Mechanisms of Ataxin-3 Misfolding and Fibril Formation: Kinetic Analysis of a Disease-associated Polyglutamine Protein

Journal of Molecular Biology

Volumn 368, Issue 2, 2007, Pages 595-605

  Ellisdon, Andrew M ^a   Pearce, Mary C ^a   Bottomley, Stephen P ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

amyloid fibril; ataxin 3; polyglutamine; protein aggregation; protein misfolding

Indexed keywords

AMYLOID; ATAXIN 3; MONOMER; POLYGLUTAMINE;

ARTICLE; DISEASE ASSOCIATION; FIBER; KINETICS; MACHADO JOSEPH DISEASE; POLYMERIZATION; PRIORITY JOURNAL; THERMODYNAMICS;

EID: 33947586837     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.02.058     Document Type: Article

References (47)

1. Paulson H.L., Das S.S., Crino P.B., Perez M.K., Patel S.C., Gotsdiner D., et al. Machado-Joseph disease gene product is a cytoplasmic protein widely expressed in brain. Ann. Neurol. 41 (1997) 453-462
2. Masino L., Musi V., Menon R.P., Fusi P., Kelly G., Frenkiel T.A., et al. Domain architecture of the polyglutamine protein ataxin-3: a globular domain followed by a flexible tail. FEBS Letters 549 (2003) 21-25
3. Scheel H., Tomiuk S., and Hofmann K. Elucidation of ataxin-3 and ataxin-7 function by integrative bioinformatics. Hum. Mol. Genet. 12 (2003) 2845-2852
4. Padiath Q.S., Srivastava A.K., Roy S., Jain S., and Brahmachari S.K. Identification of a novel 45 repeat unstable allele associated with a disease phenotype at the MJD1/SCA3 locus. Am. J. Med. Genet. B 133 (2005) 124-126
5. Kawaguchi Y., Okamoto T., Taniwaki M., Aizawa M., Inoue M., Katayama S., et al. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nature Genet. 8 (1994) 221-228
6. Zoghbi H.Y., and Orr H.T. Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23 (2000) 217-247
7. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P., and Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277 (1997) 1990-1993
8. Holmberg M., Duyckaerts C., Durr A., Cancel G., Gourfinkel-An I., Damier P., et al. Spinocerebellar ataxia type 7 (SCA7): a neurodegenerative disorder with neuronal intranuclear inclusions. Hum. Mol. Genet. 7 (1998) 913-918
9. Paulson H.L., Perez M.K., Trottier Y., Trojanowski J.Q., Subramony S.H., Das S.S., et al. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 19 (1997) 333-344
10. Chai Y., Koppenhafer S.L., Shoesmith S.J., Perez M. K., and Paulson H.L. 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 (1999) 673-682
11. Abel A., Walcott J., Woods J., Duda J., and Merry D.E. Expression of expanded repeat androgen receptor produces neurologic disease in transgenic mice. Hum. Mol. Genet. 10 (2001) 107-116
12. Cummings C.J., Mancini M.A., Antalffy B., DeFranco D.B., Orr H.T., and Zoghbi H.Y. Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nature Genet. 19 (1998) 148-154
13. Schmidt T., Lindenberg K.S., Krebs A., Schols L., Laccone F., Herms J., et al. Protein surveillance machinery in brains with spinocerebellar ataxia type 3: redistribution and differential recruitment of 26S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann. Neurol. 51 (2002) 302-310
14. Stenoien D.L., Cummings C.J., Adams H.P., Mancini M.G., Patel K., DeMartino G.N., et al. Polyglutamine-expanded androgen receptors form aggregates that sequester heat shock proteins, proteasome components and SRC-1, and are suppressed by the HDJ-2 chaperone. Hum. Mol. Genet. 8 (1999) 731-741
15. Scherzinger E., Lurz R., Turmaine M., Mangiarini L., Hollenbach B., Hasenbank R., et al. Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90 (1997) 5458-5495
16. Scherzinger E., Sittler A., Schweiger K., Heiser V., Lurz R., Hasenbank R., et al. Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc. Natl Acad. Sci. USA 96 (1999) 4604-4609
17. Chen S., Ferrone F.A., and Wetzel R. Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation. Proc. Natl Acad. Sci. USA 99 (2002) 11884-11889
18. Bevivino A.E., and Loll P.J. An expanded glutamine repeat destabilizes native ataxin-3 structure and mediates formation of parallel beta-fibrils. Proc. Natl Acad. Sci. USA 98 (2001) 11955-11960
19. Ellisdon A.M., Thomas B., and Bottomley S.P. The two-stage pathway of ataxin-3 fibrillogenesis involves a polyglutamine-independent step. J. Biol. Chem. 281 (2006) 16888-16896
20. Ignatova Z., and Gierasch L.M. Extended polyglutamine tracts cause aggregation and structural perturbation of an adjacent beta barrel protein. J. Biol. Chem. 281 (2006) 12959-12967
21. Perutz M.F., Johnson T., Suzuki M., and Finch J.T. Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc. Natl Acad. Sci. USA 91 (1994) 5355-5358
22. Colby D.W., Cassady J.P., Lin G.C., Ingram V.M., and Wittrup K.D. Stochastic kinetics of intracellular huntingtin aggregate formation. Nature Chem. Biol. 2 (2006) 319-323
