Deferoxamine inhibits iron induced hippocampal tau phosphorylation in the Alzheimer transgenic mouse brain

Neurochemistry International

Volumn 62, Issue 2, 2013, Pages 165-172

  Guo, Chuang ^a,b   Wang, Pu ^a   Zhong, Man Li ^c   Wang, Tao ^a   Huang, Xue Shi ^a   Li, Jia Yi ^a   Wang, Zhan You ^a  

^a NORTHEASTERN UNIVERSITY   (China)

^b HEBEI UNITED UNIVERSITY   (China)

^c CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Cyclin dependent kinase 5; Deferoxamine; Glycogen synthase kinase 3; Tau

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CYCLIN DEPENDENT KINASE 5; DEFEROXAMINE; GLYCOGEN SYNTHASE KINASE 3BETA; IRON; PRESENILIN 1; TAU PROTEIN; THREONINE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BLOTTING, WESTERN; DEFEROXAMINE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IRON; MALE; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PRESENILIN-1; TAU PROTEINS;

MUS MUSCULUS;

EID: 84871958441     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.12.005     Document Type: Article

References (57)

1. J.C. Augustinack, A. Schneider, E.M. Mandelkow, and B.T. Hyman Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease Acta Neuropathol. 103 2002 26 35
2. K. Baumann, E.M. Mandelkow, J. Biernat, H. Piwnica-Worms, and E. Mandelkow Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5 FEBS Lett. 336 1993 417 424
3. G.T. Bramblett, M. Goedert, R. Jakes, S.E. Merrick, J.Q. Trojanowski, and V.M. Lee Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding Neuron 10 1993 1089 1099
4. J.H. Cho, and G.V. Johnson Primed phosphorylation of tau at Thr231 by glycogen synthase kinase 3beta (GSK3beta) plays a critical role in regulating tau's ability to bind and stabilize microtubules J. Neurochem. 88 2004 349 358
5. G.A. Czapski, M. Gassowska, M. Songin, U.D. Radecka, and J.B. Strosznajder Alterations of cyclin dependent kinase 5 expression and phosphorylation in amyloid precursor protein (APP)-transfected PC12 cells FEBS Lett. 585 2011 1243 1248
6. M.N.M. de Lima, J. Presti-Torres, F. Caldana, M.M. Grazziotin, F.S. Scalco, M.R. Guimaraes, E. Bromberg, S.I.R. Franke, J.A.P. Henriques, and N. Schroder Desferoxamine reverses neonatal iron-induced recognition memory impairment in rats Eur. J. Pharmacol. 570 2007 111 114
7. D.M. de Silva, and S.D. Aust Ferritin and ceruloplasmin in oxidative damage: review and recent findings Can. J. Physiol. Pharmacol. 71 1993 715 720
8. Y. Ding, A. Qiao, Z. Wang, J.S. Goodwin, E.S. Lee, M.L. Block, M. Allsbrook, M.P. McDonald, and G.H. Fan Retinoic acid attenuates beta-amyloid deposition and rescues memory deficits in an Alzheimer's disease transgenic mouse model J. Neurosci. 28 2008 11622 11634
9. J.A. Duce, A. Tsatsanis, M.A. Cater, S.A. James, E. Robb, K. Wikhe, S.L. Leong, K. Perez, T. Johanssen, M.A. Greenough, H.H. Cho, D. Galatis, R.D. Moir, C.L. Masters, C. McLean, R.E. Tanzi, R. Cappai, K.J. Barnham, G.D. Ciccotosto, J.T. Rogers, and A.I. Bush Iron-export ferroxidase activity of beta-amyloid precursor protein is inhibited by zinc in Alzheimer's disease Cell 142 2010 857 867
10. J.T. Egana, C. Zambrano, M.T. Nunez, C. Gonzalez-Billault, and R.B. Maccioni Iron-induced oxidative stress modify tau phosphorylation patterns in hippocampal cell cultures Biometals 16 2003 215 223
11. M.F. Falangola, S.P. Lee, R.A. Nixon, K. Duff, and J.A. Helpern Histological co-localization of iron in Abeta plaques of PS/APP transgenic mice Neurochem. Res. 30 2005 201 205
