Positive correlation between elevated plasma cholesterol levels and cognitive impairments in LDL receptor knockout mice: Relevance of cortico-cerebral mitochondrial dysfunction and oxidative stress

Neuroscience

Volumn 197, Issue , 2011, Pages 99-106

  de Oliveira, J ^a   Hort, M A ^a   Moreira, E L G ^a   Glaser, V ^a   Ribeiro do Valle, R M ^a   Prediger, R D ^a   Farina, M ^a   Latini, A ^a   de Bem, A F ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Alzheimer's disease; Cognitive impairment; Hypercholesterolemia; Low density lipoprotein receptor (LDLr) deficient mice; Mitochondrial dysfunctional; Oxidative stress

Indexed keywords

CHOLESTEROL; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; LOW DENSITY LIPOPROTEIN RECEPTOR; MITOCHONDRIAL COMPLEX II; MITOCHONDRIAL ENZYME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; GENE SILENCING; HYPERCHOLESTEROLEMIA; LEARNING; MALE; MEMORY; MEMORY DISORDER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; SPATIAL LEARNING; WILD TYPE;

ALZHEIMER DISEASE; ANIMALS; BRAIN; CHOLESTEROL; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYPERCHOLESTEROLEMIA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATIVE STRESS; RECEPTORS, LDL;

EID: 82855172098     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.09.009     Document Type: Article

References (67)

