Intranasal deferoxamine reverses iron-induced memory deficits and inhibits amyloidogenic APP processing in a transgenic mouse model of Alzheimer's disease

Neurobiology of Aging

Volumn 34, Issue 2, 2013, Pages 562-575

  Guo, Chuang ^a,b   Wang, Tao ^a   Zheng, Wei ^a   Shan, Zhong Yan ^a   Teng, Wei Ping ^a   Wang, Zhan You ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b HEBEI UNITED UNIVERSITY   (China)

Author keywords

amyloid peptide; Alzheimer's disease; Deferoxamine; Iron; Transgenic mouse

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN 695; COPPER; DEFEROXAMINE; IRON; PRESENILIN 1; UNCLASSIFIED DRUG; ZINC;

ALZHEIMER DISEASE; AMNESIA; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CHELATION; COGNITIVE DEFECT; CONTROLLED STUDY; IRON BALANCE; IRON OVERLOAD; LEARNING; MALE; MEMORY CONSOLIDATION; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SPATIAL LEARNING; TRANSGENIC MOUSE;

ADMINISTRATION, INTRANASAL; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CELL LINE, TUMOR; DEFEROXAMINE; DISEASE MODELS, ANIMAL; HUMANS; IRON; IRON CHELATING AGENTS; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; PRESENILIN-1; TREATMENT OUTCOME;

EID: 84869080922     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.05.009     Document Type: Article

References (72)

