Ataxin-3 and its E3 partners: Implications for Machado-Joseph disease

Frontiers in Neurology

Volumn 4 MAY, Issue , 2013, Pages

  Durcan, Thomas M ^a   Fon, Edward A ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Ataxin 3; CHIP; Machado Joseph disease; Parkin; Parkinson's disease; Polyglutamine expansion.

Indexed keywords

ATAXIN 3; PARKIN; UBIQUITIN PROTEIN LIGASE E3;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; ENZYME ACTIVITY; GENE MUTATION; HUMAN; MACHADO JOSEPH DISEASE; NEUROPROTECTION; PARKINSON DISEASE; PROTEIN FUNCTION; PROTEIN STABILITY; SYMPTOMATOLOGY; UBIQUITINATION;

EID: 84878801656     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2013.00046     Document Type: Article

References (40)

1. Bettencourt, C., Santos, C., Coutinho, P., Rizzu, P., Vasconcelos, J., Kay, T., et al. (2011). Parkinsonian phenotype in Machado-Joseph disease (MJD/SCA3): a two-case report. BMC Neurol. 11:131. doi:10.1186/1471-2377-11-131
2. 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.
3. Burnett, B. G., and Pittman, R. N. (2005). The polyglutamine neurodegenerative protein ataxin 3 regulates aggresome formation. Proc. Natl. Acad. Sci. U.S.A. 102, 4330-4335.
4. Chai, Y., Wu, L., Griffin, J. D., and Paulson, H. L. (2001). The role of protein composition in specifying nuclear inclusion formation in polyglutamine disease. J. Biol. Chem. 276, 44889-44897.
5. Daviet, L., and Colland, F. (2008). Targeting ubiquitin specific proteases for drug discovery. Biochimie 90, 270-283.
6. de Bie, P., Zaaroor-Regev, D., and Ciechanover, A. (2010). Regulation of the Polycomb protein RING1B ubiquitination by USP7. Biochem. Biophys. Res. Commun. 400, 389-395.
7. 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. U.S.A. 100, 8892-8897.
8. 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.
9. Durcan, T. M., and Fon, E. A. (2011). Mutant ataxin-3 promotes the autophagic degradation of parkin. Autophagy 7, 233-234.
10. Durcan, T. M., Kontogiannea, M., Bedard, N., Wing, S. S., and Fon, E. A. (2012). Ataxin-3 deubiquitination is coupled to parkin ubiquitination via E2 ubiquitin-conjugating enzyme. J. Biol. Chem. 287, 531-541.
11. Durcan, T. M., Kontogiannea, M., Thorarinsdottir, T., Fallon, L., Williams, A. J., Djarmati, A., et al. (2011). The Machado-Joseph disease-associated mutant form of ataxin-3 regulates parkin ubiquitination and stability. Hum. Mol. Genet. 20, 141-154.
12. Fujigasaki, H., Uchihara, T., Koyano, S., Iwabuchi, K., Yagishita, S., Makifuchi, T., 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.
13. Gwinn-Hardy, K., Singleton, A., O'Suilleabhain, P., Boss, M., Nicholl, D., Adam, A., et al. (2001). Spinocerebellar ataxia type 3 phenotypically resembling Parkinson disease in a black family. Arch. Neurol. 58, 296-299.
14. Jana, N. R., Dikshit, P., Goswami, A., Kotliarova, S., Murata, S., Tanaka, K., et al. (2005). Co-chaperone CHIP associates with expanded polyglutamine protein and promotes their degradation by proteasomes. J. Biol. Chem. 280, 11635-11640.
15. Kao, W. H., Beaudenon, S. L., Talis, A. L., Huibregtse, J. M., and Howley, P. M. (2000). Human papillomavirus type 16 E6 induces self-ubiquitination of the E6AP ubiquitin-protein ligase. J. Virol. 74, 6408-6417.
16. Kawaguchi, Y., Okamoto, T., Taniwaki, M., Aizawa, M., Inoue, M., Katayama, S., et al. (1994). CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat. Genet. 8, 221-228.
17. Kazachkova, N., Raposo, M., Montiel, R., Cymbron, T., Bettencourt, C., Silva-Fernandes, A., et al. (2012). Patterns of mitochondrial DNA damage in blood and brain tissues of a transgenic mouse model of Machado-Joseph disease. Neurodegener. Dis. 11, 206-214.
18. Koch, P., Breuer, P., Peitz, M., Jungverdorben, J., Kesavan, J., Poppe, D., et al. (2011). Excitation-induced ataxin-3 aggregation in neurons from patients with Machado-Joseph disease. Nature 480, 543-546.
19. Laco, M. N., Oliveira, C. R., Paulson, H. L., and Rego, A. C. (2012). Compromised mitochondrial complex II in models of Machado-Joseph disease. Biochim. Biophys. Acta 1822, 139-149.
