Expanded polyglutamine peptides alone are intrinsically cytotoxic and cause neurodegeneration in Drosophila

Human Molecular Genetics

Volumn 9, Issue 1, 2000, Pages 13-25

  Marsh, J Lawrence ^b   Walker, Heli ^b   Theisen, Heidi ^a,b   Zhu, Ya Zhen ^c   Fielder, Tom ^c   Purcell, Judy ^b   Thompson, Leslie M ^c  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYGLUTAMINE; PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DROSOPHILA; GENETIC ENGINEERING; HUNTINGTON CHOREA; LETHALITY; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; TOXICITY TESTING; TRANSGENE;

ANIMALIA; DROSOPHILA;

EID: 0034110465     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/9.1.13     Document Type: Article

References (50)

1. Reddy, H.P., Williams, M. and Tagle, D.A. (1999) Recent advances in understanding the pathogenesis of Huntington's disease. Trends Neurosci., 22, 248-255.
2. Zhuchenko, O., Bailey, J., Bonnen, P., Ashizawa, T., Stockton, D., Dobyns, W.B., Subramony, S.H., Zoghbi, H.Y. and Lee, C.C. (1997) Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the a1A-voltage-dependent calcium channel. Nature Genet, 15, 62-69.
3. Kakizuka, A. (1998) Protein precipitation: a common etiology in neurodegenerative disorders? Trends Genet., 14, 396-402.
4. Ross, C.A. (1997) Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative diseases. Neuron, 19, 1147-1150.
5. Duyao, M.P., Auerbach, A.B., Ryan, A., Persichetti, F., Barnes, G.T., McNeil, S.M., Ge, P., Vonsattel, J.-P., Gusella, J.F., Joyner, A.L. et al. (1995) Inactivation of the mouse Huntington's disease gene homolog Hdh, Science, 269, 407-410.
6. Zeitlin, S., Liu, J.-P., Chapman, D.L., Papaioannou, V.E. and Efstratiadis, A. (1995) Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nature Genet., 11, 155-163.
7. Burright, E.N., Clark, H.B., Servadio, A., Matilla, T., Feddersen, R.M., Yunis, W.S., Duvick, L.A., Zoghbi, H.Y. and Orr, H.T. (1995) SCA1 transgenic mice: a model for neurodegeneration caused by an expanded CAG trinucleotide repeat. Cell, 82, 937-948.
8. Hodgson, J.G. et al. (1999) YAC mouse model for Hunlington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron, 23, 181-192.
9. 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.
10. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Hetherington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S.W. et al. (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.
11. 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.
12. 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.
13. Bates, G.P., Mangiarini, L. and Davies, S.W. (1998) Transgenic mice in the study of polyglulamine repeat expansion diseases. Brain Pathol., 8, 699-714.
14. Paulson, H.L. (1999) Human Genetics '99: trinucleotide repeats. Protein fate in neurodegenerative proteinopathies: polyglutamine diseases join the (mis)fold. Am. J. Hum. Genet., 64, 339-345.
15. Klement, I.A., Skinner, P.J., Kaytor, M.D., Yi, H., Hersch, S.M., Clark, H.B., Zoghbi, H.Y. and Orr, H.T. (1998) Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell, 95, 41-53.
16. Saudou, F., Finkbeiner, S., Devys, D. and Greenberg, M.E. (1998) Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell, 95, 55-66.
17. Gutekunst, C.A., Li, S.-H., Yi, H., Mulroy, J.S., Kuemmerle, S., Jones, R., Rye, D., Ferrante, R.J., Hersch, S.M. and Li, X.-J. (1999) Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci., 19, 2522-2534.
18. Li, H., Li, S.H., Cheng, A.L., Mangiarini, L., Bates, G.P. and Li, X.J. (1999) Ultrastructural localization and progressive formation of neuropil aggregates in Huntington's disease transgenic mice. Hum. Mol. Genet., 8, 1227-1236.
19. Scherzinger, E., Sittler, A., Schweiger, K., Heiser, V., Lurz, R., Hasenbank, R., Bates, G.P., Lehrach, H. and Wanker, E.E. (1999) Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc. Natl Acad. Sci. USA, 96, 4604-4609.
20. Perutz, M.F. (1999) Glutamine repeats and neurodegenerative diseases: molecular aspects. Trends Biochem. Sci., 24, 58-63.
21. Koshy, B.T. and Zoghbi, H.Y. (1997) The CAG/polyglutamine trace diseases: gene products and moleuclar pathogenesis. Brain Pathol., 7, 927-942.
22. Ordway, J.M., Tallaksen-Greene, S., Gutekunst, C.-A., Bernstein, E.M., Cearley, J.A., Wiener, H.W., Dure IV, L.S., Lindsey, R., Hersch, S.M., Jope, R.S. et al. (1997) Ectopically espressed CAG repeats cause intranuclear inclusions and a progressive late onset neurological phenotype in the mouse. Cell, 91, 753-763.
23. La Spada, A.R., Wilson, E.M., Lubahn, D.B., Harding, A.E. and Fischbeck, K. (1991) Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature, 352, 77-79.
