Prion peptide induces neuronal cell death through a pathway involving glycogen synthase kinase 3

Biochemical Journal

Volumn 372, Issue 1, 2003, Pages 129-136

  Pérez, Mar ^a   Rojo, Ana I ^a   Wandosell, Francisco ^a   Díaz Nido, Javier ^a   Avila, Jesús ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Apoptosis; Glycogen synthase kinase 3; Lithium; Microtubule associated protein; Neurodegeneration; Neurotoxicity; Prion; Spongiform encephalopathy

Indexed keywords

CELLS; DEPOSITION; DISEASES; PROTEINS;

NEURONAL CELL DEATH;

BIOCHEMISTRY;

GLYCOGEN SYNTHASE KINASE 3; INSULIN; LITHIUM; MICROTUBULE ASSOCIATED PROTEIN 2; PRION PROTEIN; TAU PROTEIN;

AMYLOIDOSIS; ANIMAL CELL; ARTICLE; ATROPHY; CELL PROLIFERATION; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; GLIA CELL; MICROTUBULE; MOUSE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROBLASTOMA CELL; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION;

ANIMALS; APOPTOSIS; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; HYPOGLYCEMIC AGENTS; INSULIN; MICE; NEURONS; PEPTIDE FRAGMENTS; PRIONS;

ANIMALIA;

EID: 0038292054     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021596     Document Type: Article

