Immunocytochemistry of tau phosphoserine 413 and tau protein kinase I in Alzheimer pathology

Brain Research

Volumn 737, Issue 1-2, 1996, Pages 119-132

  Shiurba, Robert A ^a,b   Ishiguro, Koichi ^b   Takahashi, Miho ^b   Sato, Kazuki ^b   Spooner, Edward T ^a   Mercken, Marc ^a,b   Yoshida, Rie ^a   Wheelock, Timothy R ^a   Yanagawa, Hiroshi ^b   Imahori, Kazutomo ^b   Nixon, Ralph A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MITSUBISHI KASEI INST OF LIFE SCI   (Japan)

Author keywords

Alzheimer's disease; Glycogen synthase kinase 3 ; Tau protein kinase I

Indexed keywords

PROTEIN KINASE; SERINE; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MALE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0030597165     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/0006-8993(96)00717-2     Document Type: Article

References (58)

1. [1] Arioka, M., Tsukamoto, M., Ishiguro, K., Kato, R., Sato, K., Imahori, K. and Uchida, T., τ protein kinase II is involved in the regulation of the normal phosphorylation state of τ protein, J. Neurochem., 60 (1993) 461-468.
2. [2] Cataldo, A.M., Thayer, C.Y., Bird, E.D., Wheelock, T.R. and Nixon, R.A., Lysosomal proteinase antigens are prominently localized within senile plaques of Alzheimer's disease: evidence for a neuronal origin, Brain Res., 513 (1990) 181-192.
3. [3] Gibson, P.H. and Tomlison, B.E., Numbers of Hirano bodies in the hippocampus of normal and demented people with Alzheimer's disease, J. Neurol. Sci., 33 (1977) 199-206.
4. [4] Goedert, M., Tau protein and the neurofibrillary pathology of Alzheimer's disease, Trends Neurosci., 16 (1993) 460-465.
5. PHF proteins display the same biochemical properties as normal τ, J. Biol. Chem., 267 (1992) 564-569.
6. [6] Hanger, D.P., Hughes, K., Woodgett, J.R., Brion, J.-P. and Anderton, B., 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.
7. [7] Harlow, E. and Lane, D., Antibodies: A Laboratory Manual, Cold Spring Harbor, New York, 1988, pp. 78-79.
8. [8] Hirano, A., Hirano bodies and related neuronal inclusions. Neuropathol. Appl. Neurobiol., 20 (1994) 3-11.
9. [9] Hirano, A., Malamud, N., Elizan, T.S. and Kurland, L.T., Amyotrophic lateral sclerosis and Parkinsonism-dementia complex on Guam, Arch. Neurol., 15 (1966) 35-51.
10. [10] Hoshi, M., Sato, M., Kondo, S., Takashima, A., Noguchi, K., Takahashi, M., Ishiguro, K. and Imahori, K., Different localization of tau protein kinase I/glycogen synthase kinase-3β from glycogen synthase kinase-3α in cerebellum mitochondria, J. Biochem., 118 (1995) 683-685.
11. [11] Hoshi, M., Takashima, A., Noguchi, K., Murayama, M., Sato, M., Kondo, S., Saitoh, Y., Ishiguro, K., Hoshino, T. and Imahori, K., Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase-3β in brain, Proc. Natl. Acad. Sci. USA, 93 (1996) 2719-2713.
12. [12] Hyman, B.T., Kromer, L.J. and Van Hoesen, G.W., A direct demonstration of the perforant pathway terminal zone in Alzheimer's disease using the monoclonal antibody Alz-50, Brain Res., 450 (1988) 392-397.
13. [13] Ishiguro, K., Ihara, Y., Uchida, T. and Imahori, K., A novel tubulin-dependent protein kinase forming a paired helical filament epitope of tau, J. Biochem. (Tokyo), 104 (1988) 319-321.
14. [14] Ishiguro, K., Omori, A., Sato. K., Tomizawa, K.. Imahori, K. and Uchida, T., A serine/threonine proline kinase activity is included in the tau protein kinase fraction forming a paired helical filament epitope, Neurosci. Lett., 128 (1941) 195-198.
15. [15] Ishiguro, K., Omori, A., Takamatsu, M., Sato, K., Arioka, M., Uchida, T. and Imahori, K., Phosphorylation sites on tau by tau protein kinase I, a bovine derived kinase generating an epitope of paired helical filaments, Neurosci Lett., 148 (1992) 202-206.
16. [16] Ishiguro, K., Sato, K., Takamatsu, M., Park, J., Uchida, T. and Imahori, K., Analysis of phosphorylation of tau with antibodies specific for phosphorylation sites, Neurosci. Lett., 202 (1995) 81-84.
17. [17] Ishiguro, K., Shiratsuchi, A., Sato, S., Omori, A., Arioka, M., Kobayashi, S., Uchida, T. and Imahori, K., Glycogen synthase kinase 3β is identical to tau protein kinase I generating several epitopes of paired helical filaments. FEBS Lett., 325 (1993) 167-172.
