Interaction between 24-hydroxycholesterol, oxidative stress, and amyloid-β in amplifying neuronal damage in Alzheimer's disease: Three partners in crime

Aging Cell

Volumn 10, Issue 3, 2011, Pages 403-417

  Gamba, Paola ^a   Leonarduzzi, Gabriella ^a   Tamagno, Elena ^a   Guglielmotto, Michela ^a   Testa, Gabriella ^a   Sottero, Barbara ^a   Gargiulo, Simona ^a   Biasi, Fiorella ^a   Mauro, Alessandro ^b   Viña, José ^c   Poli, Giuseppe ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^c UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Alzheimer's disease; Amyloid ; Cholesterol; Neurotoxicity; Oxidative stress; Oxysterols

Indexed keywords

24 HYDROXYCHOLESTEROL; AMYLOID BETA PROTEIN[1-42]; CHOLESTEROL DERIVATIVE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NERVE CELL LESION; NEUROTOXICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN INTERACTION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANTIGENS, CD36; ANTIOXIDANTS; APOPTOSIS; BRAIN; CELL LINE, TUMOR; GENISTEIN; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; HYDROXYCHOLESTEROLS; INTEGRIN BETA CHAINS; NADPH OXIDASE; NECROSIS; NEURONS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; QUERCETIN; REACTIVE OXYGEN SPECIES; UP-REGULATION;

EID: 79955955895     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2011.00681.x     Document Type: Article

References (55)

