Mitotic phosphorylation of tau protein in neuronal cell lines resembles phosphorylation in Alzheimer's disease

European Journal of Cell Biology

Volumn 76, Issue 3, 1998, Pages 176-184

  Preuss, Ute ^a,b   Mandelkow, Eva Maria ^a  

^a MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Alzheimer's disease; Mitosis; Neuronal cells; Phosphorylation; Tau protein

Indexed keywords

ANTIBODY; PHOSPHOPROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA TRANSFECTION; INTERPHASE; MITOSIS; MOUSE; NERVE CELL CULTURE; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALIA; MURINAE;

EID: 0031928259     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0171-9335(98)80032-0     Document Type: Article

References (82)

1. Aizawa, H., H. Kawasak, H. Murofush, S. Kotani, K. Suzuki, H. Sakai: A common amino acid sequence in 190-kDa microtubule-associated protein and tau for the promotion of microtubule assembly. J. Biol. Chem. 264, 5885-5890 (1989).
2. Arriagada, P. V., J. H. Growdon, E. T. Hedleywhyte, B. T. Hyman: Neurofibrillary tangles but not senile plaques parallel duration and seventy of alzheimers-disease. Neurology 42, 631-639 (1992).
3. Bancher, C., I. Grundke-Iqbal, K. Iqbal, V. Fried, H. Smith, H. Wisniewski: Abnormal phosphorylation of tau precedes ubiquitination in neurofibrillary pathology of Alzheimer disease. Brain Research 539, 11-18 (1991).
4. Baumann, K., E. M. Mandelkow, J. Biernat, H. Piwnica-Worms, E. Mandelkow: Abnormal Alzheimer-like phosphorylation of tau protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett. 336, 417-424 (1993).
5. Belmont, L. D., A. A. Hyman, K. E. Sawin, T. J. Mitchison: Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62, 579-589 (1990).
6. Belmont, L. D., T. J. Mitchison: Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84, 623-631 (1996).
7. Biernat, J., E. M. Mandelkow, C. Schröten B. Lichtenberg-Kraag, B. Steiner, B. Berling, H. E. Meyer, M. Mercken, A. Vandermeeren, M. Goedert, E. Mandelkow: The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region. EMBO J. 11, 1593-1597 (1992).
8. Biernat, J., N. Gustke, G. Drewes, E. M. Mandelkow, E. Mandelkow: Phosphorylation of serine 262 strongly reduces the binding of tau protein to microtubules: Distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11, 153-163 (1993).
9. Binder, L. I., A. Frankfurter, L. Rebhun: The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378 (1985).
10. Braak, H., E. Braak: Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 82, 239-259 (1991).
11. Braak, E., H. Braak, E. M. Mandelkow: A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol. 87, 554-567 (1994).
12. Bradford, M. M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).
13. Bramblett, G. T., M. Goedert, R. Jakes, S. E. Merrick, J. Q. Trojanowski, V. M. Y. Lee: Abnormal tau phosphorylation at Ser(396) in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099 (1993).
14. Brandt, R., G. Lee, D. B. Teplow, D. Shalloway, M. Abdelghany: Differential effect of phosphorylation and substrate modulation on tau's ability to promote microtubule growth and nucleation. J. Biol. Chem. 269, 11776-11782 (1994).
15. Brion, J. P., C. Smith, A. M. Couck, J. M. Gallo, B. H. Anderton: Developmental changes in tau phosphorylation: fetal tau is transiently phosphorylated in a manner similar to paired helical filament-tau characteristic of Alzheimer's disease. J. Neurochem. 61, 2071-2080 (1993).
16. Brugg, B., A. Matus: Phosphorylation determines the binding of microtubule-associated protein-2 (MAP2) to microtubules in living cells. J. Cell Biol. 114, 735-743 (1991).
17. Buendia, B., G. Draetta, E. Karsenti: Regulation of the microtubule nucleating activity of centrosomes in Xenopus egg extracts: Role of cyclin A-associated protein kinase. J. Cell Biol. 116, 1431-1442 (1992).
18. Butler, M., M. L. Shelanski: Microheterogeneity of microtubule-associated tau-proteins is due to differences in phosphorylation. J. Neurochem. 47, 1517-1522 (1986).
