High level expression of expanded full-length ataxin-3 in vitro causes cell death and formation of intranuclear inclusions in neuronal cells

Human Molecular Genetics

Volumn 8, Issue 7, 1999, Pages 1169-1176

  Evert, Bernd O ^e   Wüllner, Ullrich ^a   Schulz, Jörg B ^e   Weller, Michael ^e   Groscurth, Peter ^b   Trottier, Yvon ^c   Brice, Alexis ^d   Klockgether, Thomas ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 3; CELL PROTEIN; STAUROSPORINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; ATAXIA; CELL DEATH; CELL NUCLEUS INCLUSION BODY; CELL NUCLEUS MEMBRANE; CELL ULTRASTRUCTURE; CELL VACUOLE; CONTROLLED STUDY; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINOCEREBELLAR DEGENERATION;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CELL DEATH; CELL LINE; HUMANS; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; RATS; RECOMBINANT PROTEINS; REPRESSOR PROTEINS;

EID: 0345436080     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/8.7.1169     Document Type: Article

References (41)

1. Rosenberg, R.N. (1992) Machado-Joseph disease: an autosomal dominant motor system degeneration. Mov. Disord., 7, 193-203.
2. Takiyama, Y., Oyanagi, S., Kawashima, S., Sakamoto, H., Saito, K., Yoshida, M., Tsuji, S., Mizuno, Y. and Nishizawa, M. (1994) A clinical and pathologic study of a large Japanese family with Machado-Joseph disease tightly linked to the DNA markers on chromosome 14q. Neurology, 44, 1302-1308.
3. Wellington, C.L., Brinkman, R.R., O'Kusky, J.R. and Harden, M.R. (1997) Toward understanding the molecular pathology of Huntington's disease. Brain Pathol., 7, 979-1002.
4. Kakizuka, A. (1997) Degenerative ataxias: genetics, pathogenesis and animal models. Curr. Opin. Neurol., 10, 285-290.
5. Robitaille, Y., Loppes-Cendes, I., Becher, M., Rouleau, G.A. and Clark, A.W. (1997) The neuropathology of CAG repeat diseases: review and update of genetic and molecular features. Brain Pathol., 7, 901-926.
6. Koshi, B.T. and Zoghbi, H.Y. (1997) The CAG/polyglutamine tract diseases: gene products and molecular pathogenesis. Brain Pathol., 7, 927-942.
7. Ross, A.C. (1997) Intranuclear neuronal inclusions: a common pathogenic mechanism for for glutamine-repeat neurodegenerative diseases? Neuron. 19, 1147-1150.
8. David, G., Abbas, N., Stevanin, G., Dürr, A., Yvert, G., Cancel, G., Weber, C., Imbert, G., Saudou, F., Antoniou, E., Drabkin, H., Gemmill, R., Giunti, P., Benomar, A., Wood, N., Ruberg, M., Agid, Y., Mandel, J.L. and Brice, A. (1997) Cloning of the SCA7 gene reveals a highly unstable CAG repeat expansion. Nature Genet., 17, 65-70.
9. 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, 221-227.
10. Dürr, A., Stevanin, G., Cancel, G., Duyckaerts, C., Abbas, N., Didierjean, O., Chneiweiss, H., Benomar, A., Lyon-Caen, O., Julien, J., Serdaru, M., Penet, C., Agid, Y. and Brice, A. (1996) Spinocerebellar ataxia 3 and Machado-Joseph disease: clinical, molecular and neuropathological features. Ann. Neurol., 39, 490-499.
11. Trottier, Y., Lutz, Y., Stevanin, G., Imbert, G., Devys, D., Cancel, G., Saudou, F., Weber, C., David, G., Tora, L., Agid, Y., Brice, A. and Mandel, J.L. (1995) Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature, 378, 403-406.
12. Paulson, H.L., Das, S.S., Crino, P.B., Perez, M.K., Patel, S.C., Gotsdiner, D., Fischbeck, K.H. and Pittman, R.N. (1997) Machado-Joseph disease gene product is a cytoplasmic protein widely expressed in brain. Ann. Neurol., 41, 453-462.
13. Schmidt, T., Landwehrmeyer, G.B., Schmitt, I., Trottier, Y., Auburger, G., Laccone, F., Klockgether, T., Völpel, M., Epplen, J.T., Schöls, L. and Riess, O. (1998) An isoform of ataxin-3 accumulates in the nucleus of neuronal cells in affected brain regions of SCA3 patients. Brain Pathol., 8, 669-679.
14. 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.
15. 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. (1997) Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron, 19, 333-344.
16. 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.
