β-amyloid and ionophore A23187 evoke tau hyperphosphorylation by distinct intracellular pathways: Differential involvement of the calpain/protein kinase C system

Journal of Neuroscience Research

Volumn 49, Issue 6, 1997, Pages 759-768

  Shea, Thomas B ^a   Prabhakar, Sathya ^a   Ekinci, Fatma J ^a  

^a UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

Author keywords

amyloid; Alzheimer's disease; Calcium; Calcium ionophore; Calpain; Paired helical filaments; PHF 1; Phosphorylation; Protein kinase C; Tau

Indexed keywords

1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; AMINO ACID; AMYLOID BETA PROTEIN; ANTIBODY; ANTISENSE OLIGONUCLEOTIDE; CALCIMYCIN; CALCIUM; CALPAIN; CALPEPTIN; EGTAZIC ACID; EPITOPE; PHOSPHATE; PROTEIN KINASE C; SYNTHETIC PEPTIDE; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMYLOID BETA-PROTEIN; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; BIOLOGICAL MARKERS; CALCIMYCIN; CALCIUM; CALPAIN; EPITOPES; HUMANS; IONOPHORES; NEUROBLASTOMA; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE C; TAU PROTEINS; TUMOR CELLS, CULTURED;

EID: 0030986545     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19970915)49:6<759::AID-JNR10>3.0.CO;2-N     Document Type: Article

References (58)