19. Butner, K. A., M. W. Kirschner: Tau-protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 115, 717-730 (1991).
20. Davis, F. M., T. H. Tsao, S. K. Fowler, P. N. Rao: Monoclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. USA 80, 2926-2930 (1983).
21. Drechsel, D. N., A. A. Hyman, M. H. Cobb, M. W. Kirschner: Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol. Biol. Cell 3, 1141-1154 (1992).
22. Drewes, G., B. Lichtenberg-Kraag, F. Döring, E. M. Mandelkow, J. Biernat, J. Goris, M. Dorée, E. Mandelkow: Mitogen-activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBO J. 11, 2131-2138 (1992).
23. Engle, D. B., J. H. Doonan, N. R. Morris: Cell cycle modulation of MPM-2 specific spindle pole body phosphorylation in Aspergillus nidulans. Cell Motil. Cytoskeleton 10, 432-437 (1988).
24. Ennulat, D. J., R. K. H. Liem, G. A. Hashim, M. L. Shelanski: Two separate 18-amino acid domains of tau promote the polymerization of tubulin. J. Biol. Chem. 264, 5327-5330 (1989).
25. Ferralli, J., T. Doll, A. Matus: Sequence analysis of MAP2 function in living cells. J. Cell Sci. 107, 3115-3125 (1994).
26. Gallo, J., D. Hanger, E. Twist, K. Kosik, B. H. Anderton: Expression and phosphorylation of a 3-repeat isoform of tau in transfected nonneuronal cells. Biochem. J. 286, 399-404 (1992).
27. Goedert, M., R. Jakes, R. A. Crowther, J. Six, U. Lübke, M. Vandermeeren, P. Cras, J. Q. Trojanowski, V. M. Y. Lee: The abnormal phosphorylation of tau protein at Ser202 in Alzheimer's disease recapitulates phosphorylation during development. Proc. Natl. Acad. Sci. USA 90, 5066-5070 (1993).
28. Goedert, M., R. Jakes, R. A. Crowther, P. Cohen, E. Vanmechelen, M. Vandermeeren, P. Cras: Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein. Biochem. J. 301, 871-877 (1994).
29. Greenberg, S. G., P. Davies: A preparation of Alzheimer paired helical filaments that displays distinct tau-proteins by polyacrylamide-gel electrophoresis. Proc. Natl. Acad. Sci. USA 87, 5827-5831 (1990).
30. Grundke-Iqbal, I., K. Iqbal, Y. Tung, M. Quinlan, H. Wisniewski, L. Binder: Abnormal phosphorylation of the microtubule-associated protein tau in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83, 4913-4917 (1986).
31. Gustke, N., B. Trinczek, J. Biernat, E. M. Mandelkow, E. Mandelkow: Domains of tau protein and interactions with microtubules. Biochemistry 33, 9511-9522 (1994).
32. Hirokawa, N.: Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr. Opin. Cell Biol. 6, 74-81 (1994).
33. Illenberger, S., Q. Zheng-Fischhöfer, U. Preuss, K. Stamer, K. Baumann, B. Trinczek, J. Biernat, R. Godemann, E. M. Mandelkow, E. Mandelkow: The endogenous and cell cycle-dependent phosphorylation of the microtubule-associated protein tau in living cells: Implication for Alzheimer's disease. Mol. Biol. Cell, in press (1998).
34. Joly, J. C., D. L. Purich: Peptides corresponding to the 2nd repeated sequence in map-2 inhibit binding of microtubule-associated proteins to microtubules. Biochemistry 29, 8916-8920 (1990).
35. Kanai, Y., R. Takemura, T. Oshima, H. Mori, Y. Ihara, M. Yanagisawa, T. Masaki, N. Hirokawa: Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J. Cell Biol. 109, 1173-1184 (1989).
36. Kanemaru, K., K. Takio, R. Miura, K. Titani, Y. Ihara: Fetal-type phosphorylation of the tau in paired helical filaments. J. Neurochem. 58, 1667-1675 (1992).
37. Karsenti, E.: Severing microtubules in mitosis. Curr. Biol. 3, 208-210 (1993).
38. Keryer, G., F. M. Davis, P. N. Rao, J. Beisson: Protein phosphorylation and dynamics of cytoskeletal structures associated with basal bodies in Paramecium. Cell Motil. Cytoskeleton 12, 90-103 (1987).
39. Kilmartin, J. V., B. Wright, C. Milstein: Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J. Cell Biol. 93, 576-582 (1982).
