Molecular pathogenesis of spinocerebellar ataxia type 1 disease

Molecules and Cells

Volumn 27, Issue 6, 2009, Pages 621-627

  Kang, Seongman ^a   Hong, Sunghoi ^a  

^a Korea University   (South Korea)

Author keywords

Aggregates; Ataxin 1; Cell therapy; Cellular dysfunction; Polyglutamine; Protein interaction

Indexed keywords

ANTIBODY; ATAXIN 1; CHAPERONE; DISACCHARIDE; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; HISTONE DEACETYLASE INHIBITOR; LEUPRORELIN; POLYGLUTAMINE; RECOMBINANT PROTEIN; SHORT HAIRPIN RNA;

ATAXIA; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL SURVIVAL; DRUG MECHANISM; EMBRYONIC STEM CELL; GENE THERAPY; GRANULE CELL; HUMAN; HUNTINGTON CHOREA; MOLECULAR DYNAMICS; MOTOR DYSFUNCTION; NERVE CELL; NONHUMAN; PATHOGENESIS; PHENOTYPE; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PURKINJE CELL; RNA INTERFERENCE; SHORT SURVEY; SPINOCEREBELLAR ATAXIA TYPE 1; SPINOCEREBELLAR DEGENERATION; STEM CELL TRANSPLANTATION;

ANIMALS; HUMANS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDES; PROTEIN BINDING; SPINOCEREBELLAR ATAXIAS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 67650330344     PISSN: 10168478     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10059-009-0095-y     Document Type: Short Survey

References (85)

