The order of exposure of tau to signal transduction kinases alters the generation of 'AD-like' phosphoepitopes

Cellular and Molecular Neurobiology

Volumn 19, Issue 2, 1999, Pages 223-233

  Shea, Thomas B ^a   Cressman, Corrine M ^a  

^a UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

Author keywords

Alzheimer's disease; Kinases; Paired helical filaments; Phosphorylation; Signal transduction; Tau

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; EPITOPE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE C;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CATALYSIS; DENSITOMETRY; DEPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGENETICS; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADULT; ALZHEIMER DISEASE; ANTIGENS; BINDING, COMPETITIVE; BRAIN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EPITOPES; HUMANS; NERVE TISSUE PROTEINS; NEUROFIBRILLARY TANGLES; PHOSPHATIDYLSERINES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE C; SIGNAL TRANSDUCTION; TAU PROTEINS;

ANIMALIA;

EID: 0033048702     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006977127422     Document Type: Article

References (46)

1. Arioka, M., Tsukamoto, M., Ishiguro, K., Kato, R., Sato, K., Imahori, K., and Uchida, T. (1993). Tau protein kinase-1 is involved in the regulation of the normal phosphorylation state of tau protein. J. Neurochem. 60:461-468.
2. 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.
3. 2+/phospholipid-dependent protein kinase C. J. Biol. Chem. 262:17584-17590.
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. FEBS Lett. 336:417-424.
5. Biemat, J., Mandelkow, E.-M., and Schroter, C. (1992). 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.
6. Blanchard, B. J., Raghunandan, R. D., Roder, H. M., and Ingram, V. M. (1994). Hyperphosphorylation of human tau by brain kinase PK40erk beyond phosphorylation by cAMP-dependent PKA: Relation to Alzheimer's disease. Biochem. Biophys. Res. Commun. 200:187-194.
7. Brambett, G. T., Goedert, M., Jakes, R., Merrick, S. E., Trojanowski, J. Q., and Lee, V. M.-Y. (1993). Abnormal tau phosphorylation at ser-396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10:1089-1099.
8. Boyce, J. J., and Shea, T. B. (1997). Phosphorylation events mediated by protein kinase Ca and e participate in regulation of tau steady-state levels and generation of certain "Alzheimer-like" phospho-epitopes. Int. J. Dev. Neurosci. 15:295-307.
9. Cressman, C. M., and Shea, T. B. (1995). Hyperphosphorylation of tau and filopodial retraction following microinjection of protein kinase C catalytic subunits. J. Neurosci. Res. 42:648-656.
10. Cressman, C. M., Mercken, M. M., and Shea, T. B. (1995). Alteration in tau antigenicity and electrophoretic migration by PKC under cell-free conditions. Neurosci. Res. Commun. 17:61-64.
11. Goedert, M., Jakes, R., Crowther, R. A., Six, J., Lubke, U., Vandermeeren, M., Cras, P., Trojanowski, J. Q., and Lee, V. M.-Y. (1993a). The abnormal phosphorylation of tau proteins at ser-202 in Alzheimer's disease recapitulates phosphorylation during development. Proc. Natl. Acad. Sci. USA. 90:5066-5070.
12. Goedert, M., Jakes, R., Crowther, R. A., Six, J., Lubke, U., Vandermeeren, M., Cras, P., Trojanowski, J. Q., and Lee, V. M.-Y. (1993b). The abnormal phosphorylation of tau proteins at ser-202 in Alzheimer's disease recapitulates phosphorylation during development. Proc. Natl. Acad. Sci. USA 90:5066-5070.
13. Goedert, M., Jakes, R., Crowther, R. A., Cohen, P., Vanmechelen, E., Vandermeeren, M., and Cras, P. (1994a). Epitope mapiated protein tau are dephosphorylated by protein phosphatase 2A-1. FEBS Lett. 312:95-99.
14. Goedert, M., Jakes, R., Crowther, R. A., Cohen, P., Vanmechelen, E., Vandermeeren, M., and Cras, P. (1994b). 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.
15. 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 localization of the kinase. Neurosci. Lett. 147:58-62.
16. Hollingsworth, E. B., Ukena, D., and Daly, J. W. (1986). The protein kinase C activator phorbol12myristate-13-acetate enhances cyclic AMP accumulation in pheochromocytoma cells. FEBS Lett. 196:131-134.
17. Kobayashi, S., Ishiguro, K., Omori, A., Takamatsu, M., Arioka, M., Imahora, K., and Uchida, T. (1993). A cdc-related kinase PSSALRE/cdk5 is homologous with the 30kDa subunit of tau protein kinase-1, a proline-directed kinase associated with microtubules. FEBS Lett. 335:171-175.
18. Kosik, K. S., and Greenberg, S. M. (1994). Tau protein and Alzheimer's disease. In Terry, R. D., Katzman, R., and Bick, K. L. (eds.), Alzheimer's Disease, Raven Press, New York, pp. 335-344.
19. Lang, E., and Otvos, L. (1992). A serine-proline change in the Alzheimer's disease-associated epitope Tau-2 results in altered secondary structure, but phosphorylation overcomes the conformational gap. Biochem. Biophys. Res. Commun. 188:162-169.