24. Warrick, J.M., Paulson, H.L., Gray-Board, G.L., Bui, Q.T., Fischbeck, K.H., Pittman, R.N. and Bonini, N.M. (1998) Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell, 93, 939-949.
25. Jackson, G.R., Salecker, I., Dong, X., Yao, X., Arnheim, N., Faber, P.W., MacDonald, M.E. and Zipursky, S.L. (1998) Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron, 21, 633-642.
26. Brand, A. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
27. 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.
28. Speicher, S.A., Thomas, U., Hinz, U. and Knust, E. (1994) The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginai discs: control of cell proliferation. Development, 120, 535-544.
29. Wolff, T., Martin, K.A., Rubin, G.M. and Zipursky, S.L. (1997) The development of the Drosophila visual system. In Jessell, T.M. and Zipursky, S.L. (eds), Molecular and Cellular Approaches to Neuronal Development. Oxford University Press, New York. NY, pp. 474-508.
30. Klingensmith, J., Nusse, R. and Perrimon, N. (1994) The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wg signal. Genes DFV., 8, 118-130.
31. Theisen, H., Purcell, J., Bennett, M., Kansagara, D., Syed, A. and Marsh, J.L. (1994) Dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development, 120, 347-360.
32. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell, 72, 971-983.
33. Strong, T.V., Tagle, D.A., Valdes, J.M., Elmer, L.W., Boehm, K., Swaroop, M., Kaatz, K.W., Collins, F.S. and Albin, R.L. (1993) Widespread expression of the human and rat Huntington's disease gene in brain and nonneural tissues. Nature Genet., 5, 259-265.
34. Sussman, D.J., Klingensmith, J., Salinas, P., Adams, P.S., Nusse, R. and Perrimon, N. (1994) Isolation and characterization of a mouse homolog of the Drosophila segment polarity gene dishevelled. Develop. Biol., 166, 73-86.
35. Axelrod, J.D., Miller, J.R., Shulman, J.M., Moon, R.T. and Perrimon, N. (1998) Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev., 12, 2610-2622.
36. Stevanin, G., Trottier, Y., Cancel, G., Dün, A., David, G., Didierjean, O., Bürk, K., Imbert, G., Saudou, F., Abada-Bendib, M. et al. (1996) Screening for proteins with polyglutamine expansions in autosomal dominant cerebellar ataxias. Hum. Mol. Genet., 5, 1887-1892.
37. Warner, C.L., Griffin, J.E., Wilson, J.D., Jacobs, L.D., Murray, K.R., Fischbeck, K.H., Dickoff, D. and Griggs, R.C. (1992) X-linked spinomuscular atrophy: a kindred with associated abnormal androgen receptor binding. Neurology, 42, 2181-2184.
38. White, J.K., Auerbach, W., Duyao, M.P., Vonsattel, J., Gusella, J.F., Joyner, A.L. and MacDonald, M.E. (1997) Huntingtin is required for neurogenesis and is not impaired by the Huntington's disease CAG expansion. Nature Genet., 17, 404-410.
39. Wexler, N.S. et al. (1987) Homozygotes for Huntington's disease. Nature, 326, 194-197.
40. Faber, P.W., Alter, J.R., MacDonald, M.E. and Hart, A.C. (1999) Polyglutamine-mediated dysfunction and apoptotic death of a Caenorhabditis elegans sensory neuron. Proc. Natl Acad. Sci. USA, 96, 179-184.
41. Harper, P.S. (ed.) (1991) Huntington's Disease. Major Problems in Neurology, Vol. 22. W.B. Saunders, London, pp. 141-178.
42. Penny Jr, J.B., Vonsattel, J.-P., MacDonald, M.E., Gusella, J.F. and Myers, R.H. (1997) CAG repeat number governs the development rate of pathology in Huntington's disease. Ann. Neurol., 41, 689-692.
43. Rubin, G.M. and Spradling, A.C. (1982) Genetic transformation of Drosophila with transposable elements vectors. Science, 218, 348-353.
44. Spradling, A.C. and Rubin, G.M. (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science, 218, 341-347.
45. Park, S. and Lim, J.K. (1995) A microinjection technique for ethanoltreated eggs and a mating scheme for detection of germ line transformants. Dros. Info. Sev., 76, 197-199.
46. Ellis, M.C., O'Neill, E.M. and Rubin, G.M. (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.
47. Robinow, S. and White, K. (1988) The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev. Biol., 126, 294-303.
48. Staehling-Hampton, K., Jackson, P.D., Clark, M.J., Brand, A.M. and Hoffmann, F.M. (1994) Specificity of bone morphogenetic protein-related factors: cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A. Cell Growth Differ., 5, 585-593.
49. Yanagawa, S., van Leeuwen, F., Wodarz, A., Klingensmith, J. and Nusse, R. (1995) The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev., 9, 1087-1097.
50. Grieder, N.C., Nellen, D., Burke, R., Basler, K. and Affolter, M. (1995) Schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BFI. Cell, 81, 791-800.