1. Al-Ramahi, I., Lam, Y.C., Chen, H.K., de Gouyon, B., Zhang, M., Perez, A.M., Branco, J., de Haro, M., Patterson, C., Zoghbi, H.Y., et al. (2006). CHIP protects from the neurotoxicity of expanded and wild-type ataxin-1 and promotes their ubiquitination and degradation. J. Biol. Chem. 281, 26714-26724.
2. Banfi, S., Servadio, A., Chung, M.Y., Kwiatkowski, T.J., Jr., McCall, A.E., Duvick, L.A., Shen, Y., Roth, E.J., Orr, H.T., and Zoghbi, H.Y. (1994). Identification and characterization of the gene causing type 1 spinocerebellar ataxia. Nat. Genet. 7, 513-520.
3. Becher, M.W., Kotzuk, J.A., Sharp, A.H., Davies, S.W., Bates, G.P., Price, D.L., and Ross, C.A. (1998). Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length. Neurobiol. Dis. 4, 387-397.
4. Burright, E.N., Davidson, J.D., Duvick, L.A., Koshy, B., Zoghbi, H.Y., and Orr, H.T. (1997). Identification of a self-association region within the SCA1 gene product, ataxin-1. Hum. Mol. Genet. 6, 513-518.
5. Chan, H.Y., Warrick, J.M., Gray-Board, G.L., Paulson, H.L., and Bonini, N.M. (2000). Mechanisms of chaperone suppression of polyglutamine disease: Selectivity, synergy and modulation of protein solubility in Drosophila. Hum. Mol. Genet. 9, 2811-2820.
6. Chen, S., Berthelier, V., Yang, W., and Wetzel, R. (2001). Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity. J. Mol. Biol. 311, 173-182.
7. Chen, H.K., Fernandez-Funez, P., Acevedo, S.F., Lam, Y.C., Kaytor, M.D., Fernandez, M.H., Aitken, A., Skoulakis, E.M., Orr, H.T., Botas, J., et al. (2003). Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell. 113, 457-468.
8. Chung, M.Y., Ranum, L.P., Duvick, L.A., Servadio, A., Zoghbi, H.Y., and Orr, H.T. (1993). Evidence for a mechanism predisposing to intergenerational CAG repeat instability in spinocerebellar ataxia type I. Nat. Genet. 5, 254-258.
9. Cummings, C.J., Mancini, M.A., Antalffy, B., DeFranco, D.B., Orr, H.T., and Zoghbi, H.Y. (1998). Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet. 19, 148-154.
10. Cummings, C.J., Orr, H.T., and Zoghbi, H.Y. (1999a). Progress in pathogenesis studies of spinocerebellar ataxia type 1. Philos. Trans. R Soc. Lond B Biol. Sci. 354, 1079-1081.
11. Cummings, C.J., Reinstein, E., Sun, Y., Antalffy, B., Jiang, Y., Ciechanover, A., Orr, H.T., Beaudet, A.L., and Zoghbi, H.Y. (1999b). Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron 24, 879-892.
12. Cummings, C.J., Sun, Y., Opal, P., Antalffy, B., Mestril, R., Orr, H.T., Dillmann, W.H., and Zoghbi, H.Y. (2001). Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum. Mol. Genet. 10, 1511-1518.
13. Cvetanovic, M., Rooney, R.J., Garcia, J.J., Toporovskaya, N., Zoghbi, H.Y., and Opal, P. (2007). The role of LANP and ataxin 1 in E4F-mediated transcriptional repression. EMBO Rep. 8, 671-677.
14. 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.
15. de Chiara, C., Giannini, C., Adinolfi, S., de Boer, J., Guida, S., Ramos, A., Jodice, C., Kioussis, D., and Pastore, A. (2003). The AXH module: An independently folded domain common to ataxin-1 and HBP1. FEBS Lett. 551, 107-112.
16. 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.
17. Emamian, E.S., Kaytor, M.D., Duvick, L.A., Zu, T., Tousey, S.K., Zoghbi, H.Y., Clark, H.B., and Orr, H.T. (2003). Serine 776 of ataxin-1 is critical for polyglutamine-induced disease in SCA1 transgenic mice. Neuron 38, 375-387.
18. Fernandez-Funez, P., Nino-Rosales, M.L., de Gouyon, B., She, W.C., Luchak, J.M., Martinez, P., Turiegano, E., Benito, J., Capovilla, M., Skinner, P.J.I et al. (2000). Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408, 101-106.
19. Gatchel, J.R., Watase, K., Thaller, C., Carson, J.P., Jafar-Nejad, P., Shaw, C., Zu, T., Orr, H.T., and Zoghbi, H.Y. (2008). The insulinlike growth factor pathway is altered in spinocerebellar ataxia type 1 and type 7. Proc. Natl. Acad. Sci. USA 105, 1291-1296.
20. Goold, R., Hubank, M., Hunt, A., Holton, J., Menon, R.P., Revesz, T., Pandolfo, M., and Matilla-Duenas, A. (2007). Down-regulation of the dopamine receptor D2 in mice lacking ataxin 1. Hum. Mol. Genet. 16, 2122-2134.
21. Heiser, V., Scherzinger, E., Boeddrich, A., Nordhoff, E., Lurz, R., Schugardt, N., Lehrach, H., and Wanker, E.E. (2000). Inhibition of huntingtin fibrillogenesis by specific antibodies and small molecules: implications for Huntington's disease therapy. Proc. Natl. Acad. Sci. USA 97, 6739-6744.
