Absence of ataxin-3 leads to cytoskeletal disorganization and increased cell death

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1803, Issue 10, 2010, Pages 1154-1163

  Rodrigues, Ana João ^a   do Carmo Costa, Maria ^a,b   Silva, Teresa Luísa ^a   Ferreira, Daniela ^a   Bajanca, Fernanda ^a,d   Logarinho, Elsa ^a,c   Maciel, Patrícia ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PORTO   (Portugal)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Polyglutamine; Sinocerebellar ataxia type 3; Tubulin; Ubiquitin proteasome

Indexed keywords

ALPHA1 INTEGRIN; ATAXIN 3; POLYGLUTAMINE; PROTEASOME; SMALL INTERFERING RNA; TALIN; UBIQUITIN; ATXN3 PROTEIN, HUMAN; MJD PROTEIN, MOUSE; NERVE PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CYCLE; CELL DEATH; CELL LINE; CONTROLLED STUDY; CYTOSKELETON; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; MACHADO JOSEPH DISEASE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UBIQUITINATION; 3T3 CELL LINE; ANIMAL; APOPTOSIS; CONFOCAL MICROSCOPY; FOCAL ADHESION; GENETICS; HELA CELL LINE; METABOLISM; NICK END LABELING; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

3T3 CELLS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CYTOSKELETON; FOCAL ADHESIONS; HELA CELLS; HUMANS; IN SITU NICK-END LABELING; INTEGRIN ALPHA1; MICE; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION FACTORS;

EID: 77955655871     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.07.004     Document Type: Article

References (49)

