Deferiprone reduces amyloid-β and tau phosphorylation levels but not reactive oxygen species generation in hippocampus of rabbits fed a cholesterol-enriched diet

Journal of Alzheimer's Disease

Volumn 30, Issue 1, 2012, Pages 167-182

  Prasanthi, Jaya R P ^a   Schrag, Matthew ^b,c   Dasari, Bhanu ^a   Marwarha, Gurdeep ^a   Dickson, April ^b   Kirsch, Wolff M ^b   Ghribi, Othman ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; cholesterol; deferiprone; iron; oxidative stress; tau

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; CHOLESTEROL; DEFERIPRONE; REACTIVE OXYGEN METABOLITE; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CONTROLLED STUDY; HIPPOCAMPUS; HYPERCHOLESTEROLEMIA; IRON BLOOD LEVEL; IRON CHELATION; MALE; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION;

EID: 84861525034     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-111346     Document Type: Article

References (82)

1. Cairo G, Recalcati S, Pietrangelo A, Minotti G (2002) The iron regulatory proteins: Targets and modulators of free radical reactions and oxidative damage. Free Radic Biol Med 32, 1237-1243. (Pubitemid 34607627)
2. Kuhn LC, Schulman HM, Ponka P (1990) Iron-transferrin requirements and transferrin receptor expression in proliferating cells. In:Iron Transport and Storage. Ponka P, Schulman HM, Woodworth RC (Eds). CRC Press, Boca Raton, pp. 149-191
3. Jefferies WA, Food MR, Gabathuler R, Rothenberger S, Yamada T, Yasuhara O, McGeer PL (1996) Reactive microglia specifically associated with amyloid plaques in Alzheimer's disease brain tissue express melanotransferrin. Brain Res 712, 122-126. (Pubitemid 26099932)
4. Lee HP, Zhu X, Liu G, Chen SG, Perry G, Smith MA, Lee HG (2010) Divalent metal transporter, iron, and Parkinson's disease: A pathological relationship. Cell Res 20, 397-399.
5. Qian ZM, Wang Q (1998) Expression of iron transport proteins and excessive iron accumulation in the brain in neurodegenerative disorders. Brain Res Brain Res Rev 27, 257-267. (Pubitemid 28389311)
6. Stone JG, Siedlak SL, Tabaton M, Hirano A, Castellani RJ, Santocanale C, Perry G, Smith MA, Zhu X, Lee HG (2011) The cell cycle regulator phosphorylated retinoblastoma protein is associated with tau pathology in several tauopathies. J Neuropathol Exp Neurol 70, 578-587.
7. Swaiman KF (1991) Hallervorden-Spatz syndrome and brain iron metabolism. Arch Neurol 48, 1285-1293.
8. Bonda DJ, Lee HG, Blair JA, Zhu X, Perry G, Smith MA (2011) Role of metal dyshomeostasis in Alzheimer's disease. Metallomics 3, 267-270.
9. Mascitelli L, Pezzetta F, Goldstein MR (2009) Iron, type 2 diabetes mellitus, and Alzheimer's disease. Cell Mol Life Sci 66, 2943.
10. Silvestri L, Camaschella C (2008) A potential pathogenetic role of iron in Alzheimer's disease. J Cell Mol Med 12, 1548-1550.
11. Malecki EA, Connor JR (2002) The case for iron chela-tion and/or antioxidant therapy in Alzheimer's disease. Drug Devel Res 56, 526-530. (Pubitemid 35168328)
12. 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.
13. Smith MA, Harris PL, Sayre LM, Perry G (1997) Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc Natl Acad Sci USA 94, 9866-9868. (Pubitemid 27408156)
14. Bush AI (2003) The metallobiology of Alzheimer's disease. Trends Neurosci 26, 207-214. (Pubitemid 36412003)
15. Okada S (1996) Iron-induced tissue damage and cancer: The role of reactive oxygen species-free radicals. Pathol Int 46, 311-332. (Pubitemid 26230953)
16. Rogers JT, Lahiri DK (2004) Metal and inflammatory targets for Alzheimer's disease. Curr Drug Targets 5, 535-551. (Pubitemid 39004428)
17. Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23, 134-147. (Pubitemid 27217017)
18. Maynard CJ, Bush AI, Masters CL, Cappai R, Li QX (2005) Metals and amyloid-beta in Alzheimer's disease. Int J Exp Pathol 86, 147-159.
