Proteomic and biochemical analyses unveil tight interaction of ataxin-3 with tubulin

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 12, 2009, Pages 2485-2492

  Mazzucchelli, Serena ^a   De Palma, Antonella ^b   Riva, Matteo ^a   D'Urzo, Annalisa ^a   Pozzi, Chiara ^a   Pastori, Valentina ^a   Comelli, Francesca ^a   Fusi, Paola ^a   Vanoni, Marco ^a   Tortora, Paolo ^a   Mauri, Pierluigi ^b   Regonesi, Maria Elena ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b CNR   (Italy)

Author keywords

Aggresomes; Ataxin 3; Mass spectrometry; Microtubules; Surface plasmon resonance

Indexed keywords

ALPHA TUBULIN; ATAXIN 3; BETA TUBULIN;

AGGRESOME; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL STRAIN COS7; CELLULAR DISTRIBUTION; CHEMICAL ANALYSIS; CHROMATOGRAPHY; CONTROLLED STUDY; DISSOCIATION CONSTANT; GENE OVEREXPRESSION; IMMUNOPRECIPITATION; IN VIVO STUDY; MICROTUBULE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RAT; SURFACE PLASMON RESONANCE; TANDEM MASS SPECTROMETRY;

ANIMALS; BRAIN; CERCOPITHECUS AETHIOPS; CLONING, MOLECULAR; COS CELLS; HUMANS; MACHADO-JOSEPH DISEASE; MASS SPECTROMETRY; MICE; MICROTUBULES; NERVE TISSUE PROTEINS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RATS; TIGHT JUNCTIONS; TRANSGENES; TUBULIN;

RATTUS;

EID: 70350339099     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.08.003     Document Type: Article

References (50)

