Phosphorylation of tau by glycogen synthase kinase-3β in intact mammalian cells: The effects on the organization and stability of microtubules

Neuroscience

Volumn 73, Issue 4, 1996, Pages 1145-1157

  Lovestone, S ^a   Hartley, C L ^a   Pearce, J ^a   Anderton, B H ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Alzheimer's disease; glycogen synthase kinase 3; intact cells; microtubules; phosphorylation; tan

Indexed keywords

GLYCOGEN SYNTHASE; TUBULIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CYTOARCHITECTURE; ENZYME ACTIVITY; GENE EXPRESSION; MICROTUBULE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0029994754     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00126-1     Document Type: Article

References (61)

1. Anderton B. H., Couck A., Davis D. R., Gallo J.-M., Hanger D. P., Ladhani K., Latimer D. A., Lewis C., Lovestone S., Marquardt B., et al. (1994) Modulation of PHF-like tau phosphorylation in cultured neurones and transfected cells. Neurobiol. Agng 16, 389-402.
2. Baas P. W., Pienkowski T. P., Cimbalnik K. A., Toyama K., Bakalis S., Ahmad F. J. and Kosik K. S. (1994) Tau confers drug stability but not cold stability to microtubules in living cells. J. Cell Sci. 107, 135-143.
3. Barlow S., Gonzalez-Garay M. L., West R. R., Olmsted J. A. and Cabral F. (1994) Stable expression of heterologous microtubule-associated proteins in chinese hamster ovary cells: evidence for differing roles of MAPs in microtubule organisation. J. Cell Biol. 126, 1017-1029.
4. Baumann K., Mandelkow E.-M., Biernat J., Piwnica-Worms H. and Mandelkow E. (1993) Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. Fedn Eur. biochem. Socs Lett. 336, 417-424.
5. 262 strongly reduces binding of tau to microtubules: Distinction bewteen PHF-like immunoreactivity and microtubule binding. Neuron 11, 153-163.
6. Brady S. T., Tytell M. and Lasek R. J. (1984) Axonal tubulin and axonal microtubules; biochemical evidence for stability. J. Cell Biol. 99, 1716-1724.
7. Bramblett G. T., Goedert M., Jakes R., Merrick S. E., Trojanowski J. Q. and Lee V. M. (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099.
8. Brion J.-P., Couck A.-M., Robertson J., Loviny T. L. F. and Anderton B. H. (1993) Neurofilament monoclonal antibodies RT97 and 8D8 recognize different modified epitopes in paired helical filament-τ in Alzheimer's disease. J. Neurochem. 60, 1372-1382.
9. Brion J. P., Hanger D. P., Bruce M. T., Couck A. M., Flament-Durand J. and Anderton B. H. (1991) Tau in Alzheimer neurofibrillary tangles. N- and C-terminal regions are differentially associated with paired helical filaments and the location of a putative abnormal phosphorylation site. Biochem. J. 273, 127-133.
10. Brion J. P., Octave J. N. and Couck A. M. (1994) Distribution of the phosphorylated microtubule-associated protein tau in developing cortical neurons. Neuroscience 63, 895-909.
11. Brion J.-P., Smith C., Couck A.-M., Gallo J.-M. and Anderton B. H. (1993) Developmental changes in τ phosphorylation: Fetal τ is transiently phosphorylated in a manner similar to paired helical filament-τ characteristic of Alzheimer's disease. J. Neurochem. 61, 2071-2080.
12. Caceres A. and Kosik K. S. (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
13. Caceres A., Potrebic S. and Kosik K. S. (1991) The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J. Neurosci. 11, 1515-1523.
14. Del C. Alonso A., Zaidi T., Grundke-Iqbal I. and Iqbal K. (1994) Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease. Proc. natn Acad. Sci. U.S.A. 91, 5562-5566.
15. Drechsel D. N., Hyman A. A., Cobb M. H. and Kirschner M. W. (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Molec. biol. Cell 3, 1141-1154.
16. Drewes G., Lichtenberg Kraag B., Doring F., Mandelkow E. M., Biernat J., Goris J., Doree M. and Mandelkow E. (1992) Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. Eur. molec. Biol. Org. J. 11, 2131-2138.
17. Dupont-Wallois L., Sautière P. E., Cocquerelle C., Bailleul B., Delacourte A. and Caillet-Boudin M. L. (1995) Shift from fetal-type to Alzheimer-type phosphorylated Tau proteins in SKNSH-SY 5Y cells treated with okadaic acid. Fedn Eur. biochem. Socs Lett. 357, 197-201.
