Silencing ataxin-3 mitigates degeneration in a rat model of Machado-Joseph disease: No role for wild-type ataxin-3?

Human Molecular Genetics

Volumn 19, Issue 12, 2010, Pages 2380-2394

  Alves, Sandro ^a,b,d   Nascimento Ferreira, Isabel ^a,b   Dufour, Noëlle ^d,e   Hassig, Raymonde ^d,e   Auregan, Gwennaëlle ^d,e   Nóbrega, Clévio ^a   Brouillet, Emmanuel ^d,e   Hantraye, Philippe ^d,e   Pedroso de Lima, Maria C ^a,c   Déglon, Nicole ^d,e   de Almeida, Luís Pereira ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^e SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; GENE; GENE OVEREXPRESSION; GENE SILENCING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MACHADO JOSEPH DISEASE; MALE; MJD1 GENE; NERVE CELL DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; HUMANS; MACHADO-JOSEPH DISEASE; MALE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; RATS; RATS, WISTAR; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING;

RATTUS;

EID: 77955290123     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq111     Document Type: Article

References (74)

1. 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.
2. Sudarsky, L. and Coutinho, P. (1995) Machado-Joseph disease. Clin. Neurosci., 3, 17-22.
3. Rosenberg, R.N. (1992) Machado-Joseph disease: an autosomal dominant motor system degeneration. Mov. Disord., 7, 193-203.
4. Subramony, S.H., Hernandez, D., Adam, A., Smith-Jefferson, S., Hussey, J., Gwinn-Hardy, K., Lynch, T., McDaniel, O., Hardy, J., Farrer, M. and Singleton, A. (2002) Ethnic differences in the expression of neurodegenerative disease: Machado-Joseph disease in Africans and Caucasians. Mov. Disord., 17, 1068-1071.
5. Gwinn-Hardy, K., Singleton, A., O'Suilleabhain, P., Boss, M., Nicholl, D., Adam, A., Hussey, J., Critchley, P., Hardy, J. and Farrer, M. (2001) Spinocerebellar ataxia type 3 phenotypically resembling parkinson disease in a black family. Arch. Neurol., 58, 296-299.
6. Lu, C.S., Chang, H.C., Kuo, P.C., Liu, Y.L., Wu, W.S., Weng, Y.H., Yen, T.C. and Chou, Y.H. (2004) The parkinsonian phenotype of spinocerebellar ataxia type 3 in a Taiwanese family. Parkinsonism Relat. Disord., 10, 369-373.
7. Durr, 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 neuropathological features. Ann. Neurol., 39, 490-499.
8. 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.
9. Fowler, H.L. (1984) Machado-Joseph-Azorean disease. A 10-year study. Arch. Neurol., 41, 921-925.
10. Yen, T.C., Lu, C.S., Tzen, K.Y., Wey, S.P., Chou, Y.H., Weng, Y.H., Kao, P.F. and Ting, G. (2000) Decreased dopamine transporter binding in Machado-Joseph disease. J. Nucl. Med., 41, 994-998.
11. Yen, T.C., Tzen, K.Y., Chen, M.C., Chou, Y.H., Chen, R.S., Chen, C.J., Wey, S.P., Ting, G. and Lu, C.S. (2002) Dopamine transporter concentration is reduced in asymptomatic Machado-Joseph disease gene carriers. J. Nucl. Med., 43, 153-159.
12. Taniwaki, T., Sakai, T., Kobayashi, T., Kuwabara, Y., Otsuka, M., Ichiya, Y., Masuda, K. and Goto, I. (1997) Positron emission tomography (PET) in Machado-Joseph disease. J. Neurol. Sci., 145, 63-67.
13. Alves, S., Regulier, E., Nascimento-Ferreira, I., Hassig, R., Dufour, N., Koeppen, A., Carvalho, A.L., Simoes, S., Pedroso de Lima, M.C., Brouillet, E. et al. (2008) Striatal and nigral pathology in a lentiviral rat model of Machado-Joseph disease. Hum. Mol. Genet., 17, 2071-2083.
