SUMO-1 interacts with mutant ataxin-1 and colocalizes to its aggregates in purkinje cells of SCA1 transgenic mice

Archives Italiennes de Biologie

Volumn 148, Issue 4, 2010, Pages 351-363

  Kang, S ^a   Hong, S ^a  

^a Korea University   (South Korea)

Author keywords

Aggregates; Mutant ataxin 1; Polyglutamine; SCA1; SUMO 1

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; ATAXIN 1; ATAXIN-1; DIAGNOSTIC AGENT; INDOLE DERIVATIVE; NERVE PROTEIN; NUCLEAR PROTEIN; SUMO 1 PROTEIN; UBIQUITIN;

ANIMAL; ARTICLE; CELL LINE; CELL NUCLEUS; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; METHODOLOGY; MOUSE; MUTATION; PATHOLOGY; PHYSIOLOGY; PROTEIN BINDING; PURKINJE CELL; SPINOCEREBELLAR DEGENERATION; TRANSGENIC MOUSE; TWO HYBRID SYSTEM; ULTRASTRUCTURE;

ANIMALS; CELL LINE, TRANSFORMED; CELL NUCLEUS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; INDOLES; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PURKINJE CELLS; SPINOCEREBELLAR ATAXIAS; SUMO-1 PROTEIN; TRANSFECTION; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN;

MUS MUSCULUS;

EID: 79551524400     PISSN: 00039829     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

