Resistance of cell lines to prion toxicity aided by phospho-ERK expression

Journal of Neurochemistry

Volumn 105, Issue 3, 2008, Pages 842-852

  Uppington, Kay M ^a   Brown, David R ^a  

^a University of Bath   (United Kingdom)

Author keywords

Caspase; MAP kinase; Prion; Scrapie; Toxicity

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CASPASE; FR 180204; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PRION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; DRUG INHIBITION; MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CASPASE 12; CELL CULTURE TECHNIQUES; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CYTOPROTECTION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; MANGANESE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PHOSPHORYLATION; PRION DISEASES; PRIONS; PROTEIN FOLDING; PRPSC PROTEINS; RECOMBINANT PROTEINS; SCRAPIE;

EID: 42449102282     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05192.x     Document Type: Article

References (69)

1. Almeida R. D., Manadas B. J., Melo C. V., Gomes J. R., Mendes C. S., Graos M. M., Carvalho R. F., Carvalho A. P. Duarte C. B. (2005) Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ. 12, 1329 1343.
2. Anderson C. N. Tolkovsky A. M. (1999) A role for MAPK/ERK in sympathetic neuron survival: protection against a p53-dependent, JNK-independent induction of apoptosis by cytosine arabinoside. J. Neurosci. 19, 664 673.
3. Arai K., Lee S. R., van Leyen K., Kurose H. Lo E. H. (2004) Involvement of ERK MAP kinase in endoplasmic reticulum stress in SH-SY5Y human neuroblastoma cells. J. Neurochem. 89, 232 239.
4. Birkett C. R., Hennion R. M., Bembridge D. A., Clarke M. C., Chree A., Bruce M. E. Bostock C. J. (2001) Scrapie strains maintain biological phenotypes on propagation in a cell line in culture. EMBO J. 20, 3351 3358.
5. Bonetto V., Massignan T., Chiesa R. et al. (2002) Synthetic miniprion PrP106. J. Biol. Chem. 277, 31327 31334.
6. Bourteele S., Oesterle K., Weinzierl A. O., Paxian S., Riemann M., Schmid R. M. Planz O. (2007) Alteration of NF-kappaB activity leads to mitochondrial apoptosis after infection with pathological prion protein. Cell Microbiol. 9, 2202 2217.
7. Brandner S., Isenmann S., Raeber A., Fischer M., Sailer A., Kobayashi Y., Marino S., Weissmann C. Aguzzi A. (1996) Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379, 339 343.
8. Brown D. R. (1999) Prion protein peptide neurotoxicity can be mediated by astrocytes. J. Neurochem. 73, 1105 1113.
9. Brown D. R. (2001) Prion and prejudice: normal protein at the synapse. Trends Neurosci. 24, 85 90.
10. Brown D. R. (2002) Mayhem of the multiple mechanisms: modelling neurodegeneration in prion disease. J. Neurochem. 82, 209 215.
11. Brown D. R., Herms J. Kretzschmar H. A. (1994) Mouse cortical cells lacking cellular PrP survive in culture with a neurotoxic PrP fragment. Neuroreport 5, 2057 2060.
12. Brown D. R., Schmidt B. Kretzschmar H. A. (1996) Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380, 345 347.
13. Brown D. R., Qin K., Herms J. W. et al. (1997) The cellular prion protein binds copper in vivo. Nature 390, 684 687.
14. Brown D. R., Pitschke M., Riesner D. Kretzschmar H. A. (1998) Cellular effects of a neurotoxic prion protein peptide are related to its β-sheet content. Neurosci. Res. Comm. 23, 119 128.
15. Brown D. R., Hafiz F., Glasssmith L. L., Wong B.-S., Jones I. M., Clive C. Haswell S. J. (2000) Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J. 19, 1180 1186.
16. Brown D. R., Nicholas R. St. J. Canevari L. (2002) Lack of prion protein expression results in a neuronal phenotype sensitive to stress. J. Neurosci. Res. 67, 211 224.
17. Büeler H., Fischer M., Lang Y., Bluethmann H., Lipp H. P., DeArmond S. J., Prusiner S. B., Aguet M. Weissmann C. (1992) Normal development and behaviour of mice lacking the neuronal cellsurface PrP protein. Nature 356, 577 582.
18. Carimalo J., Cronier S., Petit G., Peyrin J. M., Boukhtouche F., Arbez N., Lemaigre-Dubreuil Y., Brugg B. Miquel M. C. (2005) Activation of the JNK-c-Jun pathway during the early phase of neuronal apoptosis induced by PrP106-126 and prion infection. Eur. J. Neurosci. 21, 2311 2319.
19. Caughey B. Lansbury P. T. Jr. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Ann. Rev. Neurosci. 26, 267 298.