14. Kawaguchi, Y., Okamoto, T., Taniwaki, M., Aizawa, M., Inoue, M., Katayama, S., Kawakami, H., Nakamura, S., Nishimura, M., Akiguchi, I. et al. (1994) CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat. Genet., 8, 221-228.
15. Matilla, T., McCall, A., Subramony, S.H. and Zoghbi, H.Y. (1995) Molecular and clinical correlations in spinocerebellar ataxia type 3 and Machado-Joseph disease. Ann. Neurol., 38, 68-72.
16. Wang, G., Ide, K., Nukina, N., Goto, J., Ichikawa, Y., Uchida, K., Sakamoto, T. and Kanazawa, I. (1997) Machado-Joseph disease gene product identified in lymphocytes and brain. Biochem. Biophys. Res. Commun., 233, 476-479.
17. Chai, Y., Berke, S.S., Cohen, R.E. and Paulson, H.L. (2004) Poly-ubiquitin binding by the polyglutamine disease protein ataxin-3 links its normal function to protein surveillance pathways. J. Biol. Chem., 279, 3605-3611.
18. Doss-Pepe, E.W., Stenroos, E.S., Johnson, W.G. and Madura, K. (2003) Ataxin-3 interactions with rad23 and valosin-containing protein and its associations with ubiquitin chains and the proteasome are consistent with a role in ubiquitin-mediated proteolysis. Mol. Cell. Biol., 23, 6469-6483.
19. Scheel, H., Tomiuk, S. and Hofmann, K. (2003) Elucidation of ataxin-3 and ataxin-7 function by integrative bioinformatics. Hum. Mol. Genet., 12, 2845-2852.
20. Burnett, B., Li, F. and Pittman, R.N. (2003) The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. Hum. Mol. Genet., 12, 3195-3205.
21. Mao, Y., Senic-Matuglia, F., Di Fiore, P.P., Polo, S., Hodsdon, M.E. and De Camilli, P. (2005) Deubiquitinating function of ataxin-3: insights from the solution structure of the Josephin domain. Proc. Natl. Acad. Sci. USA, 102, 12700-12705.
22. Nicastro, G., Menon, R.P., Masino, L., Knowles, P.P., McDonald, N.Q. and Pastore, A. (2005) The solution structure of the Josephin domain of ataxin-3: structural determinants for molecular recognition. Proc. Natl. Acad. Sci. USA, 102, 10493-10498.
23. Mauri, P.L., Riva, M., Ambu, D., De Palma, A., Secundo, F., Benazzi, L., Valtorta, M., Tortora, P. and Fusi, P. (2006) Ataxin-3 is subject to autolytic cleavage. Febs. J., 273, 4277-4286.
24. Li, F., Macfarlan, T., Pittman, R.N. and Chakravarti, D. (2002) Ataxin-3 is a histone-binding protein with two independent transcriptional corepressor activities. J. Biol. Chem., 277, 45004-45012.
25. Wang, G., Sawai, N., Kotliarova, S., Kanazawa, I. and Nukina, N. (2000) Ataxin-3, the MJD1 gene product, interacts with the two human homologs of yeast DNA repair protein RAD23, HHR23A and HHR23B. Hum. Mol. Genet., 9, 1795-1803.
26. Cummings, C.J. and Zoghbi, H.Y. (2000) Fourteen and counting: unraveling trinucleotide repeat diseases. Hum. Mol. Genet., 9, 909-916.
27. Cummings, C.J. and Zoghbi, H.Y. (2000) Trinucleotide repeats: mechanisms and pathophysiology. Annu. Rev. Genomics Hum. Genet., 1, 281-328.
28. Maciel, P., Costa, M.C., Ferro, A., Rousseau, M., Santos, C.S., Gaspar, C., Barros, J., Rouleau, G.A., Coutinho, P. and Sequeiros, J. (2001) Improvement in the molecular diagnosis of Machado-Joseph disease. Arch. Neurol., 58, 1821-1827.
29. Schmidt, T., Landwehrmeyer, G.B., Schmitt, I., Trottier, Y., Auburger, G., Laccone, F., Klockgether, T., Volpel, M., Epplen, J.T., Schols, 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.
