Phosphorylation events mediated by protein kinase Cα and ε participate in regulation of tau steady-state levels and generation of certain 'Alzheimer-like' phospho-epitopes

International Journal of Developmental Neuroscience

Volumn 15, Issue 3, 1997, Pages 295-307

  Boyce, John J ^a   Shea, Thomas B ^a  

^a University of Massachusetts Lowell   (United States)

Author keywords

Alzheimer's disease; Antisense oligonucleotides; Paired helical filaments; Phosphorylation; Protein kinase C; Signal transduction; tau

Indexed keywords

ANTIBODY; ANTISENSE OLIGONUCLEOTIDE; CALCIUM ION; ISOENZYME; MESSENGER RNA; PHORBOL ESTER; PHOSPHOPROTEIN; PROTEIN KINASE C; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DNA TRANSFECTION; ENZYME REGULATION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ALZHEIMER DISEASE; CALCIUM; EPITOPES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOENZYMES; MICROINJECTIONS; NEUROBLASTOMA; NEURONS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN KINASE C-EPSILON; RNA, ANTISENSE; SIGNAL TRANSDUCTION; TAU PROTEINS; TUMOR CELLS, CULTURED;

EID: 0030793593     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0736-5748(97)00010-5     Document Type: Article

References (47)

1. Azzi A., Boscobionik D. and Hensey C. (1992) The protein kinase C family. European Journal of Biochemistry 208, 547-557.
2. Bancher C., Grundke-Iqbal I., Iqbal K., Fried V. A., Smith H. T. and Wisniewski H. M. (1991) Abnormal phosphorylation of tau precedes ubiquitination in neurofibrillary pathology of Alzheimer's disease. Brain Research 539, 11-18.
3. Baudier J. and Cole D. R. (1987) Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalysed by a calcium/calmodulin-dependent kinase and modulated by phospholipids. Journal of Biological Chemistry 262, 17577-17583.
4. Baum L., Seger R., Woodgett J. R., Kawabata S., Maruyama K., Koyama M., Silver J. and Saito T. (1995) Overexpressed tau protein in cultured cells is phosphorylated without formation of PHF: implication of phosphoprotein phosphatase involvement. Molecular Brain Research 34, 1-17.
5. Baumann K., Mandelkow E.-M., Biernat J., Piwnica-Worms H. and Mandelkow E. (1993) Abnormal Alzheimer-like phosphorylation of tau-protein by cyclindependent kinases cdk2 and cdk5. FEBS Letters 336, 417-424.
6. Berra E., Diaz-Meco M. T., Lozano J., Frutos S., Munico M. M., Sanchez P., Sanz L. and Moscat J. (1995) Evidence for a role of MEK and MAPK during signal transduction by protein kinase C ζ. EMBO Journal 14, 6157-6163.
7. 2+ on the activation of conventional and new PKC isoforms and on TPA and endothelin-1 inducted translocations of these isozymes in intact cells. FEBS Letters 348, 21-26.
8. 2+-dependent proteinases (μ-calpain and m-calpain). Journal of Biological Chemistry 264, 10096-10103.
9. Correas I., Diaz-Nido J. and Avila J. (1992) Microtubule-associated protein tau is phosphorylated by protein kinase C on its tubulin-binding domain. Journal of Biological Chemistry 267, 15721-15728.
10. Cressman C. M. and Shea T. B. (1995) Hyperphosphorylation of tau and filopodial retraction following microinjection of protein kinase C catalytic subunits. Journal of Neuroscience Research 42, 648-656.
11. Cressman C. M., Mercken M. M. and Shea T. B. (1995) Alteration in tau antigenicity and electrophoretic migration by PKC α under cell-free conditions. Neuroscience Research Communications 17, 61-64.
12. Drewes G., Lichtenberg-Kragg B., Doring F., Mandelkow E.-M., Bienart J., Doree M. and Mandelkow E. (1992) Mitogen activated protein (MAP) kinase transform tau protein into an Alzheimer-like state. EMBO Journal 11, 2131-2138.
13. Goedert M., Cohen E. S., Jakes R. and Cohen P. (1992) p42 MAP kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2A1. FEBS Letters 312, 95-99.
14. Goedert M., Jakes R., Crowther R. A., Six J., Lubke U., Vandermeeren M., Cras P., Trojanowski J. Q. and Lee V. M.-Y. (1993) The abnormal phosphorylation of tau proteins at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proceedings of the National Academy of Science of the U.S.A. 90, 5066-5070.
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. Neuroscience Letters 147, 58-62.
16. 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 Letters 217, 237-241.
17. Hug H. and Sarre T. F. (1993) Protein kinase C isoenzymes: divergence in signal transduction?. Biochemistry Journal 291, 329-343.
18. Johnson G. V. W., Jope R. S. and Binder L. I. (1989) Proteolysis of tau by calpain. Biochemistry and Biophysics Research Communications 163, 1505-1511.
19. 2+/calmodulin-dependent protein kinase II. Journal of Neuroscience Research 34, 642-647.
20. Kobayahi 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 30 kDa subunit of tau protein kinase II, a proline-directed kinase associated with microtubules. FEBS Letters 335, 171-175.
21. Ledesma M. D., Correas L., Avila J. and Diaz-Nido J. (1992) Implication of brain cdc2 and MAP kinases in the phosphorylation of tau protein in Alzheimer's disease. FEBS Letters 308, 218-224.
