Scrapie-like prion protein accumulates in aggresomes of cyclosporin A-treated cells

EMBO Journal

Volumn 22, Issue 3, 2003, Pages 404-417

  Cohen, Ehud ^a   Taraboulos, Albert ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Aggresome; Cyclophilin; Cyclosporin A; Encephalopathy; Prion protein

Indexed keywords

CHAPERONE; CYCLOPHILIN; CYCLOSPORIN A; NOCODAZOLE; PRION PROTEIN; PROLINE; PROTEASOME;

ANIMAL CELL; ARTICLE; BRAIN DISEASE; CELL CULTURE; CONTROLLED STUDY; CYTOTOXICITY; GERSTMANN STRAUSSLER SCHEINKER SYNDROME; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN METABOLISM; SCRAPIE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CHO CELLS; CRICETINAE; CYCLOSPORINE; CYSTEINE ENDOPEPTIDASES; IMMUNOSUPPRESSIVE AGENTS; INCLUSION BODIES; MODELS, BIOLOGICAL; MULTIENZYME COMPLEXES; MUTATION; PROLINE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PRPC PROTEINS; PRPSC PROTEINS; TUBULIN; UBIQUITIN; VIMENTIN;

ANIMALIA;

EID: 0037415754     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg045     Document Type: Article

References (48)