19. Stadtman ER, Oliver CN (1991) Metal-catalyzed oxidation of proteins. Physiological consequences. J Biol Chem 266, 2005-2008. (Pubitemid 21909019)
20. Morel I, Cillard J, Lescoat G, Sergent O, Pasdeloup N, Ocak-tan AZ, Abdallah MA, Brissot P, Cillard P (1992) Antioxidant and free radical scavenging activities of the iron chelators pyoverdin and hydroxypyrid-4-ones in iron-loaded hepato-cyte cultures: Comparison of their mechanism of protection with that of desferrioxamine. Free Radic Biol Med 13, 499-508.
21. Suzer T, Coskun E, Demir S, Tahta K (2000) Lipid peroxi-dation and glutathione levels after cortical injection of ferric chlorideinrats: Effectoftrimetazidine and deferoxamine. Res Exp Med (Berl) 199, 223-229. (Pubitemid 30122044)
22. Molina-Holgado F, Gaeta A, Francis PT, Williams RJ, Hider RC (2008) Neuroprotective actions of deferiprone in cultured cortical neurones and SHSY-5Y cells. J Neurochem105, 2466-2476. (Pubitemid 351782272)
23. Matthews AJ, Vercellotti GM, Menchaca HJ, Bloch PH, Michalek VN, Marker PH, Murar J, Buchwald H (1997) Iron and atherosclerosis: Inhibition by the iron chelator deferiprone (L1). J Surg Res 73, 35-40. (Pubitemid 28068315)
24. Ghoti H, Amer J, Winder A, Rachmilewitz E, Fibach E (2007) Oxidative stress in red blood cells, platelets and polymor-phonuclear leukocytes from patients with myelodysplastic syndrome. Eur J Haematol 79, 463-467. (Pubitemid 350126678)
25. Mitchell KM, Dotson AL, Cool KM, Chakrabarty A, Benedict SH, LeVine SM (2007) Deferiprone, an orally deliverable iron chelator, ameliorates experimental autoimmune encephalomyelitis. Mult Scler 13, 1118-1126. (Pubitemid 351541415)
26. Santos AF, Baldanzi G, Leonart MSS, Nascimento AJ (2009) Protective action of deferiprone and deferoxamine in erythrocytes isolated from patients with fj-thalassemias. Rev Bras Hematol Hemoter 31, 444-448.
27. Zorzi G, Zibordi F, Chiapparini L, Bertini E, Russo L, Piga A, Longo F, Garavaglia B, Aquino D, Savoiardo M, Solari A, Nardocci N (2011) Iron-related MRI images in patients with pantothenate kinase-associated neurodegeneration (PKAN) treated with deferiprone: Results of a phase II pilot trial. Mov Disord 26, 1756-1759.
28. Solomon A, Kivipelto M, Wolozin B, Zhou J, Whitmer RA (2009) Midlife serum cholesterol and increased risk of Alzheimer's and vascular dementia three decades later. Dement Geriatr Cogn Disord 28, 75-80.
29. Sparks DL, Kuo YM, Roher A, Martin T, Lukas RJ (2000) Alterations of Alzheimer's disease in the cholesterol-fed rabbit, including vascular inflammation. Preliminary observations. Ann N YAcad Sci 903, 335-344. (Pubitemid 30251574)
30. Woodruff-Pak DS (2008) Animal models of Alzheimer's disease: Therapeutic implications. J Alzheimers Dis 15, 507-521.
31. Ghribi O, Golovko MY, Larsen B, Schrag M, Murphy EJ (2006) Deposition of iron and beta-amyloid plaques is associated with cortical cellular damage in rabbits fed with long-term cholesterol-enriched diets. J Neurochem 99, 438-449. (Pubitemid 44477201)
32. Ghribi O, Larsen B, Schrag M, Herman MM (2006) High cholesterol content in neurons increases BACE, beta-amyloid, and phosphorylated tau levels in rabbit hippocampus. Exp Neurol 200, 460-467. (Pubitemid 44107924)
33. Prasanthi JRP, Dasari B, Marwarha G, Larson T, Chen X, Geiger JD, Ghribi O (2010) Caffeine protects against oxidative stress and Alzheimer's disease-like pathology in rabbit hippocampus induced by cholesterol-enriched diet. Free Radic Biol Med 49, 1212-1220.