1. Arias C, Arrieta I, Tapia R (1995): β-amyloid peptide fragment 25-35 potentiates the calcium-dependent release of excitatory amino acids from depolarized hippocampal slices. J Neurosci Res 41:561-566.
2. Arispe N, Rojas E, Pollard HB (1993): Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: Block-age by tromethamine and aluminum, Proc Natl Acad Sci USA 90:567-571.
3. Baudier J, Cole DR (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.
4. Baumann K, Mandelkow E-M, Biernat J, Piwnica-Worms H, Mandelkow E (1993): Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett 336:417-424.
5. Boyce JJ, Shea TB (in press): Phosphorylation events mediated by protein kinase Ca and e participate in the regulation of tau steady-state levels and generation of certain "Alzheimer-like" phospho-epitopes. Int J Dev Neurosci, in press.
6. Busciglio J, Lorenzo A, Yeh J, Yankner BA (1995): β-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14:879-888.
7. Cotman CW, Pike CJ, Copani A (1992): β-amyloid neurotoxicity: A discussion of in vitro findings. Neurobiol Aging 13:587-590.
8. Cressman CM, Shea TB (1995): Hyperphosphorylation of tau and filopodial retraction following microinjection of protein kinase C catalytic subunits. J Neurosci Res 42:648-656.
9. Cressman CM, Mercken MM, Shea TB (1995): Alteration in tau antigenicity and electrophoretic migration by PKCα under cell-free conditions. Neurosci Res Commun 17:61-64.
10. Drewes G, Lichtenberg-Kragg B, Doring F, Mandelkow E-M, Bienart J, Doree M, Mandelkow E (1992): Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBO J 11:2131-2138.
11. Goedert M, Cohen ES, Jakes R, Cohen P (1992): p42 MAP kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2Al. FEBS Lett 312:95-99.
12. Goedert M, Jakes R, Crowther RA, Six J, Lubke U, Vandermeeren M, Cras P, Trojanowski JQ, Lee VM-Y (1993): The abnormal phosphorylation of tau proteins at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proc Natl Acad Sci USA 90:5066-5070.
13. Furukawa K, Smith-Swintosky VL, Mattson MP (1995): Actin depolymerization protects hippocampal neurons against excitoxicity and amyloid β-peptide toxicity by stabilizing calcium homeostasis. In Fiskum G (ed): "Neurodegenerative Diseases '95: Molecular and Cellular Mechanisms and Therapeutic Advances." Proceedings of the XVth Washington International Spring Symposium p 109.
14. Gibson GE, Peterson C (1987): Calcium and the aging nervous system. Neurobiol Aging 8:329-343.
15. Gray CW, Patel AJ (1995): Neurodegeneration mediated by glutamate and β-amyloid peptide: a comparison and possible interaction. Brain Res 691:169-179.
16. Haass C, Schlossmacher MG, Hung AY, Vigo-Pelfrey C, Mellon A, Ostaszewski BL, Lieberburg I, Koo EH, Schenk D, Teplow DB, Selkoe DJ (1992): Amyloid β-peptide is produced by cultured cells during normal metabolism. Nature 359:322-325.
17. Hanger DP, Hughes K, Woodgett JR, Brion JP, Anderton BH (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.
18. Hartmann H, Eckert A, Muller WE (1993): β-amyloid protein amplifies calcium signalling in central neurons from the adult mouse. Biochem Biophys Res Commun 194:1216-1220.
19. Higaki J, Quon D, Zhong Z, Cordell B (1995): Inhibition of β-amyloid formation identifies proteolytic precursors and subcellular site of catabolism. Neuron 14:651-659.
20. Johnson GVW, Jope RS, Binder LI (1989): Proteolysis of tau by calpain. Biochem Biophys Res Commun 163:1505-1511.
21. 2+/calmodulin-dependent protein kinase II. J Neurosci Res 34:642-647.
22. Khafki H-W, Paganetti PA, Sommer B, Staufenbiek M (1996): Calpain inhibitor I decreases βA4 secretion from human embryonal kidney cells expressing β-amyloid precursor protein carrying the APP670/671 double mutation. Neurosci Lett 201:29-32.
23. Kampfl A, Whitson JS, Zhao X, Posmantur R, Clifton GL, Hayes RL (1995): Calpain inhibitors reduce depolarization induced loss of tau protein in primary septo-hippocampal cultures. Neurosci Lett 194:149-152.
24. Kobayahi S, Ishiguro K, Omori A, Takamatsu M, Arioka M, Imahora K, 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 Lett 335:171-175.
25. Kosik KS (1992): Alzheimer's disease: A cell biological perspective. Science 256:780-783.
26. Kosik KS, Orecchio LD, Binder L, Trojanowski JQ, Lee VM-Y, Lee G (1988): Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1:817-825.
27. Kowall NW, Beal MF, Busciglio J, Duffy K, Yankner BA (1991): An in vivo model for the neurodegenerative effects of β-amyloid and protection by substance P. Proc Natl Acad Sci USA 88:7247-7251.
28. Lambert MP, Stevens G, Sabo S, Barber K, Wang G, Wade W, Krafft G, Snyder S, Holzman TF, Klein WL (1994): β/A4-evoked degeneration of differentiated SH-SY5Y human neuroblastoma cells. J Neurosci Res 39:377-385.
29. Ledesma MD, Correas L, Avila J, Diaz-Nido J (1992): Implication of brain cdc2 and MAP kinases in the phosphorylation of tau protein in Alzheimer's disease. FEBS Lett 308:218-224.
30. Litersky JM, Scott CW, Johnson GVW (1993): Phosphorylation, calpain proteolysis and tubulin binding of recombinant human tau isoforms. Brain Res 604:32-40.
31. Mandelkow E-M, Drewes G, Biernat J, Gustke N, Van Lint J, Vandenheede JR, Mandelkow E (1992): Glycogen synthase kinase 3 and the Alzheimer's disease-like state of microtubule-associated protein tau. FEBS Lett 314:315-321.
