Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo

Cell

Volumn 90, Issue 3, 1997, Pages 549-558

  Scherzinger, Eberhard ^a   Lurz, Rudi ^a   Turmaine, Mark ^c   Mangiarini, Laura ^b   Hollenbach, Birgit ^a   Hasenbank, Renate ^a   Bates, Gillian P ^b   Davies, Stephen W ^c   Lehrach, Hans ^a   Wanker, Erich E ^a  

^a FU Berlin   (Germany)

^b GUY S HOSPITAL   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL DEATH; CENTRAL NERVOUS SYSTEM; GENE MUTATION; MICROSCOPY; NERVE DEGENERATION; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

ANIMALIA;

EID: 18544400323     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80514-0     Document Type: Article

References (41)

1. Bates, G.P., Mangiarini, L., Mahal, A., and Davies, S.W. (1997). Transgenic models of Huntington's disease. Hum. Mol. Genet., in press.
2. Booth, D.R., Stunde, M., Bellotti, V., Robinson, C.V., Hutchinson, W.L., Fraser, P.E., Hawkins, P.N., Dobson, C.M., Radford, S.E., Blake, C.C.F., and Pepys, M.B. (1997). Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385, 787-793.
3. Burke, J.R., Enghild, J.J., Martin, M.E., Jou, Y.-S., Myers, R.M., Roses, A.D., Vance, J.M., and Strittmatter, W.J. (1996). Huntingtin and DRPLA proteins selectively interact with the enzyme GAPDH. Nat. Med. 2, 347-350.
4. Caputo, C.B., Fraser, P.E., Sobel, I.E., and Krischner, D.A. (1992). Amyloid-like properties of a synthetic peptide corresponding to the carboxy terminus of β-amyloid protein precursor. Arch. Biochem. Biophys. 292, 199-205.
5. Caughey, B., and Chesebro, B. (1997). Prion protein and the transmissible spongiform encephalopathies. Trends Cell Biol. 7, 56-62.
6. Davies, S.W., Trumaine, M., Cozens, B.A., DiFiglia, M., Sharp, A.H., Ross, C.A., Scherzinger, E., Wanker, E.E., Mangiarini, L., and Bates, G.P. (1997). Formation of neuronal intranuclear inclusions (NII) underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell, this issue, 90, 537-548.
7. de Rooij, K.E., Dorsman, J.C., Smoor, M.A., den Dunnen, J.T., and van Ommen, G.-J.B. (1996). Subcellular localisation of the Huntington's disease gene product in cell lines by immunofluorescence and biochemical subcellular fractionation. Hum. Mol. Genet. 5, 1093-1099.
8. DiFiglia, M., Sapp, E., Chase, K., Schwarz, C., Meloni, A., Young, C., Martin, E., Vonstattel, J.-P., Carraway, R., Reeves, S.A., Boyce, F.M., and Aronin, N.(1995). Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14, 1075-1081.
9. Duyao, M.P., Auerbach, A.A., Ryan, A., Persichetti, F., Barnes, G.T., McNeil, S.M., Ge, P., Vonstattel, J.-P., Gusella, J.F., Joyner, A.L., and MacDonald, M.E. (1995). Inactivation of the mouse Huntington's disease gene homolog Hdh. Science 269, 407-410.
10. Glenner, G.G. (1980). Amyloid deposits and amyloidosis. N. Engl. J. Med. 302, 1283-1292.
11. Goldberg, Y.P., Nicholson, D.W., Rasper, D.M., Kalchman, M.A., Koide, H.B., Graham, R.K., Bromm, M., Kazemi-Esfarjani, P., Thornberry, N.A., Vaillancourt, J.P., and Hayden, M.R. (1996). Cleavage of huntingtin by apopain, a proapoptotic cysteine protease, is modulated by the polyglutamine tract. Nat. Genet. 13, 442-449.
12. Gutekunst, C.-A., Levey, A.I., Heilman, C.J., Whaley, W.L., Yi, H., Nash, N.R., Rees, H.D., Madden, J.J., and Hersch, S.M. (1995). Identification and localization of huntingtin in brain and human lymphoblastoid cell lines with anti-fusion protein antibodies. Proc. Natl. Acad. Sci. USA 92, 8710-8714.
13. Harper, P.S. (1991). Huntington's disease, Edition 22, P.S. Harper, ed. (London: W.B. Saunders Co., Ltd).
14. The Huntington's Disease Collaborative Research Group. (1993). A novel gene containing a trinucleotide repeat that is unstable on Huntington's disease chromosomes. Cell 72, 971-983.
15. Hoogeveen, A.T., Willemsen, R., Meyer, N., de Rooij, K.E., Roos, R.A.C., van Ommen, G.-J.B., and Galjaard, H. (1993). Characterisation and localisation of the Huntington disease gene product. Hum. Mol. Genet. 2, 2069-2073.
16. Ikeda, H., Yamaguchi, M., Sugai, S., Aze, Y., Narumiya, S., and Kakizuka, A. (1996). Expanded polyglutamine in the Machado-Joseph disease protein induces cell death in vitro and in vivo. Nat. Genet. 13, 196-202.
17. Jarrett, J.T., and Lansburry, P.T. (1993). Seeding "one-dimensional-crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058.
18. Kalchman, M.A., Graham, R.K., Xia, G., Koide, H.B., Hodgson, J.G., Graham, K.C., Goldberg, Y.P., Gietz, R.D., Pickart, C.M., and Hayden, M.R. (1996). Huntingtin is ubiquinated and interacts with a specific ubiquitin-conjugating enzyme. J. Biol. Chem. 277, 19385-19394.