18. [18] Ishiguro, K., Takamatsu, M., Tomizawa, K., Omori, A., Takahashi, M., Arioka, M., Uchida, T. and Imahori, K., Tau protein kinase I converts normal tau protein into A68-like component of paired helical filaments. J. Biol. Chem., 267 (1992) 10897-10901.
19. [19] Khachaturian, Z.S., Diagnosis of Alzheimer's disease. Arch. Neurol., 42 (1985) 1097-1105.
20. [20] Langui, D., Probst, A. and Ulrich, J., Alzheimer's changes in non-demented and demented patients: a statistical approach to their relationships, Acta Neuropathol. (Berl.), 89 (1995) 57-62.
21. [21] Lovestone, S., Reynolds, C.H., Latimer, D., Davis. D.R., Anderton, B.H., Gallo, J.-M., Hanger, D., Mulot, S., Marquardt, B., Stabel, S., Woodgett, J.R. and Miller, C.C.J., Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells, Curr. Biol., 4 (1994) 1077-1086.
22. [22] Mandelkow, E.-M., Drewes, G., Biernat, J., Gustke, N., Van Lint, J., Vandenheede, J.R. and Mandelkow, E., Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau, FEBS Lett., 314 (1992) 315-321.
23. [23] Mandelkow, E.-M. and Mandelkow, E., Tau as a marker for Alzheimer's disease, Trends Biochem. Sci., 18 (1993) 480-483.
24. [24] Masliah, E., Mallory, M., Hansen, L., DeTeresa, R., Alford, M. and Terry, R., Synaptic and neuritic alterations during the progression of Alzheimer's disease, Neurosci. Lett., 174 (1994) 67-72.
25. [25] Matsuo, E.S., Shin, R.-W., Billingsley, M.L., Van de Voorde, A., O'Connor, M., Trojanowski, J.Q. and Lee, V.M.-Y., Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau, Neuron, 13 (1994) 989-1002.
26. [26] Mercken, M., Vandermeeren, M., Lübke, U., Six, J., Boons, J., Van De Voorde, A., Martin, J.-J. and Gheuens, J., Monoclonal antibodies with selective specificity for Alzheimer Tau are directed against phosphatase-sensitive epitopes, Acta Neuropathol. (Berl.), 84 (1992) 265-272.
27. [27] Mercken, M., Grynspan, F. and Nixon, R.A., Differential sensitivity to proteolysis by brain calpain of adult human tau, fetal human tau and PHF-tau, FEBS Lett., 368 (1995) 10-14.
28. [28] Mirra, S.S., Heyman, A., McKeel, D., Sumi, S.M., Crain, B.J., Brownlee, L.M., Vogel, F.S., Hughes, J.P., van Belle, G. and Berg, L., The consortium to establish a registry for Alzheimer's disease (CERAD). Part II. Standardization of neuropathological assessment of Alzheimer's disease, Neurology, 41 (1991) 479-486.
29. [29] Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Watanabe, H., Titani, K. and Ihara, Y., Proline-directed and non-proline-directed phosphorylation of PHF-tau, J. Biol. Chem., 270 (1995) 823-829.
30. [30] Mulot, S.F.C., Hughes, K., Woodgett, J.R., Anderton, B.H. and Hanger, D.P., PHF-tau from Alzheimer's brain comprises four species on SDS-PAGE which can be mimicked by in vitro phosphorylation of human brain tau by glycogen synthase kinase-3β, FEBS Lett., 349 (1994) 359-364.
31. [31] Nixon, R.A., Saito, K.-I., Grynspan, F., Griffin, W.R., Katayama, S., Honda, T., Mohan, P.S., Shea, T.B. and Beerman, M., Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer's disease, Ann. NY Acad. Sci., 747 (1994) 77-91.
32. [32] Otvos, L. Jr., Feiner, L., Lang, E., Szendrei, G.I., Goedert, M. and Lee, V.M.-Y., Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404, J. Neurosci. Res., 39 (1994) 669-673.
33. [33] Perry, E.K., Perry, R.H., Tomlinson, B.E., Blessed, G. and Gibson, P.H., Coenzyme A-acetylating enzymes in Alzheimer's disease: Possible cholinergic 'compartment' of pyruvate dehydrogenase, Neurosci. Lett., 18 (1980) 105-110.
34. [34] Plyte, S.E., Hughes, K., Nikolakaki, E., Pulverer, B.J. and Woodgett, J.R., Glycogen synthase kinase-3: functions in oncogenesis and development, Biochim. Biophys. Acta, 1114 (1992) 147-162.
35. [35] Pollock, N.J. and Wood, J.G., Differential sensitivity of the microtubule-associated protein, tau, in Alzheimer's disease tissue to formalin fixation, J. Histochem. Cytochem., 36 (1988) 1117-1121.
36. [36] Saito, K.-I., Elce, J.S., Hamos, J.E. and Nixon, R.A., Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: A potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. USA, 90 (1993) 2628-2632.
37. [37] Schmidt, M.L., Lee, V.M.-Y. and Trojanowski, J.Q., Analysis of epitopes shared by Hirano bodies and neurofilament proteins in normal and Alzheimer's disease hippocampus. Lab. Invest., 60 (1989) 513-522.