22. Heiser, V., Engemann, S., Brocker, W., Dunkel, I., Boeddrich, A., Waelter, S., Nordhoff, E., Lurz, R., Schugardt, N., Rautenberg, S.I. et al. (2002). Identification of benzothiazoles as potential polyglutamine aggregation inhibitors of Huntington's disease by using an automated filter retardation assay. Proc. Natl. Acad. Sci. USA 99, 16400-16406.
23. Holmberg, M., Duyckaerts, C., Durr, A., Cancel, G., Gourfinkel-An, I., Damier, P., Faucheux, B., Trottier, Y., Hirsch, E.C., Agid, Y., et al. (1998). Spinocerebellar ataxia type 7 (SCA7): A neurodegenerative disorder with neuronal intranuclear inclusions. Hum. Mol. Genet. 7, 913-918.
24. Hong, S., Kim, S.J., Ka, S., Choi, I., and Kang, S. (2002). USP7, a ubiquitin-specific protease, interacts with ataxin-1, the SCA1 gene product. Mol. Cell Neurosci. 20, 298-306.
25. Hong, S., Ka, S., Kim, S., Park, Y., and Kang, S. (2003). p80 coilin, a coiled body-specific protein, interacts with ataxin-1, the SCA1 gene product. Biochim. Biophys. Acta 1638, 35-42.
26. Hong, S., Lee, S., Cho, S.G., and Kang, S. (2008). UbcH6 interacts with and ubiquitinates the SCA1 gene product ataxin-1. Biochem. Biophys. Res. Commun. 371, 256-260.
27. Huynh, D.P., Del Bigio, M.R., Ho, D.H., and Pulst, S.M. (1999). Expression of ataxin-2 in brains from normal individuals and patients with Alzheimer's disease and spinocerebellar ataxia 2. Ann. Neurol. 45, 232-241.
28. Irwin, S., Vandelft, M., Pinchev, D., Howell, J.L., Graczyk, J., Orr, H.T., and Truant, R. (2005). RNA association and nucleocytoplasmic shuttling by ataxin-1. J. Cell Sci. 118, 233-242.
29. Katsuno, M., Adachi, H., Doyu, M., Minamiyama, M., Sang, C., Kobayashi, Y., Inukai, A., and Sobue, G. (2003). Leuprorelin rescues polyglutamine-dependent phenotypes in a transgenic mouse model of spinal and bulbar muscular atrophy. Nat. Med. 9, 768-773.
30. Kazantsev, A., Walker, H.A., Slepko, N., Bear, J.E., Preisinger, E., Steffan, J.S., Zhu, Y.Z., Gertler, F.B., Housman, D.E., Marsh, J.L., et al. (2002). A bivalent Huntingtin binding peptide suppresses polyglutamine aggregation and pathogenesis in Drosophila. Nat. Genet. 25, 25.
31. Kazemi-Esfarjani, P., and Benzer, S. (2000). Genetic suppression of polyglutamine toxicity in Drosophila. Science 287, 1837-1840.
32. Khoshnan, A., Ko, J., and Patterson, P.H. (2002). Effects of intracellular expression of anti-huntingtin antibodies of various specificities on mutant huntingtin aggregation and toxicity. Proc. Natl. Acad. Sci. USA 99, 1002-1007.
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 nuclear localization and aggregation: Role in polyglutamine-induced disease in SCA1 transgenic mice [see comments]. Cell 95, 41-53.
34. Lam, Y.C., Bowman, A.B., Jafar-Nejad, P., Lim, J., Richman, R., Fryer, J.D., Hyun, E.D., Duvick, L.A., Orr, H.T., Botas, J., et al. (2006). ATAXIN-1 interacts with the repressor Capicua in its native complex to cause SCA1 neuropathology. Cell 127, 1335-1347.
35. Lecerf, J.M., Shirley, T.L., Zhu, Q., Kazantsev, A., Amersdorfer, P., Housman, D.E., Messer, A., and Huston, J.S. (2001). Human single-chain Fv intrabodies counteract in situ huntingtin aggregation in cellular models of Huntington's disease. Proc. Natl. Acad. Sci. USA 98, 4764-4769.
36. Lee, S., Hong, S., and Kang, S. (2008). The ubiquitin-conjugating enzyme UbcH6 regulates the transcriptional repression activity of the SCA1 gene product ataxin-1. Biochem. Biophys. Res. Commun. 372, 735-740.
37. Li, M., Miwa, S., Kobayashi, Y., Merry, D.E., Yamamoto, M., Tanaka, F., Doyu, M., Hashizume, Y., Fischbeck, K.H., and Sobue, G. (1998). Nuclear inclusions of the androgen receptor protein in spinal and bulbar muscular atrophy. Ann. Neurol. 44, 249-254.
38. Lim, J., Hao, T., Shaw, C., Patel, A.J., Szabo, G., Rual, J.F., Fisk, C.J., Li, N., Smolyar, A., Hill, D.E.I. et al. (2006). A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell 125, 801-814.
39. Lim, J., Crespo-Barreto, J., Jafar-Nejad, P., Bowman, A.B., Richman, R., Hill, D.E., Orr, H.T., and Zoghbi, H.Y. (2008). Opposing effects of polyglutamine expansion on native protein complexes contribute to SCA1. Nature 452, 713-718.