18. Esmaeli-Azad B., McCarty J. H. and Feinstein S. C. (1994) Sense and antisense transfection analysis of tau function: Tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107, 869-879.
19. Flament-Durant J. and Couck A. (1979) Spongiform alterations in brain biopsies of presenile dementia. Acta Neuropathol. Berlin 46, 159-162.
20. Gallo J. M., Hanger D. P., Twist E. C., Kosik K. S. and Anderton B. H. (1992) Expression and phosphorylation of a three-repeat isoform of tau in transfected non-neuronal cells. Biochem. J. 286, 399-404.
21. Garver T. D., Harris K. A., Lehman R. A., Lee V. M., Trojanowski J. Q. and Billingsley M. L. (1994) Tau phosphorylation in human, primate, and rat brain: evidence that a pool of tau is highly phosphorylated in vivo and is rapidly dephosphorylated in vitro. J. Neurochem. 63, 2279-2287.
22. Garver T. D., Oyler G. A., Harris K. A., Polavarapu R., Damuni Z., Lehman R. A. W. and Billingsley M. L. (1995) Tau phosphorylation in brain slices: Pharmacological evidence for convergent effects of protein phosphatases on tau and mitogen-activated protein kinase. Molec. Pharmac. 47, 745-756.
23. Goedert M., Crowther R. A. and Garner C. C. (1991) Molecular characterization of microtubule-associated proteins tau and MAP2. Trends Neurosci. 14, 193-199.
24. Goedert M. and Jakes R. (1990) Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. Eur. molec. Biol. Org. J. 9, 4225-4230.
25. Goedert M., Jakes R., Crowther R. A., Six J., Lübke U., Vandermeeren M., Cras P., Trojanowski J. Q. and Lee V. M.-Y. (1993) The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proc. natn Acad. Sci. U.S.A. 90, 5066-5070.
26. Gray E. G., Paula Barbosa M. and Roher A. (1987) Alzheimer's disease: paired helical filaments and cytomembranes. Neuropath. appl. Neurobiol. 13, 91-110.
27. Gustke N., Steiner B., Mandelkow E. M., Biernat J., Meyer H. E., Goedert M. and Mandelkow E. (1992) The Alzheimer-like phosphorylation of tau protein reduces microtubule binding and involves Ser-Pro and Thr-Pro motifs. Fedn Eur. biochem. Socs Lett. 307, 199-205.
28. Gustke N., Trinczek B., Biernat J., Mandelkow E.-M. and Mandelkow E. (1994) Domains of τ protein and interactions with microtubules. Biochemistry 33, 9511-9522.
29. Hanger D. P., Hughes K., Woodgett J. R., Brion J.-P. and Anderton B. H. (1992) 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, 58-62.
30. Harris K. A., Oyler G. A., Doolittle G. M., Vincent I., Lehman R. A. W., Kincaid R. L. and Billingsley M. L. (1993) Okadaic acid induces hyperphosphorylated forms of tau protein in human brain slcies. Ann. Neurol. 33, 77-87.
31. Hasegawa M., Watanabe A., Takio K., Suzuki M., Arai T., Titani K. and Ihara Y. (1993) Characterization of two distinct monoclonal antibodies to paired helical fialments: Further evidence for fetal-type phosphorylation of the τ in paired helical filaments. J. Neurochem. 60, 2068-2077.
32. Hughes K., Pulverer B. J., Theocharous P. and Woodgett J. R. (1992) Baculovirus-mediated expression and characterisation of rat glycogen synthase kinase-3 beta, the mammalian homologue of the Drosophila melanogaster zeste-white 3sgg homeotic gene product. Eur. J. Biochem. 203, 305-311.
33. Iqbal K., Zaidi T., Bancher C. and Grundke-Iqbal I. (1994) Alzheimer paired helical filaments: Restoration of the biological activity by dephosphorylation. Fedn Eur. Biochem. Socs Lett. 349, 104-108.
34. Kanai Y., Chen J. and Hirokawa N. (1992) Microtubule bundling by tau proteins in vivo: Analysis of functional domains. Eur. molec. Biol. Org. J. 11, 3953-3961.
35. Kanemaru K., Takio K., Miura R., Titani K. and Ihara Y. (1992) Fetal-type phosphorylation of the tau in paired helical filaments. J. Neurochem. 58, 1667-1675.
36. Knops J., Kosik K. S., Lee G., Pardee J. D., Cohen Gould L. and McConlogue L. (1991) Overexpression of tau in a nonneuronal cell induces long cellular processes. J. Cell Biol. 114, 725-733.
37. Latimer D. A., Gallo J.-M., Lovestone S., Miller C. C. J., Reynolds C. H., Marquardt B., Stabel S., Woodgett J. R. and Anderton B. H. (1995) Stimulation of MAP kinase by v-raf transformation of fibroblasts fails to induce hyperphosphorylation of transfected tau. Fedn Eur. biochem. Socs Lett. 365, 42-46.
