An okadaic acid-induced model of tauopathy and cognitive deficiency

Brain Research

Volumn 1359, Issue , 2010, Pages 233-246

  Zhang, Zhang ^a   Simpkins, James W ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Alzheimer's disease; Cognitive deficiency; Neurofibrillary tangles; Oxidative stress; Tau phosphorylation; Tauopathy

Indexed keywords

CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3BETA; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN P25; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN CORTEX; COGNITIVE DEFECT; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISEASE MODEL; FEMALE; HIPPOCAMPUS; LEARNING; LIPID PEROXIDATION; MAZE TEST; MEMORY; MICROINJECTION; MOTOR PERFORMANCE; NEUROPATHOLOGY; NONHUMAN; OVARIECTOMY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN PHOSPHORYLATION; RAT; ROTAROD TEST; SPATIAL LEARNING; TAUOPATHY;

ALZHEIMER DISEASE; ANIMALS; BLOTTING, WESTERN; BRAIN; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FEMALE; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAVENTRICULAR; MAZE LEARNING; NEUROFIBRILLARY TANGLES; OKADAIC ACID; OVARIECTOMY; OXIDATIVE STRESS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; TAUOPATHIES;

RATTUS;

EID: 77958001015     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.08.077     Document Type: Article

References (71)

1. S. Abrahams, A. Pickering, C.E. Polkey, and R.G. Morris Spatial memory deficits in patients with unilateral damage to the right hippocampal formation Neuropsychologia 35 1997 11 24
2. M.K. Ahlijanian, N.X. Barrezueta, R.D. Williams, A. Jakowski, K.P. Kowsz, S. McCarthy, T. Coskran, A. Carlo, P.A. Seymour, J.E. Burkhardt, R.B. Nelson, and J.D. McNeish Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5 Proc. Natl. Acad. Sci. U. S. A. 97 2000 2910 2915
3. M. Alvarez-de-la-Rosa, I. Silva, J. Nilsen, M.M. Perez, L.M. Garcia-Segura, J. Avila, and F. Naftolin Estradiol prevents neural tau hyperphosphorylation characteristic of Alzheimer's disease Ann. N. Y. Acad. Sci. 1052 2005 210 224
4. T. Arendt, M. Holzer, M.K. Bruckner, C. Janke, and U. Gartner The use of okadaic acid in vivo and the induction of molecular changes typical for Alzheimer's disease Neuroscience 85 1998 1337 1340
5. T. Arendt, M. Holzer, R. Fruth, M.K. Bruckner, and U. Gartner Phosphorylation of tau, abeta-formation, and apoptosis after in vivo inhibition of PP-1 and PP-2A Neurobiol. Aging 19 1998 3 13
6. P.V. Arriagada, J.H. Growdon, E.T. Hedley-Whyte, and B.T. Hyman Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease Neurology 42 1992 631 639
7. J. Avila, J.J. Lucas, M. Perez, and F. Hernandez Role of tau protein in both physiological and pathological conditions Physiol. Rev. 84 2004 361 384
8. J. Baudier, and R.D. Cole Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalyzed by a calcium/calmodulin-dependent kinase and modulated by phospholipids J. Biol. Chem. 262 1987 17577 17583
9. M.L. Billingsley, and R.L. Kincaid Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration Biochem. J. 323 Pt 3 1997 577 591
10. V.D. Bohbot, M. Kalina, K. Stepankova, N. Spackova, M. Petrides, and L. Nadel Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex Neuropsychologia 36 1998 1217 1238
11. R. Brandt, M. Hundelt, and N. Shahani Tau alteration and neuronal degeneration in tauopathies: mechanisms and models Biochim. Biophys. Acta 1739 2005 331 354
12. R.J. Castellani, H.G. Lee, X. Zhu, G. Perry, and M.A. Smith Alzheimer disease pathology as a host response J. Neuropathol. Exp. Neurol. 67 2008 523 531