34. Pappolla MA, Smith MA, Bryant-Thomas T, Bazan N, Petanceska S, Perry G, Thal LJ, Sano M, Refolo LM (2002) Cholesterol, oxidative stress, and Alzheimer's disease: Expanding the horizons of pathogenesis. Free Radic Biol Med 33, 173-181. (Pubitemid 34775189)
35. Arthur AS, Fergus AH, Lanzino G, Mathys J, Kassell NF, Lee KS (1997) Systemic administration of the iron chelator deferiprone attenuates subarachnoid hemorrhage-induced cerebral vasospasm in the rabbit. Neurosurgery 41, 1385-1391.
36. Barman Balfour JA, Foster RH (1999) Deferiprone: A review of its clinical potential in iron overload in beta-thalassaemia major and other transfusion-dependent diseases. Drugs 58, 553-578. (Pubitemid 29427867)
37. Olivieri NF, Brittenham GM, Matsui D, Berkovitch M, Blendis LM, Cameron RG, McClelland RA, Liu PP, Templeton DM, Koren G (1995) Iron-chelation therapy with oral deferipronein patients with thalassemia major. N Engl J Med 332, 918-922.
38. Lim GP, Calon F, Morihara T, Yang F, Teter B, Ubeda O, Salem N Jr, Frautschy SA, Cole GM (2005) A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci 25, 3032-3040. (Pubitemid 40463537)
39. Ma QL, Lim GP, Harris-White ME, Yang F, Ambegaokar SS, Ubeda OJ, Glabe CG, Teter B, Frautschy SA, Cole GM (2006) Antibodies against beta-amyloid reduce Abeta oligomers, glycogen synthase kinase-3beta activation and tau phosphorylation in vivo and in vitro. J Neurosci Res 83, 374-384. (Pubitemid 43184401)
40. Sharma S, Prasanthi RPJ, Schommer E, Feist G, Ghribi O (2008) Hypercholesterolemia-induced Abeta accumulation in rabbit brain is associated with alteration in IGF-1 signaling. Neurobiol Dis 32, 426-432.
41. Schrag M, Dickson A, Jiffry A, Kirsch D, Vinters HV, Kirsch W (2010) The effect of formalin fixation on the levels of brain transition metals in archived samples. Biometals 23, 1123-1127.
42. Connor JR, Menzies SL, St Martin SM, Mufson EJ (1992) A histochemical study of iron, transferrin, and ferritin in Alzheimer's diseased brains. J Neurosci Res 31, 75-83.
43. Connor JR, Snyder BS, Beard JL, Fine RE, Mufson EJ (1992) Regional distribution of iron and iron-regulatory proteins in the brain in aging and Alzheimer's disease. J Neurosci Res 31, 327-335.
44. Loeffler DA, Connor JR, Juneau PL, Snyder BS, Kanaley L, DeMaggio AJ, Nguyen H, Brickman CM, LeWitt PA (1995) Transferrin and iron in normal, Alzheimer's disease, and Parkinson's disease brain regions. J Neurochem 65, 710-724.
45. Thompson CM, Markesbery WR, Ehmann WD, Mao YX, Vance DE (1988) Regional brain trace-element studies in Alzheimer's disease. Neurotoxicology 9, 1-7.
