Physiology and pathology of tau protein kinases in relation to Alzheimer's disease

Journal of Biochemistry

Volumn 121, Issue 2, 1997, Pages 179-188

  Imahori, Kazutomo ^a   Uchida, Tsuneko ^a  

^a MITSUBISHI KASEI INST OF LIFE SCI   (Japan)

Author keywords

Alzheimer's disease; Amyloid protein; Phosphorylation of tau; Pyruvate dehydrogenase; Tau protein kinases I and II

Indexed keywords

PROTEIN KINASE; PYRUVATE DEHYDROGENASE; TAU PROTEIN;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; DOWN SYNDROME; ENZYME ACTIVE SITE; HIPPOCAMPUS; HUMAN; MOLECULAR CLONING; NEUROFIBRILLARY TANGLE; NEWBORN PERIOD; PAIRED HELICAL FILAMENT; PROTEIN PHOSPHORYLATION; SENILE PLAQUE; TRAFFIC AND TRANSPORT;

ALZHEIMER DISEASE; ANIMALS; APOPTOSIS; BINDING SITES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASES; HUMANS; NEURONS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PYRUVATE DEHYDROGENASE COMPLEX; RATS; UP-REGULATION;

EID: 0031045216     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Arriagada, P.A., Growdon, J.H., Hedley-White, E.T., and Hyman, B.T. (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42, 631-639
2. Ihara, Y., Nukina, N., Miura, R., and Ogawara, M. (1986) Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer's disease. J. Biochem. 99, 1807-1810
3. Grundke-Iqbal, I., Iqbal, K.,Tung, Y.-C., Quinlan, M., Wisniewski, H.M., and Binder, L.I. (1986) Abnormal phosphorylation of the microtubule-associated protein τ (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83. e4913-4917
4. Mori, H., Kondo, J., and Ihara, Y. (1987) Ubiquitin is a component of paired helical filament in Alzheimer's disease. Science 235, 1641-1644
5. Weingarten, M.D., Lockwood, A.H., Hwo, S.Y., and Kirschner, M.W. (1975) A protein factor essential for microtubule assembly. Proc. Natl. Acad. Sci. USA 72, 1858-1862
6. Cleveland, D.W., Hwo, S.Y., and Kirschner, M.W. (1977) Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J. Mol. Biol. 116, 207-225
7. Kondo, J., Honda, Y., Mori, H., Hamada, Y., Miura, R., Ogawara, R., and Ihara, Y. (1988) The carboxyl third of tau is tightly bound to paired helical filaments. Neuron 1, 827-834
8. Lee, V.M.-Y., Balin, B.J., Otvos, L., Jr., and Trojanowski, J.O. (1991) A68: a major subunit of paired helical filaments and derivatized forms of normal tau. Science 251, 675-678
9. Ishiguro, K., Ihara, Y., Uchida, T., and Imahori, K. (1988) A novel tubulin-dependent protein kinase forming a paired helical filament epitope on tau. J. Biochem. 104, 319-321
10. Webb, E.G. (1990) Enzyme nomenclature. Recommendations 1984. Supplement 3: corrections and additions. Eur. J. Biochem. 187, 263-281
11. Ishiguro, K., Takamatsu, M., Tomizawa, K., Omori, A., Takahashi, M., Arioka, M., Uchida, T., and Imahori, K. (1992) Tau protein kinase I converts normal tau protein into A68-like component of paired helical filaments. J. Biol. Chem. 267, 10897-10901
12. Arioka, M., Tsukamoto, M., Ishiguro, K., Kato, R., Sato, K., Imahori, K., and Uchida, T. (1993) τ protein kinase II is involved in the regulation of the normal phosphorylation state of τ protein. J. Neurochem. 60, 461-468