13. I. Correas, J. Diaz-Nido, and J. Avila Microtubule-associated protein tau is phosphorylated by protein kinase C on its tubulin binding domain J. Biol. Chem. 267 1992 15721 15728
14. F. Devred, P. Barbier, S. Douillard, O. Monasterio, J.M. Andreu, and V. Peyrot Tau induces ring and microtubule formation from alphabeta-tubulin dimers under nonassembly conditions Biochemistry 43 2004 10520 10531
15. G. Drewes, B. Lichtenberg-Kraag, F. Doring, E.M. Mandelkow, J. Biernat, J. Goris, M. Doree, and E. Mandelkow Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state EMBO J. 11 1992 2131 2138
16. K. Duff, and E. Planel Untangling memory deficits Nat. Med. 11 2005 826 827
17. C.M. Filley Alzheimer's disease in women Am. J. Obstet. Gynecol. 176 1997 1 7
18. M. Goedert, M.G. Spillantini, R. Jakes, D. Rutherford, and R.A. Crowther Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease Neuron 3 1989 519 526
19. M. Goedert, R. Jakes, and E. Vanmechelen Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205 Neurosci. Lett. 189 1995 167 169
20. C.X. Gong, I. Grundke-Iqbal, Z. Damuni, and K. Iqbal Dephosphorylation of microtubule-associated protein tau by protein phosphatase-1 and -2C and its implication in Alzheimer disease FEBS Lett. 341 1994 94 98
21. C.X. Gong, I. Grundke-Iqbal, and K. Iqbal Dephosphorylation of Alzheimer's disease abnormally phosphorylated tau by protein phosphatase-2A Neuroscience 61 1994 765 772
22. C.X. Gong, T.J. Singh, I. Grundke-Iqbal, and K. Iqbal Alzheimer's disease abnormally phosphorylated tau is dephosphorylated by protein phosphatase-2B (calcineurin) J. Neurochem. 62 1994 803 806
23. C.X. Gong, F. Liu, I. Grundke-Iqbal, and K. Iqbal Dysregulation of protein phosphorylation/dephosphorylation in Alzheimer's disease: a therapeutic target J. Biomed. Biotechnol. 2006 2006 31825
24. C.A. Grimes, and R.S. Jope The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling Prog. Neurobiol. 65 2001 391 426
25. I. Grundke-Iqbal, K. Iqbal, M. Quinlan, Y.C. Tung, M.S. Zaidi, and H.M. Wisniewski Microtubule-associated protein tau. A component of Alzheimer paired helical filaments J. Biol. Chem. 261 1986 6084 6089
26. I. Grundke-Iqbal, K. Iqbal, Y.C. Tung, M. Quinlan, H.M. Wisniewski, and L.I. Binder Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology Proc. Natl. Acad. Sci. U. S. A. 83 1986 4913 4917
27. D.P. Hanger, K. Hughes, J.R. Woodgett, J.P. Brion, and B.H. Anderton Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase Neurosci. Lett. 147 1992 58 62
28. J. He, Y. Yang, H. Xu, X. Zhang, and X.M. Li Olanzapine attenuates the okadaic acid-induced spatial memory impairment and hippocampal cell death in rats Neuropsychopharmacology 30 2005 1511 1520
29. F. Hernandez, and J. Avila Tauopathies Cell. Mol. Life Sci. 64 2007 2219 2233
30. K. Ishiguro, A. Shiratsuchi, S. Sato, A. Omori, M. Arioka, S. Kobayashi, T. Uchida, and K. Imahori Glycogen synthase kinase 3 beta is identical to tau protein kinase I generating several epitopes of paired helical filaments FEBS Lett. 325 1993 167 172
31. G.V. Johnson, and W.H. Stoothoff Tau phosphorylation in neuronal cell function and dysfunction J. Cell Sci. 117 2004 5721 5729
32. G. Lace, G.M. Savva, G. Forster, R. de Silva, C. Brayne, F.E. Matthews, J.J. Barclay, L. Dakin, P.G. Ince, S.B. Wharton on behalf of MRC-CFAS Hippocampal tau pathology is related to neuroanatomical connections: an ageing population-based study Brain 132 2009 1324 1334
