Co-localization of glycogen synthase kinase-3 with neurofibrillary tangles and granulovacuolar degeneration in transgenic mice

American Journal of Pathology

Volumn 163, Issue 3, 2003, Pages 1057-1067

  Ishizawa, Takashi ^a   Sahara, Narahiko ^a   Ishiguro, Koichi ^b   Kersh, Jay ^a   McGowan, Eileen ^a   Lewis, Jada ^a   Hutton, Michael ^a   Dickson, Dennis W ^a   Yen, Shu Hui ^a  

^a MAYO CLINIC   (United States)

^b MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; GLYCOGEN SYNTHASE KINASE 3; TAU PROTEIN;

ADOLESCENT; AGED; ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME LOCALIZATION; IMMUNOHISTOCHEMISTRY; MOUSE; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE DISTRIBUTION; TRANSGENIC MOUSE;

EID: 0042425738     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63465-7     Document Type: Article

References (51)

1. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM: Microtubule-associated protein tau: A component of Alzheimer-paired helical filaments. J Biol Chem 1986, 261:6084-6089
2. Lee VM, Goedert M, Trojanowski JQ: Neurodegenerative tauopathies. Ann Rev Neurosci 2001, 24:1121-1159
3. Ishihara T, Zhang B, Higuchi M, Yoshiyama Y, Trojanowski JQ, Lee VM: Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am J Pathol 2001, 158:555-562
4. Götz J, Chen F, Barmettler R, Nitsch RM: Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem 2001, 276:529-534
5. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, Gwinn-Hardy K, Paul Murphy M, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin WL, Yen SH, Dickson DW, Davies P, Hutton M: Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 2000, 25:402-405
6. Probst A, Götz J, Wiederhold KH, Tolnay M, Mistl C, Jaton AL, Hong M, Ishihara T, Lee VM, Trojanowski JQ, Jakes R, Crowther RA, Spillantini MG, Bürki K, Goedert M: Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol 2000, 99:469-481
7. Spittaels K, Van den Haute C, Van Dorpe J, Bruynseels K, Vandezande K, Laenen I, Geerts H, Mercken M, Sciot R, Van Lommel A, Loos R, Van Leuven F: Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 1999, 155:2153-2165
8. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, Virdee K, Yoshida H, Holzer M, Craxton M, Emson PC, Atzori C, Migheli A, Crowther RA, Ghetti B, Spillantini MG, Goedert M: Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 2002, 2:9340-9351
9. Sahara N, Lewis J, DeTure M, McGowan E, Dickson DW, Hutton M, Yen S-H: Assembly of tau transgenic animals expressing P301L tau: alteration of phosphorylation and solubility. J Neurochem 2002, 83: 1498-1508
10. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, Yen SH, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton M, McGowan E: Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293:1487-1491
11. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP: The prolyl isomerase Pinl restores the function of Alzheimer-associated phosphorylated tau protein. Nature 1999, 399:784-788
12. Zheng-Fischhofer Q, Biernat J, Mandelkow EM, Illenberger S, Godemann R, Mandelkow E: Sequential phosphorylation of tau by glycogen synthase kinase-3β and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical filament-like conformation Eur J Biochem 1998, 252:542-552
13. Jicha GA, Lane E, Vincent I, Otvos L Jr., Hoffmann R, Davies P: A conformation- and phosphorylation-dependent antibody recognizing the paired helical filaments of Alzheimer's disease. J Neurochem 1997, 69:2087-2095
14. Daly NL, Hoffmann R, Otvos L Jr, Craik DJ: Role of phosphorylation in the conformation of tau peptides implicated in Alzheimer's disease. Biochemistry 2000, 39:9039-9046