1. Boeddrich A., Gaumer S., Haacke A., Tzvetkov N., Albrecht M., Evert B.O., et al. An arginine/lysine-rich motif is crucial for VCP/p97-mediated modulation of ataxin-3 fibrillogenesis. EMBO J 25 (2006) 1547-1558
2. Burnett B., Li F., and Pittman R.N. The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. Hum Mol Genet 12 (2003) 3195-3205
3. Burnett B.G., and Pittman R.N. The polyglutamine neurodegenerative protein ataxin 3 regulates aggresome formation. Proc Natl Acad Sci USA 12 (2005) 4330-4335
4. Chai Y., Berke S.S., Cohen R.E., and Paulson H.L. Poly-ubiquitin binding by the polyglutamine disease protein ataxin-3 links its normal function to protein surveillance pathways. J Biol Chem 279 (2004) 3605-3611
5. Cummings C.J., and Zoghbi H.Y. Trinucleotide repeats: mechanisms and pathophysiology. Annu Rev Genomics Hum Genet 1 (2000) 281-328
6. Cusick M.E., Klitgord N., Vidal M., and Hill D.E. Interactome: gateway into systems biology. Hum Mol Genet 14 (2005) R171-R181
7. Donaldson K.M., Li W., Ching K.A., Batalov S., Tsai C.C., and Joazeiro C.A. Ubiquitin-mediated sequestration of normal cellular proteins into polyglutamine aggregates. Proc Natl Acad Sci USA 100 (2003) 8892-8897
8. Doss-Pepe E.W., Stenroos E.S., Johnson W.G., and 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 23 (2003) 6469-6483
9. García-Mata R., Bebök Z., Sorscher E.J., and Sztul E.S. Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J Cell Biol 146 (1999) 1239-1254
10. García-Mata R., Gao Y.S., and Sztul E. Hassles with taking out the garbage: aggravating aggresomes. Traffic 3 (2002) 388-396
11. Goswami A., Dikshit P., Mishra A., Nukina N., and Jana N.R. Expression of expanded polyglutamine proteins suppresses the activation of transcription factor NFkB. J Biol Chem 281 (2006) 37017-37024
12. Gygi S.P., Rist B., Gerber S.A., Turecek F., Gelb M.H., and Aebersold R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17 (1999) 994-999
13. Harries P.A., Palanichelvam K., Yu W., Schoelz J.E., and Nelson R.S. The cauliflower mosaic virus protein p6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol 149 (2009) 1005-1016
14. Jeffery C.J. Molecular mechanisms for multitasking: recent crystal structures of moonlighting proteins. Curr Opin Struct Biol 14 (2004) 663-668
15. Johnsson B., Lofas S., and Lindquist G. Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal Biochem 198 (1991) 268-277
16. Kawaguchi Y., Kovacs J.J., McLaurin A., Vance J.M., Ito A., and Yao T.P. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115 (2003) 727-738
17. Kumar M.D.S., and Gromiha M.M. PINT: protein-protein interactions thermodynamic database. Nucleic Acids Res 34 (2007) D195-D198
18. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
19. Li F., Macfarlan T., Pittman R.N., and Chakravarti D. Ataxin-3 is a histone-binding protein with two independent transcriptional corepressor activities. J Biol Chem 277 (2002) 45004-45012
20. Malmqvist M. BIACORE: an affinity biosensor system for characterization of biomolecular interactions. Biochem Soc Trans 27 (1999) 335-340
21. Maly I.V., and Borisy G.G. Self-organization of treadmilling microtubules into a polar array. Trends Cell Biol 12 (2002) 462-465
22. Mao Y., Senic-Matuglia F., Di Fiore P.P., Polo S., Hodsdon M.E., and De Camilli P. Deubiquitinating function of ataxin-3: insights from the solution structure of the Josephin domain. Proc Natl Acad Sci USA 102 (2005) 12700-12705
23. Marchal S., Shehi E., Barricane M.C., Fusi P., Heitz F., Tortora P., et al. Structural instability and fibrillar aggregation of non-expanded human ataxin-3 revealed under high pressure and temperature. J Biol Chem 278 (2003) 31554-31563
24. Masino L., Musi V., Menon R.P., Fusi P., Kelly G., Frenkiel A., et al. Domain architecture of the polyglutamine protein ataxin-3: a globular domain followed by a flexible tail. FEBS Lett 549 (2003) 21-25
25. Mauri P., Scarpa A., Nascimbeni A.C., Benazzi L., Parmagnani E., Mafficini A., et al. Identification of proteins released by pancreatic cancer cells by multidimensional protein identification technology: a strategy for identification of novel cancer markers. FASEB J 19 (2005) 1125-1127
26. Mauri P., Riva M., Ambu D., De Palma A., Secundo F., Benazzi L., et al. Ataxin-3 is subject to autolytic cleavage. FEBS J 273 (2006) 4277-4286
27. Mauri P., and Dehò G. A proteomic MudPIT approach to the analysis of RNA degradosome composition in Escherichia coli. Methods Enzymol 447 (2008) 99-117
28. McNiven M.A., and Porter K.R. Microtubule polarity confers direction to pigment transport in chromatophores. J Cell Biol 103 (1986) 1547-1555
29. Nagayama K., and Matsumoto T. Contribution of actin filaments and microtubules to quasi-in situ tensile properties and internal force balance of cultured smooth muscle cells on a substrate. Am J Physiol Cell Physiol 295 (2008) 1569-1578
30. Nicastro G., Masino L., Frenkiel T.A., Kelly G., McCormick J., Menon R.P., et al. Assignment of the 1H, 13C, and 15N resonances of the Josephin domain of human ataxin-3. J Biomol NMR 30 (2004) 457-458
31. Nicastro G., Menon R.P., Masino L., Knowles P.P., McDonald N.Q., and Pastore A. The solution structure of the Josephin domain of ataxin-3: structural determinants for molecular recognition. Proc Natl Acad Sci USA 102 (2005) 10493-10498
32. Orr T.H. Beyond the Qs in the polyglutamine diseases. Genes Dev 15 (2001) 925-932
33. 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
34. Paulson H.L. Dominantly inherited ataxias: lessons learned from Machado-Joseph disease/spinocerebellar ataxia type 3. Semin Neurol 27 (2007) 133-142
35. Pozzi C., Valtorta M., Tedeschi G., Galbusera E., Pastori V., Bigi A., et al. Study of subcellular localization and proteolysis of ataxin-3. Neurobiol Dis 30 (2008) 190-200
36. Rathinasamy K., and Panda D. Kinetic stabilization of microtubule dynamic instability by benomyl increases the nuclear transport of p53. Biochem Pharmacol 76 (2008) 1669-1680
37. Regonesi M.E., Del Favero M., Basilico F., Briani F., Benazzi L., Tortora P., et al. Analysis of the Escherichia coli RNA degradosome composition by a proteomic approach. Biochimie 88 (2006) 151-161
38. Sambrook J., Fritsch E.F., and Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. (1989), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
39. Schuck P., and Minton A.P. Kinetic analysis of biosensor data: elementary tests for self-consistency. Trends Biochem Sci 21 (1996) 458-460
40. 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
41. Smith J.C., and Figeys D. Proteomics technology in systems biology. Mol Biosyst 2 (2006) 364-370
42. Stelzl U., and Wanker E.E. The value of high quality protein-protein interaction networks for systems biology. Curr Opin Chem Biol 10 (2006) 551-558
43. Stawoska I., Wesełucha-Birczyńska A., Regonesi M.E., Riva M., Tortora P., and Stochel G. Interaction of selected divalent metal ions with human ataxin-3 Q36. J Biol Inorg Chem (2009) [Epub ahead of print] PMID: 19575245
44. Valiron O., Caudron N., and Job D. Microtubule dynamics. Cell Mol Life Sci 258 (2001) 2069-2084
45. Vidal M. Interactome modeling. FEBS Lett 579 (2005) 1834-1838
46. Wolters D.A., Washburn M.P., and Yates III J.R. An automated multidimensional protein identification technology for shotgun proteomics. Anal Chem 73 (2001) 5683-5690
47. Zhong X., and Pittman R.N. Ataxin-3 binds VCP/p97 and regulates retrotranslocation of ERAD substrates. Hum Mol Genet 15 (2006) 2409-2420
48. Zoghbi H.Y., and Orr H.T. Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23 (2000) 217-247
49. Zuccato C., Ciammola A., Rigamonti D., Leavitt B.R., Goffredo D., Conti L., et al. Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293 (2001) 493-498
50. Zuccato C., Tartari M., Crotti A., Goffredo D., Valenza M., Conti L., et al. Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat Genet 35 (2003) 76-83