22. Lee J. H., Goedert M., Hill W. D., Lee V. M.-Y. and Trojanowski J. Q. (1993) Tau proteins are abnormally expressed in olfactory epithelium of Alzheimer's disease and developmentally regulated in fetal spinal cord. Experimental Neurology 121, 93-105.
23. Leli U., Cataldo A. M., Shea T. B., Nixon R. A. and Hauser G. (1992) Distinct mechanisms of differentiation of SH-SY-5Y neuroblastoma cells by protein kinase C activators and inhibitors. Journal of Neurochemistry 58, 1191-1198.
24. Leli U., Parker P. J. and Shea T. B. (1992) Intracellular delivery of protein kinase C-a or -e isoform-specific antibodies promotes acquisition of a morphologically differentiated phenotype in neuroblastoma cells. FEBS Letters 297, 91-94.
25. Litersky J. M., Scott C. W. and Johnson G. V. W. (1993) Phosphorylation, calpain proteolysis and tubulin binding of recombinant human tau isoforms. Brain Research 604, 32-40.
26. Magoura D., Segos V. and Dawson G. (1993) protein kinase C-e is a developmentally regulated, neuronal isoform in the chick embryo central nervous system. Journal of Neuroscience Research 35, 488-498.
27. 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 Letters 314, 315-321.
28. Matstio 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.
29. Mattson M. P. (1991) Evidence for the involvement of protein kinase C in neurodegenerative changes in cultured human cortical neurons. Experimental Neurology 112, 95-103.
30. Mulot S. F. C., Hughes K., Woodgett J. R., Anderton B. H. and Hanger D. P. (1994) PHF-tau a 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-3b. FEBS Letters 349, 359-364.
31. Ono K., Fuji T., Ogita K., Kikkawa U., Igarahi K., Nishizuka Y. (1989) Proceedings National Academy of Science U.S.A. 86, 3099-3103.
32. Parker P. J., Coussens L., Totty N., Rhee L., Young S., Chen E., Stable S., Waterfield M., Ullrich A. (1986) Science 233, 853-859.
33. Paudel H. K., Lew J., Zenobia A. and Wang J. H. (1993) Brain proline-directed kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments. Journal of Biological Chemistry 268, 23512-23518.
34. Pope W. B., Enam S. A., Bawa N., Miller B. E., Ghanbari H. A. and Klein W. L. (1993) Phosphorylated tau epitope of Alzheimer's disease is coupled to axon development in the avian central nervous system. Experimental Neurology 120, 106-113.
35. Pope W. B., Lambert M. P., Leypold B., Seupaul R., Sletten L., Kraffi G. and Klein W. L. (1994) Microtubule-associated protein tau is hyperphosphorylated during mitosis in the human neuroblastoma cell line SH-SY-5Y. Experimental Neurology 126, 185-194.
36. Shea T. B. (1990) Neuritogenesis in mouse NB2a/d1 neuroblastoma cells: Triggering by calcium influx and involvement of actin and tubulin dynamics. Cell Biology International Reports 14, 967-979.
37. Shea T. B., Cressman C. M., Beermann M. L. and Nixon R. A. (1994) Hyperphosphorylation of tau following calcium influx into human neuroblastoma: role of calpain and PKC. Molecular Biology of the Cell 5, 168a.
38. Shea T. B., Beermann M. L., Spencer M. A. and Nixon R. A. (1995) Enhancement of neurite outgrowth following calpain inhibition is mediated by protein kinase C. Journal of Neurochemistry 65, 517-527.
39. Shea T. B., Spencer M. J., Beermann 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. Journal of Neurochemistry 66, 1539-1549.
40. Shea T. B. and Beermann M. L. (1991) Stauroporine-induced morphological differentiation of human neuroblastoma cells. Cell Biology International Reports 15, 161-168.
41. Singh, T. J., Zaidi, T., Grundke-Iqbal, I. and Iqbal, K., Modulation of GSK-3-catalyzed phosphorylation of microtubule-associated protein tau by non-proline directed kinases. FEBS Letters, 1995, 4-8.
42. 2+-calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO Journal 9, 3539-3544.
43. Tanaka T., Iqbal K., Trenkner E., Liu D. J. and Grundke-Iqbal I. (1995) Abnormally phosphorylated tau in SY5Y human neuroblastoma cells. FEBS Letters 360, 5-9.
44. Trojanowski J. Q., Schmidt M. L., Shin R.-W., Bramblett G. T., Rao D. and Lee V. M.-Y. (1993) Altered tau and neurofilament proteins in neurodegenative diseases: diagnostic implications for Alzheimer's disease and Lewy body dementias. Brain Pathology 3, 45-54.
45. Trojanowski J. Q., Schmidt M. L., Shin R. W., Bramblett G. T., Goedert M. and Lee V. M.-Y. (1993) PHF tau (A68): from pathological marker to potential mediator of neuronal dysfunction and degeneration in Alzheimer's disease. Clinical Neuroscience 1, 184-191.
46. Vincent U. and Davies P. (1990) ATP-induced less of Alz-50 immunoreactivity with the A68 proteins from Alzheimer brain is mediated by ubiquitin. Proceedings of the National Academy of Science of the U.S.A. 87, 4840-4844.
47. Vulliet R., Halloran S. M., Braun R. K., Smith A. J. and Lee G. (1992) Proline-directed phosphorylation of human tau protein. Journal of Biological Chemistry 267, 22570-22574.