Caspase-mediated proteolysis of the polyglutamine disease protein ataxin-3

Journal of Neurochemistry

Volumn 89, Issue 4, 2004, Pages 908-918

  Shoesmith Berke, Sarah J ^a,b   Flores Schmied, Francisca A ^b   Brunt, Ewout R ^c   Ellerby, Lisa M ^d   Paulson, Henry L ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

Ataxin 3; Caspase; Machado Joseph disease; Polyglutamine disease; Proteolysis; Spinocerebellar ataxia type 3

Indexed keywords

ATAXIN 3; CASPASE; CASPASE INHIBITOR; GLUTAMINE; POLYGLUTAMINE; PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; ATXN3 PROTEIN, HUMAN; ATXN3 PROTEIN, RAT; ENZYME INHIBITOR; INTERLEUKIN 1BETA CONVERTING ENZYME; MJD PROTEIN, MOUSE; NERVE PROTEIN; NUCLEAR PROTEIN; PEPTIDE; PEPTIDE FRAGMENT; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL DEATH; CONTROLLED STUDY; DEGENERATIVE DISEASE; HUMAN; HUMAN CELL; MACHADO JOSEPH DISEASE; NUCLEOTIDE REPEAT; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; SITE DIRECTED MUTAGENESIS; SPINOCEREBELLAR DEGENERATION; ADULT; AMINO ACID SEQUENCE; ANIMAL; APOPTOSIS; BINDING SITE; BRAIN; BRAIN LEVEL; CELL CULTURE; DRUG EFFECT; FEMALE; GENETICS; MACROMOLECULE; MALE; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; RAT; TRINUCLEOTIDE REPEAT;

ATAXIA;

ADULT; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BINDING SITES; BRAIN; BRAIN CHEMISTRY; CASPASE 1; CASPASES; CELLS, CULTURED; ENZYME INHIBITORS; FEMALE; HUMANS; MACHADO-JOSEPH DISEASE; MACROMOLECULAR SUBSTANCES; MALE; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PEPTIDES; RATS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 2542445545     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02369.x     Document Type: Article

References (42)