1. Atwood C.S., Obrenovich M.E., Liu T., Chan H., Perry G., Smith M.A., Martins R.N. Amyloid-beta: a chameleon walking in two worlds: a review of the trophic and toxic properties of amyloid-beta. Brain Res. Brain Res. Rev 2003, 43:1-16.
2. Atwood C.S., Scarpa R.C., Huang X., Moir R.D., Jones W.D., Fairlie D.P., Tanzi R.E., Bush A.I. Characterization of copper interactions with alzheimer amyloid beta peptides: identification of an attomolar-affinity copper binding site on amyloid beta1-42. J. Neurochem 2000, 75:1219-1233.
3. Avramovich-Tirosh Y., Bar-Am O., Amit T., Youdim M.B., Weinreb O. Up-regulation of hypoxia-inducible factor (HIF)-1α and HIF-target genes in cortical neurons by the novel multifunctional iron chelator anti-Alzheimer drug, M30. Curr. Alzheimer Res 2010, 7:300-306.
4. Avramovich-Tirosh Y., Reznichenko L., Mit T., Zheng H., Fridkin M., Weinreb O., Mandel S., Youdim M.B. Neurorescue activity, APP regulation and amyloid-beta peptide reduction by novel multi-functional brain permeable iron- chelating- antioxidants, M-30 and green tea polyphenol, EGCG. Curr. Alzheimer Res 2007, 4:403-411.
5. Bandyopadhyay S., Hartley D.M., Cahill C.M., Lahiri D.K., Chattopadhyay N., Rogers J.T. Interleukin-1α stimulates non-amyloidogenic pathway by α-secretase (ADAM-10 and ADAM-17) cleavage of APP in human astrocytic cells involving p38 MAP kinase. J. Neurosci. Res 2006, 84:106-118.
6. Bodles A.M., Barger S.W. Secreted beta-amyloid precursor protein activates microglia via JNK and p38-MAPK. Neurobiol. Aging 2005, 26:9-16.
7. Bush A.I. The metallobiology of Alzheimer's disease. Trends Neurosci 2003, 26:207-214.
8. Bush A.I., Tanzi R.E. Therapeutics for Alzheimer's disease based on the metal hypothesis. Neurotherapeutics 2008, 5:421-432.
9. Castellani R.J., Honda K., Zhu X., Cash A.D., Nunomura A., Perry G., Smith M.A. Contribution of redox-active iron and copper to oxidative damage in Alzheimer disease. Ageing Res. Rev 2004, 3:319-326.
10. Chaston T.B., Richardson D.R. Iron chelators for the treatment of iron overload disease: Relationship between structure, redox activity, and toxicity. Am. J. Hematol 2003, 73:200-210.
11. Cherny R.A., Atwood C.S., Xilinas M.E., Gray D.N., Jones W.D., McLean C.A., Barnham K.J., Volitakis I., Fraser F.W., Kim Y., Huang X., Goldstein L.E., Moir R.D., Lim J.T., Beyreuther K., Zheng H., Tanzi R.E., Masters C.L., Bush A.I. Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 2001, 30:665-676.
12. Cherny R.A., Legg J.T., McLean C.A., Fairlie D.P., Huang X., Atwood C.S., Beyreuther K., Tanzi R.E., Masters C.L., Bush A.I. Aqueous dissolution of Alzheimer's disease Abeta amyloid deposits by biometal depletion. J. Biol. Chem 1999, 274:23223-23228.
13. Cho H.H., Cahill C.M., Vanderburg C.R., Scherzer C.R., Wang B., Huang X., Rogers J.T. Selective translational control of the Alzheimer amyloid precursor protein transcript by iron regulatory protein-1. J. Biol. Chem 2010, 285:31217-31232.
14. Crapper McLachlan D.R., Dalton A.J., Kruck T.P., Bell M.Y., Smith W.L., Kalow W., Andrews D.F. Intramuscular desferrioxamine in patients with Alzheimer's disease. Lancet 1991, 337:1304-1308.
15. Crowe A., Morgan E.H. Effects of chelators on iron uptake and release by the brain in the rat. Neurochem. Res 1994, 19:71-76.
16. Crowe A., Morgan E.H. Iron and copper interact during their uptake and deposition in the brain and other organs of developing rats exposed to dietary excess of the two metals. J. Nutr 1996, 126:183-194.
17. Cuajungco M.P., Fagét K.Y., Huang X., Tanzi R.E., Bush A.I. Metal chelation as a potential therapy for Alzheimer's disease. Ann. N. Y. Acad. Sci 2000, 920:292-304.
18. De Lima M.N., Dias C.P., Torres J.P., Dornelles A., Garcia V.A., Scalco F.S., Guimarães M.R., Petry R.C., Bromberg E., Constantino L., Budni P., Dal-Pizzol F., Schröder N. Reversion of age-related recognition memory impairment by iron chelation in rats. Neurobiol. Aging 2008, 29:1052-1059.
19. Esch F.S., Keim P.S., Beattie E.C., Blacher R.W., Culwell A.R., Oltersdorf T., McClure D., Ward P.J. Cleavage of amyloid beta peptide during constitutive processing of its precursor. Science 1990, 248:1122-1124.
20. Fox P.L. The copper-iron chronicles: the story of an intimate relationship. Biometals 2003, 16:9-40.
21. Freedman M.H., Boyden M., Taylor M., Skarf B. Neurotoxicity associated with deferoxamine therapy. Toxicology 1988, 49:283-290.
22. 125I-NGF to the brain via the olfactory route. Drug Deliv 1997, 4:87-92.
23. Gunshin H., Mackenzie B., Berger U.V., Gunshin Y., Romero M.F., Boron W.F., Nussberger S., Gollan J.L., Hediger M.A. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 1997, 388:482-488.
24. Haass C., Koo E.H., Mellon A., Hung A.Y., Selkoe D.J. Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 1992, 357:500-503.