23. Ellisdon A.M., and Bottomley S.P. The role of protein misfolding in the pathogenesis of human diseases. IUBMB Life 56 (2004) 119-123
24. Taylor J.P., Tanaka F., Robitschek J., Sandoval C.M., Taye A., Markovic-Plese S., and Fischbeck K.H. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum. Mol. Genet. 12 (2003) 749-757
25. Arrasate M., Mitra S., Schweitzer E.S., Segal M.R., and Finkbeiner S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431 (2004) 805-810
26. Shimohata T., Sato A., Burke J.R., Strittmatter W.J., Tsuji S., and Onodera O. Expanded polyglutamine stretches form an 'aggresome'. Neurosci. Letters 323 (2002) 215-218
27. Saudou F., Finkbeiner S., Devys D., and Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95 (1998) 55-66
28. Bhattacharyya A.M., Thakur A.K., and Wetzel R. polyglutamine aggregation nucleation: thermodynamics of a highly unfavorable protein folding reaction. Proc. Natl Acad. Sci. USA 102 (2005) 15400-15405
29. Esler W.P., Stimson E.R., Jennings J.M., Vinters H.V., Ghilardi J.R., Lee J.P., et al. Alzheimer's disease amyloid propagation by a template-dependent dock-lock mechanism. Biochemistry 39 (2000) 6288-6295
30. Collins S.R., Douglass A., Vale R.D., and Weissman J.S. Mechanism of prion propagation: amyloid growth occurs by monomer addition. PLoS Biol. 2 (2004) e321
31. Berthelier V., Hamilton J.B., Chen S., and Wetzel R. A microtiter plate assay for polyglutamine aggregate extension. Anal. Biochem. 295 (2001) 227-236
32. Masino L., Nicastro G., Menon R.P., Dal Piaz F., Calder L., and Pastore A. Characterization of the structure and the amyloidogenic properties of the Josephin domain of the polyglutamine-containing protein ataxin-3. J. Mol. Biol. 344 (2004) 1021-1035
33. Gales L., Cortes L., Almeida C., Melo C.V., do Carmo Costa M., Maciel P., et al. Towards a structural understanding of the fibrillization pathway in Machado-Joseph's disease: trapping early oligomers of non-expanded ataxin-3. J. Mol. Biol. 353 (2005) 642-654
34. Chow M.K., Ellisdon A.M., Cabrita L.D., and Bottomley S.P. Polyglutamine expansion in ataxin-3 does not affect protein stability: implications for misfolding and disease. J. Biol. Chem. 279 (2004) 47643-47651
35. Chow M.K., Paulson H.L., and Bottomley S.P. Destabilization of a non-pathological variant of ataxin-3 results in fibrillogenesis via a partially folded intermediate: a model for misfolding in polyglutamine disease. J. Mol. Biol. 335 (2004) 333-341
36. Marchal S., Shehi E., Harricane M.C., Fusi P., Heitz F., Tortora P., and Lange R. Structural instability and fibrillar aggregation of non-expanded human ataxin-3 revealed under high pressure and temperature. J. Biol. Chem. 278 (2003) 31554-31563
37. Shehi E., Fusi P., Secundo F., Pozzuolo S., Bairati A., and Tortora P. Temperature-dependent, irreversible formation of amyloid fibrils by a soluble human ataxin-3 carrying a moderately expanded polyglutamine stretch (Q36). Biochemistry 42 (2003) 14626-14632
38. Menon R.P., and Pastore A. Expansion of amino acid homo-sequences in proteins: insights into the role of amino acid homo-polymers and of the protein context in aggregation. Cell Mol. Life Sci. 63 (2006) 1677-1685
39. Haacke A., Broadley S.A., Boteva R., Tzvetkov N., Hartl F.U., and Breuer P. Proteolytic cleavage of polyglutamine-expanded ataxin-3 is critical for aggregation and sequestration of non-expanded ataxin-3. Hum. Mol. Genet. 15 (2006) 555-568
40. Ferrone F. Analysis of protein aggregation kinetics. Methods Enzymol. 309 (1999) 256-274
41. Chen S., Berthelier V., Hamilton J.B., O'Nuallain B., and Wetzel R. Amyloid-like features of polyglutamine aggregates and their assembly kinetics. Biochemistry 41 (2002) 7391-7399
42. Frankenfield K.N., Powers E.T., and Kelly J.W. Influence of the N-terminal domain on the aggregation properties of the prion protein. Protein Sci. 14 (2005) 2154-2166
43. de Chiara C., Menon R.P., Dal Piaz F., Calder L., and Pastore A. Polyglutamine is not all: the functional role of the AXH domain in the ataxin-1 protein. J. Mol. Biol. 354 (2005) 883-893
44. Cabrita L.D., Dai W., and Bottomley S.P. A family of E. coli expression vectors for laboratory scale and high throughput soluble protein production. BMC Biotechnol. 6 (2006) 12
45. Chow M.K., Mackay J.P., Whisstock J.C., Scanlon M.J., and Bottomley S.P. Structural and functional analysis of the Josephin domain of the polyglutamine protein ataxin-3. Biochem. Biophys. Res. Commun. 322 (2004) 387-394
46. Schuck P., and Rossmanith P. Determination of the sedimentation coefficient distribution by least-squares boundary modeling. Biopolymers 54 (2000) 328-341
47. Wanker E.E., Scherzinger E., Heiser V., Sittler A., Eickhoff H., and Lehrach H. Membrane filter assay for detection of amyloid-like polyglutamine-containing protein aggregates. Methods Enzymol. 309 (1999) 375-386