Stress-activated protein kinase/c-Jun N-terminal kinase phosphorylates τ protein

Journal of Neurochemistry

Volumn 68, Issue 4, 1997, Pages 1736-1744

  Reynolds, C Hugh ^a   Utton, Michelle A ^a,b   Gibb, Graham M ^a   Yates, Alexandra ^a   Anderton, Brian H ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GUY S HOSPITAL   (United Kingdom)

Author keywords

Alzheimer's disease; c Jun N terminal kinase; Paired helical filaments; Stress activated protein kinase; protein

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; RECOMBINANT ENZYME; RECOMBINANT PROTEIN; SERINE; TAU PROTEIN; THREONINE;

ALZHEIMER DISEASE; ARTICLE; IMMUNOBLOTTING; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0030943263     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.68041736.x     Document Type: Article

References (75)

1. Anderson A. J., Cummings B. J., and Cotman C. W. (1994) Increased immunoreactivity for Jun- and Fos-related proteins in Alzheimer's disease: association with pathology. Exp. Neurol. 125, 286-295.
2. Anderson A. J., Pike C. J., and Cotman C. W. (1995) Differential induction of immediate early gene proteins in cultured neurons by β-amyloid (Aβ): association of c-Jun with Aβ-induced apoptosis. J. Neurochem. 65, 1487-1498.
3. Anderson A. J., Su J. H., and Cotman C. W. (1996) DNA damage and apoptosis in Alzheimer's disease: colocalization with c-Jun immunoreactivity, relationship to brain area, and effect of postmortem delay. J. Neurosci. 16, 1710-1719.
4. Baudier J. and Cole R. D. (1987) Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalyzed by a calcium/ calmodulin-dependent kinase and modulated by phospholipids. J. Biol. Chem. 262, 17577-17583.
5. 2+/phospholipid-dependent protein kinase C. J. Biol. Chem. 262, 17584-17590.
6. 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. FEBS Lett. 336, 417-424.
7. Ben-Levy R., Leighton I. A., Doza Y. N., Attwood P., Morrice N., Marshall C. J., and Cohen P. (1995) Identification of novel phosphorylation sites required for activation of MAPKAP kinase-2. EMBO J. 14, 5920-5930.
8. Boyle W. J., van der Geer P., and Hunter T. (1991) Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201, 110-149.
9. Brion J. P., Hanger D. P., Couck A. M., and Anderton B. H. (1991) A68 proteins in Alzheimer's disease are composed of several tau isoforms in a phosphorylated state which affects their electrophoretic mobilities. Biochem. J. 279, 831-836.
10. Brion J.-P., Couck A.-M., Robertson J., Loviny T. L. F., and Anderton B. H. (1993a) Neurofilament monoclonal antibodies RT97 and 8D8 recognize different modified epitopes in paired helical filament-τ in Alzheimer's disease. J. Neurochem. 60, 1372-1382.
11. Brion J.-P., Smith C., Couck A.-M., Gallo J.-M., and Anderton B. H. (1993b) 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. Carletti R., Tacconi S., Bettini E., and Ferraguti F. (1995) Stress activated protein kinases, a novel family of mitogen-activated protein kinases, are heterogeneously expressed in the adult rat brain and differentially distributed from extracellular-signal-regulated protein kinases. Neuroscience 69, 1103-1110.
13. Coleman M. P. and Anderton B. H. (1990) Phosphate-dependent monoclonal antibodies to neurofilaments and Alzheimer neurofibrillary tangles recognize a synthetic phosphopeptide. J. Neurochem. 54, 1548-1555.
14. Correas I., Diaz-Nido J., and Avila J. (1992) Microtubule-associated protein tau is phosphorylated by protein kinase C on its tubulin binding domain. J. Biol. Chem. 267, 15721-15728.
15. Davis D. R., Brion J.-P., Couck A.-M., Gallo J.-M. Hanger D. P., Ladhani K., Lewis C., Miller C. C. J., Rupniak T., Smith C., and Anderton B. H. (1995) The phosphorylation state of the microtubule-associated protein tau as affected by glutamate, colchicine and β-amyloid in primary rat cortical neuronal cultures. Biochem. J. 309, 941-949.
16. Davis R. J. (1994) MAPKs: new JNK expands the group. Trends Biochem. Sci. 19, 470-473.
17. Dérijard B., Hibi M., Wu I.-H., Barrett T., Su B., Deng T., Karin M., and Davis R. J. (1994) JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76, 1025-1037.
18. Drewes G., Lichtenberg-Kraag B., Doring F., Mandelkow E., Biernat J., Goris J., Doree M., and Mandelkow E. (1992) Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBO J. 11, 2131-2138.
19. mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262. J. Biol. Chem. 270, 7679-7688.