References (62)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
2. Collinge, J. (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550
3. Brown, D. R. (2001) Prion and prejudice: normal protein and the synapse. Trends Neurosci. 24, 85-90
4. Chiesa, R. and Harris, D. A. (2001) Prion diseases what is the neurotoxic molecule? Neurobiol Dis. 8, 743-763
5. Giese, A., Groschup, M. H., Hess, B. and Kretzschmar, H. A. (1995) Neuronal cell death in scrapie-infected mice is due to apoptosis. Brain Pathol. 5, 213-221
6. Lucassen, P. J., Williams, A., Chung, W. C. and Fraser, H. (1995) Detection of apoptosis in murine scrapie. Neurosci. Lett. 198, 185-188
7. Williams, A., Lucassen, P. J., Ritchie, D. and Bruce, M. (1997) PrP deposition, microglial activation and neuronal apoptosis in murine scrapie. Exp. Neurol. 144, 433-438
8. Dorandeu, A., Wingertsmann, L., Chretien, F., Delisle, M. B., Vital, C., Parchi, P., Montagna, P., Lugaresi, E., Ironside, J. W., Budka, H. et al. (1998) Neuronal apoptosis in fatal familial insomnia. Brain Pathol. 8, 531-537
9. Gray, F., Chretien, F., Adle-Biassette, H., Dorandeu, A., Ereau, T., Delisle, M. B., Kopp, N., Ironside, J. W. and Vital, C. (1999) Neuronal apoptosis in Creutzfeldt-Jakob disease. J. Neuropathol. Exp. Neurol. 58, 321-328
10. Jamieson, E., Jeffrey, M., Ironside, J. W. and Fraser, J. R. (2001) Apoptosis and dendritic dysfunction precede prion protein accumulation in 87V scrapie. Neuroreport 12, 2147-2153
11. Muller, W. E., Ushijima, H., Schroder, H. C., Forrest, J. M., Schatton, W. F., Rytik, P. G. and Heffner-Lauc, M. (1993) Cytoprotective effect of NMDA receptor antagonists on prion protein (PrionSc)-induced toxicity in rat cortical cell cultures. Eur. J. Pharmacol. 246, 261-267
12. Post, K., Brown, D. R., Groschup, M., Kretzschmar, H. A. and Riesner, D. (2000) Neurotoxicity but not infectivity of prion proteins can be induced reversibly in vitro. Arch. Virol. 16(Suppl.), 265-273
13. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O. and Tagliavini, F. (1993) Neurotoxicity of a prion protein fragment. Nature (London) 362, 543-546
14. Brown, D. R., Herms, J. and Kretzschmar, H. A. (1994) Mouse cortical cells lacking cellular PrP survive in culture with a neurotoxic PrP fragment. Neuroreport 5, 2057-2060
15. White, A. R., Guirguis, R., Brazier, M. W., Jobling, M. F., Hill, A. F., Beyreuther, K., Barrow, C. J., Masters, C. L., Collins, S. J. and Cappai, R. (2001) Sublethal concentrations of prion peptide PrP 106-126 or the amyloid β peptide of Alzheimer's disease activates expression of proapoptotic markers in primary cortical neurons. Neurobiol. Dis. 8, 299-316
16. White, A. R., Huang, X. Jobling, M. F., Barrow, C. J., Beyreuther, K., Masters, C. L., Bush, A. I. and Cappai, R. (2001) Homocysteine potentiates copper- and amyloid β peptide-mediated toxicity in primary neuronal cultures: possible risk factors in the Alzheimer's-type neurodegenerative pathways. J. Neurochem. 76, 1509-1520
17. Brown, D. R., Schmidt, B. and Kretzschmar, H. A. (1996) Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature (London) 380, 345-347
18. Florio, T., Thellung, S., Amico, C., Robello, M., Salmona, M., Bugiani, O., Tagliavini, F., Forloni, G. and Schettini, G. (1998) Prion protein fragment 106-126 induces apoptotic cell death and impairment of L-type voltage-sensitive calcium channel activity in the GH3 cell line. J. Neurosci. Res. 54, 341-352
19. Perez, M., Wandosell, F., Colaco, C. and Avila, J. (1998) Sulphated glycosaminoglycans prevent the neurotoxicity of a human prion protein fragment. Biochem. J. 335, 369-374
20. Della-Bianca, V., Rossi, F., Armato, U., Dal-Pra, I., Costantini, O., Perini, G., Politi, V., Della and Valle, G. (2001) Neurotrophin p75 receptor is involved in neuronal damage by prion peptide (106-126). J. Biol. Chem. 276, 38929-38933
21. O'Donovan, C. N., Tobin, D. and Cotter, T. G. (2001) Prion protein fragment PrP (106-126) induces apoptosis via mitochondrial disruption in human neuronal SH-SY5Y cells. J. Biol. Chem. 276, 43516-43523
22. Ettaiche, M., Pichot, R., Vincent, J. P. and Chabry, J. (2000) In vivo cytotoxicity of the prion protein fragment 106-126. J. Biol. Chem. 275, 36487-36490
23. Selvaggini, C., De Gioia, L., Cantu, L., Ghibaudi, E., Diomede, L., Passerini, F., Forloni, G., Bugiani, O., Tagliavini, F. and Salmona, M. (1993) Molecular characteristics of a protease-resistant, amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. Biochem. Biophys. Res Commun. 194, 1380-1386
24. De Gioia, L., Selvaggini, C., Ghibaudi, E., Diomede, L., Bugiani, O., Forloni, G., Tagliavini, F. and Salmona, M. (1994) Conformational polymorphism of the amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. J. Biol. Chem. 269, 7859-7862
25. Jobling, M. F., Stewart, L. R., White, A. R., McLean, C. Friedhuber, A., Maher, F., Beyreuther, K., Masters, C. L., Barrow, C. J., Collins, S. J. et al. (1999) The hydrophobic core sequence modulates the neurotoxic and secondary structure properties of the prion peptide 106-126. J. Neurochem. 73, 1557-1565
26. Tagliavini, F., Lievens, P. M., Tranchant, C., Warter, J. M., Mohr, M., Giaccone, G., Perini, F. Rossi, G., Salmona, M., Piccardo, P. et al. (2001) A 7-kDa prior protein (PrP) fragment, an integral component of the PrP region required for infectivity, is the major amyloid protein in Gerstmann-Straussler-Scheinker disease A117V. J. Biol. Chem. 276, 6009-6015
27. Yankner, B. A. (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16, 921-932
28. Saez-Valero, J., Angeretti, N. and Forloni, G. (2000) Caspase-3 activation by β-amyloid and prion protein peptides is independent from their neurotoxic effect. Neurosci. Lett. 293, 207-210
29. Mattson, M. P. (2000) Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell. Biol. 1, 120-129
30. Roth, K. A. (2001) Caspases, apoptosis and Alzheimer disease: causation, correlation and confusion. J. Neuropathol. Exp. Neurol. 60, 829-838