30. Trottier, Y., Cancel, G., An-Gourfinkel, I., Lutz, Y., Weber, C., Brice, A., Hirsch, E. and Mandel, J.L. (1998) Heterogeneous intracellular localization and expression of ataxin-3. Neurobiol. Dis., 5, 335-347.
31. Cancel, G., Abbas, N., Stevanin, G., Durr, A., Chneiweiss, H., Neri, C., Duyckaerts, C., Penet, C., Cann, H.M., Agid, Y. et al. (1995) Marked phenotypic heterogeneity associated with expansion of a CAG repeat sequence at the spinocerebellar ataxia 3/Machado-Joseph disease locus. Am. J. Hum. Genet., 57, 809-816.
32. Mello, C.C. and Conte, D. Jr (2004) Revealing the world of RNA interference. Nature, 431, 338-342.
33. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature, 411, 494-498.
34. Machida, Y., Okada, T., Kurosawa, M., Oyama, F., Ozawa, K. and Nukina, N. (2006) rAAV-mediated shRNA ameliorated neuropathology in Huntington disease model mouse. Biochem. Biophys. Res. Commun., 343, 190-197.
35. DiFiglia, M., Sena-Esteves, M., Chase, K., Sapp, E., Pfister, E., Sass, M., Yoder, J., Reeves, P., Pandey, R.K., Rajeev, K.G. et al. (2007) Therapeutic silencing of mutant huntingtin with siRNA attenuates striatal and cortical neuropathology and behavioral deficits. Proc. Natl. Acad. Sci. USA, 104, 17204-17209.
36. Harper, S.Q., Staber, P.D., He, X., Eliason, S.L., Martins, I.H., Mao, Q., Yang, L., Kotin, R.M., Paulson, H.L. and Davidson, B.L. (2005) RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc. Natl. Acad. Sci. USA, 102, 5820-5825.
37. Rodriguez-Lebron, E., Denovan-Wright, E.M., Nash, K., Lewin, A.S. and Mandel, R.J. (2005) Intrastriatal rAAV-mediated delivery of anti-huntingtin shRNAs induces partial reversal of disease progression in R6/1 Huntington's disease transgenic mice. Mol. Ther., 12, 618-633.
38. Franich, N.R., Fitzsimons, H.L., Fong, D.M., Klugmann, M., During, M.J. and Young, D. (2008) AAV vector-mediated RNAi of mutant huntingtin expression is neuroprotective in a novel genetic rat model of Huntington's disease. Mol. Ther., 16, 947-956.
39. Ralph, G.S., Radcliffe, P.A., Day, D.M., Carthy, J.M., Leroux, M.A., Lee, D.C., Wong, L.F., Bilsland, L.G., Greensmith, L., Kingsman, S.M. et al. (2005) Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat. Med., 11, 429-433.
40. Raoul, C., Abbas-Terki, T., Bensadoun, J.C., Guillot, S., Haase, G., Szulc, J., Henderson, C.E. and Aebischer, P. (2005) Lentiviral-mediated silencing of SOD1 through RNA interference retards disease onset and progression in a mouse model of ALS. Nat. Med., 11, 423-428.
41. 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.
42. Gaspar, C., Lopes-Cendes, I., DeStefano, A.L., Maciel, P., Silveira, I., Coutinho, P., MacLeod, P., Sequeiros, J., Farrer, L.A. and Rouleau, G.A. (1996) Linkage disequilibrium analysis in Machado-Joseph disease patients of different ethnic origins. Hum. Genet., 98, 620-624.
43. Miller, V.M., Xia, H., Marrs, G.L., Gouvion, C.M., Lee, G., Davidson, B.L. and Paulson, H.L. (2003) Allele-specific silencing of dominant disease genes. Proc. Natl. Acad. Sci. USA, 100, 7195-7200.
44. Alves, S., Nascimento-Ferreira, I., Auregan, G., Hassig, R., Dufour, N., Brouillet, E., Pedroso de Lima, M.C., Hantraye, P., Pereira de Almeida, L. and Deglon, N. (2008) Allele-specific RNA silencing of mutant ataxin-3 mediates neuroprotection in a rat model of Machado-Joseph disease. PLoS ONE, 3, e3341.