20. Garver T. D., Harris K. A., Lehman R. A. W., Lee V. M.-Y., Trojanowski J. Q., and Billingsley M. L. (1994) τ phosphorylation in human, primate, and rat brain: Evidence that a pool of τ is highly phosphorylated in vivo and is rapidly dephosphorylated in vitro. J. Neurochem. 63, 2279-2287.
21. Goedert M., Spillantini M. G., Jakes R., Rutherford D., and Crowther R. A. (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519-526.
22. Goedert M., Spillantini M. G., Cairns N. J., and Crowther R. A. (1992) Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8, 159-168.
23. 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. Natl. Acad. Sci. USA 90, 5066-5070.
24. Goedert M., Jakes R., Crowther R. A., Cohen P., Vanmechelen E., Vandermeeren M., and Cras P. (1994) 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.
25. Goedert M., Jakes R., and Vanmechelen E. (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci. Lett. 189, 167-170.
26. Greenberg S. G., Davies P., Schein J. D., and Binder L. I. (1992) Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J. Biol. Chem. 267, 564-569.
27. Greenwood J. A., Scott C. W., Spreen R. C., Caputo C. B., and Johnson G. V. W. (1994) Casein kinase II preferentially phosphorylates human tau isoforms containing an amino-terminal insert Identification of threonine 39 as the primary phosphate acceptor. J. Biol. Chem. 269, 4373-4380.
28. Gupta S., Campbell D., Derijard B., and Davis R. J. (1995) Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267, 389-393.
29. Ham J., Whitfield J., Eilers A., Lallemand D., and Rubin L. L. (1996) c-Jun and programmed cell death in the developing nervous system. (Abstr. 412). Keystone Symposium: Signaling in Neuronal Development, Differentiation and Degeneration, Taos, New Mexico, p. 153.
30. 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.
31. Hasegawa M., Jakes R., Crowther R. A., Lee V. M. Y., Ihara Y., and Goedert M. (1996) Characterization of mAb AP422, a novel phosphorylation-dependent monoclonal antibody against tau protein. FEBS Lett. 384, 25-30.
32. Hibi M., Lin A., Smeal T., Minden A., and Karin M. (1993) Identfication of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7, 2135-2148.
33. Hoshi M., Nishida E., Miyata Y., Sakai H., Miyoshi T., Ogawara H., and Akiyama T. (1987) Protein kinase C phosphorylates tau and induces its functional alterations. FEBS Lett. 217, 237-241.
34. 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.
35. 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. (Tokyo) 104, 319-321.
36. Ishiguro K., Takamatsu M., Tomizawa K., Omori A., Takahashi M., Arioka M., Uchida T., and Imahori K. (1992a) Tau protein kinase I converts normal tau into A68-like component of paired helical filaments. J. Biol. Chem. 267, 10897-10901.
37. Ishiguro K., Omori A., Takamatsu M., Sato K., Arioka M., Uchida T., and Imahori K. (1992b) 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.
38. 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.
39. 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.
40. Kenessey A. and Yen S.-H. C. (1993) The extent of phosphorylation of fetal tau is comparable to that of PHF-tau from Alzheimer paired helical filaments. Brain Res. 629, 40-46.
41. Kobayashi S., Ishiguro K., Omori A., Takamatsu M., Arioka M., Imahori K., and Uchida T. (1993) A cdc2-related kinase PSSA-LRE/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.
42. Köpke E., Tung Y.-C., Shaikh S., Alonso A. C., Iqbal K., and Grundke-Iqbal I. (1993) Microtubule-associated protein tau: abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J. Biol. Chem. 268, 24374-24384.
43. Ksiezak-Reding H., Liu W.-K., and Yen S.-H. (1992) Phosphate analysis and dephosphorylation of modified tau associated with paired helical filaments. Brain Res. 597, 209-219.
44. Kyriakis J. M., Banerjee P., Nikolakaki E., Dai T., Rubie E. A., Ahmad M. F., Avruch J., and Woodgett J. R. (1994) The stress-activated protein kinase subfamily of c-Jun kmases. Nature 369, 156-160.
45. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
46. 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. FEBS Lett. 365, 42-46.
47. Ledesma M. D., Correas I., Avila J., and Diaz Nido J. (1992) Implication of brain cdc2 and MAP2 kinases in the phosphorylation of tau protein in Alzheimer's disease. FEBS Lett. 308, 218-224.
48. Lee J. C., Laydon J. T., McDonnell P. C., Gallagher T. F., Kumar S., Green D., McNulty D., Blumenthal M. J., Heys J. R., Landvatter S. W., Strickler J. E., McLaughlin M. M., Siemens I. R., Fisher S. M., Livi G. P., White J. R., Adams J. L., and Young P. R. (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372, 739-746.