31. Takashima, A., Noguchi, K., Sato, K., Hoshino, T. and Imahori, K. (1993) Tau protein kinase I is essential for amyloid β-protein-induced neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 90, 7789-7793
32. Alvarez, G., Munoz-Montano, J. R., Satrustegui, J., Avila, J. Bogonez, E. and Diaz-Nido, J. (1999) Lithium protects cultured neurons against β-amyloid-induced neurodegeneration. FEBS Lett. 453, 260-264
33. Cohen, P. and Frame, S. (2001) The renaissance of GSK-3. Nat. Rev. Mol. Cell. Biol. 2, 769-776
34. Grimes, C. A. and Jope, R. S. (2001) The multifaceted roles of glycogen synthase kinase 3β in cellular signaling Prog. Neurobiol. 65, 391-426
35. Pap, M. and Cooper, G. M. (1998) Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 273, 19929-19932
36. Bhat, R. V., Shanley, J., Correll, M. P., Fieles, W. E., Keith, R. A., Scott, C. W. and Lee, C. M. (2000) Regulation and localization of tyrosine 216 phosphorylation of glycogen synthase kinase-3β in cellular and animal models of neuronal degeneration. Proc. Natl. Acad. Sci. U.S.A. 97, 11074-11079
37. Bijur, G. N., De Sarno, P. and Jope, R. S. (2000) Glycogen synthase kinase-3β facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J. Biol. Chem. 276, 7583-7590
38. Crowder, R. J. and Freeman, R. S. (2000) Glycogen synthase kinase-3β activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal. J. Biol. Chem. 275, 34266-34271
39. Hetman, M., Cavanaugh, J. E., Kimelman, D. and Xia, Z. (2000) Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20, 2567-2574
40. King, T. D., Bijur, G. N. and Jope, R. S. (2001) Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3β and attenuated by lithium. Brain Res. 919, 106-114
41. Lucas, J. J., Hernandez, F., Gomez-Ramos, P., Moran, M. A., Hen, R. and Avila, J. (2001) Decreased nuclear β-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mice. EMBO J. 20, 27-39
42. Sanchez Martin, C., Diaz-Nido, J. and Avila, J. (1998) Regulation of a site-specific phosphorylation of the microtubule-associated protein 2 during the development of cultured neurons. Neuroscience 87, 861-870
43. Sanchez Martin, C., Ledesma, D., Dotti, C. G. and Avila, J. (2000) Microtubule-associated protein-2 located in growth regions of rat hippocampal neurons is highly phosphorylated at its proline-rich region. Neuroscience 101, 885-893
44. Mattson, M. P., Barger, S. W., Begley, J. G. and Mark, R. J. (1995) Calcium, free radicals and excitotoxic neuronal death in primary cell culture. Methods Cell Biol. 46, 187-216
45. Ryves, W. J., Fryer, L., Dale, T. and Harwood, A. J. (1998) An assay for glycogen synthase kinase 3 (GSK-3) for use in crude cell extracts. Anal. Biochem. 264, 124-127
46. Sayas, C. L., Moreno-Flores, M. T., Avila, J. and Wandosell, F. (1999) The neurite retraction induced by LPA increases Alzheimer's disease like tau phosphorylation. J. Biol. Chem. 274, 37046-37052
47. Klein, P. S. and Melton, D. A. (1996) A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U.S.A. 93, 8455-8459
48. Novak, M., Jakes, R., Edwards, P. C., Milstein, C. and Wischik, C. M. (1991) Difference between the tau protein of Alzheimer paired hetical filament core and normal tau revealed by epitope analysis of monoclonal antibodies 423 and 7.51. Proc. Natl. Acad. Sci. U.S.A. 88, 5837-5841
49. Dominguez, I., Itoh, K. and Sokol, S. Y. (1995) Role of glycogen synthase kinase 3β as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. U.S.A. 92, 8498-8502
50. Munoz-Montano, J. R., Moreno, F. J., Avila, J. and Diaz-Nido, J. (1999) Downregulation of glycogen synthase kinase-3β (GSK-3β) protein expression during neuroblastoma IMR-32 cell differentiation. J. Neurosci. Res. 55, 278-285
51. Takashima, A., Honda, T., Yasutake, K., Michel, G., Murayama, O., Murayama, M., Ishiguro, K. and Yamaguchi, H. (1998) Activation of tau protein kinase I/glycogen synthase kinase-3β by amyloid β peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci. Res. 31, 317-323
52. Hughes, K., Nikolakaki, E., Plyte, S. E., Totty, N. F. and Woodgett, J. R. (1993) Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 12, 803-808
53. Munoz-Montano, J. R., Moreno, F. J., Avila, J. and Diaz-Nido, J. (1997) Lithium inhibits Alzheimer's disease-like tau protein phosphorylation in neurons. FEBS Lett. 411, 183-188
54. Stambolic, V., Ruel, L. and Woodgett, J. R. (1996) Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6, 1664-1668
55. Manji, H. K., Moore, G. J., Rajkowska, G. and Chen, G. (2000) Neuroplasticity and cellular resilience in mood disorders. Mol. Psychiatry 5, 578-593
56. Sanchez, S., Sayas, C. L., Lim, F., Diaz-Nido, J, Avila, J. and Wandosell, F. (2001) The inhibition of phosphatidylinositol-3-kinase induces neurite retraction and activates GSK3. J. Neurochem. 78, 468-481
57. Gu, Y., Fujioka, H., Mishra, R. S., Li, R. and Singh, N. (2002) Prion peptide 106-126 modulates the aggregation of cellular prion protein and induces the synthesis of potentially neurotoxic transmembrane PrP. J. Biol. Chem. 277, 2275-2286
58. Combs, C. K., Johnson, D. E., Cannady, S. B., Lehman, T. M. and Landreth, G. E. (1999) identification of microglial signal transduction pathways mediating a neurotoxic response to amyloidogenic fragments of β-amyloid and prion proteins. J Neurosci. 19, 928-939
59. Hartigan, J. A. and Johnson, G. V. (1999) Transient increases in intracellular calcium result in prolonged site-selective increases in tau phosphorylation through a glycogen synthase kinase 3β-dependent pathway. J Biol. Chem. 274, 21395-21401
60. Lesort, M., Jope, R. S. and Johnson, G. V. (1999) Insulin transiently increases tau phosphoryration: involvement of glycogen synthase kinase-3β and fyn tyrosine kinase. J. Neurochem. 72, 576-584
61. Avila, J., Dominguez, J. and Diaz-Nido, J. (1994) Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int. J. Dev. Biol. 38, 13-25
62. Sanchez, C., Diaz-Nido, J. and Avila, J. (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog. Neurobiol. 61, 133-168