46. Whitnall M, Richardson DR (2006) Iron: A new target for pharmacological intervention in neurodegenerative diseases. Semin Pediatr Neurol 13, 186-197. (Pubitemid 44709656)
47. Gonzales S, Erario MA, Tomaro ML (2002) Heme oxygenase-1 induction and dependent increase in ferritin. A protective antioxidant stratagem in hemin-treated rat brain. Dev Neurosci 24, 161-168. (Pubitemid 36151446)
48. Torti SV, Kwak EL, Miller SC, Miller LL, Ringold GM, Myambo KB, Young AP, Torti FM (1988) The molecular cloning and characterization of murine ferritin heavy chain, a tumor necrosis factor-inducible gene. J Biol Chem 263, 12638-12644. (Pubitemid 19000447)
49. Duce JA, Tsatsanis A, Cater MA, James SA, Robb E, Wikhe K, Leong SL, Perez K, Johanssen T, Greenough MA, Cho HH, Galatis D, Moir RD, Masters CL, McLean C, Tanzi RE, Cappai R, Barnham KJ, Ciccotosto GD, Rogers JT, Bush AI (2010) Iron-export ferroxidase activity of beta-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 142, 857-867.
50. Rogers JT, Randall JD, Cahill CM, Eder PS, Huang X, Gun-shin H, Leiter L, McPhee J, Sarang SS, Utsuki T, Greig NH, Lahiri DK, Tanzi RE, Bush AI, Giordano T, Gullans SR (2002) An iron-responsive element type II in the 5'-untranslated region of the Alzheimer's amyloid precursor protein transcript. J Biol Chem 277, 45518-45528. (Pubitemid 36159162)
51. Goedert M, Jakes R, Crowther RA, Cohen P, Vanmeche-len E, Vandermeeren M, Cras P (1994) Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: Identification of phosphorylation sites in tau protein. Biochem J 301 (Pt 3), 871-877. (Pubitemid 24239324)
52. Johnson GV, Stoothoff WH (2004) Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117, 5721-5729. (Pubitemid 40123939)
53. Abraha A, Ghoshal N, Gamblin TC, Cryns V, Berry RW, Kuret J, Binder LI (2000) C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J Cell Sci 113 (Pt 21), 3737-3745.
54. Schneider A, Biernat J, von BM, Mandelkow E, Mandelkow EM (1999) Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochemistry 38, 3549-3558.
55. Hughes K, Nikolakaki E, Plyte SE, Totty NF, Woodgett JR (1993) Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J 12, 803-808. (Pubitemid 23073729)
56. Hanger DP, Byers HL, Wray S, Leung KY, Saxton MJ, Seereeram A, Reynolds CH, Ward MA, Anderton BH (2007) Novel phosphorylation sites in tau from Alzheimer brain support a role for casein kinase 1 in disease pathogenesis. J Biol Chem 282, 23645-23654. (Pubitemid 47311907)
57. Sperber BR, Leight S, Goedert M, Lee VM (1995) Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci Lett 197, 149-153.
58. Mainous AG III, Eschenbach SL, Wells BJ, Everett CJ, Gill JM (2005) Cholesterol, transferrin saturation, and the development of dementia and Alzheimer's disease: Results from an 18-year population-based cohort. Fam Med 37, 36-42. (Pubitemid 40094090)
59. Schrag M, Mueller C, Oyoyo U, Smith MA, Kirsch WM (2011) Iron, zinc and copper in the Alzheimer's disease brain: A quantitative meta-analysis. Some insight on the influence of citation bias on scientific opinion. Prog Neurobiol 94, 296-306.
60. Kalaria RN, Sromek SM, Grahovac I, Harik SI (1992) Transferrin receptors of rat and human brain and cerebral microvessels and their status in Alzheimer's disease. Brain Res 585, 87-93.
61. Testa U, Petrini M, Quaranta MT, Pelosi-Testa E, Mastrober-ardino G, Camagna A, Boccoli G, Sargiacomo M, Isacchi G, Cozzi A, et al. (1989) Iron up-modulates the expression of transferrin receptors during monocyte-macrophage maturation. J Biol Chem 264, 13181-13187. (Pubitemid 19194894)
62. Theil EC (1990) Regulation of ferritin and transferrin receptor mRNAs. J Biol Chem 265, 4771-4774.
63. Kakhlon O, Cabantchik ZI (2002) The labile iron pool: Characterization, measurement, and participation in cellular processess. Free Radic Biol Med 33, 1037-1046.
