A region within the C-terminal domain of Ure2p is shown to interact with the molecular chaperone Ssa1p by the use of cross-linkers and mass spectrometry

FEBS Journal

Volumn 277, Issue 24, 2010, Pages 5112-5123

  Redeker, Virginie ^a   Bonnefoy, Jonathan ^a   Le Caer, Jean Pierre ^b   Pemberton, Samantha ^a   Laprévote, Olivier ^b   Melki, Ronald ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b CNRS   (France)

Author keywords

cross linker; mass spectrometry; molecular chaperone; oligomerization; prion; Ure2p

Indexed keywords

1 (3 DIMETHYLAMINOPROPYL) 3 ETHYLCARBODIIMIDE; CHAPERONE; LYSINE; N HYDROXYSUCCINIMIDE; POLYPEPTIDE; PROTEIN SSA1P; PROTEIN URE2P; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS LINKING; MASS SPECTROMETRY; PEPTIDE ANALYSIS; PRION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY;

ADENOSINE TRIPHOSPHATASES; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLUTATHIONE PEROXIDASE; HSP70 HEAT-SHOCK PROTEINS; LYSINE; MOLECULAR CHAPERONES; PRIONS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 78649991956     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07915.x     Document Type: Article

References (40)

1. Masison DC, Maddelein ML, &, Wickner RB, (1997) The prion model for [URE3] of yeast: spontaneous generation and requirements for propagation. Proc Natl Acad Sci USA 94, 12503-12508.
2. Masison DC, &, Wickner RB, (1995) Prion-inducing domain of yeast Ure2p and protease resistance of Ure2p in prion-containing cells. Science 270, 93-95.
3. Moriyama H, Edskes HK, &, Wickner RB, (2000) [URE3] prion propagation in Saccharomyces cerevisiae: requirement for chaperone Hsp104 and curing by overexpressed chaperone Ydj1p. Mol Cell Biol 20, 8916-8922.
4. Schwimmer C, &, Masison DC, (2002) Antagonistic interactions between yeast [PSI(+)] and [URE3] prions and curing of [URE3] by Hsp70 protein chaperone Ssa1p but not by Ssa2p. Mol Cell Biol 22, 3590-3598.
5. Roberts BT, Moriyama H, &, Wickner RB, (2004) [URE3] prion propagation is abolished by a mutation of the primary cytosolic Hsp70 of budding yeast. Yeast 21, 107-117.
6. Savistchenko J, Krzewska J, Fay N, &, Melki R, (2008) Molecular chaperones and the assembly of the prion Ure2p in vitro. J Biol Chem 283, 15732-15739.
7. Thual C, Bousset L, Komar AA, Walter S, Buchner J, Cullin C, &, Melki R, (2001) Stability, folding, dimerization, and assembly properties of the yeast prion Ure2p. Biochemistry 40, 1764-1773.
8. Bousset L, Belrhali H, Janin J, Melki R, &, Morera S, (2001) Structure of the globular region of the prion protein Ure2 from the yeast Saccharomyces cerevisiae. Structure (Camb.) 9, 39-46.
9. Sinz A, (2006) Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions. Mass Spectrom Rev 25, 663-682.
10. Lutter LC, &, Kurland CG, (1975) Chemical determination of protein neighbourhoods in a cellular organelle. Mol Cell Biochem 7, 105-116.
11. Cohen FE, &, Sternberg MJ, (1980) On the use of chemically derived distance constraints in the prediction of protein structure with myoglobin as an example. J Mol Biol 137, 9-22.
12. Heymann M, Paramelle D, Subra G, Forest E, Martinez J, Geourjon C, &, Deléage G, (2008) MSX-3D: a tool to validate 3D protein models using mass spectrometry. Bioinformatics 24, 2782-2783.
13. Pimenova T, Nazabal A, Roschitzki B, Seebacher J, Rinner O, &, Zenobi R, (2008) Epitope mapping on bovine prion protein using chemical cross-linking and mass spectrometry. J Mass Spectrom 43, 185-195.
14. Pimenova T, Pereira CP, Schaer DJ, &, Zenobi R, (2009) Characterization of high molecular weight multimeric states of human haptoglobin and hemoglobin-based oxygen carriers by high-mass MALDI MS. J Sep Sci 32, 1224-1230.
15. Kalkhof S, &, Sinz A, (2008) Chances and pitfalls of chemical cross-linking with amine-reactive N-hydroxysuccinimide esters. Anal Bioanal Chem 392, 305-312.
16. Seebacher J, Mallick P, Zhang N, Eddes JS, Aebersold R, &, Gelb MH, (2006) Protein cross-linking analysis using mass spectrometry, isotope-coded cross-linkers, and integrated computational data processing. J Proteome Res 5, 2270-2282.
17. Gao QX, Doneanu CE, Shaffer SA, Adman ET, Goodlett DR, &, Nelson SD, (2006) Identification of the interactions between cytochrome P450 2E1 and cytochrome b(5) by mass spectrometry and site-directed mutagenesis. J Biol Chem 281, 20404-20417.
18. Kalkhof S, Ihling C, Mechtler K, &, Sinz A, (2005) Chemical cross-linking and high-performance Fourier transform ion cyclotron resonance mass spectrometry for protein interaction analysis: application to a calmodulin/target peptide complex. Anal Chem 77, 495-503. (Pubitemid 40116828)