40. Kondratick, C. M., D. D. Vandre: Alzheimer's disease neurofibrillary tangles contain mitosis-specific phosphoepitopes. J. Neurochem. 67, 2405-2416 (1996).
41. Kosik, K., L. Orecchio, L. Binder, J. Trojanowski, V. Lee, G. Lee: Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1, 817-825 (1988).
42. Kowall, N. W., K. S. Kosik: Axonal disruption and aberrant localization of tau protein characterize the neuropil pathology of Alzheimer's disease. Ann. Neurol. 22, 639-643 (1987).
43. Laemmli, U. K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970).
44. Lang, E., G. I. Szendrei, V. M. Y. Lee, L. Otvos: Immunological and conformation characterization of a phosphorylated immuno-dominant epitope on the paired helical filaments found in Alzheimer's disease. Biochem. Biophys. Res. Commun. 187, 783-790 (1992).
45. Lassmann, H., C. Bancher, H. Breitschopf, J. Wegiel, M. Bobinski, K. Jellinger, H. M. Wisniewski: Cell-death in Alzheimers-disease evaluated by DNA fragmentation in-situ. Acta Neuropathol. 89, 35-41 (1995).
46. Latimer, D. A., J. M. Gallo, S. Lovestone, C. C. J. Miller, C. H. Reynolds, B. Marquardt, S. Stabel, J. R. Woodgett, B. H. Anderton: Stimulation of mapkinase by v-raf transformation of fibroblasts fails to induce hyperphosphorylation of transfected tau. FEBS Lett. 365, 42-16 (1995).
47. Lee, G., R. L. Neve, K. S. Kosik: The microtubule binding domain of tau-protein. Neuron 2, 1615-1624 (1989).
48. Lee, V. M. Y., B. J. Balin, L. Otvos, J. Q. Trojanowski: A68 - a major subunit of paired helical filaments and derivatized forms of normal tau. Science 251, 675-678 (1991).
49. Lewis, S. A., I. E. Ivanov, G. H. Lee, N. J. Cowan: Organization of microtubules in dendrites and axons is determined by a short hydrophobic zipper in microtubule-associated proteins MAP2 and tau. Nature 342, 498-505 (1989).
50. Lichtenberg-Kraag, B., E. M. Mandelkow, J. Biernat, B. Steiner, C. Schröter, N. Gustke, H. E. Meyer, E. Mandelkow: Phosphorylation dependent interaction of neurofilament antibodies with tau protein: Epitopes, phosphorylation sites, and relationship with Alzheimer tau. Proc. Natl. Acad. Sci. USA 89, 5384-5388 (1992).
51. Lieuvin, A., J. C. Labbe, M. Dorée, D. Job: Intrinsic microtubule stability in interphase cells. J. Cell Biol. 124, 985-996 (1994).
52. Mandelkow, E. M., G. Drewes, J. Biernat, N. Gustke, J. Van-Lint, J. R. Vandenheede, E. Mandelkow: Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett. 314, 315-321 (1992).
53. Masson, D., T. E. Kreis: Binding of E-MAP-115 to microtubules is regulated by cell cycle-dependent phosphorylation. J. Cell Biol. 131, 1015-1024 (1995).
54. Matsuo, E. S., R. W. Shin, M. L. Billingsley, A. Vandevoorde, M. Oconnor, J. Q. Trojanowski, V. M. Y. Lee: Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13, 989-1002 (1994).
55. Matus, A.: Stiff microtubules and neuronal morphology. Trends in Neurosci. 17, 19-22 (1994).
56. McIntosh, J. R., G. E. Hering: Spindle fiber action and chromosome movement. Annu. Rev. Cell Biol. 7, 403-426 (1991).
57. Mercken, M., M. Vandermeeren, U. Lübke, J. Six, J. Boons, A. Van de Voorde, J. J. Martin, J. Gheuens: Monoclonal antibodies with selective specificity for Alzheimer tau are directed against phosphatase-sensitive epitopes. Acta Neuropathol. 84, 265-272 (1992).
58. Morishima-Kawashima, M., K. Kosik: The pool of mapkinase associated with microtubules is small but constitutively active. Mol. Biol. Cell 7, 893-905 (1996).
59. Nigg, E.: Cellular substrates of p34(cdc2) and its companion cyclin-dependent kinases. Trends Cell Biol. 3, 296-301 (1993).
60. Obar, R. A., J. Dingus, H. Bayley, R. B. Vallee: The RII subunit of cAMP-dependent protein-kinase binds to a common amino-terminal domain in microtubule-associated proteins 2a, 2b, and 2c. Neuron 3, 639-645 (1989).
61. Otvos, L., L. Feiner, E. Lang, G. Szendrei, M. Goedert, V. M. Y. M. Lee: Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residue 396 and residue 404. J. Neurosci. Res. 39, 669-673 (1994).