45. Gaspar, C., Lopes-Cendes, I., Hayes, S., Goto, J., Arvidsson, K., Dias, A., Silveira, I., Maciel, P., Coutinho, P., Lima, M. et al. (2001) Ancestral origins of the Machado-Joseph disease mutation: a worldwide haplotype study. Am. J. Hum. Genet., 68, 523-528.
46. Warrick, J.M., Morabito, L.M., Bilen, J., Gordesky-Gold, B., Faust, L.Z., Paulson, H.L. and Bonini, N.M. (2005) Ataxin-3 suppresses polyglutamine neurodegeneration in Drosophila by a ubiquitin-associated mechanism. Mol. Cell., 18, 37-48.
47. Schmitt, I., Linden, M., Khazneh, H., Evert, B.O., Breuer, P., Klockgether, T. and Wuellner, U. (2007) Inactivation of the mouse Atxn3 (ataxin-3) gene increases protein ubiquitination. Biochem. Biophys. Res. Commun., 362, 734-739.
48. Donaldson, K.M., Li, W., Ching, K.A., Batalov, S., Tsai, C.C. and Joazeiro, C.A. (2003) Ubiquitin-mediated sequestration of normal cellular proteins into polyglutamine aggregates. Proc. Natl. Acad. Sci. USA, 100, 8892-8897.
49. Boeddrich, A., Gaumer, S., Haacke, A., Tzvetkov, N., Albrecht, M., Evert, B.O., Muller, E.C., Lurz, R., Breuer, P., Schugardt, N. et al. (2006) An arginine/lysine-rich motif is crucial for VCP/p97-mediated modulation of ataxin-3 fibrillogenesis. Embo. J., 25, 1547-1558.
50. Thrower, J.S., Hoffman, L., Rechsteiner, M. and Pickart, C.M. (2000) Recognition of the polyubiquitin proteolytic signal. Embo. J., 19, 94-102.
51. Winborn, B.J., Travis, S.M., Todi, S.V., Scaglione, K.M., Xu, P., Williams, A.J., Cohen, R.E., Peng, J. and Paulson, H.L. (2008) The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J. Biol. Chem., 283, 26436-26443.
52. Uchihara, T., Fujigasaki, H., Koyano, S., Nakamura, A., Yagishita, S. and Iwabuchi, K. (2001) Non-expanded polyglutamine proteins in intranuclear inclusions of hereditary ataxias-triple-labeling immunofluorescence study. Acta. Neuropathol., 102, 149-152.
53. Takahashi, J., Tanaka, J., Arai, K., Funata, N., Hattori, T., Fukuda, T., Fujigasaki, H. and Uchihara, T. (2001) Recruitment of nonexpanded polyglutamine proteins to intranuclear aggregates in neuronal intranuclear hyaline inclusion disease. J. Neuropathol. Exp. Neurol., 60, 369-376.
54. Fujigasaki, H., Uchihara, T., Koyano, S., Iwabuchi, K., Yagishita, S., Makifuchi, T., Nakamura, A., Ishida, K., Toru, S., Hirai, S. et al. (2000) Ataxin-3 is translocated into the nucleus for the formation of intranuclear inclusions in normal and Machado-Joseph disease brains. Exp. Neurol., 165, 248-256.
55. Fujigasaki, H., Uchihara, T., Takahashi, J., Matsushita, H., Nakamura, A., Koyano, S., Iwabuchi, K., Hirai, S. and Mizusawa, H. (2001) Preferential recruitment of ataxin-3 independent of expanded polyglutamine: an immunohistochemical study on Marinesco bodies. J. Neurol. Neurosurg. Psychiatry, 71, 518-520.
56. Kettner, M., Willwohl, D., Hubbard, G.B., Rub, U., Dick, E.J. Jr, Cox, A.B., Trottier, Y., Auburger, G., Braak, H. and Schultz, C. (2002) Intranuclear aggregation of nonexpanded ataxin-3 in marinesco bodies of the nonhuman primate substantia nigra. Exp. Neurol., 176, 117-121.
