Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila

Cell

Volumn 93, Issue 6, 1998, Pages 939-949

  Warrick, John M ^a   Paulson, Henry L ^b   Gray Board, Gladys L ^a   Bui, Quang T ^a   Fischbeck, Kenneth H ^a   Pittman, Randall N ^a   Bonini, Nancy M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMINE; POLYGLUTAMINE PROTEIN; PROTEIN P35; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; DEGENERATIVE DISEASE; DROSOPHILA; HISTOPATHOLOGY; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TARGETING; SPINOCEREBELLAR DEGENERATION;

ARACHNIDA; ATAXIA; HEXAPODA; INSECTA; INVERTEBRATA;

EID: 18544392423     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81200-3     Document Type: Article

References (40)

1. Abrams, J.M., White, K., Fessier, L.I., and Steller, H. (1993). Programmed cell death during Drosophila embryogenesis. Development 117, 29-43.
2. Andrew, S.E., Goldberg, Y.P., and Hayden, M.R. (1997). Rethinking genotype and phenotype correlations in polyglutamine expansion disorders. Hum. Mol. Genet. 6, 2005-2010.
3. Blackman, R., Sanicola, M., Raftery, L., Gillevet, T., and Gelbart, W. (1991). An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development 111, 657-665.
4. Bonini, N.M., Leiserson, W.M., and Benzer, S. (1993). The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72, 379-395.
5. Brand, A.H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
6. Burke, J.R., Wingfield, M.S., Lewis, K.E., Roses, A.D., Lee, J.E., Hulette, C., Pericak-Vance, M.A., and Vance, J.M. (1994). The Haw River syndrome: dentatorubral-pallidoluysian atrophy (DRLA) in an African-American family. Nature Genet. 7, 521-524.
7. Cagan, R.L., and Ready, D.F. (1989). The emergence of order in the Drosophila pupal retina. Dev. Biol. 136, 346-362.
8. Chen, P., Nordstrom, W., Gish, B., and Abrams, J. (1996). grim, a novel cell death gene in Drosophila. Genes Dev. 10, 1773-1782.
9. Davies, S.W., Turmaine, 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 underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90, 537-548.
10. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P., and Aronin, N. (1997). Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993.
11. Dürr, A., Stevanin, G., Cancel, G., Duyckaerts, C., Abbas, N., Didierjean, O., Chneiweiss, H., Benomar, A., Lyon-Caen, O., Julien, J., et al. (1996). Spinocerebellar ataxia 3 and Machado-Joseph disease: clinical, molecular and neuropathologic features. Ann. Neurol. 39, 490-491.
12. Ellis, M., O'Neill, E., and Rubin, G. (1993). Expression of Drosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein. Development 119, 855-865.
13. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 57,651-660.
14. Grether, M.E., Abrams, J.M., Agapite, J., White, K., and Steller, H. (1995). The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9, 1694-1708.
15. Hay, B.A., Wolff, T., and Rubin, G.M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
16. Igarashi, S., Koide, R., Shimohata, T., Yamada, M., Hayashi, Y., Takano, H., Date, H., Oyake, M., Sato, T., Sato, A., et al. (1998). Suppression of aggregate formation and apoptosis by transglutaminase inhibitors in cells expressing truncated DRPLA protein with an expanded polyglutamine stretch. Nature Genet 18, 111-117.
17. 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. Nature Genet. 13, 196-202.
18. Kawaguchi, Y., Okamoto, T., Taniwaki, M., Aizawa, M., Inoue, M., Katayama, H., Nakamura, S., Nishimura, M., Akiguchi, I., Kimura, J., Narumiya, S., and Kakizuka, A. (1994). CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nature Genet. 8, 221-228.
19. Lin, D.M., and Goodman, C.S. (1994). Ectopic and increased expression of fasciclin II alters motoneuron growth cone guidance. Neuron 13, 507-523.
20. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Heterington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S.W. and Bates, G.P. (1996). Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87, 493-506.
21. Matilla, A., Koshy, B.T., Cummings, C.J., Isobe, T., Orr, H.T., and Zoghbi, H.Y. (1997). The cerebellar leucine-rich acidic nuclear protein interacts with ataxin-1. Nature 389, 974-978.
22. O'Neill, E.M., Rebay, I., Tijan, R., and Rubin, G.M. (1994). The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78, 137-147.
23. Ordway, J.M., Tallaksen-Greene, S., Gutekunst, C.-A., Bernstein, E. M., Cearley, J.A., Wiener, H.W., Dure, L.S., IV, Lindsley, R., Hersch, S.M., Jope, R.S., Albin, R.L., and Detloff, P.J. (1997). Ectopically expressed CAG repeats cause intranuclear inclusions and a progressive late onset neurological phenotype in the mouse. Cell 91, 753-763.
24. Paulson, H.L., Das, S.S., Crino, P.B., Perez, M.K., Patel, S.C., Gotsdiner, D., Fischbeck, K.H., and Pittman, R.N. (1997a). Machado-Joseph disease gene product is a cytoplasmic protein widely expressed in brain. Ann. Neurol. 41, 453-462.
25. Paulson, H.L., Perez, M.K., Trottier, Y., Trojanowski, J.Q., Subramony, S.H., Das, S.S., Vig, P., Mandel, J.-L., Fischbeck, K.H., and Pittman, R.N. (1997b). Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxiatype 3. Neuron 19, 333-344.
26. Raftery, L.A., Sanicola, M., Blackman, R.K., and Gelbart, W.M. (1991). The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary? Development 113, 27-33.
27. Ranum, L., Lundgren, J., Schut, L., Ahrens, M., Perlman, S., Aita, J., Bird, T., Gomez, C., and Orr, H. (1995). Spinocerebellar ataxia type 1 and Machado-Joseph disease: incidence of CAG expansions among adult-onset ataxia patients from 311 families with dominant, recessive, or sporadic ataxia. Amer. J. Hum. Genet. 57, 603-603.
28. Ready, D.F., Hanson, T.E., and Benzer, S. (1976). Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53, 217-240.
29. Reddy, P.S., and Housman, D.E. (1997). The complex pathology of trinucleotide repeats. Curr. Opin. Cell Biol. 9, 364-372.
30. Robinow, S., and White, K. (1988). The locus elav of Drosophila melanogaster is expressed in all neurons at all developmental stages. Dev. Biol. 126, 294-303.
31. Ross, C. (1997). Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative diseases? Neuron 19, 1147-1150.
32. Scherzinger, E., Lurz, R., Turmaine, M., Mangiarini, L., Holenbach, B., Hasenbank, R., Bates, G.P., Davies, S.W., Lehrach, H., and Wanker, E.E. (1997). Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90, 549-558.
33. Schols, L., Vieri-Saecker, A.M.M., Schols, S., Przuntek, H., Epplen, J.T., and Riess, O. (1995). Trinucleotide expansion within the MJD1 gene presents clinically as spinocerebellar ataxia and occurs most frequently in German SCA patients. Hum. Mol. Gen. 4, 1001-1005.
34. Shubin, N., Tabin, C., and Carroll, S. (1997). Fossils, genes and the evolution of animal limbs. Nature 388, 639-648.
35. Spradling, A.C., and Rubin, G.M. (1983). The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell 34, 47-57.
36. White, K., Tahaoglu, E., and Steller, H. (1996). Cell killing by the Drosophila gene reaper. Science 271, 805-807.
37. Wolff, T., and Ready, D.F. (1993). Pattern formation in the Drosophila retina. In The Development of Drosophila melanogaster. M. Bate and A. Martinez-Arias, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 1277-1325.
38. Yin, J., and Tully, T. (1996). CREB and the formation of long-term memory. Curr. Opin. Neurobiol. 6, 264-268.
39. Zipursky, S.L., and Rubin, G.M. (1994). Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila. Annu. Rev. Neurosci. 17, 373-397.
40. Zipursky, S.L., Venkatesh, T.R., Teplow, D.B., and Benzer, S. (1984). Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36, 15-26.