62. Pope, W. B., M. P. Lambert, B. Leypold, R. Seupaul, L. Sletten, G. Krafft, W. L. Klein: Microtubule-associated protein-tau is hyperphosphorylated during mitosis in the human neuroblastoma cell-line SH-SY5Y. Exp. Neurol. 126, 185-194 (1994).
63. Preuss, U., F. Döring, S. Illenberger, E. M. Mandelkow: Cell cycle-dependent phosphorylation and microtubule binding of tau protein stably transfected into Chinese hamster ovary cells. Mol. Biol. Cell 6, 1397-1410 (1995).
64. Preuss, U., J. Biernat, E. M. Mandelkow, E. Mandelkow: The "jaws" model of tau-microtubule interaction examined in CHO cells. J. Cell Sci. 110, 789-800 (1997).
65. Reszka, A. A., R. Seger, C. D. Diltz, E. G. Krebs, E. H. Fischer: Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc. Natl. Acad. Sci. USA 92, 8881-8885 (1995).
66. Rubin, L. L., C. L. Gatchalian, G. Rimon, S. F. Brooks: The molecular mechanisms of neuronal apoptosis. Curr. Opin. Neurobiol. 4, 696-702 (1994).
67. Saxton, W. M., D. L. Stemple, R. J. Leslie, E. D. Salmon, M. Zavortink, J. R. McIntosh: Tubulin dynamics in cultured mammalian cells. J. Cell Biol. 99, 2175-2186 (1984).
68. Schoenfeld, T. A., R. A. Obar: Diverse distribution and function of fibrous microtubule-associated proteins in the nervous system. Int. Rev. Cytol. 151, 67-137 (1994).
69. Schweers, O., E. M. Mandelkow, J. Biernat, E. Mandelkow: Oxidation of cysteine 322 in the repeat domain of microtubule-associated protein tau controls the assembly of Alzheimer paired helical filaments. Proc. Natl. Acad. Sci. USA 92, 8463-8467 (1995).
70. Seeger, R. C., Y. L. Danon, S. A. Rayner, F. Hoover: Definition of a Thy-1 determinant on human neuroblastoma, glioma, sarcoma, and teratoma cells with a monoclonal antibody. J. Immunol. 128, 983-989 (1982).
71. Sontag, E., V. Nunbhakdicraig, G. S. Bloom, M. C. Mumby: A novel pool of protein phosphatase 2a is associated with microtubules and is regulated during the cell cycle. J. Cell Biol. 128, 1131-1144 (1995).
72. Szendrei, G. I., V. M. Y. Lee, L. Otvos: Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location. J. Neurosci. Res. 34, 243-249 (1993).
73. Tanaka, T., K. Iqbal, E. Trenkner, D. J. Liu, I. Grundke-Iqbal: Abnormally phosphorylated tau in SY5Y human neuroblastoma cells. FEBS Lett. 360, 5-9 (1995).
74. Trinczek, B., J. Biernat, K. Baumann, E. M. Mandelkow, E. Mandelkow: Domains of tau-protein, differential phosphorylation, and dynamic instability of microtubules. Mol. Biol. Cell 6, 1887-1902 (1995).
75. Vandre, D. D., F. M. Davis, P. N. Rao, G. G. Borisy: Phosphoproteins are components of mitotic microtubule organizing centers. Proc. Natl. Acad. Sci. USA 81, 4439-1443 (1984).
76. Vandre, D. D., F. M. Davis, P. N. Rao, G. G. Borisy: Distribution of cytoskeletal proteins sharing a conserved phosphorylated epitope. Eur. J. Cell Biol. 41, 72-81 (1986).
77. Vandre, D. D., V. Centonze, J. Peloquin, R. Tombes, G. G. Borisy: Proteins of the mammalian mitotic spindle: Phosphorylation/dephosphorylation of MAP-4 during mitosis. J. Cell Sci. 98, 577-588 (1991).
78. Vincent, I., M. Rosado, P. Davies: Mitotic mechanisms in Alzheimer's disease. J. Cell Biol. 132, 413-425 (1996).
79. Vincent, I., G. Jicha, M. Rosado, M. D. W. Dickson: Aberrant expression of mitotic cdc2/B1 kinase in degenerating neurons of Alzheimers-disease brain. J. Neurosci. 17, 3588-3598 (1997).
80. Yoshida, H., Y. Ihara: Tau in paired helical filaments is functionally distinct from fetal tau: Assembly incompetence of paired helical filament tau. J. Neurochem. 61, 1183-1186 (1993).
81. Zheng-Fischhöfer, Q.: Mapping of epitopes of phosphorylation-dependent antibodies on tau protein. Diploma thesis, Hamburg, Germany. University of Hamburg 1994.
82. Zheng-Fischhöfer, Q., J. Biernat, E. M. Mandelkow, S. Illenberger, R. Godemann, E. Mandelkow: Sequential phosphorylation of tau-protein by GSK-3b 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. 252, 542-552 (1998).