1. Berke S. J. and Paulson H. L. (2003) Protein aggregation and the ubiquitin proteasome pathway: gaining the upper hand on neurodegeneration. Curr. Opin. Genet Dev 13, 253-261.
2. Brophy V. A., Tavare J. M. and Rivett A. J. (2002) Treatment of COS-7 cells with proteasome inhibitors or gamma-interferon reduces the increase in caspase 3 activity associated with staurosporine-induced apoptosis. Arch. Biochem. Biophys. 397, 199-205.
3. 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.
4. Caballero-Benitez A. and Moran J. (2003) Caspase activation pathways induced by staurosporine and low potassium: role of caspase-2. J. Neurosci. Res. 71, 383-396.
5. Chai Y., Berke S. S., Cohen R. E. and Paulson H. L. (2003) Poly-ubiquitin binding by the polyglutamine disease protein ataxin-3 links its normal function to protein surveillance pathways. J Biol Chem. 279, 3605-3611.
6. Chai Y., Koppenhafer S. L., Bonini N. M. and Paulson H. L. (1999a) Analysis of the role of heat shock protein (Hsp) molecular chaperones in polyglutamine disease. J. Neurosci. 19, 10338-10347.
7. Chai Y., Koppenhafer S. L., Shoesmith S. J., Pere Z. M. K. and Paulson H. L. (1999b) Evidence for proteasome involvement in polyglutamine disease: localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum Mol Genet 8, 673-682.
8. 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.
9. 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.
10. 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.
11. Earnshaw W. C., Martins L. M. and Kaufmann S. H. (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68, 383-424.
12. Ellerby L. M., Andrusiak R. L., Wellington C. L., Hackam A. S., Propp S. S., Wood J. D., Sharp A. H., Margolis R. L., Ross C. A., Salvesen G. S., Hayden M. R. and Bredesen D. E. (1999a) Cleavage of atrophin-1 at caspase site aspartic acid 109 modulates cytotoxicity. J. Biol. Chem. 274, 8730-8736.
13. Ellerby L. M., Hackam A. S., Propp S. S., Ellerby H. M., Rabizadeh S., Cashman N. R., Trifiro M. A., Pinsky L., Wellington C. L., Salvesen G. S., Hayden M. R. and Bredesen D. E. (1999b) Kennedy's disease: caspase cleavage of the androgen receptor is a crucial event in cytotoxicity. J. Neurochem. 72, 185-195.
14. Evert B. O., Wullner U., Schul Z. J. B., Weller M., Groscurth P., Trottier Y., Brice A. and Klockgether T. (1999) High level expression of expanded full-length ataxin-3 in vitro causes cell death and formation of intranuclear inclusions in neuronal cells. Hum Mol Genet 8, 1169-1176.
15. Gafni J. and Ellerby L. M. (2002) Calpain activation in Huntington's disease. J. Neurosci. 22, 4842-4849.
16. Garden G. A., Libby R. T., Fu Y. H., Kinoshita Y., Huang J., Possin D. E., Smith A. C., MartineZ. R. A., Fine G. C., Grote S. K., Ware C. B., Einum D. D., Morrison R. S., Ptacek L. J., Sopher B. L. and La Spada A. R. (2002) Polyglutamine-expanded ataxin-7 promotes non-cell-autonomous purkinje cell degeneration and displays proteolytic cleavage in ataxic transgenic mice. J. Neurosci. 22, 4897-4905.
17. Goffredo D., Rigamonti D., Tartari M., De Micheli A., Verderio C., Matteoli M., Zuccato C. and Cattaneo E. (2002) Calcium-dependent cleavage of endogenous wild-type huntingtin in primary cortical neurons. J. Biol. Chem. 277, 39594-39598.
18. Goti D. and Colomer V. (2003) A mutant ataxin-3 cleavage fragment was detected in brain of MJD patients, characterized in MJD transgenic mouse brain, and toxic to transfected cells. Society for Neuroscience, Abstract 308.1.
19. Ikeda H., Yamaguchi M., Sugai S., Aze Y., Nammiya S. and Kakizuka A. (1996) Expanded polyglutamine in the Machado-Joseph disease protein induces cell death in vitro and in vivo. Nat Genet 13, 196-202.
20. Kawaguchi Y., Okamoto T., Taniwaki M., Aizawa M., Inoue M., Katayama S., Kawakami H., Nakamura S., Nishimura M., Akiguchi I. and et al. (1994) CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 8, 221-228.
21. Kim M., Lee H. S., LaForet G., McIntyre C., Martin E. J., Chang P., Kim T. W., Williams M., Reddy P. H., Tagle D., Boyce F. M., Won L., Heller A., Aronin N. and DiFiglia M. (1999) Mutant huntingtin expression in clonal striatal cells: dissociation of inclusion formation and neuronal survival by caspase inhibition. J Neurosci. 19, 964-973.
22. Kim Y. J., Yi Y., Sapp E., Wang Y., Cuiffo B., Kegel K. B., Qin Z. H., Aronin N. and DiFiglia M. (2001) Caspase 3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain-dependent proteolysis. Proc. Natl Acad. Sci. USA 98, 12784-12789.
23. LaFevre-Bernt M. A. and Ellerby L. M. (2003) Kennedy's Disease: phosphorylation of the polyglutamine-expanded form of androgen receptor regulates its clevage by caspase-3 and enhances cell death. J. Biol. Chem. 278, 34918-34924.
24. Li S. H., Lam S., Cheng A. L. and Li X. J. (2000) Intranuclear huntingtin increases the expression of caspase-1 and induces apoptosis. Hum Mol Genet 9, 2859-2867.
25. Lunkes A., Lindenberg K. S., Ben-Haiem L., Weber C., Devys D., Landwehrmeyer G. B., Mandel J. L. and Trottier Y. (2002) Proteases acting on mutant huntingtin generate cleaved products that differentially build up cytoplasmic and nuclear inclusions. Mol Cell 10, 259-269.
26. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S. W. and Bates G. P. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87, 493-506.
27. Morley J. F., Brignull H. R., Weyers J. J. and Morimoto R. I. (2002) The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 99, 10417-10422.
28. Ona V. O., Li M., Vonsattel J. P., Andrews L. J., Khan S. Q., Chung W. M., Frey A. S., Menon A. S., Li X. J., Stieg P. E., Yuan J., Penney J. B., Young A. B., Cha J. H. and Friedlander R. M. (1999) Inhibition of caspase-1 slows disease progression in a mouse model of Huntington's disease. Nature 399, 263-267.
29. Paulson H. L. (2000) Toward an understanding of polyglutamine neurodegeneration. Brain Pathol 10, 293-299.
30. Paulson H. L., Das S. S., Crino P. B., Pere Z. M. K., Patel S. C., Gotsdiner D., Fischbeck K. H. and Pittman R. N. (1997a) Machado-Joseph disease gene product is a cytoplasmic protein widely expressed in brain. Ann. Neurol. 41, 453-462.
31. 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. and Pittman R. N. (1997b) Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3, Neuron 19, 333-344.
32. Sanchez I., Mahlke C. and Yuan J. (2003) Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature 421, 373-379.
33. Sanchez I., Xu C. J., Juo P., Kakizaka A., Blenis J. and Yuan J. (1999) Caspase-8 is required for cell death induced by expanded polyglutamine repeats. Neuron 22, 623-633.
34. Satyal S. H., Schmidt E., Kitagawa K., Sondheimer N., Lindquist S., Kramer J. M. and Morimoto R. I. (2000) Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 97, 5750-5755.
35. 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.
36. Trottier Y., Cancel G., An-Gourfinkel I., Lut Z. 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.
37. Troy C. M. and Salvesen G. S. (2002) Caspases on the brain. J. Neurosci. Res. 69, 145-150.
38. 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.
39. Wellington C. L., Ellerby L. M., Gutekunst C. A., Rogers D., Warby S., Graham R. K., Loubser O., van Raamsdonk J., Singaraja R., Yang Y. Z., Gafni J., Bredesen D., Hersch S. M., Leavitt B. R., Roy S., Nicholson D. W. and Hayden M. R. (2002) Caspase cleavage of mutant huntingtin precedes neurodegeneration in Huntington's disease. J. Neurosci. 22, 7862-7872.
40. Wellington C. L., Ellerby L. M., Hackam A. S., Margolis R. L., Trifiro M. A., Singaraja R., McCutcheon K., Salvesen G. S., Propp S. S., Bromm M., Rowland K. J., Zhang T., Rasper D., Roy S., Thornberry N., Pinsky L., Kakizuka A., Ross C. A., Nicholson D. W., Bredesen D. E. and Hayden M. R. (1998) Caspase cleavage of gene products associated with triplet expansion disorders generates truncated fragments containing the polyglutamine tract. J. Biol. Chem. 273, 9158-9167.
41. Wellington C. L., Singaraja R., Ellerby L., Savill J., Roy S., Leavitt B., Cattaneo E., Hackam A., Sharp A., Thomberry N., Nicholson D. W., Bredesen D. E. and Hayden M. R. (2000) Inhibiting caspase cleavage of huntingtin reduces toxicity and aggregate formation in neuronal and nonneuronal cells. J. Biol. Chem. 275, 19831-19838.
42. Zoghbi H. Y. and Orr H. T. (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23, 217-247.