15. Reynolds CH, Betts JC, Blackstock WP, Nebreda AR, Adnerton BH: Phosphorylation sites on tau identified by nanoelectrospray mass sprectroscopy: differences in vitro between the mitogen-activated protein kinases ERK2, c-Jun N-terminal kinase and P38, and glycogen synthase kinase 3β. J Neurochem 2000, 74:1587-1595
16. Lee VM, Goedert M, Trojanowski JQ: Neurodegenerative tauopathies. Ann Rev Neurosci 2001, 24:1121-1159
17. Planel E, Sun X, Takashima A: Role of GSK-3β in Alzheimer's disease pathology. Drug Development Res 2002, 56:491-510
18. Singh TJ, Zaidi T, Grundke-Iqbal I, Iqbal K: Modulation of GSK-3-catalyzed phosphorylation of microtubule-associated protein tau by non-proline-dependent protein kinases. FEBS Lett 1995, 358:4-8
19. Liu WK, Williams RT, Hall FL, Dickson DW, Yen SH: Detection of a Cdc2-related kinase associated with Alzheimer-paired helical filaments. Am J Pathol 1995, 146:228-238
20. Yamaguchi H, Ishiguro K, Uchida T, Takashima A, Lemere CA, Imahori K: Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3β and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol 1996, 92:232-241
21. Vincent I, Jicha G, Rosado M, Dickson DW: Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J Neurosci 1997, 17:3588-3598
22. Pei JJ, Tanaka T, Tung YC, Braak E, Iqbal K, Grundke-Iqbal I: Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J Neuropathol Exp Neurol 1997, 56:70-78
23. Pei JJ, Braak E, Braak H, Grundke-Iqbal I, Iqbal K, Winblad B, Cowburn RF: Distribution of active glycogen synthase kinase 3β (GSK-3β) in brains staged for Alzheimer disease neurofibrillary changes. J Neuropathol Exp Neurol 1999, 58:1010-1019
24. Schwab C, DeMaggio AJ, Ghoshal N, Binder LI, Kuret J, McGeer PL: Casein kinase 1δ is associated with pathological accumulation of tau in several neurodegenerative diseases. Neurobiol Aging 2000, 21: 503-510
25. Chin JY, Knowles RB, Schneider A, Drewes G, Mandelkow EM, Hyman BT: Microtubule-affinity regulating kinase (MARK) is tightly associated with neurofibrillary tangles in Alzheimer brain: a fluorescence resonance energy transfer study. J Neuropathol Exp Neurol 2000, 59:966-971
26. Zhu X, Raina AK, Rottkamp CA, Aliev G, Perry G, Boux H, Smith MA: Activation and redistribution of c-jun N-terminal kinase/stress-activated protein kinase in degenerating neurons in Alzheimer's disease. J Neurochem 2001, 76:435-441
27. Borghi R, Giliberto L, Assini A, Delacourte A, Perry G, Smith MA, Strocchi P, Zaccheo D, Tabaton M: Increase of cdk5 is related to neurofibrillary pathology in progressive supranuclear palsy, Neurology 2002, 58:5895-5892
28. Ferrer I, Blanco R, Carmona M, Puig B: Phosphorylated mitogen-activated protein kinase (MAPK/ERK-P), protein kinase of 38 kd (p38-P), stress-activated protein kinase (SAPK/JNK-P), and calcium/calmodulin-dependent kinase II (CaM kinase II) are differentially expressed in tau deposits in neurons and glial cells in tauopathies. J Neural Transm 2001, 108:1397-1415
29. Ferrer I, Blanco R, Carmona M, Ribera R, Goutan E, Puig B, Rey MJ, Cardozo A, Vinals F, Ribalta T: Phosphorylationed map kinase (ERK1, ERK2) expression is associated with early tau deposition in neurons and glial cells, but not with increased nuclear DNA vulnerability and cell death, in Alzheimer's disease, Pick's disease, progressive supranuclear palsy, and corticobasal degeneration. Brain Pathol 2001, 11:144-158
30. Baum L, Hansen L, Masliah E, Saitoh T: Glycogen synthase kinase 3 alteration in Alzheimer disease is related to neurofibrillary tangle formation. Mol Chem Neuropathol 1996, 29:253-261
31. Ferreira A, Lu Q, Orecchio L, Kosik KS: Selective phosphorylation of adult tau isoforms in mature hippocampal neurons exposed to fibrillar Aβ. Mol Cell Neurosci 1997, 9:220-234