25. Hamrick S.E., McQuillen P.S., Jiang X., Mu D., Madan A., Ferriero D.M. A role for hypoxia-inducible factor-1alpha in desferoxamine neuroprotection. Neurosci. Lett 2005, 379:96-100.
26. Hanson L.R., Fine J.M., Renner D.B., Svitak A.L., Burns R.B., Nguyen T.M., Tuttle N.J., Marti D.L., Panter S.S., Frey W.H. Intranasal delivery of deferoxamine reduces spatial memory loss in APP/PS1 mice. Drug Deliv. Transl. Res 2012, 10.1007/s13346-011-0050-2.
27. Hanson L.R., Roeytenberg A., Martinez P.M., Coppes V.G., Sweet D.C., Rao R.J., Marti D.L., Hoekman J.D., Matthews R.B., Frey W.H., Panter S.S. Intranasal deferoxamine provides increased brain exposure and significant protection in rat ischemic stroke. J. Pharmacol. Exp. Ther 2009, 330:679-686.
28. 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.
29. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992, 256:184-185.
30. House E., Collingwood J., Khan A., Korchazkina O., Berthon G., Exley C. Aluminium, iron, zinc and copper influence the in vitro formation of amyloid fibrils of Abeta42 in a manner which may have consequences for metal chelation therapy in Alzheimer's disease. J. Alzheimers Dis 2004, 6:291-301.
31. Jiang D., Li X., Williams R., Patel S., Men L., Wang Y., Zhou F. Ternary complexes of iron, amyloid-beta, and nitrilotriacetic acid: binding affinities, redox properties, and relevance to iron-induced oxidative stress in Alzheimer's disease. Biochemistry 2009, 48:7939-7947.
32. Lee M.S., Kao S.C., Lemere C.A., Xia W., Tseng H.C., Zhou Y., Neve R., Ahlijanian M.K., Tsai L.H. APP processing is regulated by cytoplasmic phosphorylation. J. Cell Biol 2003, 163:83-95.
33. Leskovjan A.C., Kretlow A., Lanzirotti A., Barrea R., Vogt S., Miller L.M. Increased brain iron coincides with early plaque formation in a mouse model of Alzheimer's disease. NeuroImage 2011, 5:32-38.
34. Lindnér P., Naredi P., Peterson A., Hafström L. Influence of hepatic artery occlusion and desferrioxamine on liver-tumour growth. Int. J. Cancer 1995, 63:592-596.
35. Lovell M.A., Robertson J.D., Teesdale W.J., Campbell J.L., Markesbery W.R. Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci 1998, 158:47-52.
36. Lovell M.A., Xiong S., Xie C., Davies P., Markesbery W.R. Induction of hyperphosphorylated tau in primary rat cortical neuron cultures mediated by oxidative stress and glycogen synthase kinase-3. J. Alzheimers Dis 2004, 6:659-671.
37. May P.M., Bulman R. The present status of chelating agents in medicine. Prog. J. Med. Chem 1983, 20:225-336.
38. Maynard C.J., Cappai R., Volitakis I., Laughton K.M., Masters C.L., Bush A.I., Li Q.X. Chronic exposure to high levels of zinc or copper has little effect on brain metal homeostasis or Abeta accumulation in transgenic APP-C100 mice. Cell. Mol. Neurobiol 2009, 29:757-767.
39. Mills E., Dong A., Wang F., Xu H. Mechanisms of brain iron transport: insight into neurodegeneration and CNS disorders. Future. J. Med. Chem 2010, 2:51-64.
40. Molina-Jijón E., Zarco-Márquez G., Medina-Campos O.N., Zataraín-Barrón Z.L., Hernández-Pando R., Pinzón E., Zavaleta R.M., Tapia E., Pedraza-Chaverri J. Deferoxamine pretreatment prevents Cr(VI)-induced nephrotoxicity and oxidant stress: Role of Cr(VI) chelation. Toxicology 2012, 291:93-101.
41. Moreira P.I., Sayre L.M., Zhu X., Nunomura A., Smith M.A., Perry G. Detection and localization of markers of oxidative stress by in situ methods: application in the study of Alzheimer disease. Methods Mol. Biol 2010, 610:419-434.
42. Morse L.J., Payton S.M., Cuny G.D., Rogers J.T. FDA-preapproved drugs targeted to the translational regulation and processing of the amyloid precursor protein. J. Mol. Neurosci 2004, 24:129-136.
43. Newhouse I., Clement D., Lai C. Effects of iron supplementation and discontinuation on serum copper, zinc, calcium and magnesium levels in women. Med. Sci. Sports Exer 1993, 25:562-571.
44. Perez V.P., de Lima M.N., da Silva R.S., Dornelles A.S., Vedana G., Bogo M.R., Bonan C.D., Schröder N. Iron leads to memory impairment that is associated with a decrease in acetylcholinesterase pathways. Curr. Neurovasc Res 2010, 7:15-22.
45. Praticò D., Delanty N. Oxidative injury in diseases of the central nervous system: focus on Alzheimer's disease. Am. J. Med 2000, 109:577-585.
46. Robson K.J., Lehmann D.J., Wimhurst V.L., Livesey K.J., Combrinck M., Merryweather-Clarke A.T., Warden D.R., Smith A.D. Synergy between the C2 allele of transferrin and the C282Y allele of the haemochromatosis gene (HFE) as risk factors for developing Alzheimer's disease. J. Med. Genet 2004, 41:261-265.
47. Rogers J.T., Bush A.I., Cho H.H., Smith D.H., Thomson A.M., Friedlich A.L., Lahiri D.K., Leedman P.J., Huang X., Cahill C.M. Iron and the translation of the amyloid precursor protein (APP) and ferritin mRNAs: riboregulation against neural oxidative damage in Alzheimer's disease. Biochem. Soc. Trans 2008, 36:1282-1287.