12. L.L. Fernandez, M. Carmona, M. Portero-Otin, A. Naudi, R. Pamplona, N. Schroder, and I. Ferrer Effects of increased iron intake during the neonatal period on the brain of adult AbetaPP/PS1 transgenic mice J. Alzheimers Dis. 19 2010 1069 1080
13. J.M. Fine, A.M. Baillargeon, D.B. Renner, N.S. Hoerster, J. Tokarev, S. Colton, A. Pelleg, A. Andrews, K.A. Sparley, K.M. Krogh, W.H. Frey, and L.R. Hanson Intranasal deferoxamine improves performance in radial arm water maze, stabilizes HIF-1alpha, and phosphorylates GSK3beta in P301L tau transgenic mice Exp. Brain Res. 219 2012 381 390
14. A. Fredriksson, N. Schroder, P. Eriksson, I. Izquierdo, and T. Archer Maze learning and motor activity deficits in adult mice induced by iron exposure during a critical postnatal period Brain Res. Dev. Brain Res. 119 2000 65 74
15. P.F. Good, D.P. Perl, L.M. Bierer, and J. Schmeidler Selective accumulation of aluminum and iron in the neurofibrillary tangles of Alzheimer's disease: a laser microprobe (LAMMA) study Ann. Neurol. 31 1992 286 292
16. C. Guo, T. Wang, W. Zheng, Z.-Y. Shan, W.-P. Teng, and Z.-Y. Wang Intranasal deferoxamine reverses iron-induced memory deficits and inhibits amyloidogenic APP processing in a transgenic mouse model of Alzheimer's disease Neurobiol. Aging 34 2013 562 575
17. D.P. Hanger, B.H. Anderton, and W. Noble Tau phosphorylation: the therapeutic challenge for neurodegenerative disease Trends Mol. Med. 15 2009 112 119
18. L.R. Hanson, J.M. Fine, D.B. Renner, A.L. Svitak, R.B. Burns, T.M. Nguyen, N.J. Tuttle, D.L. Marti, S. Scott Panter, and W.H.I. Frey Intranasal delivery of deferoxamine reduces spatial memory loss in APP/PS1 mice Drug Deliv. Transl. Res. 2 2012 160 168
19. L.R. Hanson, A. Roeytenberg, P.M. Martinez, V.G. Coppes, D.C. Sweet, R.J. Rao, D.L. Marti, J.D. Hoekman, R.B. Matthews, W.H. Frey 2nd, and S.S. Panter Intranasal deferoxamine provides increased brain exposure and significant protection in rat ischemic stroke J. Pharmacol. Exp. Ther. 330 2009 679 686
20. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
21. J.P. Hu, J.W. Xie, C.Y. Wang, T. Wang, X. Wang, S.L. Wang, W.P. Teng, and Z.Y. Wang Valproate reduces tau phosphorylation via cyclin-dependent kinase 5 and glycogen synthase kinase 3 signaling pathways Brain Res. Bull. 85 2011 194 200
22. Y. Hui, D. Wang, W. Li, L. Zhang, J. Jin, N. Ma, L. Zhou, O. Nakajima, W. Zhao, and X. Gao Long-term overexpression of heme oxygenase 1 promotes tau aggregation in mouse brain by inducing tau phosphorylation J. Alzheimers Dis. 26 2011 299 313
23. K. Iijima, K. Ando, S. Takeda, Y. Satoh, T. Seki, S. Itohara, P. Greengard, Y. Kirino, A.C. Nairn, and T. Suzuki Neuron-specific phosphorylation of Alzheimer's beta-amyloid precursor protein by cyclin-dependent kinase 5 J. Neurochem. 75 2000 1085 1091
24. K. Iqbal, C. Alonso Adel, S. Chen, M.O. Chohan, E. El-Akkad, C.X. Gong, S. Khatoon, B. Li, F. Liu, A. Rahman, H. Tanimukai, and I. Grundke-Iqbal Tau pathology in Alzheimer disease and other tauopathies Biochim. Biophys. Acta 1739 2005 198 210
25. T. Li, C. Hawkes, H.Y. Qureshi, S. Kar, and H.K. Paudel Cyclin-dependent protein kinase 5 primes microtubule-associated protein tau site-specifically for glycogen synthase kinase 3beta Biochemistry 45 2006 3134 3145
26. T. Li, and H.K. Paudel Glycogen synthase kinase 3beta phosphorylates Alzheimer's disease-specific Ser396 of microtubule-associated protein tau by a sequential mechanism Biochemistry 45 2006 3125 3133