38. Lee G. and Rook S. L. (1992) Expression of tau protein in non-neuronal cells: microtubule binding and stabilisation. J. Cell Sci. 102, 237.
39. Lindwall G. and Cole R. D. (1984) Phosphorylation affects the ability of tau protein to promote microtubule assembly. J. biol. Chem. 259, 5301-5305.
40. Lo M. M. S., Fieles A. W., Norris T. E., Dargis P. G., Caputo C. B., Scott C. W., Lee V. M.-Y. and Goedert M. (1993) Human tau isoforms confer distinct morphological and functional properties to stably transfected fibroblasts. Molec. Brain Res. 20, 209-220.
41. Lovestone S. and Anderton B. H. (1992) Cytoskeletal abnormalities in Alzheimer's disease. Curr. Opin. Neurol. Neurosurg. 5, 883-888.
42. Lovestone S., Reynolds C. H., Latimer D., Davis D. R., Anderton B. H., Gallo J.-M., Hanger D., Mulot S., Marquardt B., Stabel S., et al. (1994) Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol. 4, 1077-1086.
43. Matsuo E. S., Shin R.-W., Billingsley M. L., Van DeVoorde A., O'Connor M., Trojanowski J. Q. and Lee V. M.-Y. (1994) 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.
44. Matus A. (1994) Stiff microtubules and neuronal morphology. Trends Neurosci. 17, 19-22.
45. McKee A. C., Kowall N. W. and Kosik K. S. (1989) Microtubular reorganization and dendritic growth response in Alzheimer's disease. Ann. Neurol. 26, 652-659.
46. Medina M., De Garcini E. M. and Avila J. (1995) The role of tau phosphorylation in transfected COS-1 cells. Molec. Cell Biochem. 148, 79-88.
47. Montejo de Garcini E., De la Luna S., Dominguez J. E. and Avila J. (1994) Overexpression of tau protein in COS-1 cells results in the stabilization of centrosome-independent microtubules and extension of cytoplasmic processes. Molec. Cell Biochem. 130, 187-196.
48. Nagy Z., Esiri M. M., Jobst K. A., Morris J. H., King E. M., McDonald B., Litchfield S., Smith A., Barnetson L. and Smith A. D. (1995) Relative roles of plaques and tangles in the dementia of Alzheimer's disease: correlations using three sets of neuropathological criteria. Dementia 6, 21-31.
49. Pope W. B., Lambert M. P., Leypold B., Seupaul R., Sletten L., Krafft G. and Klein W. L. (1994) Microtubule-associated protein tau is hyperphosphorylated during mitosis in the human neuroblastoma cell line SH-SY5Y. Expl Neurol. 126, 185-194.
50. Scott C. W., Blowers D. P., Barth P. T., Lo M. M., Salama A. I. and Caputo C. B. (1991) Differences in the abilities of human tau isoforms to promote microtubule assembly. J. Neurosci. Res. 30, 154-162.
51. Scott C. W., Spreen R. C., Herman J. L., Chow F. P., Davison M. D., Young J. and Caputo C. B. (1993) Phosphorylation of recombinant tau by cAMP-dependent protein kinase. Identification of phosphorylation sites and effect on microtubule assembly. J. biol. Chem. 268, 1166-1173.
52. cyclin A) decreases tau-induced microtubule assembly and antibody SMI33 reactivity. Brain Res. 611, 237-242.
53. 262 in fetal tau, adult tau, and paired helical filament tau. J. Biol. Chem. 270, 18,917-18,922.
54. Singh T. J., Grundke-Iqbal I. and Iqbal K. (1995) Phosphorylation of τ protein by casein kinase-1 converts it to an abnormal Alzheimer-like state. J. Neurochem. 64, 1420-1423.
55. Sperber B. R., Leight S., Goedert M. and Lee V. M.-Y. (1995) Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci. Lett. 197, 149-153.
56. Sygowski L. A., Fieles A. W., Lo M. M. S., Scott C. W. and Caputo C. B. (1993) Phosphorylation of tau protein in tau-transfected 3T3 cells. Molec. Brain Res. 20, 221-228.
57. 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.
58. Takemura R., Okabe S., Umeyama T., Kanai Y., Cowan N. J. and Hirokawa N. (1992) Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. J. Cell Sci. 103, 953-964.
59. Trojanowski J. Q. and Lee V. M.-Y. (1994) Paired helical filament τ in Alzheimer's disease: The kinase connection. Am. J. Path. 144, 449-453.
60. Tucker R. P. (1990) The roles of microtubule-associated proteins in brain morphogenesis: a review. Brain Res. Rev. 15, 101-120.
61. Yoshida H. and Ihara Y. (1993) τ in paired helical filaments is functionally distinct from fetal τ: Assembly incompetence of paired helical filament-τ. J. Neurochem. 61, 1183-1186.