64. Bouton C, Drapier JC (2003) Iron regulatory proteins as NO signal transducers. Sci STKE 2003, e17.
65. Hentze MW, Kuhn LC (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 93, 8175-8182. (Pubitemid 26269529)
66. Iwai K, Drake SK, Wehr NB, Weissman AM, LaVaute T, Minato N, Klausner RD, Levine RL, Rouault TA (1998) Iron-dependent oxidation, ubiquitination, and degradation of iron regulatory protein 2: Implications for degradation of oxidized proteins. Proc Natl Acad Sci USA 95, 4924-4928. (Pubitemid 28208526)
67. Klausner RD, Rouault TA, Harford JB (1993) Regulating the fate of mRNA: The control of cellular iron metabolism. Cell 72, 19-28. (Pubitemid 23029689)
68. Todorich BM, Connor JR (2004) Redox metalsinAlzheimer's disease. Ann N Y Acad Sci 1012, 171-178.
69. Wallander ML, Leibold EA, Eisenstein RS (2006) Molecular control of vertebrate iron homeostasis by iron regulatory proteins. Biochim Biophys Acta 1763, 668-689. (Pubitemid 44189547)
70. Fleming J, Joshi JG (1987) Ferritin: Isolation of aluminum-ferritin complex from brain. Proc Natl Acad Sci USA 84, 7866-7870.
71. Smith MA, Wehr K, Harris PL, Siedlak SL, Connor JR, Perry G (1998) Abnormal localization of iron regulatory protein in Alzheimer's disease. Brain Res 788, 232-236. (Pubitemid 28202166)
72. Cairo G, Tacchini L, Pogliaghi G, Anzon E, Tomasi A, Bernelli-Zazzera A (1995) Induction of ferritin synthesis by oxidative stress. Transcriptional and post-transcriptional regulation by expansion of the "free" iron pool. J Biol Chem 270, 700-703.
73. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S (2010) Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 80, 1895-1903.
74. Ringheim GE, Szczepanik AM (2006) Brain inflammation, cholesterol, and glutamate as interconnected participants in the pathology of Alzheimer's disease. Curr Pharm Des 12, 719-738.
75. Tsuji Y, Miller LL, Miller SC, Torti SV, Torti FM (1991) Tumor necrosis factor-alpha and interleukin 1-alpha regulate transferrin receptor in human diploid fibroblasts. Relationship to the induction of ferritin heavy chain. J Biol Chem 266, 7257-7261. (Pubitemid 21906360)
76. Castellani RJ, Zhu X, Lee HG, Moreira PI, Perry G, Smith MA (2007) Neuropathology and treatment of Alzheimer disease: Did we lose the forest for the trees? Expert Rev Neurother 7, 473-485. (Pubitemid 46743441)
77. Smith MA, Richey PL, Taneda S, Kutty RK, Sayre LM, Mon-nier VM, Perry G (1994) Advanced Maillard reaction end products, free radicals, and protein oxidation in Alzheimer's disease. Ann N YAcad Sci 738, 447-454.
78. Smith MA, Taneda S, Richey PL, Miyata S, Yan SD, Stern D, Sayre LM, Monnier VM, Perry G (1994) Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc Natl Acad Sci USA 91, 5710-5714. (Pubitemid 24174398)
79. Sultana R, Butterfield DA (2010) Role of oxidative stress in the progression of Alzheimer's disease. J Alzheimers Dis 19, 341-353.
80. Bernhardt PV (2007) Coordination chemistry and biology of chelators for the treatment of iron overload disorders. Dalton Trans 3214-3220. (Pubitemid 47457459)
81. Fredenburg AM, Sethi RK, Allen DD, Yokel RA (1996) The pharmacokinetics and blood-brain barrier permeation of the chelators 1, 2 dimethly-, 1, 2 diethyl-, and 1-[ethan-1'ol]-2-methyl-3-hydroxypyridin-4-one in the rat. Toxicology 108, 191-199.
82. Hamilton KO, Stallibrass L, Hassan I, Jin Y, Halleux C, Mackay M (1994) The transport of two iron chelators, des-ferrioxamine B and L1, across Caco-2 monolayers. Br J Haematol86, 851-857. (Pubitemid 24194447)