27. M.A. Lovell, J.D. Robertson, W.J. Teesdale, J.L. Campbell, and W.R. Markesbery Copper, iron and zinc in Alzheimer's disease senile plaques J. Neurol. Sci. 158 1998 47 52
28. T. Lynch, R.A. Cherny, and A.I. Bush Oxidative processes in Alzheimer's disease: the role of abeta-metal interactions Exp. Gerontol. 35 2000 445 451
29. T. Maas, J. Eidenmuller, and R. Brandt Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments J. Biol. Chem. 275 2000 15733 15740
30. T.M. Malm, H. Iivonen, G. Goldsteins, V. Keksa-Goldsteine, T. Ahtoniemi, K. Kanninen, A. Salminen, S. Auriola, T. Van Groen, H. Tanila, and J. Koistinaho Pyrrolidine dithiocarbamate activates Akt and improves spatial learning in APP/PS1 mice without affecting beta-amyloid burden J. Neurosci. 27 2007 3712 3721
31. E.M. Mandelkow, J. Biernat, G. Drewes, N. Gustke, B. Trinczek, and E. Mandelkow Tau domains, phosphorylation, and interactions with microtubules Neurobiol. Aging 16 1995 355 362 discussion 362-353
32. D.R.C. McLachlan, T.P.A. Kruck, W. Kalow, D.F. Andrews, A.J. Dalton, M.Y. Bell, and W.L. Smith Intramuscular desferrioxamine in patients with Alzheimer's disease Lancet 337 1991 1304 1308
33. H. Murayama, R.W. Shin, J. Higuchi, S. Shibuya, T. Muramoto, and T. Kitamoto Interaction of aluminum with PHFtau in Alzheimer's disease neurofibrillary degeneration evidenced by desferrioxamine-assisted chelating autoclave method Am. J. Pathol. 155 1999 877 885
34. K.E. Plant, E. Anderson, N. Simecek, R. Brown, S. Forster, J. Spinks, N. Toms, G.G. Gibson, J. Lyon, and N. Plant The neuroprotective action of the mood stabilizing drugs lithium chloride and sodium valproate is mediated through the up-regulation of the homeodomain protein Six1 Toxicol. Appl. Pharmacol. 235 2009 124 134
35. F. Plattner, M. Angelo, and K.P. Giese The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation J. Biol. Chem. 281 2006 25457 25465
36. M.A. Reger, G.S. Watson, P.S. Green, L.D. Baker, B. Cholerton, M.A. Fishel, S.R. Plymate, M.M. Cherrier, G.D. Schellenberg, W.H. Frey 2nd, and S. Craft Intranasal insulin administration dose-dependently modulates verbal memory and plasma amyloid-beta in memory-impaired older adults J. Alzheimers Dis. 13 2008 323 331
37. K. Rezai-Zadeh, G.W. Arendash, H. Hou, F. Fernandez, M. Jensen, M. Runfeldt, R.D. Shytle, and J. Tan Green tea epigallocatechin-3-gallate (EGCG) reduces beta-amyloid mediated cognitive impairment and modulates tau pathology in Alzheimer transgenic mice Brain Res. 1214 2008 177 187
38. J. Savory, Y. Huang, M.R. Wills, and M.M. Herman Reversal by desferrioxamine of tau protein aggregates following 2 days of treatment in aluminum-induced neurofibrillary degeneration in rabbit: implications for clinical trials in Alzheimer's disease Neurotoxicology 19 1998 209 214
39. J.F. Schenck, E.A. Zimmerman, Z. Li, S. Adak, A. Saha, R. Tandon, K.M. Fish, C. Belden, R.W. Gillen, A. Barba, D.L. Henderson, W. Neil, and T. O'Keefe High-field magnetic resonance imaging of brain iron in Alzheimer disease Top. Magn. Reson. Imaging 17 2006 41 50
40. L. Sereno, M. Coma, M. Rodriguez, P. Sanchez-Ferrer, M.B. Sanchez, I. Gich, J.M. Agullo, M. Perez, J. Avila, C. Guardia-Laguarta, J. Clarimon, A. Lleo, and T. Gomez-Isla A novel GSK-3beta inhibitor reduces Alzheimer's pathology and rescues neuronal loss in vivo Neurobiol. Dis. 35 2009 359 367
