpel C. Hypercholesterolemia in rats impairs the cholinergic system and leads to memory deficits. Mol. Cell. Neurosci. 2010, 45:408-417.
59. Umeda T., Tomiyama T., Kitajima E., Idomoto T., Nomura S., Lambert M.P., Klein W.L., Mori H. Hypercholesterolemia accelerates intraneuronal accumulation of Abeta oligomers resulting in memory impairment in Alzheimer's disease model mice. Life Sci. 2012, 91:1169-1176.
60. Wilhelmus M.M., de Jager M., Drukarch B. Tissue transglutaminase: a novel therapeutic target in cerebral amyloid angiopathy. Neurodegener. Dis. 2012, 10:317-319.
61. Wood W.G., Li L., Muller W.E., Eckert G.P. Cholesterol as a causative factor in Alzheimer's disease: a debatable hypothesis. J. Neurochem. 2014, 129:559-572.
62. Xie Z., Yang D., Stephenson D., Morton D., Hicks C., Brown T., Bocan T. Characterizing the regional structural difference of the brain between tau transgenic (rTg4510) and wild-type mice using MRI. Med. Image Comput. Comput. Assist. Interv. 2010, 13:308-315.
63. Xue Q.S., Sparks D.L., Streit W.J. Microglial activation in the hippocampus of hypercholesterolemic rabbits occurs independent of increased amyloid production. J. Neuroinflammation 2007, 4:20.
64. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.