38. [38] Shi, S.-R., Chaiwun, B., Young, L., Cote, R.J. and Taylor, C.R., Antigen retrieval technique utilizing citrate buffer or urea solution for immunohistochemical demonstration of androgen receptor in formalin-fixed paraffin sections. J. Histochem. Cytochem., 41 (1993) 1599-1604.
39. [39] Shi, S.-R., Gu, J., Kalra, K.L., Chen, T., Cote, R.J. and Taylor, C.L., Antigen retrieval technique: A novel approach to immunohistochemistry on routinely processed tissue sections. Cell Vision, 2 (1995) 6-22.
40. [40] Shi, S.-R., Key, M.E. and Kalra, K.L., Antigen retrieval in formalin-fixed, paraffin-embedded tissues: An enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections, J. Histochem. Cytochem., 39 (1991) 741-748.
41. [41] Shin, R.-W., Iwaki, T., Kitamoto, T. and Tateishi, J., Hydrated autoclave pretreatment enhances tau immunoreactivity in formalin-fixed normal and Alzheimer's disease brain tissues. Lab. Invest., 64 (1991) 693-702.
42. [42] Sorbi, S., Bird. E.D. and Blass. J.P., Decreased pyruvate dehydrogenase activity in Huntington and Alzheimer brain. Ann. Neurol., 13 (1983) 72-78.
43. [43] Takahashi, M., Tomizawa, K., Ishiguro, K., Takamatsu, M.. Fujita, S.C. and Imahori, K., Involvement of τ protein kinase I in paired helical filament-like phosphorylation of the juvenile τ in rat brain. J. Neurochem., 64 (1995) 1759-1768.
44. [44] Takahashi, M., Tomizawa, K., Kato, R., Sato, K., Uchida, T., Fujita, S.C. and Imahori, K., Localization and developmental changes of τ protein kinase I/glycogen synthase-3β in rat brain, J. Neurochem., 63 (1994) 245-255.
45. [45] Takashima, A., Noguchi, K., Sato, K., Hoshino, T. and Imahori, K., tau protein kinase I is essential for amyloid β protein-induced neurotoxicity, Proc. Natl. Acad. Sci. USA, 90 (1993) 7789-7793.
46. [46] Takashima, A., Yamaguchi, H., Noguchi, K.. Michel, G., Ishiguro, K., Sato, K.. Hoshino, T., Hoshi, M. and Imahori, K., Amyloid β peptide induces cytoplasmic accumulation of amyloid protein precursor via tau protein kinase I/glycogen synthase kinase-3β in rat hippocampal neurons, Neurosci. Lett., 198 (1995) 83-86.
47. [47] Tomlinson, B.E., Ageing and the Dementias. In J.H. Adams and L.W. Duchen (Eds.), Greenfields Neuropathology. Chap. 20. Oxford Univ. Press. New York, 1992, pp. 1314-1315.
48. [48] Trojanowski, J.Q. and Lee, V.M.-Y., Phosphorylation of neuronal cytoskeleton proteins in Alzheimer's disease and Lewy body dementias. In J.F. Disterhoft, W.H. Gispen, J. Traber and Z.S. Khachaturian (Eds.), Calcium Hypothesis of Aging and Dementia, New York Academy of Sciences. New York, 1994, pp. 92-109.
49. [49] Trojanowski, J.Q., Schuek, T., Schmidt, M.L. and Lee, V.M.-Y., Distribution of tau proteins in the normal human central and peripheral nervous system. J. Histochem. Cytochem., 37 (1989) 209-215.
50. [50] Tsukamoto, M., Kato, R., Ishiguro, K., Uchida, T. and Sato, K., Improved protective groups for phosphate of O-phosphoserine useful for the solid-phase peptide synthesis, Tetrahedron Lett., 32 (1991) 7083-7086.
51. 1 activating kinase from bovine brain cytosolic and particulate fractions, J. Biol. Chem., 264 (1989) 2985-2990.
52. [52] Vandesande, F. and Dierickx, K., Identification of the vasopressin producing and of the oxytocin producing neurons in the hypothalamic magnocellular neurosecretory system of the rat. Cell Tiss. Res., 164 (1975) 153-162.
53. [53] West, M.J., Coleman, P.D., Flood, D.G. and Troncoso, J.C., Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet, 344 (1994) 769-772.
54. [54] Wisniewski, H.M. and Terry, R.D., Reexamination of the pathogenesis of the senile plaque, Prog. Neuropathol., 2 (1973) 1-26.
55. [55] Woodgett, J.R., Molecular cloning and expression of glycogen synthase kinase-3/Factor A, EMBO J., 9 (1990) 2431-2438.
56. [56] Woodgett, J.R., Regulation and functions of the glycogen synthase kinase-3 subfamily. Semin. Cancer Biol., 5 (1994) 269-275.
57. [57] Yamamoto, T. and Hirano, A., A comparative study of modified Bielschowsky, Bodian and thioflavin S stains on Alzheimer's neurofibrillary tangles, Neuropathol. Appl. Neurobiol., 12 (1986) 3-9.
58. A), Biochem. Biophys. Res. Commun., 193 (1993) 1202-1210.