17. Scherzinger, E., Lurz, R., Turmaine, M., Mangiarini, L., Hollenbach, B., Hasenbank, R., Bates, G.B., 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.
18. 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 neuntes in brain. Science, 277, 1990-1993.
19. Skinner, P.J., Koshy, B.T., Cummings, C.J., Klement, I.A., Helin, K., Servadio, A., Zoghbi, H.Y. and Orr, H.T. (1997) Ataxin-1 with an expanded glutamine tract alters nuclear matrix-associated structures. Nature, 389, 971-974.
20. 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.
21. Klockgether, T. and Evert, B. (1998) Genes involved in hereditary ataxias. Trends Neurosci., 21, 413-418.
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 HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell, 87, 493-506.
23. 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.
24. Ordway, J.M., Tallaksen-Greene, S., Gutekunst, C.A., Bernstein, E.M., Cearley, J.A., Wiener, H.W., Dure, L.S.IV, Lindsey, 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.
25. 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.
26. Reddy, P.H., Williams, M., Charles, V., Garrett, L., Pike-Buchanan, L., Whetsell, W.O., Miller, G. and Tagle, D.A. (1998) Behavioural abnormalities and selective neuronal loss in HD transgenic mice expressing mutated full-length HD cDNA. Nature Genet., 20, 198-202.
27. Martindale, D., Hackam, A., Wieczorek, A., Ellerby, L., Wellington, C., McCutcheon, K., Singaraja, R., Kazemi-Esfarjani, P., Devon, R., Kim, S.U., Bredesen, D.E., Tufaro, F. and Hayden, M.R. (1998) Length of huntingtin and its polyglutamine tract influences localization and frequency of intracellular aggregates. Nature Genet., 18, 150-154.
28. 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.
29. Lunkes, A. and Mandel, J.L. (1998) A cellular model that recapitulates major pathogenic steps of Huntington's disease. Hum. Mol. Genet., 7, 1355-1361.
30. Durand, M.M., Chugani D.C., Mahmoudi, M. and Phelps, M.E. (1990) Characterization of neuron-like cell line immortalized from primary rat mesencephalon cultures. Neurosci. Abstr., 16, 40.
31. Gossen, M. and Bujard, H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl Acad. Sci. USA, 89, 5547-5551.
32. Trottier, Y., Cancel, G., An-Gourfinkel, I., Lutz, Y., Weber, C., Brice, A., Hirsch, E. and Mandel, J.L. (1998) Heterogenous intracellular localization and expression of ataxin-3. Neurobiol. Dis., 5, 335-347.
33. 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 localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell, 95, 41-53.
34. Chai, Y., Koppenhafer, S.L., Shoesmith, S.J., Perez, M.K. and Paulson, H.L. (1999) Evidence for proteasome involvement in polyglutamine disease: localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum. Mol. Genet., 8, 673-682.
35. Tait, D., Riccio, M., Sittler, A., Scherzinger, E., Santi, S., Ognibene, A., Maraldi, N.M., Lehrach, H. and Wanker, E.E. (1998) Ataxin-3 is transported into the nucleus and associates with the nuclear matrix. Hum. Mol. Genet., 7, 991-997.
36. Sisodia, S.S. (1998) Nuclear inclusions in glutamine repeat disorders: are they pernicious, coincidental, or beneficial? Cell, 95, 1-4.
37. Kim, T.W. and Tanzi, R.E. (1998) Neuronal intranuclear inclusions in polyglutamine diseases: nuclear weapons or nuclear fallout? Neuron, 21, 657-659.
38. Clark, H.B., Burright, E.N., Yunis, W.S., Larson, S., Wilcox, C., Hartman, B., Matilla, A., Zoghbi, H.Y. and Orr, H.T. (1997) Purkinje cell expression of a mutant allele of SCA1 in transgenic mice leads to disperate effects on motor behaviors, followed by a progressive cerebellar dysfunction and histological alterations. J. Neurosci., 17, 7385-7395.
39. Jentsch, S. and Ulrich, H.D. (1998) Ubiquitous déjà vu. Nature, 395, 321-323.
40. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65, 55-63.
41. Kressel, M. and Groscurth, P. (1994) Distinction of apoptotic and necrotic cell death by in situ labelling of fragmented DNA. Cell Tissue Res., 278, 549-556.