1. Aksenov M.Y., Aksenova M.V., Butterfield D.A., Geddes J.W., Markesbery W.R. Protein oxidation in the brain in Alzheimer's disease. Neuroscience 2001, 103:373-383.
2. Assini F.L., Duzzioni M., Takahashi R.N. Object location memory in mice: pharmacological validation and further evidence of hippocampal CA1 participation. Behav Brain Res 2009, 204:206-211.
3. Ballinger S.W. Mitochondrial dysfunction in cardiovascular disease. Free Radic Biol Med 2005, 38:1278-1295.
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
5. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004, 287:C817-C833.
6. Brozoski T.J., Brown R.M., Rosvold H.E., Goldman P.S. Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 1979, 205:929-932.
7. Cadenas E., Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000, 29:222-230.
8. Carlberg I., Mannervik B. Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 1975, 250:5475-5480.
9. Cassina A., Radi R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 1996, 328:309-316.
10. Chen H., Chan D.C. Critical dependence of neurons on mitochondrial dynamics. Curr Opin Cell Biol 2006, 18:453-459.
11. Colell A., García-Ruiz C., Morales A., Ballesta A., Ookhtens M., Rodés J., Kaplowitz N., Fernández-Checa J.C. Transport of reduced glutathione in hepatic mitochondria and mitoplasts from ethanol-treated rats: effect of membrane physical properties and S-adenosyl-l-methionine. Hepatology 1997, 26:699-708.
12. Cramer C., Haan M.N., Galea S., Langa K.M., Kalbfleisch J.D. Use of statins and incidence of dementia and cognitive impairment without dementia in a cohort study. Neurology 2008, 71:344-350.
13. Crisby M., Rahman S.M., Sylvén C., Winblad B., Schultzberg M. Effects of high cholesterol diet on gliosis in apolipoprotein E knockout mice. Implications for Alzheimer's disease and stroke. Neurosci Lett 2004, 369:87-92.
14. Di Paolo G., Kim T.W. Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat Rev Neurosci 2011, 12:284-296.
15. Dringen R., Hirrlinger J. Glutathione pathways in the brain. Biol Chem 2003, 384:505-516.
16. Elder G.A., Cho J.Y., English D.F., Franciosi S., Schmeidler J., Sosa M.A., Gasperi R.D., Fisher E.A., Mathews P.M., Haroutunian V., Buxbaum J.D. Elevated plasma cholesterol does not affect brain Abeta in mice lacking the low-density lipoprotein receptor. J Neurochem 2007, 102:1220-1231.
17. Elder G.A., Ragnauth A., Dorr N., Franciosi S., Schmeidler J., Haroutunian V., Buxbaum J.D. Increased locomotor activity in mice lacking the low-density lipoprotein receptor. Behav Brain Res 2008, 191:256-265.
18. Ellman G.L. Tissue sulfhydryl groups. Arch Biochem Biophys 1959, 82:70-77.
19. Ennaceur A., Neave N., Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 1997, 113:509-519.
20. Esposito L.A., Kokoszka J.E., Waymire K.G., Cottrell B., MacGregor G.R., Wallace D.C. Mitochondrial oxidative stress in mice lacking the glutathione peroxidase-1 gene. Free Radic Biol Med 2000, 28:754-766.
21. Evans R.M., Emsley C.L., Gao S., Sahota A., Hall K.S., Farlow M.R., Hendrie H. Serum cholesterol, APOE genotype, and the risk of Alzheimer's disease: a population-based study of African Americans. Neurology 2000, 54:240-242.
22. Evola M., Hall A., Wall T., Young A., Grammas P. Oxidative stress impairs learning and memory in apoE knockout mice. Pharmacol Biochem Behav 2010, 96:181-186.
23. Faivre E., Gault V.A., Thorens B., Hölscher C. Glucose-dependent insulinotropic polypeptide receptor knockout mice are impaired in learning, synaptic plasticity, and neurogenesis. J Neurophysiol 2011, 105:1574-1580.
24. Fernández A., Llacuna L., Fernández-Checa J.C., Colell A. Mitochondrial cholesterol loading exacerbates amyloid beta peptide-induced inflammation and neurotoxicity. J Neurosci 2009, 29:6394-6405.
25. Fischer J.C., Ruitenbeek W., Berden J.A., Trijbels J.M., Veerkamp J.H., Stadhouders A.M., Sengers R.C., Janssen A.J. Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 1985, 153:23-36.
26. Fontanesi F., Diaz F., Barrientos A. Evaluation of the mitochondrial respiratory chain and oxidative phosphorylation system using yeast models of OXPHOS deficiencies. Curr Protoc Hum Genet 2009, vol 63:1-20. Unit 19.5. A. Boyle (Ed.).
27. 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.
28. Hafezi-Moghadam A., Thomas K.L., Wagner D.D. ApoE deficiency leads to a progressive age-dependent blood-brain barrier leakage. Am J Physiol Cell Physiol 2007, 292:C1256-C1262.
29. Hauptmann S., Scherping I., Dröse S., Brandt U., Schulz K.L., Jendrach M., Leuner K., Eckert A., Müller W.E. Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol Aging 2009, 30:1574-1586.
30. Herrmann W., Knapp J.P. Hyperhomocysteinemia: a new risk factor for degenerative diseases. Clin Lab 2002, 48:471-481.
31. Hort M.A., Straliotto M.R., Netto P.M., da Rocha J.B., de Bem A.F., Ribeiro-do-Valle R.M. Diphenyl diselenide effectively reduces atherosclerotic lesion in LDLr-/- mice by attenuation of oxidative stress and inflammation. J Cardiovasc Pharmacol 2011, 58:91-101.
32. Ishibashi S., Brown M.S., Goldstein J.L., Gerard R.D., Hammer R.E., Herz J. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest 1993, 92:883-893.
33. Ishibashi S., Goldstein J.L., Brown M.S., Herz J., Burns D.K. Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J Clin Invest 1994, 93:1885-1893.
34. Kowaltowski A.J., Vercesi A.E. Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med 1999, 26:463-471.