40. 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.
41. McCampbell, A., Taye, A.A., Whitty, L., Penney, E., Steffan, J.S., and Fischbeck, K.H. (2001). Histone deacetylase inhibitors reduce polyglutamine toxicity. Proc. Natl. Acad. Sci. USA 98, 15179-15184.
42. Michalik, A., and Van Broeckhoven, C. (2003). Pathogenesis of polyglutamine disorders: Aggregation revisited. Hum. Mol. Genet. 12, R173-186.
43. Mizutani, A., Wang, L., Rajan, H., Vig, P.J., Alaynick, W.A., Thaler, J.P., and Tsai, C.C. (2005). Boat, an AXH domain protein, suppresses the cytotoxicity of mutant ataxin-1. EMBO J. 24, 3339-3351.
44. Muchowski, P.J., Schaffar, G., Sittler, A., Wanker, E.E., Hayer-Hartl, M.K., and Hartl, F.U. (2000). Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl. Acad. Sci. USA 97, 7841-7846.
45. Nagai, Y., Tucker, T., Ren, H., Kenan, D.J., Henderson, B.S., Keene, J.D., Strittmatter, W.J., and Burke, J.R. (2000). Inhibition of polyglutamine protein aggregation and cell death by novel peptides identified by phage display screening. J. Biol. Chem. 275, 10437-10442.
46. Okazawa, H., Rich, T., Chang, A., Lin, X., Waragai, M., Kajikawa, M., Enokido, Y., Komuro, A., Kato, S., Shibata, M.I et al. (2002). Interaction between mutant ataxin-1 and PQBP-1 affects transcription and cell death. Neuron 34, 701-713.
47. Okuda, T., Hattori, H., Takeuchi, S., Shimizu, J., Ueda, H., Palvimo, J.J., Kanazawa, I., Kawano, H., Nakagawa, M., and Okazawa, H. (2003). PQBP-1 transgenic mice show a late-onset motor neuron disease-like phenotype. Hum. Mol. Genet. 12, 711-725.
48. Orr, H.T. (2000). The ins and outs of a polyglutamine neurodegenerative disease: Spinocerebellar ataxia type 1 (SCA1). Neurobiol. Dis. 7, 129-134.
49. Orr, H.T., and Zoghbi, H.Y. (2001). SCA1 molecular genetics: A history of a 13 year collaboration against glutamines. Hum. Mol. Genet. 10, 2307-2311.
50. Orr, H.T., and Zoghbi, H.Y. (2007). Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30, 575-621.
51. Orr, H.T., Chung, M.Y., Banfi, S., Kwiatkowski, T.J., Jr., Servadio, A., Beaudet, A.L., McCall, A.E., Duvick, L.A., Ranum, L.P., and Zoghbi, H.Y. (1993). Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nat. Genet. 4, 221-226.
52. Paulson, H. (2003). Polyglutamine neurodegeneration: Minding your Ps and Qs. Nat. Med. 9, 825-826.
53. 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.
54. Perutz, M.F., Johnson, T., Suzuki, M., and Finch, J.T. (1994). Glutamine repeats as polar zippers: Their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. USA 91, 5355-5358.
55. Ren, H., Nagai, Y., Tucker, T., Strittmatter, W.J., and Burke, J.R. (2001). Amino acid sequence requirements of peptides that inhibit polyglutamine-protein aggregation and cell death. Biochem. Biophys. Res. Commun. 288, 703-710.
56. Riley, B.E., Zoghbi, H.Y., and Orr, H.T. (2005). SUMOylation of the polyglutamine repeat protein, ataxin-1, is dependent on a functional nuclear localization signal. J. Biol. Chem. 280, 21942-21948.
57. Sanchez, I., Mahlke, C., and Yuan, J. (2003). Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature 421, 373-379.
58. Scherzinger, E., Lurz, R., Turmaine, M., Mangiarini, L., Hollenbach, 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 vitro. Cell 90, 549-558.
59. 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.
60. Schmidt, T., Lindenberg, K.S., Krebs, A., Schols, L., Laccone, F., Herms, J., Rechsteiner, M., Riess, O., and Landwehrmeyer, G.B. (2002). Protein surveillance machinery in brains with spinocerebellar ataxia type 3: Redistribution and differential recruitment of 26S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann. Neurol. 51, 302-310.
61. Serra, H.G., Byam, C.E., Lande, J.D., Tousey, S.K., Zoghbi, H.Y., and Orr, H.T. (2004). Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Hum. Mol. Genet. 13, 2535-2543.
62. Serra, H.G., Duvick, L., Zu, T., Carlson, K., Stevens, S., Jorgensen, N., Lysholm, A., Burright, E., Zoghbi, H.Y., Clark, H.B., et al. (2006). RORalpha-mediated Purkinje cell development determines disease severity in adult SCA1 mice. Cell 127, 697-708.
63. Servadio, A., Koshy, B., Armstrong, D., Antalffy, B., Orr, H.T., and Zoghbi, H.Y. (1995). Expression analysis of the ataxin-1 protein in tissues from normal and spinocerebellar ataxia type 1 individuals. Nat. Genet. 10, 94-98.