33. H. Li, K. Matsumoto, and H. Watanabe Different effects of unilateral and bilateral hippocampal lesions in rats on the performance of radial maze and odor-paired associate tasks Brain Res. Bull. 48 1999 113 119
34. C.F. Lin, C.L. Chen, C.W. Chiang, M.S. Jan, W.C. Huang, and Y.S. Lin GSK-3beta acts downstream of PP2A and the PI 3-kinase-akt pathway, and upstream of caspase-2 in ceramide-induced mitochondrial apoptosis J. Cell Sci. 120 2007 2935 2943
35. F. Liu, I. Grundke-Iqbal, K. Iqbal, and C.X. Gong Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation Eur. J. Neurosci. 22 2005 1942 1950
36. M. Liu, S. Choi, G.D. Cuny, K. Ding, B.C. Dobson, M.A. Glicksman, K. Auerbach, and R.L. Stein Kinetic studies of Cdk5/p25 kinase: phosphorylation of tau and complex inhibition by two prototype inhibitors Biochemistry 47 2008 8367 8377
37. S. Lovestone, and C.H. Reynolds The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes Neuroscience 78 1997 309 324
38. J.J. Lucas, F. Hernandez, P. Gomez-Ramos, M.A. Moran, R. Hen, and J. Avila Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice EMBO J. 20 2001 27 39
39. J.R. Manns, R.O. Hopkins, J.M. Reed, E.G. Kitchener, and L.R. Squire Recognition memory and the human hippocampus Neuron 37 2003 171 180
40. J.R. Manns, R.O. Hopkins, and L.R. Squire Semantic memory and the human hippocampus Neuron 38 2003 127 133
41. W.R. Markesbery, and J.M. Carney Oxidative alterations in Alzheimer's disease Brain Pathol. 9 1999 133 146
42. C.M. Marques, L.O. Caboclo, T.I. da Silva, M.H. Noffs, H. Carrete Jr., K. Lin, J. Lin, A.C. Sakamoto, and E.M. Yacubian Cognitive decline in temporal lobe epilepsy due to unilateral hippocampal sclerosis Epilepsy Behav. 10 2007 477 485
43. M. Morishima-Kawashima, M. Hasegawa, K. Takio, M. Suzuki, H. Yoshida, K. Titani, and Y. Ihara Proline-directed and non-proline-directed phosphorylation of PHF-tau J. Biol. Chem. 270 1995 823 829
44. E. Moser, M.B. Moser, and P. Andersen Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions J. Neurosci. 13 1993 3916 3925
45. M.B. Moser, E.I. Moser, E. Forrest, P. Andersen, and R.G. Morris Spatial learning with a minislab in the dorsal hippocampus Proc. Natl. Acad. Sci. U. S. A. 92 1995 9697 9701
46. A. Mudher, and S. Lovestone Alzheimer's disease-do Tauists and Baptists finally shake hands? Trends Neurosci. 25 2002 22 26
47. L. Nadel The hippocampus and space revisited Hippocampus 1 1991 221 229
48. Z. Nagy, M.M. Esiri, K.A. Jobst, J.H. Morris, E.M. King, B. McDonald, S. Litchfield, A. Smith, L. Barnetson, and A.D. Smith Relative roles of plaques and tangles in the dementia of Alzheimer's disease: correlations using three sets of neuropathological criteria Dementia 6 1995 21 31
49. A. Nunomura, R.J. Castellani, X. Zhu, P.I. Moreira, G. Perry, and M.A. Smith Involvement of oxidative stress in Alzheimer disease J. Neuropathol. Exp. Neurol. 65 2006 631 641
50. G.N. Patrick, L. Zukerberg, M. Nikolic, S. de la Monte, P. Dikkes, and L.H. Tsai Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration Nature 402 1999 615 622
51. H.K. Paudel, J. Lew, Z. Ali, and J.H. Wang Brain proline-directed protein kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments J. Biol. Chem. 268 1993 23512 23518
52. E. Planel, K. Yasutake, S.C. Fujita, and K. Ishiguro Inhibition of protein phosphatase 2A overrides tau protein kinase I/glycogen synthase kinase 3 beta and cyclin-dependent kinase 5 inhibition and results in tau hyperphosphorylation in the hippocampus of starved mouse J. Biol. Chem. 276 2001 34298 34306