1. Andrews NC, Faller DV (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19, 2499.
2. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J. Neurosci. 23, 2665-2674.
3. Björkhem I (2006) Crossing the barrier: oxysterols as cholesterol transporters and metabolic modulators in the brain. J. Intern. Med. 260, 493-508.
4. Björkhem I, Meaney S (2004) Brain cholesterol: long secret life behind a barrier. Arterioscler. Thromb. Vasc. Biol. 24, 806-815.
5. Bogdanovic N, Bretillon L, Lund EG, Diczfalusy U, Lannfelt L, Winblad B, Russell DW, Björkhem I (2001) On the turnover of brain cholesterol in patients with Alzheimer's disease. Abnormal induction of the cholesterol-catabolic enzyme CYP46 in glial cells. Neurosci. Lett. 314, 45-48.
6. Bonda DJ, Wang X, Perry G, Nunomura A, Tabaton M, Zhu X, Smith MA (2010) Oxidative stress in Alzheimer disease: a possibility for prevention. Neuropharmacology 59, 290-294.
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
8. Brown AJ, Jessup W (1999) Oxysterols and atherosclerosis. Atherosclerosis 142, 1-28.
9. Brown J 3rd, Theisler C, Silberman S, Magnuson D, Gottardi-Littell N, Lee JM, Yager D, Crowley J, Sambamurti K, Rahman MM, Reiss AB, Eckman CB, Wolozin B (2004) Differential expression of cholesterol hydroxylases in Alzheimer's disease. J. Biol. Chem. 279, 34674-34681.
10. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261, 921-923.
11. Cutler RG, Kelly J, Storie K, Pedersen WA, Tammara A, Hatanpaa K, Troncoso JC, Mattson MP (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc. Natl Acad. Sci. USA 101, 2070-2075.
12. Evans RM, Hui S, Perkins A, Lahiri DK, Poirier J, Farlow MR (2004) Cholesterol and APOE genotype interact to influence Alzheimer disease progression. Neurology 62, 1879-1881.
13. Ferrera P, Mercado-Gómez O, Silva-Aguilar M, Valverde M, Arias C (2008) Cholesterol potentiates beta-amyloid-induced toxicity in human neuroblastoma cells: involvement of oxidative stress. Neurochem. Res. 33, 1509-1517.
14. Hashimoto M, Rockenstein E, Crews L, Masliah E (2003) Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med. 4, 21-36.
15. Heverin M, Bogdanovic N, Lütjohann D, Bayer T, Pikuleva I, Bretillon L, Diczfalusy U, Winblad B, Björkhem I (2004) Changes in the levels of cerebral and extracerebral sterols in the brain of patients with Alzheimer's disease. J. Lipid Res. 45, 185-193.
16. Heverin M, Meaney S, Lütjohann D, Diczfalusy U, Wahren J, Björkhem I (2005) Crossing the barrier: net flux of 27-hydroxycholesterol into the human brain. J. Lipid Res. 46, 1047-1052.
17. Jakóbkiewicz-Banecka J, Wêgrzyn A, Wêgrzyn G (2007) Substrate deprivation therapy: a new hope for patients suffering from neuronopathic forms of inherited lysosomal storage diseases. J. Appl. Genet. 48, 383-388.
18. Jiang D, Dinh KL, Ruthenburg TC, Zhang Y, Su L, Land DP, Zhou F (2009) A kinetic model for beta-amyloid adsorption at the air/solution interface and its implication to the beta-amyloid aggregation process. J. Phys. Chem. B 113, 3160-3168.
19. Jick H, Zornberg GL, Jick SS, Seshadri S, Drachman DA (2000) Statins and the risk of dementia. Lancet 356, 1627-1631.
20. Kandiah N, Feldman HH (2009) Therapeutic potential of statins in Alzheimer's disease. J. Neurosci. 283, 230-234.
21. Kölsch H, Lütjohann D, Tulke A, Björkhem I, Rao ML (1999) The neurotoxic effect of 24-hydroxycholesterol on SH-SY5Y human neuroblastoma cells. Brain Res. 818, 171-175.
22. Kölsch H, Ludwig M, Lütjohann D, Rao ML (2001) Neurotoxicity of 24-hydroxycholesterol, an important cholesterol elimination product of the brain, may be prevented by vitamin E and estradiol-17beta. J. Neural. Transm. 108, 475-488.
23. Leonarduzzi G, Sottero B, Poli G (2002) Oxidized products of cholesterol: dietary and metabolic origin, and proatherosclerotic effects. J. Nutr. Biochem. 13, 700-710.
24. Leonarduzzi G, Gamba P, Gargiulo S, Sottero B, Kadl A, Biasi F, Chiarpotto E, Leitinger N, Vendemiale G, Serviddio G, Poli G (2008) Oxidation as a crucial reaction for cholesterol to induce tissue degeneration: CD36 overexpression in human promonocytic cells treated with a biologically relevant oxysterol mixture. Aging Cell 7, 375-382.
25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
26. Locatelli S, Lütjohann D, Schmidt HH-J, Otto C, Beisiegel U, von Bergmann K (2002) Reduction of plasma 24S-hydroxycholesterol (cerebrosterol) levels using high-dosage simvastatin in patients with hypercholesterolemia. Arch. Neurol. 59, 213-216.
27. Lütjohann D, Breuer O, Ahlborg G, Nennesmo I, Sidén A, Diczfalusy U, Björkhem I (1996) Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation. Proc. Natl Acad. Sci. USA 93, 9799-9804.
28. Nelson TJ, Alkon DL (2005) Oxidation of cholesterol by amyloid precursor protein and beta-amyloid peptide. J. Biol. Chem. 280, 7377-7387.