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, Botas J. CHIP protects from the neurotoxicity of expanded and wild-type ataxin-1 and promotes their ubiquitination and degradation. J. Biol. Chem., 281: 26714-26724, 2006.
2. Anckar J. and Sistonen L. SUMO: getting it on. Biochem. Soc. Trans., 35: 1409-1413, 2007.
3. Buschmann T., Lerner D., Lee C.G., Ronai Z. The Mdm-2 amino terminus is required for Mdm2 binding and SUMO-1 conjugation by the E2 SUMO-1 conjugating enzyme Ubc9. J. Biol. Chem., 276: 40389-40395, 2001.
4. Cheng J., Kang X., Zhang S., Yeh E.T. SUMOspecific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell, 131: 584-595, 2007.
5. Choi J.Y., Ryu J.H., Kim H.S., Park S.G., Bae K.H., Kang S., Myung P.K., Cho S., Park B.C., Lee do H. Co-chaperone CHIP promotes aggregation of ataxin-1. Mol. Cell Neurosci., 34: 69-79, 2007.
6. Cummings C.J., Mancini M.A., Antalffy B., DeFranco D.B., Orr H.T., Zoghbi H.Y. Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet., 19: 148-154, 1998.
7. Cummings C.J., Reinstein E., Sun Y., Antalffy B., Jiang Y., Ciechanover A., Orr H.T., Beaudet A.L., Zoghbi, H.Y. Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron, 24: 879-892, 1999.
8. Desterro J.M., Thomson J., Hay R.T. Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett., 417: 297-300, 1997.
9. Desterro J.M., Rodriguez M.S., Kemp G.D., Hay R.T. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem., 274: 10618-10624, 1999.
10. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P., Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science, 277: 1990-1993, 1997.
11. Dorval V. and Fraser P.E. SUMO on the road to neurodegeneration. Biochim. Biophys. Acta, 1773: 694-706, 2007.
12. Furukawa Y., Kaneko K., Matsumoto G., Kurosawa M., Nukina N. Cross-seeding fibrillation of Q/Nrich proteins offers new pathomechanism of polyglutamine diseases. J. Neurosci., 29: 5153-5162, 2009.
13. Giraud M.F., Desterro J.M., Naismith J.H. Structure of ubiquitin-conjugating enzyme 9 displays significant differences with other ubiquitin-conjugating enzymes which may reflect its specificity for sumo rather than ubiquitin. Acta Crystallogr. D. Biol. Crystallogr., 54: 891-898, 1998.
14. Gong L., Millas S., Maul G.G., Yeh E.T.. Differential regulation of sentrinized proteins by a novel sentrin- specific protease. J. Biol. Chem., 275: 3355-3359, 2000.
15. Gutekunst C.A., Li S.H., Yi H., Mulroy J.S., Kuemmerle S., Jones R., Rye D., Ferrante R.J., Hersch S.M., Li X.J. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci., 19: 2522-2534, 1999.
16. Hay R.T. Protein modification by SUMO. Trends Biochem. Sci., 26: 332-333, 2001.
17. Hay R.T. SUMO-specific proteases: a twist in the tail. Trends Cell Biol., 17: 370-376, 2007.
18. Hochstrasser M. SP-RING for SUMO: new functions bloom for a ubiquitin-like protein. Cell, 107: 5-8, 2001.
19. Hong S., Kim S.J., Ka S., Choi I., Kang, S. USP7, a ubiquitin-specific protease, interacts with ataxin-1, the SCA1 gene product. Mol. Cell. Neurosci., 20: 298-306, 2002.
20. Hong S., Lee S., Cho S.G., Kang S. UbcH6 interacts with and ubiquitinates the SCA1 gene product ataxin-1. Biochem. Biophys. Res. Commun., 371: 256-260, 2008.
21. Igarashi S., Koide R., Shimohata T., Yamada M., Hayashi Y., Takano H., Date H., Oyake M., Sato T., Sato A., Egawa S., Ikeuchi T., Tanaka H., Nakano R., Tanaka K., Hozumi I., Inuzuka T., Takahashi H., Tsuji S. Suppression of aggregate formation and apoptosis by transglutaminase inhibitors in cells expressing truncated DRPLA protein with an expanded polyglutamine stretch. Nat. Genet., 18: 111-117, 1998.
22. Ikeda H., Yamaguchi M., Sugai S., Aze Y., Narumiya S., Kakizuka A. Expanded polyglutamine in the Machado-Joseph disease protein induces cell death in vitro and in vivo. Nat. Genet., 13: 196-202, 1996. (Pubitemid 26000440)
23. Jentsch S. and Pyrowolakis G. Ubiquitin and its kin: how close are the family ties? Trends Cell Biol., 10: 335-342, 2000.
24. Johnson E.S. and Blobel G. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem., 272: 26799-26802, 1997.
25. Johnson E.S. and Gupta A.A. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell, 106: 735-744, 2001.
26. Kahyo T., Nishida T., Yasuda H. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell, 8: 713-718, 2001.
27. Katsuno M., Banno H., Suzuki K., Takeuchi Y., Kawashima M., Tanaka F., Adachi H., Sobue G. Molecular genetics and biomarkers of polyglutamine diseases. Curr. Mol. Med., 8: 221-234, 2008.
28. Kerscher O., Felberbaum R., Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin- like proteins. Annu. Rev. Cell Dev. Biol., 22: 159-180, 2006.
29. Kim K.I., Baek S.H., Jeon Y.J., Nishimori S., Suzuki T., Uchida S., Shimbara N., Saitoh H., Tanaka K., Chung C.H. A new SUMO-1-specific protease, SUSP1, that is highly expressed in reproductive organs. J. Biol. Chem., 275: 14102-14106, 2000.
30. Kim Y.H., Sung K.S., Lee S.J., Kim Y.O., Choi C.Y., Kim Y. Desumoylation of homeodomaininteracting protein kinase 2 (HIPK2) through the cytoplasmic-nuclear shuttling of the SUMOspecific protease SENP1. FEBS Lett., 579: 6272-6278, 2005.
31. Li X., Luo Y., Yu L., Lin Y., Luo D., Zhang H., He Y., Kim Y.O., Kim Y., Tang S., Min W. SENP1 mediates TNF-induced desumoylation and cytoplasmic translocation of HIPK1 to enhance ASK1- dependent apoptosis. Cell Death Differ., 15: 739-750, 2008.