1. Atkinson, K., Biggs, J., Darveniza, P., Boland, J., Concannon, A. and Dodds, A. (1984) Cyclosporin-associated central nervous system toxicity after allogeneic bone marrow transplantation. Transplantation, 38, 34-37.
2. Balbach, J. and Schmid, F.X. (2000) Proline isomerization and its catalysis in protein folding. In Pain, R.H (ed.), Mechanisms of Protein Folding. Oxford University Press, Oxford, UK, pp. 212-249.
3. Basler, K., Oesch, B., Scott, M., Westaway, D., Walchli, M., Groth, D.F., McKinley, M.P., Prusiner, S.B. and Weissmann, C. (1986) Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell. 46, 417-428.
4. Bence, N.F., Sampat, R.M. and Kopito, R.R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science, 292, 1552-1555.
5. Bolton, D.C., McKinley, M.P. and Prusiner, S.B. (1982) Identification of a protein that purifies with the scrapie prion. Science, 218, 1309-1311.
6. Butler, D.A., Scott, M.R., Bockman, J.M., Borchelt, D.R., Taraboulos, A., Hsiao, K.K., Kingsbury, D.T. and Prusiner, S.B. (1988) Scrapie-infected murine neuroblastoma cells produce protease-resistant prion proteins. J. Virol., 62, 1558-1564.
7. Carrell, R.W. and Lomas, D.A. (1997) Conformational disease. Lancet, 350, 134-138.
8. Collinge, J., Sidle, K.C., Meads, J., Ironside, J. and Hill, A.F. (1996) Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature, 383, 685-690.
9. Dobson, C.M. (2001) The structural basis of protein folding and its links with human disease. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 356. 133-145.
10. Ellgaard, L., Molinari, M. and Helenius, A. (1999) Setting the standards: quality control in the secretory pathway. Science, 286, 1882-1888.
11. Garcia-Mata, R., Bebok, Z., Sorscher, E.J. and Sztul, E.S. (1999) Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol., 146, 1239-1254.
12. Geier, E., Pfeifer, G., Wilm, M., Lucchiari-Hartz, M., Baumeister, W., Eichmann, K. and Niedermann, G. (1999) A giant protease with potential to substitute for some functions of the proteasome. Science, 283, 978-981.
13. Giloh, H. and Sedat, J.W. (1982) Fluorescence microscopy: reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. Science, 217, 1252-1255.
14. Hamilton, G.S. and Steiner, J.P. (1998) Immunophilins: beyond immunosuppression. J. Med. Chem., 41, 5119-5143.
15. Hsiao, K., Baker, H.F., Crow, T.J., Poulter, M., Owen, F., Terwilliger, J.D., Westaway, D., Ott, J. and Prusiner, S.B. (1989) Linkage of a prion protein missense variant to Gerstmann-Straussler syndrome. Nature, 338, 342-345.
16. Johnston, J.A., Ward, C.L. and Kopito, R.R. (1998) Aggresomes: a cellular response to misfolded proteins. J. Cell Biol., 143, 1883-1898.
17. Kascsak, R.J., Rubenstein, R., Merz, P.A., Tonna-DeMasi, M., Fersko, R., Carp, R.I., Wisniewski, H.M. and Diringer, H. (1987) Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J. Virol., 61, 3688-3693.
18. Kopito, R.R. (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol., 10, 524-530.
19. Kopito, R.R. and Ron, D. (2000) Conformational disease. Nat. Cell Biol., 2, E207-E209.
20. Kopito, R.R. and Sitia, R. (2000) Aggresomes and Russell bodies. Symptoms of cellular indigestion? EMBO rep., 1, 225-231.
21. Lehmann, S. and Harris, D.A. (1995) A mutant prion protein displays an aberrant membrane association when expressed in cultured cells. J. Biol. Chem., 270, 24589-24597.
22. Lehmann, S. and Harris, D.A. (1996) Mutant and infectious prion proteins display common biochemical properties in cultured cells. J. Biol. Chem., 271, 1633-1637.
23. Lehmann, S. and Harris, D.A. (1997) Blockade of glycosylation promotes acquisition of scrapie-like properties by the prion protein in cultured cells. J. Biol. Chem., 272, 21479-21487.
24. Ma, J. and Lindquist, S. (1999) De novo generation of a PrPSc-likc conformation in living cells. Nat. Cell Biol., 1, 358-361.
25. Ma, J. and Lindquist, S. (2001) Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc. Natl. Acad. Sci. USA, 98, 14955-14960.
26. McKinley, M.P., Taraboulos, A., Kenaga, L., Serban, D., Stieber, A., DeArmond, S.J., Prusiner, S.B. and Gonatas, N. (1991) Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells. Lab. Invest., 65, 622-630.
27. Meyer, R.K., McKinley, M.P., Bowman, K.A., Braunfeld, M.B., Barry, R.A. and Prusiner, S.B. (1986) Separation and properties of cellular and scrapie prion proteins. Proc. Natl Acad. Sci. USA, 83, 2310-2314.
28. Naslavsky, N., Stein, R., Yanai, A., Friedlander, G. and Taraboulos, A. (1997) Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J. Biol. Chem., 272, 6324-6331.
29. Navon, A. and Goldberg, A.L. (2001) Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol. Cell, 8, 1339-1349.
30. Oesch, B. et al. (1985) A cellular gene encodes scrapie PrP 27-30 protein. Cell, 40, 735-746.
31. Pan, K.M. et al. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl Acad. Sci. USA, 90, 10962-10966.
32. Prusiner, S.B. (1998) Prions. Proc. Natl Acad. Sci. USA, 95, 13363-13383.
33. Reimer, U., Scherer, G., Drewello, M., Kruber, S., Schutkowski, M. and Fischer, G. (1998) Side-chain effects on peptidyl-prolyl cis/trans isomerisation. J. Mol. Biol., 279, 449-460.
34. Rogers, M., Serban, D., Gyuris, T., Scott, M., Torchia, T. and Prusiner, S.B. (1991) Epitope mapping of the Syrian hamster prion protein utilizing chimeric and mutant genes in a vaccinia virus expression system. J. Immunol., 147, 3568-3574.
35. Sc molecules with different conformations, Nat. Med., 4, 1157-1165.
36. Scheff, S.W. and Sullivan, P.G. (1999) Cyclosporin A significantly ameliorates cortical damage following experimental traumatic brain injury in rodents. J. Neurotrauma, 16, 783-792.
37. Schubert, U., Anton, L.C., Gibbs, J., Norbury, C.C., Yewdell, J.W. and Bennink, J.R. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature, 404, 770-774.
38. Scott, M.R., Kohler, R., Foster, D. and Prusiner, S.B. (1992) Chimeric prion protein expression in cultured cells and transgenic mice. Protein Sci., 1, 986-997.
39. Serban, D., Taraboulos, A., DeArmond, S.J. and Prusiner, S.B. (1990) Rapid detection of Creutzfeldt-Jakob disease and scrapie prion proteins. Neurology, 40, 110-117.
40. Stahl, N., Borchelt, D.R., Hsiao, K. and Prusiner, S.B. (1987) Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell, 51, 229-240.
41. Taraboulos, A., Serban, D. and Prusiner, S.B. (1990) Scrapie prion proteins accumulate in the cytoplasm of persistently infected cultured cells. J. Cell Biol., 110, 2117-2132.
42. Taraboulos, A., Scott, M., Semenov, A., Avrahami, D., Laszlo, L., Prusiner, S.B. and Avraham, D. (1995) Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J. Cell Biol., 129, 121-132.
43. Thompson, C.B., June, C.H., Sullivan, K.M. and Thomas, E.D. (1984) Association between cyclosporin neurotoxicity and hypomagnesaemia. Lancet, 2, 1116-1120.
44. Uittenbogaard, A., Ying, Y., and Smart, E.J. (1998) Characterization of a cytosolic heat-shock protein - caveolin chaperone complex. Involvement in cholesterol trafficking. J. Biol. Chem., 273, 6525-6532.
45. Warrens, A.N., Waters, J.B., Salama, A.D. and Lechler, R.I. (1999) Improving the therapeutic monitoring of cyclosporin A. Clin. Transplant., 13, 193-200.
46. Wigley, W.C., Fabunmi, R.P., Lee, M.G., Marino, C.R., Muallem, S., DeMartino, G.N. and Thomas, P.J. (1999) Dynamic association of proteasomal machinery with the centrosome. J. Cell Biol., 145, 481-490.
47. Yamazaki, M., Oyanagi, K., Mori, O., Kitamura, S., Ohyama, M., Terashi, A., Kitamoto, T. and Katayama, Y. (1999) Variant Gerstmann-Straussler syndrome with the P105L prion gene mutation: an unusual case with nigral degeneration and widespread neurofibrillary tangles. Acta Neuropathol. (Berl.), 98, 506-511.
48. Yedidia, Y., Horonchik, L., Tzaban, S., Yanai, A. and Taraboulos, A. (2001) Proteasomes and ubiquitin are involved in the turnover of the wild-type prion protein. EMBO J., 20, 5383-5391.