29. Nunomura A, Perry G, Aliev G, Hirai K, Takeda A, Balraj EK, Jones PK, Ghanbari H, Wataya T, Shimohama S, Chiba S, Atwood CS, Petersen RB, Smith MA (2001) Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 60, 759-767.
30. Odetti P, Angelini G, Dapino D, Zaccheo D, Garibaldi S, Dagna-Bricarelli F, Piombo G, Perry G, Smith M, Traverso N, Tabaton M (1998) Early glycoxidation damage in brains from Down's syndrome. Biochem. Biophys. Res. Commun. 243, 849-851.
31. Opazo C, Huang X, Cherny RA, Moir RD, Roher AE, White AR, Cappai R, Masters CL, Tanzi RE, Inestrosa NC, Bush AI (2002) Metalloenzyme-like activity of Alzheimer's disease beta-amyloid. Cu-dependent catalytic conversion of dopamine, cholesterol, and biological reducing agents to neurotoxic H(2)O(2). J. Biol. Chem. 277, 40302-40308.
32. Oster T, Pillot T (2010) Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice. Biochim. Biophys. Acta 1801, 791-798.
33. Owens CW, Belcher RV (1965) A colorimetric micro-method for the determination of Glutathione. Biochem. J. 94, 705-711.
34. Panza F, Capurso C, D'Introno A, Colacicco AM, De Candia D, Capurso A, Solfrizzi V (2007) Total cholesterol levels and the risk of mild cognitive impairment and Alzheimer's disease. J. Am. Geriatr. Soc. 55, 133-135.
35. Perry G, Castellani RJ, Hirai K, Smith MA (1998) Reactive oxygen species mediate cellular damage in Alzheimer Disease. J. Alzheimers Dis. 1, 45-55.
36. Poli G, Sottero B, Gargiulo S, Leonarduzzi G (2009) Cholesterol oxidation products in the vascular remodeling due to atherosclerosis. Mol. Aspects Med. 30, 180-189.
37. Puglielli L, Tanzi RE, Kovacs DM (2003) Alzheimer's disease: the cholesterol connection. Nat. Neurosci. 6, 345-351.
38. Querfurth HW, LaFerla FM (2010) Alzheimer's disease. N. Engl. J. Med. 362, 329-344.
39. Rezvani HR, Dedieu S, North S, Belloc F, Rossignol R, Letellier T, de Verneuil H, Taïeb A, Mazurier F (2007) Hypoxia-inducible factor-1alpha, a key factor in the keratinocyte response to UVB exposure. J. Biol. Chem. 282, 16413-16422.
40. Rothman SM, Mattson MP (2010) Adverse stress, hippocampal networks, and Alzheimer's disease. Neuromolecular Med. 12, 56-70.
41. Sakono M, Zako T (2010) Amyloid oligomers: formation and toxicity of Abeta oligomers. FEBS J. 277, 1348-1358.
42. Sarkar S, Das N (2006) Mannosylated liposomal flavonoid in combating age-related ischemia-reperfusion induced oxidative damage in rat brain. Mech. Ageing Dev. 127, 391-397.
43. Schönknecht P, Lütjohann D, Pantel J, Bardenheuer H, Hartmann T, von Bergmann K, Beyreutherd K, Schröder J (2002) Cerebrospinal fluid 24S-hydroxycholesterol is increased in patients with Alzheimer's disease compared to healthy controls. Neurosci. Lett. 324, 83-85.
44. Selkoe DJ (1991) Amyloid protein and Alzheimer's disease. Sci. Am. 265, 68-71.
45. Selkoe DJ (1994) Normal and abnormal biology of the β-amyloid precursor protein. Annu. Rev. Neurosci. 17, 489-517.
46. Smith MA, Zhu X, Tabaton M, Liu G, McKeel DW Jr, Cohen ML, Wang X, Siedlak SL, Dwyer BE, Hayashi T, Nakamura M, Nunomura A, Perry G (2010) Increased iron and free radical generation in preclinical Alzheimer disease and mild cognitive impairment. J. Alzheimers Dis. 19, 363-372.
47. Sottero B, Gamba P, Gargiulo S, Leonarduzzi G, Poli G (2009) Cholesterol oxidation products and disease: an emerging topic of interest in medicinal chemistry. Curr. Med. Chem. 16, 685-705.
48. Sparks DL, Schreurs BG (2003) Trace amounts of copper in water induce beta-amyloid plaques and learning deficits in a rabbit model of Alzheimer's disease. Proc. Natl Acad. Sci. USA 100, 11065-11069.
49. Tamagno E, Aragno M, Parola M, Parola S, Brignardello E, Boccuzzi G, Danni O (2000) NT2 neurons, a classical model for Alzheimer's disease, are highly susceptible to oxidative stress. Neuroreport 11, 1865-1869.
50. Vega GL, Weiner MF, Lipton AM, von Bergmann K, Lütjohann D, Moore C, Svetlik D (2003) Reduction in levels of 24S-hydroxycholesterol by statin treatment in patients with Alzheimer disease. Arch. Neurol. 60, 510-515.
51. Vejux A, Lizard G (2009) Cytotoxic effects of oxysterols associated with human diseases: induction of cell death (apoptosis and/or oncosis), oxidative and inflammatory activities, and phospholipidosis. Mol. Aspects Med. 30, 153-170.
52. Verdier Y, Zarándi M, Penke B (2004) Amyloid beta-peptide interactions with neuronal and glial cell plasma membrane: binding sites and implications for Alzheimer's disease. J. Pept. Sci. 10, 229-248.
53. Zhu X, Su B, Wang X, Smith MA, Perry G (2007a) Causes of oxidative stress in Alzheimer disease. Cell. Mol. Life Sci. 64, 2202-2210.
54. Zhu X, Lee HG, Perry G, Smith MA (2007b) Alzheimer disease, the two-hypothesis: an update. Biochim. Biophys. Acta 1772, 494-502.
55. Zoccarato F, Valente M, Alexandre A (1993) Identification of an NADH plus iron dependent, Ca2+ activated hydrogen peroxide production in synaptosomes. Biochim. Biophys. Acta 1176, 208-214.