13. Ishiguro, K., Shiratsuchi, A., Sato, S., Omori, A., Arioka, M., Kobayashi, S., Uchida, T., and Imahori, K. (1993) Glycogen synthase kinase 3β is identical to tau protein kinase I generating several epitopes of paired helical filaments. FEBS Lett. 325, 167-172
14. Woodgett, J.R. (1990) Molecular cloning and expression of glycogen synthase kinase-3/Factor A. EMBO J. 9, 2431-2438
15. Siegfried, E., Chou, T.-B., and Perrimon, N. (1992) wingless Signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71, 1167-1179
16. Ruel, L., Bourouis, M., Heitzler, P., Pantesco, V., and Simpson, P. (1993) Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch. Nature 362, 557-560
17. He, X., Saint-Jeannet, J.-P., Woodget, J.R., Varmus, H.E., and Dawid, I.B. (1995) Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 374, 617-622
18. Kobayashi, S., Ishiguro, K., Omori, A., Takamatsu, M., Arioka, M., Imahori, K., and Uchida, T. (1993) A cdc2-related kinase PSSALRE/cdk5 is homologous with the 30 kDa subunit of tau protein kinase II, a proline-directed protein kinase associated with microtubule. FEBS Lett. 335, 171-175
19. Meyerson, M., Enders, G.H., Wu, C.-L., Su, L.-K., Gorka, C., Nelson, C., Harlow, E., and Tsai, L.-H. (1992) A family of human cdc2-related protein kinases. EMBO J. 11, 2909-2917
20. Ishiguro, K., Kobayashi, S., Omori, A., Takamatsu, M., Yonekura, S., Anzai, K., Imahori, K., and Uchida, T. (1994) Identification of the 23 kDa subunit of tau protein kinase II as a putative activator of cdk5 in bovine brain. FEBS Lett. 342, 203-208
21. Uchida, T., Ishiguro, K., Ohnuma, J., Takamatsu, M., Yonekura, S., and Imahori, K. (1994) Precursor of cdk5 activator, the 23 kDa subunit of tau protein kinase II: its sequence and developmental change in brain. FEBS Lett. 355, 35-40
22. Tsai, L.-H., Delalle, I., Caviness, V.S., Jr., Chae, T., and Harlow, E. (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371, 419-423
23. Lew, J., Huang, Q.-Q., Qi, Z., Winkfein, R.J., Aebersold, R., Hunt, T., and Wang, J.H. (1994) A brain-specific activator of cyclin-dependent kinase 5. Nature 371, 423-426
24. Uchida, T., Omori, A., Ishiguro, K., and Sato, K. (1993) Sequence analysis of phosphopeptides and its application for the determination of phosphorylated sites of proteins in Methods in Protein Sequence Analysis (Imahori, K. and Sakiyama, F., eds.) pp. 199-206, Plenum Press, New York and London
25. Ishiguro, K., Omori, A., Sato, K., Tomizawa, K., Imahori, K., and Uchida, T. (1991) A serine/threonine proline kinase activity is included in the tau protein kinase fraction forming a paired helical filament epitope. Neurosci. Lett. 128, 195-198
26. Ishiguro, K., Omori, A., Takamatsu, M., Sato, K., Arioka, M., Uchida, T., and Imahori, K. (1992) Phosphorylation sites on tau by tau protein kinase I, a bovine derived kinase generating an epitope of paired helical filaments. Neurosci. Lett. 148, 202-206
27. Ishiguro, K., Sato, K., Takamatsu, M., Park, J., Uchida, T., and Imahori, K. (1995) Analysis of phosphorylation of tau with antibodies specific for phosphorylation sites. Neurosci. Lett. 202, 81-84
28. Tsukamoto, M., Kato, R., Ishiguro, K., Uchida, T., and Sato, K. (1991) Improved protective groups for phosphate of o-phosphoserine useful for the solid-phase peptide synthesis. Tetrahedron Lett. 32, 7083-7086