64. Sisodia, S.S. (1998). Nuclear inclusions in glutamine repeat disorders: are they pernicious, coincidental, or beneficial? Cell 95, 1-4.
65. 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.
66. Skinner, P.J., Vierra-Green, C.A., Emamian, E., Zoghbi, H.Y., and Orr, H.T. (2002). Amino acids in a region of ataxin-1 outside of the polyglutamine tract influence the course of disease in SCA1 transgenic mice. Neuromolecular Med. 1, 33-42.
67. Steffan, J.S., Bodai, L., Pallos, J., Poelman, M., McCampbell, A., Apostol, B.L., Kazantsev, A., Schmidt, E., Zhu, Y.Z., Greenwald, M., et al. (2001). Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413, 739-743.
68. Su, H.L., Muguruma, K., Matsuo-Takasaki, M., Kengaku, M., Watanabe, K., and Sasai, Y. (2006). Generation of cerebellar neuron precursors from embryonic stem cells. Dev. Biol. 290, 287-296.
69. Tanaka, M., Machida, Y., Niu, S., Ikeda, T., Jana, N.R., Doi, H., Kurosawa, M., Nekooki, M., and Nukina, N. (2004). Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nat. Med. 10, 148-154.
70. Taroni, F., and DiDonato, S. (2004). Pathways to motor incoordination: the inherited ataxias. Nat. Rev. Neurosci. 5, 641-655.
71. Thakur, A.K., and Wetzel, R. (2002). Mutational analysis of the structural organization of polyglutamine aggregates. Proc. Natl. Acad. Sci. USA 99, 17014-17019.
72. Tsai, C.C., Kao, H.Y., Mitzutani, A., Banayo, E., Rajan, H., McKeown, M., and Evans, R.M. (2004). Ataxin 1, a SCA1 neurodegenerative disorder protein, is functionally linked to the silencing mediator of retinoid and thyroid hormone receptors. Proc. Natl. Acad. Sci. USA 101, 4047-4052.
73. Tsuda, H., Jafar-Nejad, H., Patel, A.J., Sun, Y., Chen, H.K., Rose, M.F., Venken, K.J., Botas, J., Orr, H.T., Bellen, H.J., et al. (2005). The AXH domain of Ataxin-1 mediates neurodegeneration through its interaction with Gfi-1/Senseless proteins. Cell 122, 633-644.
74. Ueda, H., Goto, J., Hashida, H., Lin, X., Oyanagi, K., Kawano, H., Zoghbi, H.Y., Kanazawa, I., and Okazawa, H. (2002). Enhanced SUMOylation in polyglutamine diseases. Biochem. Biophys. Res. Commun. 293, 307-313.
75. Watase, K., Weeber, E.J., Xu, B., Antalffy, B., Yuva-Paylor, L., Hashimoto, K., Kano, M., Atkinson, R., Sun, Y., Armstrong, D.L., et al. (2002). A long CAG repeat in the mouse sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 34, 905-919.
76. Xia, H., Mao, Q., Eliason, S.L., Harper, S.Q., Martins, I.H., Orr, H.T., Paulson, H.L., Yang, L., Kotin, R.M., and Davidson, B.L. (2004). RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat. Med. 10, 816-820.
77. Yang, W., Dunlap, J.R., Andrews, R.B., and Wetzel, R. (2002). Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells. Hum. Mol. Genet. 11, 2905-2917.
78. Yoshida, H., Yoshizawa, T., Shibasaki, F., Shoji, S., and Kanazawa, I. (2002). Chemical chaperones reduce aggregate formation and cell death caused by the truncated Machado-Joseph disease gene product with an expanded polyglutamine stretch. Neurobiol. Dis. 10, 88-99.
79. Yue, S., Serra, H.G., Zoghbi, H.Y., and Orr, H.T. (2001). The spinocerebellar ataxia type 1 protein, ataxin-1, has RNA-binding activity that is inversely affected by the length of its polyglutamine tract. Hum. Mol. Genet. 10, 25-30.
80. Zoghbi, H.Y. (1995). Spinocerebellar ataxia type 1. Clin. Neurosci. 3, 5-11.
81. Zoghbi, H.Y. (2000). Spinocerebellar ataxias. Neurobiol. Dis. 7, 523-527.
82. Zoghbi, H.Y., Jodice, C., Sandkuijl, L.A., Kwiatkowski, T.J., Jr., McCall, A.E., Huntoon, S.A., Lulli, P., Spadaro, M., Litt, M., Cann, H.M., and et al. (1991). The gene for autosomal dominant spinocerebellar ataxia (SCA1) maps telomeric to the HLA complex and is closely linked to the D6S89 locus in three large kindreds. Am. J. Hum. Genet. 49, 23-30.
83. Zoghbi, H.Y., and Orr, H.T. (1995). Spinocerebellar ataxia type 1. Semin Cell Biol. 6, 29-35.
84. Zoghbi, H.Y., and Orr, H.T. (2000). Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23, 217-247.
85. Zoghbi, H.Y., and Orr, H.T. (2009). Pathogenic mechanisms of a polyglutamine-mediated neurodegenerative disease, Spinocerebellar Ataxia Type 1. J. Biol. Chem. 284, 7425-7429.