19. Tang XT, Munske GR, Siems WF, &, Bruce JE, (2005) Mass spectrometry identifiable cross-linking strategy for studying protein-protein interactions. Anal Chem 77, 311-318.
20. Sinz A, Kalkhof S, &, Ihling C, (2005) Mapping protein interfaces by a trifunctional cross-linker combined with MALDI-TOF and ESI-FTICR mass spectrometry. J Am Soc Mass Spectrom 16, 1921-1931.
21. Schmidt A, Kalkhof S, Ihling C, Cooper DMF, &, Sinz A, (2005) Mapping protein interfaces by chemical cross-linking and Fourier transform ion cyclotron resonance mass spectrometry: application to a calmodulin/adenylyl cyclase 8 peptide complex. Eur J Mass Spectrom 11, 525-534. (Pubitemid 41796541)
22. Dimova K, Kalkhof S, Pottratz I, Ihling C, Rodriguez-Castaneda F, Liepold T, Griesinger C, Brose N, Sinz A, &, Jahn O, (2009) Structural insights into the calmodulin-Munc13 interaction obtained by cross-linking and mass spectrometry. Biochemistry 48, 5908-5921.
23. Manolaridis I, Mumtsidu E, Konarev P, Makhov AM, Fullerton SW, Sinz A, Kalkhof S, McGeehan JE, Cary PD, Griffith JD, et al. (2009) Structural and biophysical characterization of the proteins interacting with the herpes simplex virus 1 origin of replication. J Biol Chem 284, 16343-16353.
24. Jaya N, Garcia V, &, Vierling E, (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc Natl Acad Sci USA 106, 15604-15609.
25. Bousset L, Redeker V, Decottignies P, Dubois S, Le Maréchal P, &, Melki R, (2004) Structural characterization of the fibrillar form of the yeast Saccharomyces cerevisiae prion Ure2p. Biochemistry 43, 5022-5032.
26. Fay N, Redeker V, Savischenko J, Dubois S, Bousset L, &, Melki R, (2005) Structure of the prion Ure2p in protein fibrils assembled in vitro. J Biol Chem 280, 37149-37158.
27. Ranson N, Stromer T, Bousset L, Melki R, &, Serpell LC, (2006) Insights into the architecture of the Ure2p yeast protein assemblies from helical twisted fibrils. Protein Sci 15, 2481-2487.
28. Bousset L, Bonnefoy J, Sourigues Y, Wien F, &, Melki R, (2010) Structure and assembly properties of the N-terminal domain of the prion Ure2p in isolation and in its natural context. PLoS ONE 5, e9760.
29. Maiolica A, Cittaro D, Borsotti D, Sennels L, Ciferri C, Tarricone C, Musacchio A, &, Rappsilber J, (2007) Structural analysis of multiprotein complexes by cross-linking, mass spectrometry, and database searching. Mol Cell Proteomics 6, 2200-2211.
30. Peri S, Steen H, &, Pandey A, (2001) GPMAW-a software tool for analyzing proteins and peptides. Trends Biochem Sci 26, 687-689.
31. Rinner O, Seebacher J, Walzthoeni T, Mueller LN, Beck M, Schmidt A, Mueller M, &, Aebersold R, (2008) Identification of cross-linked peptides from large sequence databases. Nat Methods 5, 315-318.
32. Leitner A, Walzthoeni T, Kahraman A, Herzog F, Rinner O, Beck M, &, Aebersold R, (2010) Probing native protein structures by chemical cross-linking, mass spectrometry and bioinformatics. Mol Cell Proteomics 9, 1634-1649.
33. Redeker V, Halgand F, Le Caer JP, Bousset L, Laprévote O, &, Melki R, (2007) Hydrogen/deuterium exchange mass spectrometric analysis of conformational changes accompanying the assembly of the yeast prion Ure2p into protein fibrils. J Mol Biol 369, 1113-1125.
34. Thual C, Komar AA, Bousset L, Fernandez-Bellot E, Cullin C, &, Melki R, (1999) Structural characterization of Saccharomyces cerevisiae prion-like protein Ure2. J Biol Chem 274, 13666-13674.
35. Krzewska J, &, Melki R, (2006) Molecular chaperones and the assembly of the prion Sup35p, an in vitro study. EMBO J 25, 822-833.
36. Mädler S, Bich C, Touboul D, &, Zenobi R, (2009) Chemical cross-linking with NHS esters: a systematic study on amino acid reactivities. J Mass Spectrom 44, 694-706.
37. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
38. Shevchenko A, Wilm M, Vorm O, &, Mann M, (1996) Mass spectrometric sequencing of proteins silverstained polyacrylamide gels. Anal Chem 68, 850-858.
39. Wenzel RJ, Kern S, Nazabal A, &, Zenobi R, (2007) Quantitative comparison of sensitivity and saturation for MALDI-TOF detectors when measuring complex and high mass samples. Proceedings of the 55th ASMS Conference on Mass Spectrometry, Indianapolis, MP082.
40. Zimmer JS, Monroe ME, Qian WJ, &, Smith RD, (2006) Advances in proteomics data analysis and display using an accurate mass and time tag approach. Mass Spectrom Rev 25, 450-482.