29. Sato, K., Ishiguro, K., Omori, A., Kato, R., Kim, J.I., Uchida, T., Saruta, K., and Wakamiya, T. (1994) Solid phase synthesis of phosphopeptides related to tau protein kinase I in Peptide Chemistry 1993 (Okada, Y., ed.) pp. 109-112, Protein Research Foundation, Osaka
30. Goedert, M. (1993) Tau protein and the neurofibrillary pathology of Alzheimer's disease. TINS 16, 460-465
31. Butner, K.A. and Kirschner, M.W. (1991) Tau protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 115, 717-730
32. Kanai, Y., Chen, J., and Hirokawa, N. (1992) Microtubule bundling by tau protein in vivo: Analysis of functional domains. EMBO J. 11, 3953-3961
33. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Titani, K., and Ihara, Y. (1995) Proline-directed and non-proline-directed phosphorylation of PHF-tau. J. Biol. Chem. 270, 823-829
34. Watanabe, A., Hasegawa, M., Suzuki, M., Takio, K., Morishima-Kawashima, M., Titani, K., Arai, T., Kosik, K.S., and Ihara, Y. (1993) In vivo phosphorylation sites in fetal and adult rat tau. J. Biol. Chem. 268, 25712-25717
35. Paudel, H.K., Lew, J., Ali, Z., and Wang, J.H. (1993) 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, 23512-23518
36. Vulliet, R., Haloran, S.M., Braun, R.K., Smith, A.J., and Lee, G. (1992) Proline-directed phosphorylation of human tau protein. J. Biol. Chem. 267, 22570-22574
37. Yang, S.-D., Yu, J.-S., Shiah, S.-G., and Huang, J.-J. (1994) Protein kinase FA/glycogen synthase kinase-3α after heparin potentiation phosphorylates τ on sites abnormally phosphorylated in Alzheimer's disease brain. J. Neurochem. 63, 1416-1425
38. Drewes, G., Trinczk, B., Illenberger, S., Biernat, J., Schmitt-Ulmms, G., Meyer, H.E., Mandelkow, E.-M., and Mandelkow, E. (1995) Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). J. Biol. Chem. 270, 7679-7688
39. Ino, H., Ishizuka, T., Chiba, T., and Tatibana, M. (1994) Expression of CDK5 (PSSALRE kinase), a neural cdc2-related protein kinase, in the mature and developing mouse central and peripheral nervous system. Brain Res. 661, 196-206
40. Altman, J. (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neurol. 145, 399-464
41. 3H-thymidine autoradiography. II. Morphogenesis during embryonic and early postnatal life. J. Comp. Neurol. 190, 87-114, 115-134
42. Ihara, Y. (1988) Massive somatodendritic sprouting of cortical neurons in Alzheimer's disease. Brain Res. 459, 138-144
43. Nikolic, M., Dudek, H., Kwon, Y.T., Ramos, Y.F.M., and Tsai, L.-H. (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10, 816-825
44. Fujita, S.C., Takahashi, M., Hasegawa, J., and Imahori, K. (1995) Immunohistochemistry of tau protein kinase I in the fetal rat nervous system. Neurochem. Res. 20, 327
45. Takahashi, M., Tomizawa, K., Kato, R., Sato, K., Uchida, T., Fujita, S.C., and Imahori, K. (1994) Localization and developmental changes of τ protein kinase I/Glycogen synthase kinase-3β in rat brain. J. Neurochem. 63, 245-255
46. Takahashi, M., Tomizawa, K., Ishiguro, K., Takamatsu, M., Fujita, S.C., and Imahori, K. (1995) Involvement of τ protein kinase I in paired helical filament-like phosphorylation of the juvenile τ in rat brain. J. Neurochem. 64, 1759-1768