53. D. Pratico Evidence of oxidative stress in Alzheimer's disease brain and antioxidant therapy: lights and shadows Ann. N. Y. Acad. Sci. 1147 2008 70 78
54. E.F. Rissman, A.L. Heck, J.E. Leonard, M.A. Shupnik, and J.A. Gustafsson Disruption of estrogen receptor beta gene impairs spatial learning in female mice Proc. Natl. Acad. Sci. U. S. A. 99 2002 3996 4001
55. K. Santacruz, J. Lewis, T. Spires, J. Paulson, L. Kotilinek, M. Ingelsson, A. Guimaraes, M. DeTure, M. Ramsden, E. McGowan, C. Forster, M. Yue, J. Orne, C. Janus, A. Mariash, M. Kuskowski, B. Hyman, M. Hutton, and K.H. Ashe Tau suppression in a neurodegenerative mouse model improves memory function Science 309 2005 476 481
56. L.M. Sayre, D.A. Zelasko, P.L. Harris, G. Perry, R.G. Salomon, and M.A. Smith 4-hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease J. Neurochem. 68 1997 2092 2097
57. S.B. Shelton, and G.V. Johnson Cyclin-dependent kinase-5 in neurodegeneration J. Neurochem. 88 2004 1313 1326
58. M. Singh, J.A. Dykens, and J.W. Simpkins Novel mechanisms for estrogen-induced neuroprotection Exp. Biol. Med. (Maywood) 231 2006 514 521
59. M.A. Smith, C.A. Rottkamp, A. Nunomura, A.K. Raina, and G. Perry Oxidative stress in Alzheimer's disease Biochim. Biophys. Acta 1502 2000 139 144
60. M.L. Steinhilb, D. Dias-Santagata, T.A. Fulga, D.L. Felch, and M.B. Feany Tau phosphorylation sites work in concert to promote neurotoxicity in vivo Mol. Biol. Cell 18 2007 5060 5068
61. L. Sun, S.Y. Liu, X.W. Zhou, X.C. Wang, R. Liu, Q. Wang, and J.Z. Wang Inhibition of protein phosphatase 2A- and protein phosphatase 1-induced tau hyperphosphorylation and impairment of spatial memory retention in rats Neuroscience 118 2003 1175 1182 (Pubitemid 36561203)
62. L.H. Tsai, I. Delalle, V.S. Caviness Jr., T. Chae, and E. Harlow P35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5 Nature 371 1994 419 423
63. T. Uchida, K. Ishiguro, J. Ohnuma, M. Takamatsu, S. Yonekura, and K. Imahori Precursor of cdk5 activator, the 23 kDa subunit of tau protein kinase II: its sequence and developmental change in brain FEBS Lett. 355 1994 35 40 (Pubitemid 24352098)
64. M.D. Weingarten, A.H. Lockwood, S.Y. Hwo, and M.W. Kirschner A protein factor essential for microtubule assembly Proc. Natl. Acad. Sci. U. S. A. 72 1975 1858 1862
65. Y. Wen, S. Yang, R. Liu, A.M. Brun-Zinkernagel, P. Koulen, and J.W. Simpkins Transient cerebral ischemia induces aberrant neuronal cell cycle re-entry and Alzheimer's disease-like tauopathy in female rats J. Biol. Chem. 279 2004 22684 22692
66. Y. Wen, S. Yang, R. Liu, and J.W. Simpkins Transient cerebral ischemia induces site-specific hyperphosphorylation of tau protein Brain Res. 1022 2004 30 38
67. J.R. Woodgett Molecular cloning and expression of glycogen synthase kinase-3/factor A EMBO J. 9 1990 2431 2438
68. S. Wu, A. Sasaki, R. Yoshimoto, Y. Kawahara, T. Manabe, K. Kataoka, M. Asashima, and L. Yuge Neural stem cells improve learning and memory in rats with Alzheimer's disease Pathobiology 75 2008 186 194
69. Z. Zhang, and J.W. Simpkins Okadaic acid induces tau phosphorylation in SH-SY5Y cells in an estrogen-preventable manner Brain Res. 1345 2010 176 181
70. X. Zhu, A.K. Raina, G. Perry, and M.A. Smith Alzheimer's disease: the two-hit hypothesis Lancet Neurol. 3 2004 219 226
71. X. Zhu, H.G. Lee, G. Perry, and M.A. Smith Alzheimer disease, the two-hit hypothesis: an update Biochim. Biophys. Acta 1772 2007 494 502