SUMO-1 Modification on K166 of PolyQ-Expanded aTaxin-3 Strengthens Its Stability and Increases Its Cytotoxicity

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Zhou, Ya Fang ^a   Liao, Shu Sheng ^a   Luo, Ying Ying ^a   Tang, Jian Guang ^b   Wang, Jun Ling ^a   Lei, Li Fang ^a   Chi, Jing Wei ^c   Du, Juan ^a   Jiang, Hong ^a,c   Xia, Kun ^c   Tang, Bei Sha ^a,c   Shen, Lu ^a,c  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 3; LYSINE; LYSINE 166; POLYGLUTAMINE; SUMO 1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STABILITY; SUMOYLATION; UBIQUITINATION;

APOPTOSIS; BINDING SITES; HEK293 CELLS; HUMANS; LYSINE; MACHADO-JOSEPH DISEASE; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPRESSOR PROTEINS; SUMO-1 PROTEIN; SUMOYLATION; UBIQUITINATION;

EID: 84873176209     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054214     Document Type: Article

References (42)

1. Tang BS, Liu C, Shen L, Dai H, Pan Q, et al. (2000) Frequency of SCA1, SCA2, SCA3/MJD, SCA6, SCA7, and DRPLA CAG trinucleotide repeat expansion in patients with hereditary spinocerebellar ataxia from Chinese kindreds. Arch Neurol 57: 540-544.
2. Orr HT, Zoghbi HY, (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30: 575-621.
3. Cummings CJ, Zoghbi HY, (2000) Fourteen and counting: unraveling trinucleotide repeat diseases. Hum Mol Genet 9: 909-916.
4. Hughes RE, (2002) Polyglutamine disease: Acetyltransferasesawry. Curr Biol 12: R141-R143.
5. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, et al. (1994) CAG expansion in novel gene from Machado-Joseph disease at chromosome 14q32.1. Nature Genet 8: 221-227.
6. Burnett BG, Pittman RN, (2005) The polyglutamine neurodegenerative protein ataxin 3 regulates aggresome formation. Proc Natl Acad Sci 102: 4330-4335.
7. Cancel G, Abbas N, Stevanin G, Dürr A, Chneiweiss H, 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.
8. Cecchin CR, Pires AP, Rieder CR, Monte TL, Silveira I, et al. (2007) Depressive symptoms in Machado-Joseph disease (SCA3) patients and their relatives. Community Genet 10: 19-26.
9. Cemal CK, Carroll CJ, Lawrence L, Lowrie MB, Ruddle P, et al. (2002) YAC transgenic mice carrying pathological alleles of the MJD1 locus exhibit a mild and slowly progressive cerebellar deficit. Hum Mol Genet 11: 1075-1094.
10. Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S, (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431: 805-810.
11. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, et al. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990-1993.
12. Pennuto M, Palazzolo I, Poletti A, (2009) Post-translational modifications of expanded polyglutamine proteins: impact on neurotoxicity. Hum Mol Genet 18: R40-47.
13. Matunis MJ, Coutavas E, Blobel G, (1996) A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J Cell Biol 135: 1457-1470.
14. Müller S, Ledl A, Schmidt D, (2004) SUMO: a regulator of gene expression and genome integrity. Oncogene 23: 1998-2008.
15. Hay RT, (2005) SUMO: a history of modification. Mol Cell 18: 1-12.
16. Bohren KM, Nadkarni V, Song JH, Gabbay KH, Owerbach D, (2004) A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem 279: 27233-27238.
17. Saitoh H, Hinchey J, (2000) Functional heterogeneity of small ubiquitinrelated protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275: 6252-6258.
18. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F, (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88: 97-107.
19. Desterro JM, Rodriguez MS, Hay RT, (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 2: 233-239.