41. R.W. Shin, T.P. Kruck, H. Murayama, and T. Kitamoto A novel trivalent cation chelator Feralex dissociates binding of aluminum and iron associated with hyperphosphorylated tau of Alzheimer's disease Brain Res. 961 2003 139 146
42. M.A. Smith, K.L. Drew, A. Nunomura, A. Takeda, K. Hirai, X. Zhu, C.S. Atwood, A.K. Raina, C.A. Rottkamp, L.M. Sayre, R.P. Friedland, and G. Perry Amyloid-beta, tau alterations and mitochondrial dysfunction in Alzheimer disease: the chickens or the eggs? Neurochem. Int. 40 2002 527 531
43. M.A. Smith, P.L. Harris, L.M. Sayre, and G. Perry Iron accumulation in Alzheimer disease is a source of redox-generated free radicals Proc. Natl. Acad. Sci. USA 94 1997 9866 9868
44. M.A. Smith, X. Zhu, M. Tabaton, G. Liu, D.W. McKeel Jr., M.L. Cohen, X. Wang, S.L. Siedlak, B.E. Dwyer, T. Hayashi, M. Nakamura, A. Nunomura, and G. Perry Increased iron and free radical generation in preclinical Alzheimer disease and mild cognitive impairment J. Alzheimers Dis. 19 2010 363 372
45. T.J. Sobotka, P. Whittaker, J.M. Sobotka, R.E. Brodie, D.Y. Quander, M. Robl, M. Bryant, and C.N. Barton Neurobehavioral dysfunctions associated with dietary iron overload Physiol. Behav. 59 1996 213 219
46. M.G. Spillantini, and M. Goedert Tau protein pathology in neurodegenerative diseases Trends Neurosci. 21 1998 428 433
47. P. Strocchi, A. Pession, and B. Dozza Up-regulation of cDK5/p35 by oxidative stress in human neuroblastoma IMR-32 cells J. Cell. Biochem. 88 2003 758 765
48. S. Turker, E. Onur, and Y. Ozer Nasal route and drug delivery systems Pharm. World Sci. 26 2004 137 142
49. R.M. Uranga, N.M. Giusto, and G.A. Salvador Iron-induced oxidative injury differentially regulates PI3K/Akt/GSK3beta pathway in synaptic endings from adult and aged rats Toxicol. Sci. 111 2009 331 344
50. R. Vulliet, S.M. Halloran, R.K. Braun, A.J. Smith, and G. Lee Proline-directed phosphorylation of human Tau protein J. Biol. Chem. 267 1992 22570 22574
51. D.M. Walsh, I. Klyubin, J.V. Fadeeva, W.K. Cullen, R. Anwyl, M.S. Wolfe, M.J. Rowan, and D.J. Selkoe Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo Nature 416 2002 535 539
52. L. Wan, G. Nie, J. Zhang, and B. Zhao Overexpression of human wild-type amyloid-beta protein precursor decreases the iron content and increases the oxidative stress of neuroblastoma SH-SY5Y cells J. Alzheimers Dis. 30 2012 523 530
53. J.Z. Wang, I. Grundke-Iqbal, and K. Iqbal Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration Eur. J. Neurosci. 25 2007 59 68
54. Y. Wen, E. Planel, M. Herman, H.Y. Figueroa, L. Wang, L. Liu, L.F. Lau, W.H. Yu, and K.E. Duff Interplay between cyclin-dependent kinase 5 and glycogen synthase kinase 3 beta mediated by neuregulin signaling leads to differential effects on tau phosphorylation and amyloid precursor protein processing J. Neurosci. 28 2008 2624 2632
55. A. Yamamoto, R.W. Shin, K. Hasegawa, H. Naiki, H. Sato, F. Yoshimasu, and T. Kitamoto Iron (III) induces aggregation of hyperphosphorylated tau and its reduction to iron (II) reverses the aggregation: implications in the formation of neurofibrillary tangles of Alzheimer's disease J. Neurochem. 82 2002 1137 1147
56. W. Zheng, N. Xin, Z.H. Chi, B.L. Zhao, J. Zhang, J.Y. Li, and Z.Y. Wang Divalent metal transporter 1 is involved in amyloid precursor protein processing and Abeta generation FASEB J. 23 2009 4207 4217
57. X. Zhu, C.A. Rottkamp, H. Boux, A. Takeda, G. Perry, and M.A. Smith Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease J. Neuropathol. Exp. Neurol. 59 2000 880 888