20. Caughey B., Race R. E., Ernst D., Buchmeier M. J. Chesebro B. (1989) Prion protein biosynthesis in scrapie-infected and uninfected neuroblastoma cells. J. Virol. 63, 175 181.
21. Cohen F. E. Prusiner S. B. (1998) Pathologic conformations of prion proteins. Ann. Rev. Biochem. 67, 793 819.
22. Corsaro A., Thellung S., Villa V. et al. (2003) Prion protein fragment 106-126 induces a p38 MAP kinase-dependent apoptosis in SH-SY5Y neuroblastoma cells independently from the amyloid fibril formation. Ann. NY Acad. Sci. 1010, 610 622.
23. Corsaro A., Paludi D., Villa V. et al. (2006) Conformation dependent pro-apoptotic activity of the recombinant human prion protein fragment 90-231. Int. J. Immunopathol. Pharmacol. 19, 339 356.
24. Daniels M., Cereghetti G. M. Brown D. R. (2001) Toxicity of novel C-terminal prion protein fragments and peptides harbouring disease-related C-terminal mutations. Eur. J. Biochem. 268, 6155 6164.
25. Fairbairn D. W., Carnahan K. G., Thwaits R. N., Grigsby R. V., Holyoak G. R. O'Neill K. L. (1994) Detection of apoptosis induced DNA cleavage in scrapie-infected sheep brain. FEMS Microbiol. Lett. 115, 341 346.
26. Forloni G., Angeretti N., Chiesa R., Monzani E., Salmona M., Bugiani O. Tagliavini F. (1993) Neurotoxicity of a prion protein fragment. Nature 362, 543 546.
27. Fuhrmann M., Mitteregger G., Kretzschmar H. Herms J. (2007) Dendritic pathology in prion disease starts at the synaptic spine. J. Neurosci. 27, 6224 6233.
28. Gambetti P., Parchi P. Chen S. G. (2003) Hereditary Creutzfeldt-Jakob disease and fatal familial insomnia. Clin. Lab. Med. 23, 43 64.
29. Ghetti B., Tagliavini F., Takao M., Bugiani O. Piccardo P. (2003) Hereditary prion protein amyloidoses. Clin. Lab. Med. 23, 65 85.
30. Giese A., Groschup M. H., Hess B. Kretzschmar H. A. (1995) Neuronal cell death in scrapie-infected mice is due to apoptosis. Brain Pathol. 5, 213 221.
31. Giese A., Brown D. R., Groschup M. H., Feldmann C., Haist I. Kretzschmar H. A. (1998) Role of microglia in neuronal cell death in prion disease. Brain Pathol. 8, 449 457.
32. Glatzel M., Giger O., Seeger H. Aguzzi A. (2004) Variant Creutzfeldt-Jakob disease: between lymphoid organs and brain. Trends Microbiol. 12, 51 53.
33. Hegde R. S., Mastrianni J. A., Scott M. R., DeFea K. A., Tremblay P., Torchia M., DeArmond S. J., Prusiner S. B. Lingappa V. R. (1998) A transmembrane form of the prion protein in neurodegenerative disease. Science 279, 827 834.
34. Hetz C., Russelakis-Carneiro M., Maundrell K., Castilla J. Soto C. (2003) Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J. 22, 5435 5445.
35. Holme A., Daniels M., Sassoon J. Brown D. R. (2003) A novel method of generating neuronal cell lines from gene-knockout mice to study prion protein membrane orientation. Eur. J. Neurosci. 18, 571 579.
36. Hope J., Reekie L. J., Hunter N., Multhaup G., Beyreuther K., White H., Scott A. C., Stack M. J., Dawson M. Wells G. A. (1988) Fibrils from brains of cows with new cattle disease contain scrapie-associated protein. Nature 336, 390 392.
37. Hunter N. (2003) Scrapie and experimental BSE in sheep. Br. Med. Bull. 66, 171 183.
38. Ironside J. W., Ritchie D. L. Head M. W. (2005) Phenotypic variability in human prion diseases. Neuropathol. Appl. Neurobiol. 31, 565 579.
39. Kayed R., Head E., Thompson J. L., McIntire T. M., Milton S. C., Cotman C. W. Glabe C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486 489.
40. Kazlauskaite J., Young A., Gardner C. E., Macpherson J. V., Venien-Bryan C. Pinheiro T. J. (2005) An unusual soluble beta-turn-rich conformation of prion is involved in fibril formation and toxic to neuronal cells. Biochem. Biophys. Res. Commun. 328, 292 305.
41. Kristiansen M., Messenger M. J., Klohn P. C., Brandner S., Wadsworth J. D., Collinge J. Tabrizi S. J. (2005) Disease-related prion protein forms aggresomes in neuronal cells leading to caspase activation and apoptosis. J. Biol. Chem. 280, 38851 38861.
42. Lee H. P., Jun Y. C., Choi J. K., Kim J. I., Carp R. I. Kim Y. S. (2005) Activation of mitogen-activated protein kinases in hamster brains infected with 263K scrapie agent. J. Neurochem. 95, 584 593.
43. Ma J., Wollmann R. Lindquist S. (2002) Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 298, 1781 1785.
44. Maher P. (2001) How protein kinase C activation protects nerve cells from oxidative stress-induced cell death. J. Neurosci. 21, 2929 2938.