20. Lazarou, M., Narendra, D. P., Jin, S. M., Tekle, E., Banerjee, S., and Youle, R. J. (2013). PINK1 drives Parkin self-association and HECT-like E3 activity upstream of mitochondrial binding. J. Cell Biol. 200, 163-172.
21. Liu, Y., Fallon, L., Lashuel, H. A., Liu, Z., and Lansbury, P. T. Jr. (2002). The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 111, 209-218.
22. Narendra, D., Tanaka, A., Suen, D. F., and Youle, R. J. (2008). Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803.
23. Nathan, J. A., Sengupta, S., Wood, S. A., Admon, A., Markson, G., Sanderson, C., et al. (2008). The ubiquitin E3 ligase MARCH7 is differentially regulated by the deubiquitylating enzymes USP7 and USP9X. Traffic 9, 1130-1145.
24. Nicastro, G., Menon, R. P., Masino, L., Knowles, P. P., McDonald, N. Q., Pastore, A., et al. (2005). The solution structure of the Josephin domain of ataxin-3: structural determinants for molecular recognition. Proc. Natl. Acad. Sci. U.S.A. 102, 10493-10498.
25. Ouyang, H., Ali, Y. O., Ravichandran, M., Dong, A., Qiu, W., MacKenzie, F., et al. (2012). Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J. Biol. Chem. 287, 2317-2327.
26. Paulson, H. L., Perez, M. K., Trottier, Y., Trojanowski, J. Q., Subramony, S. H., Das, S. S., et al. (1997). Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 19, 333-344.
27. Pozzi, C., Valtorta, M., Tedeschi, G., Galbusera, E., Pastori, V., Bigi, A., et al. (2008). Study of subcellular localization and proteolysis of ataxin-3. Neurobiol. Dis. 30, 190-200.
28. Ranganathan, S., Harmison, G. G., Meyertholen, K., Pennuto, M., Burnett, B. G., and Fischbeck, K. H. (2009). Mitochondrial abnormalities in spinal and bulbar muscular atrophy. Hum. Mol. Genet. 18, 27-42.
29. Reddy, P. H., and Shirendeb, U. P. (2012). Mutant huntingtin, abnormal mitochondrial dynamics, defective axonal transport of mitochondria, and selective synaptic degeneration in Huntington's disease. Biochim. Biophys. Acta 1822, 101-110.
30. Scaglione, K. M., Zavodszky, E., Todi, S. V., Patury, S., Xu, P., Rodríguez-Lebrón, E., et al. (2011). Ube2w and ataxin-3 coordinately regulate the ubiquitin ligase CHIP. Mol. Cell 43, 599-612.
31. 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.
32. Shimura, H., Hattori, N., Kubo, S., Mizuno, Y., Asakawa, S., Minoshima, S., et al. (2000). Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet. 25, 302-305.
33. Sugiura, A., Yonashiro, R., Fukuda, T., Matsushita, N., Nagashima, S., Inatome, R., et al. (2011). A mitochondrial ubiquitin ligase MITOL controls cell toxicity of polyglutamine-expanded protein. Mitochondrion 11, 139-146.
34. Todi, S. V., Scaglione, K. M., Blount, J. R., Basrur, V., Conlon, K. P., Pastore, A., et al. (2010). Activity and cellular functions of the deubiquitinating enzyme and polyglutamine disease protein ataxin-3 are regulated by ubiquitination at lysine 117. J. Biol. Chem. 285, 39303-39313.
35. Tsai, Y. C., Fishman, P. S., Thakor, N. V., and Oyler, G. A. (2003). Parkin facilitates the elimination of expanded polyglutamine proteins and leads to preservation of proteasome function. J. Biol. Chem. 278, 22044-22055.
36. Wang, H., Ying, Z., and Wang, G. (2012). Ataxin-3 regulates aggresome formation of copper-zinc superoxide dismutase (SOD1) by editing K63-linked polyubiquitin chains. J. Biol. Chem. 287, 28576-28585.
37. Wenzel, D. M., Lissounov, A., Brzovic, P. S., and Klevit, R. E. (2011). UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 474, 105-108.
38. Wertz, I. E., O'Rourke, K. M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., et al. (2004). De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430, 694-699.
39. Winborn, B. J., Travis, S. M., Todi, S. V., Scaglione, K. M., Xu, P., Williams, A. J., et al. (2008). The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J. Biol. Chem. 283, 26436-26443.
40. Yu, Y. C., Kuo, C. L., Cheng, W. L., Liu, C. S., and Hsieh, M. (2009). Decreased antioxidant enzyme activity and increased mitochondrial DNA damage in cellular models of Machado-Joseph disease. J. Neurosci. Res. 87, 1884-1891.