57. Arrasate, M., Mitra, S., Schweitzer, E.S., Segal, M.R. and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature, 431, 805-810.
58. Perez, M.K., Paulson, H.L. and Pittman, R.N. (1999) Ataxin-3 with an altered conformation that exposes the polyglutamine domain is associated with the nuclear matrix. Hum. Mol. Genet., 8, 2377-2385.
59. 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.
60. Sun, J., Xu, H., Negi, S., Subramony, S.H. and Hebert, M.D. (2007) Differential effects of polyglutamine proteins on nuclear organization and artificial reporter splicing. J. Neurosci. Res., 85, 2306-2317.
61. Schmitt, I., Brattig, T., Gossen, M. and Riess, O. (1997) Characterization of the rat spinocerebellar ataxia type 3 gene. Neurogenetics, 1, 103-112.
62. Nijman, S.M., Luna-Vargas, M.P., Velds, A., Brummelkamp, T.R., Dirac, A.M., Sixma, T.K. and Bernards, R. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell, 123, 773-786.
63. Rodrigues, A.J., Coppola, G., Santos, C., Costa Mdo, C., Ailion, M., Sequeiros, J., Geschwind, D.H. and Maciel, P. (2007) Functional genomics and biochemical characterization of the C. elegans orthologue of the Machado-Joseph disease protein ataxin-3. Faseb. J., 21, 1126-1136.
64. van Bilsen, P.H., Jaspers, L., Lombardi, M.S., Odekerken, J.C., Burright, E.N. and Kaemmerer, W.F. (2008) Identification and allele-specific silencing of the mutant huntingtin allele in Huntington's disease patient-derived fibroblasts. Hum. Gene. Ther., 19, 710-719.
65. Jarraya, B., Boulet, S., Ralph, G., Jan, C., Bonvento, G., Azzouz, M., Miskin, J., Shin, M., Delzescaux, T., Drouot, X. et al. (2009) Dopamine gene therapy for Parkinson's disease in a nonhuman primate without associated dyskinesia. Sci. Transl. Med., 1, 1-11.
66. de Almeida, L.P., Zala, D., Aebischer, P. and Deglon, N. (2001) Neuroprotective effect of a CNTF-expressing lentiviral vector in the quinolinic acid rat model of Huntington's disease. Neurobiol. Dis., 8, 433-446.
67. Hottinger, A.F., Azzouz, M., Deglon, N., Aebischer, P. and Zurn, A.D. (2000) Complete and long-term rescue of lesioned adult motoneurons by lentiviral-mediated expression of glial cell line-derived neurotrophic factor in the facial nucleus. J. Neurosci., 20, 5587-5593.
68. de Almeida, L.P., Ross, C.A., Zala, D., Aebischer, P. and Deglon, N. (2002) Lentiviral-mediated delivery of mutant huntingtin in the striatum of rats induces a selective neuropathology modulated by polyglutamine repeat size, huntingtin expression levels, and protein length. J. Neurosci., 22, 3473-3483.
69. Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402-408.
70. Schmued, L.C., Albertson, C. and Slikker, W. Jr (1997) Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res., 751, 37-46.
71. Arango, M., Holbert, S., Zala, D., Brouillet, E., Pearson, J., Regulier, E., Thakur, A.K., Aebischer, P., Wetzel, R., Deglon, N. and Neri, C. (2006) CA150 expression delays striatal cell death in overexpression and knock-in conditions for mutant huntingtin neurotoxicity. J. Neurosci., 26, 4649-4659.
72. Palfi, S., Brouillet, E., Jarraya, B., Bloch, J., Jan, C., Shin, M., Conde, F., Li, X.J., Aebischer, P., Hantraye, P. and Deglon, N. (2007) Expression of mutated huntingtin fragment in the putamen is sufficient to produce abnormal movement in non-human primates. Mol. Ther., 15, 1444-1451.
73. Paxinos, G., Watson, C., Pennisi, M. and Topple, A. (1985) Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J. Neurosci. Methods, 13, 139-143.
74. Clarke, P.G. (1992) How inaccurate is the Abercrombie correction factor for cell counts? Trends Neurosci., 15, 211-212.