48. Rogers J.T., Lahiri D.K. Metal and inflammatory targets for Alzheimer's disease. Curr. Drug Targets 2004, 5:535-551.
49. Rogers J.T., Randall J.D., Cahill C.M., Eder P.S., Huang X., Gunshin H., Leiter L., McPhee J., Sarang S.S., Utsuki T., Greig N.H., Lahiri D.K., Tanzi R.E., Bush A.I., Giordano T., Gullans S.R. An iron-responsive element type II in the 5'-untranslated region of the Alzheimer's amyloid precursor protein transcript. J. Biol. Chem 2002, 277:45518-45528.
50. Savory J., Huang Y., Wills M.R., Herman M.M. Reversal by desferrioxamine of tau protein aggregates following two days of treatment in aluminum-induced neurofibrillary degeneration in rabbit: implications for clinical trials in Alzheimer's disease. Neurotoxicology 1998, 19:209-214.
51. Sayre L.M., Smith M.A., Perry G. Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr. Med. Chem 2001, 8:721-738.
52. Schäfer S., Pajonk F.G., Multhaup G., Bayer T.A. Copper and clioquinol treatment in young APP transgenic and wild-type mice: effects on life expectancy, body weight, and metal-ion levels. J. Mol. Med 2007, 85:405-413.
53. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron 1991, 6:487-498.
54. Shachar D.B., Kahana N., Kampel V., Warshawsky A., Youdim M.B. Neuroprotection by a novel brain permeable iron chelator, VK-28, against 6-hydroxydopamine lesion in rats. Neuropharmacology 2004, 46:254-263.
55. Shoji M., Golde T.E., Ghiso J., Cheung T.T., Estus S., Shaffer L.M., Cai X.D., McKay D.M., Tintner R., Frangione B., et al. Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science 1992, 258:126-129.
56. Smith M.A., Hirai K., Hsiao K., Pappolla M.A., Harris P.L., Siedlak S.L., Tabaton M., Perry G. Amyloid-beta deposition in Alzheimer transgenic mice is associated with oxidative stress. J. Neurochem 1998, 70:2212-2215.
57. Sobotka T.J., Whittaker P., Sobotka J.M., Brodie R.E., Quander D.Y., Robl M., Bryant M., Barton C.N. Neurobehavioral dysfunctions associated with dietary iron overload. Physiol. Behav 1996, 59:213-219.
58. Strozyk D., Launer L.J., Adlard P.A., Cherny R.A., Tsatsanis A., Volitakis I., Blennow K., Petrovitch H., White L.R., Bush A.I. Zinc and copper modulate Alzheimer Abeta levels in human cerebrospinal fluid. Neurobiol. Aging 2009, 30:1069-1077.
59. El Tannir El Tayara N., Delatour B., Le Cudennec C., Guégan M., Volk A., Dhenain M. Age-related evolution of amyloid burden, iron load, and MR relaxation times in a transgenic mouse model of Alzheimer's disease. Neurobiol. Dis 2006, 22:199-208.
60. Treiber C., Simons A., Strauss M., Hafner M., Cappai R., Bayer T.A., Multhaup G. Clioquinol mediates copper uptake and counteracts copper efflux activities of the amyloid precursor protein of Alzheimer's disease. J. Biol. Chem 2004, 279:51958-51964.
61. Unger E.L., Beard J.L., Jones B.C. Iron regulation in C57BLI6 and DBA/2 mice subjected to iron overload. Nutr. Neurosci 2007, 10:89-95.
62. Venti A., Giordano T., Eder P., Bush A.I., Lahiri D.K., Greig N.H., Rogers J.T. The integrated role of desferrioxamine and phenserine targeted to an iron-responsive element in the APP-mRNA 5'-untranslated region. Ann. N. Y. Acad. Sci 2004, 1035:34-48.
63. Waggoner D.J., Bartnikas T.B., Gitlin J.D. The role of copper in neurodegenerative disease. Neurobiol. Dis 1999, 6:221-230.
64. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
65. Wang X., Zheng W., Xie J.W., Wang T., Wang S.L., Teng W.P., Wang Z.Y. Insulin deficiency exacerbates cerebral amyloidosis and behavioral deficits in an Alzheimer transgenic mouse model. Mol. Neurodegener 2010, 5:46.
66. Whitnall M., Richardson D.R. Iron: a new target for pharmacological intervention in neurodegenerative diseases. Semin. Pediatr. Neurol 2006, 13:186-197.
67. Winterbourn C.C. Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicol. Lett 1995, 82-83:969-974.
68. Yu S., West C.E., Beynen A.C. Increasing intakes of iron reduce status, absorption and biliary excretion of copper in rats. Br. J. Nutr 1994, 71:887-895.
69. Zecca L., Youdim M.B., Riederer P., Connor J.R., Crichton R.R. Iron, brain ageing and neurodegenerative disorders. Nat. Rev. Neurosci 2004, 5:863-873.
70. Zhang L.H., Wang X., Zheng Z.H., Ren H., Stoltenberg M., Danscher G., Huang L., Rong M., Wang Z.Y. Altered expression and distribution of zinc transporters in APP/PS1 transgenic mouse brain. Neurobiol. Aging 2010, 31:74-87.
71. Zheng W., Xin N., Chi Z.H., Zhao B.L., Zhang J., Li J.Y., Wang Z.Y. Divalent metal transporter 1 is involved in amyloid precursor protein processing and Abeta generation. FASEB J 2009, 23:4207-4217.
72. Zhu W.Z., Zhong W.D., Wang W., Zhan C.J., Wang C.Y., Qi J.P., Wang J.Z., Lei T. Quantitative MR phase-corrected imaging to investigate increased brain iron deposition of patients with Alzheimer disease. Radiology 2009, 253:497-504.