Deactivation of TBP contributes to SCA17 pathogenesis

Human Molecular Genetics

Volumn 23, Issue 25, 2014, Pages 6878-6893

  Hsu, Tun Chieh ^a   Wang, Cheng Kuang ^b   Yang, Chun Yen ^a   Lee, Li Ching ^a   Hsieh Li, Hsiu Mei ^a   Ro, Long Sun ^c   Chen, Chiung Mei ^c   Lee Chen, Guey Jen ^a   Su, Ming Tsan ^a  

^a NATIONAL TAIWAN NORMAL UNIVERSITY   (Taiwan)

^b JEN TEH JUNIOR COLLEGE OF MEDICINE   (Taiwan)

^c CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE; POLYGLUTAMINE; PROTEIN AGGREGATE; PROTEIN BINDING; TATA BINDING PROTEIN;

ANIMAL; CHEMISTRY; DISEASE MODEL; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; HETEROZYGOTE; HUMAN; HUNTINGTON CHOREA; LONGEVITY; MACHADO JOSEPH DISEASE; METABOLISM; PATHOLOGY; PHENOTYPE; RETINA DEGENERATION; SIGNAL TRANSDUCTION; SPINOCEREBELLAR DEGENERATION;

ANIMALS; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; HETEROZYGOTE; HUMANS; HUNTINGTON DISEASE; LONGEVITY; MACHADO-JOSEPH DISEASE; PEPTIDES; PHENOTYPE; PROTEIN AGGREGATES; PROTEIN BINDING; RETINAL DEGENERATION; SIGNAL TRANSDUCTION; SPINOCEREBELLAR ATAXIAS; TATA-BOX BINDING PROTEIN;

EID: 84938703664     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu410     Document Type: Article

References (44)