35. Latini A., da Silva C.G., Ferreira G.C., Schuck P.F., Scussiato K., Sarkis J.J., Dutra Filho C.S., Wyse A.T., Wannmacher C.M., Wajner M. Mitochondrial energy metabolism is markedly impaired by D-2-hydroxyglutaric acid in rat tissues. Mol Genet Metab 2005, 86:188-199.
36. Leonard J.V., Schapira A.H. Mitochondrial respiratory chain disorders I: mitochondrial DNA defects. Lancet 2000, 355:299-304.
37. Levin-Allerhand J.A., Lominska C.E., Smith J.D. Increased amyloid-levels in APPSWE transgenic mice treated chronically with a physiological high-fat high-cholesterol diet. J Nutr Health Aging 2002, 6:315-319.
38. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
39. Lovell M.A., Ehmann W.D., Butler S.M., Markesbery W.R. Elevated thiobarbituric acid-reactive substances and antioxidant enzyme activity in the brain in Alzheimer's disease. Neurology 1995, 45:1594-1601.
40. Madamanchi N.R., Runge M.S. Mitochondrial dysfunction in atherosclerosis. Circ Res 2007, 100:460-473.
41. Marí M., Colell A., Morales A., Caballero F., Moles A., Fernández A., Terrones O., Basañez G., Antonsson B., García-Ruiz C., Fernández-Checa J.C. Mechanism of mitochondrial glutathione-dependent hepatocellular susceptibility to TNF despite NF-kappaB activation. Gastroenterology 2008, 134:1507-1520.
42. Montilla P., Espejo I., Muñoz M.C., Bujalance I., Muñoz-Castañeda J.R., Tunez I. Protective effect of red wine on oxidative stress and antioxidant enzyme activities in the brain and kidney induced by feeding high cholesterol in rats. Clin Nutr 2006, 25:146-153.
43. Moreira P.I., Carvalho C., Zhu X., Smith M.A., Perry G. Mitochondrial dysfunction is a trigger of Alzheimer's disease pathophysiology. Biochim Biophys Acta 2010, 1802:2-10.
44. Mulder M., Jansen P.J., Janssen B.J., van de Berg W.D., van der Boom H., Havekes L.M., de Kloet R.E., Ramaekers F.C., Blokland A. Low-density lipoprotein receptor-knockout mice display impaired spatial memory associated with a decreased synaptic density in the hippocampus. Neurobiol Dis 2004, 16:212-219.
45. Murai T., Okuda S., Tanaka T., Ohta H. Characteristics of object location memory in mice: behavioral and pharmacological studies. Physiol Behav 2007, 90:116-124.
46. Nelson A.J.D., Cooper M.T., Thur K.E., Marsden C.A., Cassaday H.J. The effect of catecholaminergic depletion within the prelimbic and infralimbic medial prefrontal cortex on recognition memory for recency, location, and objects. Behav Neurosc 2011, 125:396-403.
47. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979, 95:351-358.
48. Oliveira H.C., Cosso R.G., Alberici L.C., Maciel E.N., Salerno A.G., Dorighello G.G., Velho J.A., de Faria E.C., Vercesi A.E. Oxidative stress in atherosclerosis-prone mouse is due to low antioxidant capacity of mitochondria. FASEB J 2005, 19:278-280.
49. Paim B.A., Velho J.A., Castilho R.F., Oliveira H.C., Vercesi A.E. Oxidative stress in hypercholesterolemic LDL (low-density lipoprotein) receptor knockout mice is associated with low content of mitochondrial NADP-linked substrates and is partially reversed by citrate replacement. Free Radic Biol Med 2008, 44:444-451.
50. Pamplona R., Barja G. Highly resistant macromolecular components and low rate of generation of endogenous damage: two key traits of longevity. Ageing Res Rev 2007, 6:189-210.
51. Rapp J.H., Pan X.M., Neumann M., Hong M., Hollenbeck K., Liu J. Microemboli composed of cholesterol crystals disrupt the blood-brain barrier and reduce cognition. Stroke 2008, 39:2354-2361.
52. 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.
53. Rojo L., Sjoberg M.K., Hernandez P., Zambrano C., Maccioni R.B. Roles of cholesterol and lipids in the etiopathogenesis of Alzheimer's disease. J Biomed Biotechnol 2006, 73976:2006.
54. Rustin P., Chretien D., Bourgeron T., Gérard B., Rötig A., Saudubray J.M., Munnich A. Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 1994, 228:35-51.
55. Sanz A., Pamplona R., Barja G. Is the mitochondrial free radical theory of aging intact?. Antioxid Redox Signal 2006, 8:582-599.
56. Sharrett A.R., Ding J., Criqui M.H., Saad M.F., Liu K., Polak J.F., Folsom A.R., Tsai M.Y., Burke G.L., Szklo M. Smoking, diabetes, and blood cholesterol differ in their associations with subclinical atherosclerosis: the Multiethnic Study of Atherosclerosis (MESA). Atherosclerosis 2006, 186:441-447.
57. 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.
58. Stary H.C. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis 1989, 9:I19-I32.
59. Sultana R., Butterfield D.A. Identification of the oxidative stress proteome in the brain. Free Radic Biol Med 2011, 50:487-494.
60. 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.
61. 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.
62. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007, 39:44-84.
63. Vercesi A.E., Castilho R.F., Kowaltowski A.J., Oliveira H.C. Mitochondrial energy metabolism and redox state in dyslipidemias. IUBMB Life 2007, 59:263-268.
64. Wendel A. Glutathione peroxidase. Methods Enzymol 1981, 77:325-333.
65. Witte M.E., Geurts J.J., de Vries H.E., van der Valk P., van Horssen J. Mitochondrial dysfunction: a potential link between neuroinflammation and neurodegeneration?. Mitochondrion 2010, 10:411-418.
66. Yaffe K., Barrett-Connor E., Lin F., Grady D. Serum lipoprotein levels, statin use, and cognitive function in older women. Arch Neurol 2002, 59:378-384.
67. Zadelaar S., Kleemann R., Verschuren L., de Vries-Van der Weij J., van der Hoorn J., Princen H.M., Kooistra T. Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler Thromb Vasc Biol 2007, 27:1706-1721.