32. Melchior F. SUMO-nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol., 16: 591-626, 2000.
33. Nekooki-Machida Y., Kurosawa M., Nukina N., Ito K., Oda T., Tanaka M. Distinct conformations of in vitro and in vivo amyloids of huntingtin-exon1 show different cytotoxicity. Proc. Natl. Acad. Sci. U.S.A., 106: 9679-9684, 2009.
34. Okazawa H., Rich T., Chang A., Lin X., Waragai M., Kajikawa M., Enokido Y., Komuro A., Kato S., Shibata M., Hatanaka H., Mouradian M.M., Sudol M., Kanazawa I. Interaction between Mutant Ataxin-1 and PQBP-1 Affects Transcription and Cell Death. Neuron, 34: 701-713, 2002.
35. 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., Zoghbi H.Y. Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nat. Genet., 4: 221-226, 1993.
36. Palvimo J.J. PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem. Soc. Trans., 35: 1405-1408, 2007.
37. Parfitt D.A., Michael G.J., Vermeulen E.G., Prodromou N.V., Webb T.R., Gallo J.M., Cheetham M.E., Nicoll W.S., Blatch G.L., Chapple J.P. The ataxia protein sacsin is a functional co-chaperone that protects against polyglutamine-expanded ataxin-1. Hum. Mol. Genet., 18: 1556-1565, 2009.
38. 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., Pittman R.N. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron, 19: 333-344, 1997.
39. Pichler A., Gast A., Seeler J.S., Dejean A., Melchior F. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell, 108: 109-120, 2002.
40. Pountney D.L., Huang Y., Burns R.J., Haan E., Thompson P.D., Blumbergs P.C., Gai W.P. SUMO-1 marks the nuclear inclusions in familial neuronal intranuclear inclusion disease. Exp. Neurol., 184: 436-446, 2003.
41. Ryu J., Cho S., Park B.C., Lee do H. Oxidative stress-enhanced SUMOylation and aggregation of ataxin-1: Implication of JNK pathway. Biochem. Biophys. Res. Commun., 393: 280-285, 2010.
42. Sachdev S., Bruhn L., Sieber H., Pichler A., Melchior F., Grosschedl R. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev., 15: 3088-3103, 2001.
43. Saitoh N., Uchimura Y., Tachibana T., Sugahara S., Saitoh H., Nakao M. In situ SUMOylation analysis reveals a modulatory role of RanBP2 in the nuclear rim and PML bodies. Exp. Cell Res., 312: 418-1430, 2006.
44. Shimohata T., Nakajima T., Yamada M., Uchida C., Onodera O., Naruse S., Kimura T., Koide R., Nozaki K., Sano Y., Ishiguro H., Sakoe K., Ooshima T., Sato A., Ikeuchi T., Oyake M., Sato T., Aoyagi Y., Hozumi I., Nagatsu T., Takiyama Y., Nishizawa M., Goto J., Kanazawa I., Davidson I., Tanese N., Takahashi H., Tsuji S. Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription. Nat. Genet., 26: 29-36, 2000.
45. Skinner P.J., Koshy B.T., Cummings C.J., Klement I.A., Helin K., Servadio A., Zoghbi H.Y., Orr H.T. Ataxin-1 with an expanded glutamine tract alters nuclear matrix-associated structures. Nature, 389: 971-974, 1997.
46. Steffan J.S., Agrawal N., Pallos J., Rockabrand E., Trotman L.C., Slepko N., Illes K., Lukacsovich T., Zhu Y.Z., Cattaneo E., Pandolfi P.P., Thompson L.M., Marsh J.L. SUMO modification of Huntingtin and Huntington's disease pathology. Science, 304: 100-104, 2004.
47. Terashima T., Kawai H., Fujitani M., Maeda K., Yasuda H. SUMO-1 co-localized with mutant atrophin-1 with expanded polyglutamines accel erates intranuclear aggregation and cell death. Neuroreport, 13: 2359-2364, 2002.
48. Tong H., Hateboer G., Perrakis A., Bernards R., Sixma T.K. Crystal structure of murine/human Ubc9 provides insight into the variability of the ubiquitin-conjugating system. J. Biol. Chem., 272: 21381-21387, 1997.
49. Ueda H., Goto J., Hashida H., Lin X., Oyanagi K., Kawano H., Zoghbi H.Y., Kanazawa I., Okazawa H. Enhanced SUMOylation in polyglutamine diseases. Biochem. Biophys. Res. Commun., 293: 307-313, 2002.
50. Vig P.J., Subramony S.H., Qin Z., McDaniel D.O., Fratkin J.D. Relationship between ataxin-1 nuclear inclusions and Purkinje cell specific proteins in SCA-1 transgenic mice. J. Neurol. Sci., 174: 100-110, 2000.
51. Weidtkamp-Peters S., Lenser T., Negorev D., Gerstner N., Hofmann T.G., Schwanitz G., Hoischen C., Maul G., Dittrich P., Hemmerich P. Dynamics of component exchange at PML nuclear bodies. J. Cell Sci., 121: 2731-2743, 2008.
52. Yamada M., Sato T., Shimohata T., Hayashi S., Igarashi S., Tsuji S., Takahashi H. Interaction between neuronal intranuclear inclusions and promyelocytic leukemia protein nuclear and coiled bodies in CAG repeat diseases. Am. J. Pathol., 159: 1785-1795, 2001.
53. Yamada M., Shimohata M., Sato T., Tsuji S., Takahashi H. Polyglutamine disease: recent advances in the neuropathology of dentatorubralpallidoluysian atrophy. Neuropathology, 26: 346-351, 2006.
54. Yang S., Kuo C., Bisi J.E., Kim M.K. PML-dependent apoptosis after DNA damage is regulated by the checkpoint kinase hCds1/Chk2. Nat. Cell Biol., 4: 865-870, 2002.
55. Yang S.H. and Sharrocks A.D. The SUMO E3 ligase activity of Pc2 is coordinated through a SUMO interaction motif. Mol. Cell Biol., 30: 2193-2205, 2010.
56. Yunus A.A. and Lima C.D. Purification of SUMO conjugating enzymes and kinetic analysis of substrate conjugation. Methods Mol. Biol., 497: 167-186, 2009.