1. Duenas, A.M., Goold, R. and Giunti, P. (2006) Molecular pathogenesis of spinocerebellar ataxias. Brain, 129, 1357–1370.
2. Shao, J. and Diamond, M.I. (2007) Polyglutamine diseases: emerging concepts in pathogenesis and therapy. Hum. Mol. Genet., 16 (Spec. 2), R115–R123.
3. Takahashi, Y., Okamoto, Y., Popiel, H.A., Fujikake, N., Toda, T., Kinjo, M. and Nagai, Y. (2007) Detection of polyglutamine protein oligomers in cells by fluorescence correlation spectroscopy. J. Biol. Chem., 282, 24039 – 24048.
4. Jiang, H., Nucifora, F.C. Jr, Ross, C.A. and DeFranco, D.B. (2003) Cell death triggered by polyglutamine-expanded huntingtin in a neuronal cell line is associated with degradation of CREB-binding protein. Hum. Mol. Genet., 12, 1 – 12.
5. Perez, M.K., Paulson, H.L., Pendse, S.J., Saionz, S.J., Bonini, N.M. and Pittman, R.N. (1998) Recruitment and the role of nuclear localization in polyglutamine-mediated aggregation. J. Cell. Biol., 143, 1457–1470.
6. Kazantsev, A., Preisinger, E., Dranovsky, A., Goldgaber, D. and Housman, D. (1999) Insoluble detergent-resistant aggregates form between pathological and nonpathological lengths of polyglutamine in mammalian cells. Proc. Natl. Acad. Sci. USA, 96, 11404–11409.
7. Jiang, H., Poirier, M.A., Liang, Y., Pei, Z., Weiskittel, C.E., Smith, W.W., Defranco, D.B. and Ross, C.A. (2006) Depletion of CBP is directly linked with cellular toxicity caused by mutant huntingtin. Neurobiol. Dis., 23, 543–551.
8. Dunah, A.W., Jeong, H., Griffin, A., Kim, Y.M., Standaert, D.G., Hersch, S.M., Mouradian, M.M., Young, A.B., Tanese, N. and Krainc, D. (2002) Sp1 and TAFII130 transcriptional activity disrupted in early Huntington’s disease. Science, 296, 2238 – 2243.
9. van Roon-Mom, W.M., Reid, S.J., Faull, R.L. and Snell, R.G. (2005) TATA-binding protein in neurodegenerative disease. Neuroscience, 133, 863–872.
10. Martianov, I., Viville, S. and Davidson, I. (2002) RNA polymerase II transcription in murine cells lacking the TATA binding protein. Science, 298, 1036–1039.
11. Huang, C.C., Faber, P.W., Persichetti, F., Mittal, V., Vonsattel, J.P., MacDonald, M.E. and Gusella, J.F. (1998) Amyloid formation by mutant huntingtin: threshold, progressivity and recruitment of normal polyglutamine proteins. Somat. Cell Mol. Genet., 24, 217–233.
12. van Roon-Mom, W.M., Reid, S.J., Jones, A.L., MacDonald, M.E., Faull, R.L. and Snell, R.G. (2002) Insoluble TATA-binding protein accumulation in Huntington’s disease cortex. Brain Res. Mol. Brain Res., 109, 1–10.
13. Yamada, M., Tsuji, S. and Takahashi, H. (2000) Pathology of CAG repeat diseases. Neuropathology, 20, 319–325.
14. Nakamura, K., Jeong, S.Y., Uchihara, T., Anno, M., Nagashima, K., Nagashima, T., Ikeda, S., Tsuji, S. and Kanazawa, I. (2001) SCA17, a novel autosomal dominant cerebellar ataxia caused by an expanded polyglutamine in TATA-binding protein. Hum. Mol. Genet., 10, 1441 – 1448.
15. Fujigasaki, H., Martin, J.J., De Deyn, P.P., Camuzat, A., Deffond, D., Stevanin, G., Dermaut, B., Van Broeckhoven, C., Durr, A. and Brice, A. (2001) CAG repeat expansion in the TATA box-binding protein gene causes autosomal dominant cerebellar ataxia. Brain, 124, 1939 – 1947.
16. Zuhlke, C. and Burk, K. (2007) Spinocerebellar ataxia type 17 is caused by mutations in the TATA-box binding protein. Cerebellum, 6, 300–307.
17. Gerber, H.P., Seipel, K., Georgiev, O., Hofferer, M., Hug, M., Rusconi, S. and Schaffner, W. (1994) Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science, 263, 808–811.
18. Reid, S.J., Rees, M.I., van Roon-Mom, W.M., Jones, A.L., MacDonald, M.E., Sutherland, G., During, M.J., Faull, R.L., Owen, M.J., Dragunow, M. et al. (2003) Molecular investigation of TBP allele length: a SCA17 cellular model and population study. Neurobiol. Dis., 13, 37 – 45.
19. Friedman, M.J., Wang, C.E., Li, X.J. and Li, S. (2008) Polyglutamine expansion reduces the association of TBP with DNA and induces DNA binding-independent neurotoxicity. J. Biol. Chem., 283, 8283–8290.
20. Lee, L.C., Chen, C.M., Wang, H.C., Hsieh, H.H., Chiu, I.S., Su, M.T., Hsieh-Li, H.M., Wu, C.H., Lee, G.C., Lee-Chen, G.J. et al. (2012) Role of the CCAAT-binding protein NFY in SCA17 pathogenesis. PLoS ONE, 7, e35302.
21. Ren, J., Jegga, A.G., Zhang, M., Deng, J., Liu, J., Gordon, C.B., Aronow, B.J., Lu, L.J., Zhang, B. and Ma, J. (2011) A Drosophila model of the neurodegenerative disease SCA17 reveals a role of RBP-J/Su(H) in modulating the pathological outcome. Hum. Mol. Genet., 20, 3424–3436.
22. Chen, C.M., Lee, L.C., Soong, B.W., Fung, H.C., Hsu, W.C., Lin, P.Y., Huang, H.J., Chen, F.L., Lin, C.Y., Lee-Chen, G.J. et al. (2010) SCA17 repeat expansion: mildly expanded CAG/CAA repeat alleles in neurological disorders and the functional implications. Clin. Chim. Acta, 411, 375–380.