1. La Spada A.R., Taylor J.P. Polyglutamines placed into context. Neuron 2003, 38:681-684.
2. Doss-Pepe E.W., Stenroos E.S., Johnson W.G., Madura K. 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. 2003, 23:6469-6483.
3. Burnett B., Li F., Pittman R.N. The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. Hum. Mol. Genet. 2003, 12:3195-3205.
4. Chai Y., Berke S.S., Cohen R.E., Paulson H.L. Poly-ubiquitin binding by the polyglutamine disease protein ataxin-3 links its normal function to protein surveillance pathways. J. Biol. Chem. 2004, 279:3605-3611.
5. Ferro A., Carvalho A.L., Teixeira-Castro A., Almeida C., Tome R.J., Cortes L., et al. NEDD8: a new ataxin-3 interactor. Biochim. Biophys. Acta 2007, 1773:1619-1627.
6. Berke S.J., Chai Y., Marrs G.L., Wen H., Paulson H.L. Defining the role of ubiquitin-interacting motifs in the polyglutamine disease protein, ataxin-3. J. Biol. Chem. 2005, 280:32026-32034.
7. Tsai Y.C., Fishman P.S., Thakor N.V., Oyler G.A. Parkin facilitates the elimination of expanded polyglutamine proteins and leads to preservation of proteasome function. J. Biol. Chem. 2003, 278:22044-22055.
8. Zhong X., Pittman R.N. Ataxin-3 binds VCP/p97 and regulates retrotranslocation of ERAD substrates. Hum. Mol. Genet. 2006, 15:2409-2420.
9. Wang Q., Li L., Ye Y. Regulation of retrotranslocation by p97-associated deubiquitinating enzyme ataxin-3. J. Cell Biol. 2006, 174:963-971.
10. Winborn B.J., Travis S.M., Todi S.V., Scaglione K.M., Xu P., Williams A.J., et al. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J. Biol. Chem. 2008, 283:26436-26443.
11. Woelk T., Sigismund S., Penengo L., Polo S. The ubiquitination code: a signalling problem. Cell Div. 2007, 2:11.
12. Li F., Macfarlan T., Pittman R.N., Chakravarti D. Ataxin-3 is a histone-binding protein with two independent transcriptional corepressor activities. J. Biol. Chem. 2002, 277:45004-45012.
13. Evert B.O., Araujo J., Vieira-Saecker A.M., de Vos R.A., Harendza S., Klockgether T., et al. Ataxin-3 represses transcription via chromatin binding, interaction with histone deacetylase 3, and histone deacetylation. J. Neurosci. 2006, 26:11474-11486.
14. McMurray C.T. Neurodegeneration: diseases of the cytoskeleton?. Cell Death Differ. 2000, 7:861-865.
15. Gunawardena S., Goldstein L.S. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch. Neurol. 2005, 62:46-51.
16. Alonso A.C., Grundke-Iqbal I., Iqbal K. Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat. Med. 1996, 2:783-787.
17. Engelender S., Sharp A.H., Colomer V., Tokito M.K., Lanahan A., Worley P., et al. Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum. Mol. Genet. 1997, 6:2205-2212.
18. Hoffner G., Kahlem P., Djian P. Perinuclear localization of huntingtin as a consequence of its binding to microtubules through an interaction with beta-tubulin: relevance to Huntington's disease. J. Cell Sci. 2002, 115:941-948.
19. Johnston J.A., Ward C.L., Kopito R.R. Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 1998, 143:1883-1898.
20. Kawaguchi Y., Kovacs J.J., McLaurin A., Vance J.M., Ito A., et al. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003, 115:727-738.
21. Johnston J.A., Illing M.E., Kopito R.R. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell Motil. Cytoskeleton 2002, 53:26-38.
22. Burnett B.G., Pittman R.N. The polyglutamine neurodegenerative protein ataxin 3 regulates aggresome formation. Proc. Natl. Acad. Sci. USA 2005, 102:4330-4335.
23. Costa M.C., Gomes-da-Silva J., Miranda C.J., Sequeiros J., Santos M.M., Maciel P., et al. Genomic structure, promoter activity, and developmental expression of the mouse homologue of the Machado-Joseph disease (MJD) gene. Genomics 2004, 84:361-373.
24. Rodrigues A.J., Coppola G., Santos C., Costa M.C., Ailion M., Sequeiros J., et al. Functional genomics and biochemical characterization of the C. elegans orthologue of the Machado-Joseph disease protein ataxin-3. FASEB J. 2007, 21:1126-1136.
25. Mazzucchelli S., De Palma A., Riva M., D'Urzo A., Pozzi C., Pastori V., et al. Proteomic and biochemical analyses unveil tight interaction of ataxin-3 with tubulin. Int. J. Biochem. Cell Biol. 2009.
26. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
27. Almeida A.J., Matute D.R., Carmona J.A., Martins M., Torres I., McEwen J.G., et al. Genome size and ploidy of Paracoccidioides brasiliensis reveals a haploid DNA content: flow cytometry and GP43 sequence analysis. Fungal Genet. Biol. 2007, 44:25-31.
28. Piperno G., LeDizet M., Chang X.J. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol. 1987, 104:289-302.
29. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., et al. HDAC6 is a microtubule-associated deacetylase. Nature 2002, 417:455-458.
30. Byun Y., Chen F., Chang R., Trivedi M., Green K.J., Cryns V.L. Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ. 2001, 8:443-450.
31. Burridge K., Connell L. Talin: a cytoskeletal component concentrated in adhesion plaques and other sites of actin-membrane interaction. Cell Motil. 1983, 3:405-417.
32. Critchley D.R. Focal adhesions-the cytoskeletal connection. Curr. Opin. Cell Biol. 2000, 12:133-139.
33. Hendzel M.J., Wei Y., Mancini M.A., Van Hooser A., Ranalli T., Brinkley B.R., et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997, 106:348-360.
34. Krishan A. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J. Cell Biol. 1975, 66:188-193.
35. Frisch S.M., Screaton R.A. Anoikis mechanisms. Curr. Opin. Cell Biol. 2001, 13:555-562.
36. Cattaneo E., Rigamonti D., Goffredo D., Zuccato C., Squitieri F., Sipione S., et al. Loss of normal huntingtin function: new developments in Huntington's disease research. Trends Neurosci. 2001, 24:182-188.
37. Lim J., Crespo-Barreto J., Jafar-Nejad P., Bowman A.B., Richman R., et al. Opposing effects of polyglutamine expansion on native protein complexes contribute to SCA1. Nature 2008, 452:713-718.
38. Schmitt I., Linden M., Khazneh H., Evert B.O., Breuer P., Klockgether T., et al. Inactivation of the mouse Atxn3 (ataxin-3) gene increases protein ubiquitination. Biochem. Biophys. Res. Commun. 2007, 362:734-739.
39. Garcia-Mata R., Bebok Z., Sorscher E.J., Sztul E.S. Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 1999, 146:1239-1254.
40. Ligon L.A., Karki S., Tokito M., Holzbaur E.L. Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat. Cell Biol. 2001, 3:913-917.
41. Forry-Schaudies S., Murray J.M., Toyama Y., Holtzer H. Effects of colcemid and taxol on microtubules and intermediate filaments in chick embryo fibroblasts. Cell Motil. Cytoskeleton 1986, 6:324-338.
42. Calderwood D.A., Shattil S.J., Ginsberg M.H. Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. J. Biol. Chem. 2000, 275:22607-22610.
43. Palazzo A.F., Gundersen G.G. Microtubule-actin cross-talk at focal adhesions. Sci. STKE 2002, 2002:PE31.
44. Deschesnes R.G., Patenaude A., Rousseau J.L., Fortin J.S., Ricard C., Côté M.F., et al. Microtubule-destabilizing agents induce focal adhesion structure disorganization and anoikis in cancer cells. J. Pharmacol. Exp. Ther. 2007, 320:853-864.
45. Frisch S.M., Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 1994, 124:619-626.
46. Colucci-Guyon E., Portier M.M., Dunia I., Paulin D., Pournin S., Babinet C. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 1994, 79:679-694.
47. Goldman R.D., Khuon S., Chou Y.H., Opal P., Steinert P.M. The function of intermediate filaments in cell shape and cytoskeletal integrity. J. Cell Biol. 1996, 134:971-983.
48. Rodrigues A.J., Neves-Carvalho A., Ferro A., Rokka A., Corthals G., Logarinho E., et al. ATX-3, CDC-48 and UBXN-5: a new trimolecular complex in Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 2009, 386:575-581.
49. Reina C.P., Zhong X., Pittman R.N. Proteotoxic stress increases nuclear localization of ataxin-3. Hum. Mol. Genet. 2009.