20. Latimer, D. A., Gallo, J.-M., Lovestone, S., Miller, C. C. J., Reynolds, C. H., Marquardt, B., Stable, 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.
21. Ledesma, M. D., Correas, L., Avila, J., and Diaz-Nido, J. (1992). Implication of brain cdc2 and MPA kinases in the phosphorylation of tau protein in Alzheimer's disease. FEBS Lett. 308:218-224.
22. Liu, W.-K., Moore, W. T., Williams, R. T., Hall, F. L., and Yen, S.-H. (1993). Application of synthetic phospho- and unphospho- peptides to identify phosphorylation sites in a subregion of the tau molecules, which is modified in Alzheimer's disease. J. Neurosci. Res. 34:371-376.
23. Lu, W., Soria, J. P., and Wood, J. G. (1993). p44mpk MAP kinase induces Alzheimer type alterations in tau function and in primary hippocampal neurons. J. Neurosci. Res. 35:439-444.
24. 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's disease-like state of microtubule-associated protein tau. FEBS Lett. 314:315-321.
25. Mandelkow, E.-M., Biernat, J., Drewes, G., Gustke, N., Trinczek, B., and Mandelkow, E. (1995). Tau domains, phosphorylation, and interactions with microtubules. Neurobiol. Aging 16:355-362.
26. 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.
27. Mulot, S. F. C., Hughes, K., Woodgett, 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 synthase kinase-3β. FEBS Lett. 349:359-364.
28. 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.
29. Pelech, S. L. (1995). Networking with proline-directed protein kinases implicated in tau phosphorylation. Neurobiol. Aging 16:247-261.
30. Pelech, S. L., and Sangria, J. S. (1992). Mitogen-activated protein kinases: Versatile transducers for cell signaling. Trends Biochem. Soc. 17:233-238.
31. Peraldi, P., Frodin, M., Barnier, J. V., Calleja, V., Scimeca, J.-C., Filloux, C., Calothy, G., and Van Obberghen, E. (1995). Regulation of the MAP kinase cascade in PC12 cells: B-Raf activates MEK-I (MAP kinase or ERK kinase) and is inhibited by cAMP. FEBS Lett. 357:290-296.
32. Pundreddy, S., and Shea, T. B. (1997). AD-like tau phosphorylation in human neuroblastoma cells following PKC hyperactivation is mediated by MAP kinase. Neurosci. Res. Commun. 21:173-177.
33. Raghunandan, R., and Ingram, V. M. (1995). Hyperphosphorylation of the cytoskeletal protein tau by the MAP-kinase PK40erk: Regulation by prior phosphorylation with cAMP-dependent protein kinase A. Biochem. Biophys. Res. Commun. 215:1056-1066.
34. Sengupta, A., Wu, Q., Grundkle-Iqbal, I., Iqbal, K., and Singh, T. J. (1997). Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by cdk5. Mol. Cell. Biochem. 167:99-105.
35. Shea, T. B. (1997). Phosphatidyl serine alters tau antigenicity, phosphorylation, proteolysis and association with microtubules: Implication for tau function under normal and degenerative conditions. J. Neurosci. Res. 50:114-122.
36. Shea, T. B., and Beermann, M. L. (1994). Respective roles of neurofilaments, microtubules, MAP1B and tau in the outgrowth and stabilization of axonal neurites. Mol. Biol. Cell. 5:863-875.
37. Shea, T. B., Beermann, M. L., Nixon, R. A., and Fischer, I. (1992a). Microtubule-associated protein tau is required for axonal neurite elaboration by neuroblastoma cells. J. Neurosci. Res. 32:363-374.
38. Shea, T. B., Beermann, M. L., Leli, U., and Nixon, R. A. (1992b). Opposing influences of protein kinase activities on neurite outgrowth in human neuroblastoma cells: Initiation by kinase A and restriction by kinase C. J. Neurosci. Res. 33:398-407.
39. Shea, T. B., Spencer, M. J., Beerman, M. L., Cressman, C. M., and Nixon, R. A. (1996). Calcium influx into human neuroblastoma cells induces ALZ-50 immunoreactivity: Involvement of calpain-mediated hydrolysis of protein kinase. C. J. Neurochem. 66:1539-1549.
40. Singh, T. J., Zaidi, T., Grundke-Iqbal, I., and Iqbal, K. (1994). Modulation of GSK-3-catalyzed phosphorylation of microtuble-associated protein tau by non-proline-dependent protein kinases. FEBS Lett. 358:4-8.
41. Singh, T. J., Haque, N., Grundke-Iqbal, I., and Iqbal, K. (1994b). Rapid Alzheimer-like phosphorylation of tau by the synergistic actions of non-proline dependent kinases and GSK-3. FEBS Lett. 358:267-272.
42. 2+-calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J. 9:3539-3544.
43. Szendrei, G. I., Lee, V. M.-Y., and Otvos, L. (1993). 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.
44. Trojanowski, J. Q., Schmidt, M. L., Shin, R.-W., Bramblett, G. T., Rao, D., and Lee, V. M.-Y. (1993a). Altered tau and neurofilament proteins in neurodegenerative diseases: Diagnostic implications for Alzheimer's disease and Lewy body dementias. Brain Pathol. 3:45-54.
45. Trojanowski, J. Q., Schmidt, M. L., Shin, R.-W., Bramblett, G. T., Goedert, M., and Lee, V. M.-Y. (1993b). PHF tau (A68): From pathological marker to potential mediator of neuronal dysfunction and degeneration in Alzheimer's disease. Clin. Neurosci. 1:184-191.
46. Vulliet, R., Halloran, 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.