19. Kalchman, M.A., Koide, H.B., McCutcheon, K., Graham, R.K., Nichol, K., Nishiyama, K., Kazemi-Esfariani, P., Lynn, F.C., Wellington, C., Metzler, M., et al. (1997). HIP1, a human homologue of S. cerevisiae Sla2p, interacts with membrane-associated huntingtin in the brain. Nat. Genet. 16, 44-53.
20. Li, X.-J., Li, S.-H., Sharp, A.M., Nucifora, F.C., Schilling, G., Lanahan, A., Worley, P., Snyder, S.H., and Ross, C.A. (1995). A huntingtin-associated protein enriched in brain with implications for pathology. Nature 378, 398-402.
21. Lim, K., Ho, J.X., Keeling, K., Gilliland, G.L., Ji, X., Rüker, F., and Carter, D.C. (1994). Three-dimensional structure of Schistosoma japonicum glutamine S-transferase fused with a six-amino acid conserved neutralizing epitope of gp41 from HIV. Prot. Sci. 3, 2233-2244.
22. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Hetherington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S.W., and Bates, G.P. (1996). Exon 1 of the Huntington's disease gene containing a highly expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87, 493-506.
23. Onodera, O., Roses, A.D., Tsuji, S., Vance, J.M., Stritmatter, W.J., and Burke, J.R. (1996). Toxicity of expanded polyglutamine-domain proteins in Escherichia coli. FEBS Lett. 399, 135-139.
24. Perutz, M.F. (1996). Glutamine repeats and inherited neurodegenerative diseases: molecular aspects. Curr. Opin. Struct. Biol. 6, 848-858.
25. Perutz, M.F., Johnston, T., Suzuki, M., and Finch, J.T. (1994). Glutamine repeats as polar zippers: their possible role in neurodegenerative diseases. Proc. Natl. Acad. Sci. USA 91, 5355-5358.
26. Portera-Cailliau, C., Hedreen, J.C., Price, D.L., and Koliatsos, V.E. (1995). Evidence of apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15, 3775-3787.
27. Prusiner, S.B., Kinley, M.P.M., Bowman, K.A., Bolton, D.C., Bendheim, P.E., Groth, D.F., and Glenner, G.G. (1983). Scrapie prions aggregate to form amyloid-like birefingent rods. Cell 35, 349-358.
28. Roizin, L., Stellar, S., and Liu, J.C. (1979). Neuronal nuclear-cytoplasmic changes in Huntington's chorea: electron microscope investigations. Adv. Neurol. 23, 95-122.
29. Roos, R.A.C., and Bots, G.T.A.M. (1983). Nuclear membrane indentations in Huntington's chorea. J. Neurol. Sci. 61, 37-47.
30. Ross, C.A. (1995). When more is less: pathogenesis of glutamine repeat neurodegenerative diseases. Neuron 15, 493-496.
31. Rubinsztein, D.C., Leggo, J., Coles, R., Almqvist, E., Biancalana, V., Cassiman, J.-J., Chotai, K., Connarty, M., Crauford, D., Curtis, A., et al. (1996). Phenotypic characterisation of individuals with 30-40 CAG repeats in the Huntington's disease (HD) gene reveals HD cases with 36 repeats and apparently normal elderly individuals with 36-39 repeats. Am. J. Hum. Genet. 59, 16-22.
32. Sathasivam, K., Amaechi, I., Mangiarini, L., and Bates, G.P. (1997). Identification of an HD patient with a (CAG)180 repeat expansion and the propagation of highly expanded CAG repeats in lambda phage. Hum Genet. 99, 692-695.
33. Sharp, A.H., Loev, S.J., Schilling, G., Li, S.-H., Li, X.-J., Bao, J., Wagster, M.V., Kotzuk, J.A., Steiner, J.P., Lo, A., et al. (1995). Widespread expression of Huntington's disease gene (IT15) protein product. Neuron 14, 1065-1074.
34. Smith, D.B., and Johnson, K.S. (1988). Single-step purification of peptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67, 31-40.
35. Stott, K., Blackburn, J.M., Butler, P.J.G., and Perutz, M. (1995). Incorporation of glutamine repeats makes protein oligomerize: implications for neurodegenerative diseases. Proc. Natl. Acad. Sci. USA 92, 6509-6513.
36. Tellez-Nagel, I., Johnson, B., and Terry, R.D. (1974). Studies on brain biopsies of patients with Huntington's chorea. J. Neurocyt. 3, 308-332.
37. Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
38. Trottier, Y., Devys, D., Imbert, G., Sandou, F., An, I., Lutz, Y., Weber, C., Agid, Y., Hirsch, E.C., and Mandel, J.-L.(1995a). Cellular localisation of the Huntington's disease protein and discrimination of the normal and mutated forms. Nat. Genet. 10, 104-110.
39. Trottier, Y., Lutz, Y., Stevanin, G., Imbert, G., Devys, D., Cancel, G., Sandou, F., Weber, C., David, G.,Tora, L., et al. (1995b). Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 378, 403-406.
40. Vonsattel, J.-P., Myers, R.H., Stevens, T.J., Ferrante, R.J., Bird, E.D., and Richardson, E.P. (1985). Neuropathological classification of Huntington's disease. J. Neuropath. Exp. Neurol. 44, 559-577.
41. Wanker, E.E., Rovira, C., Scherzinger, E., Hasenbank, R., Walter, S., Tait, D., Colicelli, J., and Lehrach, H. (1997). HIP-1: a huntingtin interacting protein isolated by the yeast two-hybrid system. Hum. Mol. Genet. 6, 487-495.