Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol

Science

Volumn 298, Issue 5599, 2002, Pages 1781-1785

  Ma, Jiyan ^a,c   Wollmann, Robert ^a   Lindquist, Susan ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CELL CULTURE; DEGRADATION; DISEASES; TOXICITY;

ENDOPLASMIC RETICULUM;

PROTEINS;

CELL PROTEIN; ISOPROTEIN; PRION PROTEIN; PROTEASOME;

NERVOUS SYSTEM DISORDER; PROTEIN;

ANIMAL CELL; ARTICLE; ATAXIA; CELL CULTURE; CEREBELLUM DEGENERATION; CONTROLLED STUDY; CYTOSOL; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DISEASE SEVERITY; ENDOPLASMIC RETICULUM; GLIOSIS; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; RETROGRADE NERVE FIBER TRANSPORT; SPECIES DIFFERENTIATION; SPECIES IDENTIFICATION; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; APOPTOSIS; BRAIN; CELL SURVIVAL; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; CYTOSOL; GLYCOSYLATION; IN SITU NICK-END LABELING; LEUPEPTINS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MULTIENZYME COMPLEXES; NERVE DEGENERATION; NEURONS; PRESENILIN-1; PRION DISEASES; PRIONS; PROMOTER REGIONS (GENETICS); PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN TRANSPORT; PRPSC PROTEINS; TRANSFECTION; TUMOR CELLS, CULTURED;

ANIMALIA; MUS MUSCULUS;

EID: 0037195647     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.1073725     Document Type: Article

References (51)

1. S. B. Prusiner, Proc. Natl. Acad. Sci. U.S.A. 95, 13363 (1998).
2. B. Caughey, B. Chesebro, Trends Cell Biol. 7, 56 (1997).
3. R. Chiesa, D. A. Harris, Neurobiol. Dis. 8, 743 (2001).
4. A. Aguzzi, F. L. Heppner, Cell Death Differ. 7, 889 (2000).
5. J. Collinge, Annu. Rev. Neurosci. 24, 519 (2001).
6. H. Bueler et al., Cell 73, 1339 (1993).
7. S. Brandner et al., Nature 379, 339 (1996).
8. K. K. Hsiao et al., Proc. Natl. Acad. Sci. U.S.A. 91, 9126 (1994).
9. C. I. Lasmezas et al., Science 275, 402 (1997).
10. T. Kitamoto, R. Iizuka, J. Tateishi, Biochem. Biophys. Res. Commun. 192, 525 (1993).
11. F. Tagliavini et al., Cell 79, 695 (1994).
12. R. R. Kopito, Cell 88, 427 (1997).
13. S. W. Fewell, K. J. Travers, J. S. Weissman, J. L. Brodsky, Annu. Rev. Genet. 35, 149 (2001).
14. J. Ma, S. Lindquist, Proc. Natl. Acad. Sci. U.S.A. 98, 14955 (2001).
15. Y. Yedidia, L. Horonchik, S. Tzaban, A. Yanai, A. Taraboulos, EMBO J. 20, 5383 (2001).
16. W. Swietnicki, R. B. Petersen, P. Gambetti, W. K. Surewicz, J. Biol. Chem. 273, 31048 (1998).
17. S. Liemann, R. Glockshuber, Biochemistry 38, 3258 (1999).
18. L. Ivanova, S. Barmada, T. Kummer, D. A. Harris, J. Biol. Chem. 276, 42409 (2001).
19. J. Ma, S. Lindquist, Science 298, 1785 (2002); published online 17 October 2002 (10.1126/science.1073619).
20. Cytomegalovirus promoter.
21. Experiments were performed as in (14).
22. Materials and methods are available as supporting materials on Science Online.
23. First, unglycosylated proteins are more likely to misfold in the ER and be subject to retrograde transport; second, glycosylated species that are retrograde transported are subject to cytoplasmic deglycosidases.
24. A. J. Parodi, Annu. Rev. Biochem. 69, 69 (2000).
25. T. Suzuki, H. Park, N. M. Hollingsworth, R. Sternglanz, W. J. Lennarz, J. Cell Biol. 149, 1039 (2000).
26. J. Ma, R. Wollmann, S. Lindquist, data not shown.
27. J. A. Johnston, C. L.Ward, R. R. Kopito, J. Cell Biol. 143, 1883 (1998).
28. B. Chesebro et al., Dev. Biol. Stand. 80, 131 (1993).
29. A. Helenius, M. Aebi, Science 291, 2364 (2001).
30. More than 50% of N2A cells died within 12 hours of proteasome treatment, but less than 5% of moPrP cells died during the same period.
31. C. Holscher, U. C. Bach, B. Dobberstein, J. Biol. Chem. 276, 13388 (2001).
32. D. No, T. P. Yao, R. M. Evans, Proc. Natl. Acad. Sci. U.S.A. 93, 3346 (1996).
33. D. R. Borchelt et al., Genet. Anal. 13, 159 (1996).
34. R. Chiesa, P. Piccardo, B. Ghetti, D. A. Harris, Neuron 21, 1339 (1998).
35. D. Shmerling et al., Cell 93, 203 (1998).
36. Supporting text and data are available on Science Online.
37. Slow growth might be due to ataxia-associated problems with eating and drinking, although special care was taken to provide accessible food and water.
38. R. Chiesa et al., Proc. Natl. Acad. Sci. U.S.A. 97, 5574 (2000).
39. M. Russelakis-Carneiro, G. P. Saborio, L. Anderes, C. Soto, J. Biol. Chem. 18, 18 (2002).
40. H. Lorenz, O. Windl, H. A. Kretzschmar, J. Biol. Chem. 277, 8508 (2002).
41. N. Singh et al., J. Biol. Chem. 272, 28461 (1997).
42. G. Zanusso et al., J. Biol. Chem. 274, 23396 (1999).
43. D. Doyle, M. Rogers, Trends Genet. 14, 171 (1998).
44. P. Piccardo et al., J. Neuropathol. Exp. Neurol. 57, 979 (1998).
45. J. J. Liu, S. Lindquist, Nature 400, 573 (1999).
46. J. Adams, V. J. Palombella, P. J. Elliott, Invest. New Drugs 18, 109 (2000).
47. P. Andre et al., Proc. Natl. Acad. Sci. U.S.A. 95, 13120 (1998).
48. Sc conversion appears to occur solely on the cell surface and in endocytic compartments.
49. B. Caughey, G. J. Raymond, J. Biol. Chem. 266, 18217 (1991).
50. K. Doh-Ura, T. Iwaki, B. Caughey, J. Virol. 74, 4894 (2000).
51. We thank B. Caughey, G. Thinakaran, and J. Tatzelt for providing cell lines and antibodies; X. Wang, Y. Wang, and E. Rehm for technical help; members of the Lindquist lab for critical reading of this manuscript; and NIH (GM25874) and the Howard Hughes Medical. Institute for funding this research. This work was initiated in S.L.'s laboratory at the University of Chicago and continued there under her supervision after her move to the Whitehead Institute for Biomedical Research.