47. Shiurba, R.A., Ishiguro, K., Takahashi, M., Sato, K., Spooner, E.T., Mercken, M., Yoshida, R., Wheelock, T.R., Yanagawa, H., Imahori, K., and Nixon, R.A. (1996) Immunocytochemistry of tau phosphoserine 413 and tau protein kinase I in Alzheimer pathology. Brain Res. 737, 119-132
48. Plyte, S.E., Hughes, K., Nikolakaki, E., Pulverer, B.J., and Woodgett, J.R. (1992) Glycogen synthase kinase-3: functions in oncogenesis and development. Biochim. Biophys. Acta 1114, 147-162
49. Yamaguchi, H., Ishiguro, K., Uchida, T., Takashima, A., Lemere, C.A., and Imahori, K. 11996) Preferential labeling of Alzheimer neurofibrillary tangles with antisera for protein kinase (TPK)I/GSK-3β and cdk5, a component of TPKII. Acta Neuropathol. 92, 232-241
50. Hardy, J.A. and Higgins, G.A. (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256, 184-185
51. Selkoe, D.J. (1989) Biochemistry of altered brain proteins in Alzheimer's disease. Annu. Rev. Neurosci. 12, 463-490
52. Takashima, A., Noguchi, K., Sato, K., Hoshino, T., and Imahori, K. (1993) Tau protein kinase I is essential for amyloid β-protein-induced neurotpxicity. Proc. Natl. Acad. Sci. USA 90, 7789-7793
53. Yankner, B.A., Caceres, A., and Duffy, L.K. (1990) Nerve growth factor potentiates the neurotoxicity of β-amyloid. Proc. Natl. Acad. Sci. USA 87, 9020-9023
54. Cotman, C.W., Pike, C.J., and Copani, A. (1992) β-Amyloid neurotoxicity - a discussion of in vitro findings. Neurobiol. Aging 13, 587-590
55. Hoshi, M., Takashima, A., Noguchi, K., Murayama, M., Sato, M., Kondo, S., Saitoh, Y., Ishiguro, K., Hoshino, T., and Imahori, K. (1996) Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3β in brain. Proc. Natl. Acad. Sci. USA 93, 2719-2723
56. Hoshi, M., Sato, M., Kondo, S., Takashima, A., Noguchi, K., Takahashi, M., Ishiguro, K., and Imahori, K. (1995) Different localization of tau protein kinase I/glycogen synthase kinase-3β from glycogen synthase-3α in cerebrum mitochondria. J. Biochem. 118, 683-685
57. Hoyer, S., Oesterreich, K., and Wagner, O. (1988) Glucose metabolism as the site of the primary abnormality in early-onset dementia of Alzheimer type? J. Neurol. 235, 143-148
58. Parnetti, L., Gaiti, A., Brunetti, M., Avellini, L., Polidori, C., Cecchetti, R., Palumbo, B., and Senin, U. (1995) Increased CSF pyruvate levels as a marker of impaired energy metabolism in Alzheimer's disease. J. Am. Geriatr. Soc. 43, 316-318
59. Perry, E.K., Gibson, P.H., Blessed, G., Perry, R.H., and Tomlinson, B.E. (1977) Neurotransmitter enzyme abnormalities in senile dementia: Choline acetyltransferase and glutamic-acid decarboxylase activities in necropsy brain tissue. J. Neural. Sci. 34, 247-266
60. Sorbi, S., Bird, E.D., and Blass, J.P. (1982) Decreased pyruvate dehydrogenase complex activity in Huntington and Alzheimer brain. Ann. Neural. 13, 72-78
61. Yates, C.M., Butterworth, J., Tennant, M.C., and Gordon, A. (1990) Enzyme activities in relation to pH and lactate in postmortem brain in Alzheimer-type and other dementias. J. Neurochem. 55, 1624-1630
62. 1-42 on cholinergic neurons: Suppression of acetylcholine synthesis precedes neurodegeneration. J. Biol. Chem. 272, 2038-2041
63. Whitehouse, P.J., Price, D.L., Struble, R.G., Clark, A.W., Coyle, J.T., and DeLong, M.R. (1982) Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 210, 1237-1239