45. Mallucci G., Dickinson A., Linehan J., Klohn P. C., Brandner S. Collinge J. (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302, 871 874.
46. Mallucci G. R., White M. D., Farmer M., Dickinson A., Khatun H., Powell A. D., Brandner S., Jefferys J. G. Collinge J. (2007) Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 53, 325 335.
47. Marella M., Gaggioli C., Batoz M., Deckert M., Tartare-Deckert S. Chabry J. (2005) Pathological prion protein exposure switches on neuronal mitogen-activated protein kinase pathway resulting in microglia recruitment. J. Biol. Chem. 280, 1529 1534.
48. Mead S., Poulter M., Beck J. et al. (2006) Inherited prion disease with six octapeptide repeat insertional mutation - molecular analysis of phenotypic heterogeneity. Brain. 129, 2297 2317.
49. Monnet C., Marthiens V., Enslen H., Frobert Y., Sobel A. Mege R. M. (2003) Heterogeneity and regulation of cellular prion protein glycoforms in neuronal cell lines. Eur. J. Neurosci. 18, 542 548.
50. Müller W. E., Ushijima H., Schroder H. C., Forrest J. M., Schatton W. F., Rytik P. G. 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.
51. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B. A. Yuan J. (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403, 98 103.
52. Novitskaya V., Bocharova O. V., Bronstein I. Baskakov I. V. (2006) Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. J. Biol. Chem. 281, 13828 13836.
53. O'Donovan C. N., Tobin D. 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.
54. Park S. K., Choi S. I., Jin J. K., Choi E. K., Kim J. I., Carp R. I. Kim Y. S. (2000) Differential expression of Bax and Bcl-2 in the brains of hamsters infected with 263K scrapie agent. Neuroreport 11, 1677 1682.
55. Post K., Brown D. R., Groschup M., Kretzschmar H. Riesner D. (2000) Neurotoxicity but not infectivity of prion protein can be induced reversibly in vitro. Arch. Virol. 16 (Suppl. 265 273.
56. Prusiner S. B. (1998) Prions. Proc. Natl Acad. Sci. USA 95, 13363 13383.
57. Sales N., Rodolfo K., Hassig R., Faucheux B., Di Giamberardino L. Moya K. L. (1998) Cellular prion protein localization in rodent and primate brain. Eur. J. Neurosci. 10, 2464 2471.
58. Schatzl H. M., Laszlo L., Holtzman D. M., Tatzelt J., DeArmond S. J., Weiner R. I., Mobley W. C. Prusiner S. B. (1997) A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis. J. Virol. 71, 8821 8831.
59. Silveira J. R., Raymond G. J., Hughson A. G., Race R. E., Sim V. L., Hayes S. F. Caughey B. (2005) The most infectious prion protein particles. Nature 437, 257 261.
60. Simoneau S., Rezaei H., Sales N. et al. (2007) In vitro and in vivo neurotoxicity of prion protein oligomers. PLoS Pathog. 3, e125.
61. Stahl N., Borchelt D. R., Hsiao K. Prusiner S. B. (1987) Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell. 51, 229 240.
62. Thackray A. M., Knight R., Haswell S. J., Bujdoso R. Brown D. R. (2002) Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem. J. 362, 253 258.
63. Thellung S., Villa V., Corsaro A., Arena S., Millo E., Damonte G., Benatti U., Tagliavini F., Florio T. Schettini G. (2002) p38 MAP kinase mediates the cell death induced by PrP106-126 in the SH-SY5Y neuroblastoma cells. Neurobiol. Dis. 9, 69 81.
64. Thompsett A. R., Abdelraheim S. R., Daniels M. Brown D. R. (2005) High affinity binding between copper and full-length prion protein identified by two different techniques. J. Biol. Chem. 280, 42750 42758.
65. Unterberger U., Hoftberger R., Gelpi E., Flicker H., Budka H. Voigtlander T. (2006) Endoplasmic reticulum stress features are prominent in Alzheimer disease but not in prion diseases in vivo. J. Neuropathol. Exp. Neurol. 65, 348 357.
66. Volles M. J. Lansbury P. T. Jr. (2003) Zeroing in on the pathogenic form of alpha-synuclein and its mechanism of neurotoxicity in Parkinson's disease. Biochemistry 42, 7871 7878.
67. Will R. G. (2003) Acquired prion disease: iatrogenic CJD, variant CJD, kuru. Br. Med. Bull. 66, 255 265.
68. Wong B.-S., Vénien-Bryan C., Williamson R. A., Burton D. R., Gambetti P., Sy M.-S., Brown D. R. Jones I. M. (2000) Copper refolding of prion protein. Biochem. Biophys. Res. Comm. 276, 1217 1224.
69. Wong B.-S., Liu T., Ruliang Li R. et al. (2001) Increased levels of oxidative stress markers detected in the brains of mice devoid of prion protein. J. Neurochem. 76, 565 572.