49. 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. (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.
50. Luo Y. Q., Hirashima N., Li Y. H., Alkon D. L., Sunderland T., Etcheberrigaray R., and Wolozin B. (1995) Physiological levels of β-amyloid increase tyrosine phosphorylation and cytosolic calcium. Brain Res. 681, 65-74.
51. Mandelkow E. M., Drewes G., Biernat J., Gustke N., Van Lint J., Vandenheede J. R., and Mandelkow E. (1992) Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett. 314, 315-321.
52. 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.
53. Mawal-Dewan M., Henley J., Van de Voorde A., Trojanowski J. Q., and Lee V. M.-Y. (1994) The phosphorylation state of tau in the developing rat brain is regulated by phosphoprotein phosphatases. J. Biol. Chem. 269, 30981-30987.
54. McGeer P. L. and McGeer E. G. (1995) The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res. Rev. 21, 195-218.
55. Mertens S., Craxton M., and Goedert M. (1996) SAP kinase-3, a new member of the family of mammalian stress-activated protein kinases. FEBS Lett. 383, 273-276.
56. 3F12 kinase: a novel MAP kinase expressed in a subset of neurons in the human nervouse system. Neuron 14, 67-78.
57. 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.
58. Mulot S. F. C., Hughes K., Woddgett J. R., Anderton B. H., and Hanger D. P. (1994) 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 systhase kinase-3β. FEBS Lett. 349, 359-364.
59. Pierre M. and Nunez J. (1983) Multisite phosphorylation of tau proteins from rat brain. Biochem. Biophys. Res. Commun. 115, 212-219.
60. Pulverer B. J., Hughes K., Franklin C. C., Kraft A. S., Leevers S. J., and Woodgett J. R. (1993) Co-purification of mitogen-activated protein kinases with phorbol ester-induced c-Jun kinase activity in U937 leukaemic cells. Oncogene 8, 407-415.
61. Raingeaud J., Gupta S., Rogers J. S., Dickens M., Han J., Ulevitch R. J., and Davis R. J. (1995) Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270, 7420-7426.
62. Robertson J., Loviny T. L. F., Goedert M., Jakes R., Murray K. J., Anderton B. H., and Hanger D. P. (1993) Phosphorylation of tau by cyclic-AMP-dependent protein kinase. Dementia 4, 256-263.
63. Rouse J., Cohen P., Trigon S., Morange M., Alonso-Llamazares A., Zamanillo D., Hunt T., and Nebreda A. R. (1994) A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78, 1027-1037.
64. Seger R. and Krebs E. G. (1995) The MAPK signaling cascade. FASEB J. 9, 726-735.
65. Singh T. J., Grundke-Iqbal I., McDonald B., and Iqbal K. (1994) Comparison of the phosphorylation of microtubule-associated protein tau by non-proline dependent protein kinases. Mol. Cell. Biochem. 131, 181-189.
66. Singh T. J., Grundke-Iqbal I., and Iqbal K. (1996) Differential phosphorylation of human tau isoforms containing three repeats by several protein kinases. Arch. Biochem. Biophys. 328, 43-50.
67. Smith C. and Anderton B. H. (1994) Dorothy Russell Memorial Lecture. The molecular pathology of Alzheimer's disease: are we any closer to understanding the neurodegenerative process? Neuropathol. Appl. Neurobiol. 20, 322-338.
68. Smith D. B. and Johnson K. S. (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67, 31-40.
69. Takahashi M., Tomizawa K., Sato K., Ohtake A., and Omori A. (1995a) A novel tau-tubulin kinase from bovine brain. FEBS Lett. 372, 59-64.
70. Takahashi M., Tomizawa K., Ishiguro K., Takamatsu M., Fujita S. C., and Imahori K. (1995b) Involvement of τ protein kinase I in paired helical filament-like phosphorylation of the juvenile τ in rat brain. J. Neurochem. 64, 1759-1768.
71. 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.
72. Xia Z. G., Dickens M., Raingeaud J., Davis R. J., and Greenberg M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
73. 2+, calmodulin-dependent regulation of microtubule-associated protein 2, tau factor, and tubulin, and comparison with cyclic AMP-dependent phosphorylation. J. Neurochem. 44, 759-768.
74. Yang S. D., Yu J. S., and Lai Y. G. (1991) Identification and characterization of the ATP·Mg-dependent protein phosphatase activator (FA) as a microtubule protein kinase in the brain. J. Protein Chem. 10, 171-181.
75. Zhang F., Strand A., Robbins D., Cobb M. H., and Goldsmith E. J. (1994) Atomic structure of the MAP kinase ERK2 at 2.3 Å resolution. Nature 367, 704-711.