23. Lee, L.C., Chen, C.M., Chen, F.L., Lin, P.Y., Hsiao, Y.C., Wang, P.R., Su, M.T., Hsieh-Li, H.M., Hwang, J.C., Wu, C.H. et al. (2009) Altered expression of HSPA5, HSPA8 and PARK7 in spinocerebellar ataxia type 17 identified by 2-dimensional fluorescence difference in gel electrophoresis. Clin. Chim. Acta, 400, 56 – 62.
24. Friedman, M.J., Shah, A.G., Fang, Z.H., Ward, E.G., Warren, S.T., Li, S. and Li, X.J. (2007) Polyglutamine domain modulates the TBP-TFIIB interaction: implications for its normal function and neurodegeneration. Nat. Neurosci., 10, 1519 – 1528.
25. Huang, S., Ling, J.J., Yang, S., Li, X.J. and Li, S. (2011) Neuronal expression of TATA box-binding protein containing expanded polyglutamine in knock-in mice reduces chaperone protein response by impairing the function of nuclear factor-Y transcription factor. Brain, 134, 1943 – 1958.
26. Yang, S., Huang, S., Gaertig, M.A., Li, X.J. and Li, S. (2014) Age-dependent decrease in chaperone activity impairs MANF expression, leading to Purkinje cell degeneration in inducible SCA17 mice. Neuron, 81, 349 – 365.
27. 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.
28. Iwasaki, T., Miyazaki, W., Rokutanda, N. and Koibuchi, N. (2008) Liquid chemiluminescent DNA pull-down assay to measure nuclear receptor-DNA binding in solution. Biotechniques, 45, 445 – 448.
29. Invernizzi, G., Aprile, F.A., Natalello, A., Ghisleni, A., Penco, A., Relini, A., Doglia, S.M., Tortora, P. and Regonesi, M.E. (2012) The relationship between aggregation and toxicity of polyglutamine-containing ataxin-3 in the intracellular environment of Escherichia coli. PLoS ONE, 7, e51890.
30. Verheyen, E.M., Purcell, K.J., Fortini, M.E. and Artavanis-Tsakonas, S. (1996) Analysis of dominant enhancers and suppressors of activated Notch in Drosophila. Genetics, 144, 1127–1141.
31. Schaffar, G., Breuer, P., Boteva, R., Behrends, C., Tzvetkov, N., Strippel, N., Sakahira, H., Siegers, K., Hayer-Hartl, M. and Hartl, F.U. (2004) Cellular toxicity of polyglutamine expansion proteins: mechanism of transcription factor deactivation. Mol. Cell, 15, 95 – 105.
32. Jackson-Fisher, A.J., Chitikila, C., Mitra, M. and Pugh, B.F. (1999) A role for TBP dimerization in preventing unregulated gene expression. Mol. Cell, 3, 717 – 727.
33. Slepko, N., Bhattacharyya, A.M., Jackson, G.R., Steffan, J.S., Marsh, J.L., Thompson, L.M. and Wetzel, R. (2006) Normal-repeat-length polyglutamine peptides accelerate aggregation nucleation and cytotoxicity of expanded polyglutamine proteins. Proc. Natl. Acad. Sci. USA, 103, 14367–14372.
34. Schols, L., Bauer, P., Schmidt, T., Schulte, T. and Riess, O. (2004) Autosomal dominant cerebellar ataxias: clinical features, genetics, and pathogenesis. Lancet Neurol., 3, 291–304.
35. Chen, C.M., Lane, H.Y., Wu, Y.R., Ro, L.S., Chen, F.L., Hung, W.L., Hou, Y.T., Lin, C.Y., Huang, S.Y., Chen, I.C. et al. (2005) Expanded trinucleotide repeats in the TBP/SCA17 gene mapped to chromosome 6q27 are associated with schizophrenia. Schizophr. Res., 78, 131 – 136.
36. Wild, E.J., Mudanohwo, E.E., Sweeney, M.G., Schneider, S.A., Beck, J., Bhatia, K.P., Rossor, M.N., Davis, M.B. and Tabrizi, S.J. (2008) Huntington’s disease phenocopies are clinically and genetically heterogeneous. Mov. Disord., 23, 716–720.
37. Stevanin, G., Fujigasaki, H., Lebre, A.S., Camuzat, A., Jeannequin, C., Dode, C., Takahashi, J., San, C., Bellance, R., Brice, A. et al. (2003) Huntington’s disease-like phenotype due to trinucleotide repeat expansions in the TBP and JPH3 genes. Brain, 126, 1599 – 1603.
38. Stevanin, G. and Brice, A. (2008) Spinocerebellar ataxia 17 (SCA17) and Huntington’s disease-like 4 (HDL4). Cerebellum, 7, 170–178.
39. Studier, F.W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 41, 207–234.
40. Grove, A., Galeone, A., Yu, E., Mayol, L. and Geiduschek, E.P. (1998) Affinity, stability and polarity of binding of the TATA binding protein governed by flexure at the TATA Box. J. Mol. Biol., 282, 731–739.
41. Chang, C. and Gralla, J.D. (1993) Properties of initiator-associated transcription mediated by GAL4-VP16. Mol. Cell. Biol., 13, 7469–7475.
42. Wang, Y.C., Lee, C.M., Lee, L.C., Tung, L.C., Hsieh-Li, H.M., Lee-Chen, G.J. and Su, M.T. (2011) Mitochondrial dysfunction and oxidative stress contribute to the pathogenesis of spinocerebellar ataxia type 12 (SCA12). J. Biol. Chem., 286, 21742–21754.
43. Chang, Y.C., Hung, W.T., Chang, H.C., Wu, C.L., Chiang, A.S., Jackson, G.R. and Sang, T.K. (2011) Pathogenic VCP/TER94 alleles are dominant actives and contribute to neurodegeneration by altering cellular ATP level in a Drosophila IBMPFD model. PLoS Genet., 7, e1001288.
44. Todd, A.M. and Staveley, B.E. (2004) Novel assay and analysis for measuring climbing ability in Drosophila. Drosophila Infor. Serv., 87, 101–107.