20. Desterro JM, Keegan LP, Jaffray E, Hay RT, O'Connell MA, (2005) SUMO-1 modification alters ADAR1 editing activity. Mol Biol Cell 16: 5115-5126.
21. Müller S, Hoege C, Pyrowolakis G, Jentsch S, (2001) SUMO, ubiquitin's mysterious cousin. Nat Rev Mol Cell Biol 2: 202-210.
22. Johnson ES, Gupta AA, (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106: 735-744.
23. Geiss-Friedlander R, Melchior F, (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8: 947-956.
24. Kerscher O, (2007) SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep 8: 550-555.
25. Poukka H, Karvonen U, Janne OA, Palvimo JJ, (2000) Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc Natl Acad Sci 97: 14145-14150.
26. Steffan JS, Agrawal N, Pallos J, Rockabrand E, Trotman LC, et al. (2004) SUMO modification of Huntingtin and Huntington's disease pathology. Science 304: 100-104.
27. Riley BE, Zoghbi HY, Orr HT, (2005) SUMOylation of the polyglutamine repeat protein, ataxin-1, is dependent on a functional nuclear localization signal. J Biol Chem 280: 21942-21948.
28. Janer A, Werner A, Takahashi-Fujigasaki J, Daret A, Fujigasaki H, et al. (2010) SUMOylation attenuates the aggregation propensity and cellular toxicity of the polyglutamine expanded ataxin-7. Hum Mol Genet 19: 181-195.
29. Bayer P, Arndt A, Metzger S, Mahajan R, Melchior F, et al. (1998) Structure determination of the small ubiquitinrelated modifier SUMO-1. J Mol Biol 280: 275-286.
30. Huang TT, Wuerzberger-Davis SM, Wu ZH, Miyamoto S, (2003) Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell 115: 565-576.
31. Shen L, Tang JG, Tang BS, Jiang H, Zhao GH, et al. (2005) Research on screening and identification of proteins interacting with ataxin-3. Chinese Journal of Medical Genetics 22: 242-247.
32. Tang JG, Shen L, Tang BS, Zhang YH, Jiang H, et al. (2006) Covalent Modification of ataxin-3 by SUMO-1. Progress in Biochemistry and Biophysics 33: 1037-l043.
33. Lin X, Liang M, Liang YY, Brunicardi FC, Feng XH, (2003) SUMO-1/Ubc9 promotes nuclear accumulation and metabolic stability of tumor suppressor Smad4. J Biol Chem 278: 31043-31048.
34. Buschmann T, Fuchs SY, Lee CG, Pan ZQ, Ronai Z, (2000) SUMO-1 modification of Mdm2 prevents its self-ubiquitination and increases Mdm2 ability to ubiquitinate p53. Cell 101: 753-762.
35. Shinbo Y, Niki T, Taira T, Ooe H, Takahashi-Niki K, et al. (2006) Proper SUMO-1 conjugation is essential to DJ-1 to exert its full activities. Cell Death Differ 13: 96-108.
36. Dorval V, Fraser PE, (2006) Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alpha-synuclein. J Biol Chem 281: 9919-9924.
37. Joseph J, Tan SH, Karpova TS, McNally JG, Dasso M, (2002) SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J Cell Biol 156: 595-602.
38. Dorval V, Fraser PE, (2007) SUMO on the road to neurodegeneration. Biochim Biophys Acta 1773: 694-706.
39. Michalik A, Van Broeckhoven C, (2003) Pathogenesis of polyglutamine disorders: aggregation revisited. Hum Mol Genet 2: R173-186.
40. Breuer P, Haacke A, Evert BO, Wüllner U, (2010) Nuclear aggregation of polyglutamine-expanded ataxin-3: fragments escape the cytoplasmic quality control. J Biol Chem 285 (9) (): 6532-6537.
41. Mukherjee S, Thomas M, Dadgar N, Lieberman AP, Iniguez-Lluhl JA, (2009) SUMO Modification of the Androgen Receptor Attenuates Polyglutamine-mediated Aggregation. J Biol Chem 284: 21296-21306.
42. Subramaniam S, Sixt KM, Barrow R, Snyder SH, (2009) Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity. Science 324: 1327-1330.