32. Takashima A, Honda T, Yasutake K, Michel G, Murayama O, Murayama M, Ishiguro K, Yamaguchi H: Activation of tau protein kinase I/glycogen synthase kinase-3β by amyloid β peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci Res 1998, 31:317-323
33. Liu WK, Le TV, Adamson J, Baker M, Cookson N, Hardy J, Hutton M, Yen SH, Dickson DW: Relationship of the extended tau haplotype to tau biochemistry and neuropathology in progressive supranuclear palsy. Ann Neurol 2001, 50:494-502
34. Yen SH, Dickson DW, Crowe A, Butler M, Shelanski M: Alzheimer's neurofibrillary tangles contain unique epitopes and epitopes in common with the heat-stable microtubule-associated proteins tau and MAP2. Am J Pathol 1987, 126:81-91
35. Mukai F, Ishiguro K, Sano Y, Fujita SC: Alternative splicing isoform of tau protein kinase I/glycogen synthase kinase 3β. J Neurochem 2002, 81:1073-1083
36. Imahori K, Uchida T: Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J Biochem 1997, 121:179-188
37. Anderton BH, Betts J: Blackstock WP, Brion JP, Chapman S, Connell J, Dayanandan R, Gallo JM, Gibb G, Hanger DP, Hutton M, Kardalinou E, Leroy K, Lovestone S, Mack T, Reynolds CH, Van Slegtenhorst M: sites of phosphorylation in tau and factors affecting their regulation. Biochem Soc Symp 2001, 67:73-80
38. Jicha GA, Berenfeld B, Davies P: Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease. J Neurosci Res 1999, 55:713-723
39. Liu W-K, Moore WT, Williams RT, Hall FL, Yen SH: Application of synthetic phospho- and unphospho-peptides to identify phosphorylation sites in a subregion of the tau molecule, which is modified in Alzheimer's disease. J Neurosci Res 1993, 34:371-376
40. Ferrer I, Barrachina M, Puig B: Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol 2002, 104:583-591
41. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K: Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 1998, 4:97-100
42. Leroy K, Boutajangout A, Authelet M, Woodgett JR, Anderton BH, Brion JP: The active form of glycogen synthase kinase-3β is associated with granulovacuolar degeneration in neurons in Alzheimer's disease. Acta Neuropathol 2002, 103:91-99
43. Su JH, Kesslak JP, Head E, Cotman CW: Caspase-cleaved amyloid precursor protein and activated caspase-3 are co-localized in the granules of granulovacuolar degeneration in Alzheimer's disease and Down's syndrome brain. Acta Neuropathoi 2002, 104:1-6
44. Stadelmann C, Deckwerth TL, Srinivasan A, Bancher C, Bruck W, Jellinger K, Lassmann H: Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease: evidence for apoptotic cell death. Am J Pathol 1999, 155:1459-1466
45. Planel E, Yasutake K, Fujita SC, Ishiguro K: Inhibition of protein phosphatase 2A overrides tau protein kinase I/glycogen synthase kinase 3β and cyclin-dependent kinase 5 inhibition and results in tau hyperphosphorylation in the hippocampus of starved mouse. J Biol Chem 2001, 276:34298-34306
46. Sw mice. Neurosci Lett 2001, 299:169-172
47. Demarchi F, Verardo R, Varnum B, Brancolini C, Schneider C: Gas6 anti-apoptotic signaling requires NF-κB activation. J Biol Chem 2001, 276:31738-31744
48. Binder LI, Frankfurter A, Rebhum LI: The distribution of tau in the mammalian central nervous system. J Cell Biol 1985, 101:1371-1378
49. Murai H, Okazaki M, Kikuchi A: Tyrosine dephosphorylation of glycogen synthase kinse-3 is involved in its extracellular signal-dependent inactivation. FEBS Lett 1996, 392:153-160
50. Dajani R, Fraser E, Roe M, Young N, Good V, Dale TC, Pearl LH: Crystal structure of glycogen synthase kinase 3β: Structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 2001, 105:721-732
51. Kim L, Liu J, Kimmel AR: The novel tyrosine kinase ZAK1 activates GSK3 to direct cell fate specification. Cell 1999, 99:399-408