32. Mark RJ, Mattson MP (1995): Mechanism of amyloid β-peptide neurotoxicity involves impairment of ion-motive ATPases. In Fiskum G (ed): "Neurodegenerative Diseases '95: Molecular and Cellular Mechanisms and Therapeutic Advances." Proceedings of the XVth Washington International Spring Symposium, p 84.
33. Mattson MP (1990): Antigenic changes similar to those seen in neurofibrillary tangles are elicited by glutamate and Ca2+ influx in cultured hippocampal neurons. Neuron 4:105-117.
34. Mattson MP (1991): Evidence for the involvement of protein kinase C in neurodegenerative changes in cultured human cortical neurons. Exp Neurol 112:95-103.
35. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE (1992): β-amyloid peptides destabilized calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389.
36. Mattson MP, Tomaselli KJ, Rydel RE (1993): Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res 621:35-49.
37. Mulot SFC, Hughes K, Woodgett JR, Anderton BH, Hanger DP (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 Lett 349:359-364.
38. Paudel HK, Lew J, Zenobia A, Wang JH (1993): Brain proline-directed kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments. J Biol Chem 268:23512-23518.
39. Pike CJ, Walencewitz AJ, Glabe CG, Cotman CW (1991): In vitro aging of beta-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res 563:311-314.
40. Pike CJ, Burdick D, Walencewicz AJ, Glabe CG, Cotman CW (1993): Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J Neurosci 13:1676-1687.
41. Pope WB, Enam SA, Bawa N, Miller BE, Ghanbari HA, Klein WL (1993): Phosphorylated tau epitope of Alzheimer's disease is coupled to axon development in the avian central nervous system. Exp Neurol 120:106-113.
42. Pope WB, Lambert MP, Leypold B, Seupaul R, Sletten L, Krafft G, Klein WL (1994): Microtubule-associated protein tau is hyperphosphorylated during mitosis in the human neuroblastoma cell line SH-SY-5Y. Exp Neurol 126:185-194.
43. Shea TB, Beermann ML (1991): Stauroporine-induced morphological differentiation of human neuroblastoma cells. Cell Biol Internat Rep 15:161-168.
44. Shea TB, Cressman CM, Spencer MJ, Beermann ML, Nixon RA (1995a): Enhancement of neurite outgrowth following calpain inhibition is mediated by protein kinase C. J Neurochem 65:517-527.
45. Shea TB, Klinger EP, Cressman CM (1995b): Calcium influx recruits an additional class of kinases to hyperphosphorylate tau. NeuroReport 6:1309-1312.
46. Shea TB, Cressman CM, Beermann ML, Nixon RA (1996a): Calcium influx into human neuroblastoma cells induces ALZ-50 immunoreactivity: Involvement of calpain-mediated hydrolysis of protein kinase C. J Neurochem 66:1539-1549.
47. Shea TB, Boyce JJ, Cressman CM (1996b): Potential role of hyperactivation of signal transduction pathways in Alzheimer's disease: Protein kinase C regulates PHF-like phosphorylation of tau within neuronal cells. In: "Therapies and Emerging Strategies: Procedings of the XV Washington Spring Symposium on Neurodegenerative Diseases." New York: Plenum Press, pp 447-467.
48. Shea TB, Dergay A, Ekinci FJ (1997): β-amyloid-induced hyperphosphorylation of tau in human neuroblastoma cells involves MAP kinase. Neurosci Res Commun, in press.
49. Shoji M, Golde TE, Ghiso J, Cheung TT, Estus S, Shaffer LM, Cai X-D, McKay DM, Tintner R, Frangione B, Younkin SG (1992): Production of the Alzheimer amyloid β protein by normal proteolytic processing. Science 258:126-129.
50. Siman R, Card JP, Davis LG (1990): Proteolytic processing of β-amyloid precursor by calpain I. J Neurosci 10:2400-2411.
51. Simmons LK, May PC, Tomaselli KJ, Rydel RE, Fusion KS, Brigham EF, Wright S, Lieberburg I, Becker GW, Brems DN, Li WY (1994): Secondary structure of amyloid β peptide correlates with neurotoxic activity in vitro. Mol Pharmacol 45:373-379.
52. Snow AD, Seuœiguchi R, Nochlin D, Fraser P, Kimata K, Mizutani A, Arai M, Schreier WA, Morgan DG (1994) An important role of heparin sulfate proteoglycan (Perlecan) in a model system for the deposition and persistence of fibrillar Aβ amyloid in the rat brain. Neuron 12:219-234.
53. Takashima A, Noguchi K, Sato K, Hoshino T, Imahori K (1993): Tau protein kinase I is essential for amyloid-β-protein-indued neurotoxicity. Proc Natl Acad Sci USA 90:7789-7793.
54. Trojanowski JQ, Schmidt ML, Shin R-W, Bramblett GT, Rao D, Lee VM-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.
55. Trojanowski JQ, Schmidt ML, Shin R-W, Bramblett GT, Goedert M, Lee VM-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.
56. Vulliet R, Halloran SM, Braun RK, Smith AJ, Lee G (1992): Proline-directed phosphorylation of human tau protein. J Biol Chem 267:22570-22574.
57. Yankner BA, Dawes LS, Fisher S, Villa-Komaroff L, Oster-Granite ML, Neve RL (1989): Neurotoxicity of a fragment of the amyloid precursor protein associated with Alzheimer's disease. Science 245:417-420.
58. Zhou Y, Gopalakrishnan V, Richardson JS (1996): Actions of neurotoxic beta-amyloid on calcium homeostasis and viability of PC 12 cells are blocked by antioxidants but not by calcium channel antagonists. Int J Neurochem 67:1419-1425.