Probing the transient interaction between the small heat-shock protein Hsp21 and a model substrate protein using crosslinking mass spectrometry

Cell Stress and Chaperones

Volumn 18, Issue 1, 2013, Pages 75-85

  Lambert, Wietske ^a   Rutsdottir, Gudrun ^a   Hussein, Rasha ^a   Bernfur, Katja ^a   Kjellström, Sven ^a   Emanuelsson, Cecilia ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 21; MALATE DEHYDROGENASE; SMALL HEAT SHOCK PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; ENZYME SUBSTRATE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; PROTEIN UNFOLDING; STRUCTURE ANALYSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CROSS-LINKING REAGENTS; HEAT-SHOCK PROTEINS; MALATE DEHYDROGENASE; MODELS, MOLECULAR; PLANT PROTEINS; PROTEIN BINDING; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 84870450357     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-012-0360-4     Document Type: Article

References (46)

1. E Ahrman N Gustavsson C Hultschig WC Boelens CS Emanuelsson 2007 Small heat shock proteins prevent aggregation of citrate synthase and bind to the N-terminal region which is absent in thermostable forms of citrate synthase Extremophiles 11 659 666 17486291 10.1007/s00792-007-0080-3 (Pubitemid 47341002)
2. E Ahrman W Lambert JA Aquilina CV Robinson CS Emanuelsson 2007 Chemical cross-linking of the chloroplast localized small heat-shock protein, Hsp21, and the model substrate citrate synthase Protein Sci 16 1464 1478 17567739 10.1110/ps.072831607 (Pubitemid 46984880)
3. AJ Baldwin GR Hilton H Lioe C Bagneris JL Benesch LE Kay 2011 Quaternary dynamics of alphaB-crystallin as a direct consequence of localised tertiary fluctuations in the C-terminus J Mol Biol 413 310 320 21839749 10.1016/j.jmb.2011.07.017 1:CAS:528:DC%2BC3MXhtlaksb7P
4. AJ Baldwin H Lioe GR Hilton LA Baker JL Rubinstein LE Kay JL Benesch 2011 The polydispersity of alphaB-crystallin is rationalized by an interconverting polyhedral architecture Structure 19 1855 1863 22153508 10.1016/j.str.2011.09. 015 1:CAS:528:DC%2BC3MXhs1Sgt7vN
5. AJ Baldwin H Lioe CV Robinson LE Kay JL Benesch 2011 alphaB-Crystallin polydispersity is a consequence of unbiased quaternary dynamics J Mol Biol 413 297 309 21839090 10.1016/j.jmb.2011.07.016 1:CAS:528:DC%2BC3MXhtlaksb7O
6. Basha E, O'Neill H, Vierling E (2011) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37:106-117
7. M Beck JA Malmstrom V Lange A Schmidt EW Deutsch R Aebersold 2009 Visual proteomics of the human pathogen Leptospira interrogans Nat Methods 6 817 823 19838170 10.1038/nmeth.1390 1:CAS:528:DC%2BD1MXht1Ogsr3O
8. MP Bova LL Ding J Horwitz BK Fung 1997 Subunit exchange of alphaA-crystallin J Biol Chem 272 29511 29517 9368012 10.1074/jbc.272.47.29511 1:CAS:528:DyaK2sXnsFWgur0%3D (Pubitemid 27508037)
9. MP Bova HS McHaourab Y Han BK Fung 2000 Subunit exchange of small heat shock proteins. Analysis of oligomer formation of alphaA-crystallin and Hsp27 by fluorescence resonance energy transfer and site-directed truncations J Biol Chem 275 1035 1042 10625643 10.1074/jbc.275.2.1035 1:CAS:528: DC%2BD3cXntleiuw%3D%3D (Pubitemid 30051151)
10. G Cheng E Basha VH Wysocki E Vierling 2008 Insights into small heat shock protein and substrate structure during chaperone action derived from hydrogen/deuterium exchange and mass spectrometry J Biol Chem 283 26634 26642 18621732 10.1074/jbc.M802946200 1:CAS:528:DC%2BD1cXhtFejtr%2FF
11. DeLano W (2002) The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA, USA
12. H Ecroyd JA Carver 2008 Unraveling the mysteries of protein folding and misfolding IUBMB Life 60 769 774 18767168 10.1002/iub.117 1:CAS:528: DC%2BD1cXhsFSnsbjL
13. M Ehrnsperger S Graber M Gaestel J Buchner 1997 Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation EMBO J 16 221 229 9029143 10.1093/emboj/16.2.221 1:CAS:528:DyaK2sXpvVSluw%3D%3D (Pubitemid 27049380)
14. SJ Eyles LM Gierasch 2010 Nature's molecular sponges: small heat shock proteins grow into their chaperone roles Proc Natl Acad Sci USA 107 2727 2728 20133678 10.1073/pnas.0915160107 1:CAS:528:DC%2BC3cXis1ClsLw%3D
15. R Fritzsche CH Ihling M Gotze A Sinz 2012 Optimizing the enrichment of cross-linked products for mass spectrometric protein analysis Rapid Commun Mass Spectrom 26 653 658 22328219 10.1002/rcm.6150 1:CAS:528:DC%2BC38Xit1Sktbk%3D
16. KC Giese E Basha BY Catague E Vierling 2005 Evidence for an essential function of the N terminus of a small heat shock protein in vivo, independent of in vitro chaperone activity Proc Natl Acad Sci USA 102 18896 18901 16365319 10.1073/pnas.0506169103 1:CAS:528:DC%2BD28XivVyqtA%3D%3D (Pubitemid 43049538)
17. X Guo P Bandyopadhyay B Schilling MM Young N Fujii T Aynechi RK Guy ID Kuntz BW Gibson 2008 Partial acetylation of lysine residues improves intraprotein cross-linking Anal Chem 80 951 960 18201069 10.1021/ac701636w 1:CAS:528:DC%2BD1cXntlKhug%3D%3D (Pubitemid 351272324)
18. U Harndahl RB Hall KW Osteryoung E Vierling JF Bornman C Sundby 1999 The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress Cell Stress Chaperones 4 129 138 10547062 10.1379/1466-1268(1999)004<0129:TCSHSP>2.3. CO;2 1:CAS:528:DyaK1MXms1yksbk%3D (Pubitemid 29438123)
19. U Harndahl BP Kokke N Gustavsson S Linse K Berggren F Tjerneld WC Boelens C Sundby 2001 The chaperone-like activity of a small heat shock protein is lost after sulfoxidation of conserved methionines in a surface-exposed amphipathic alpha-helix Biochim Biophys Acta 1545 227 237 11342048 10.1016/S0167-4838(00) 00280-6 1:CAS:528:DC%2BD3MXpsFKltw%3D%3D (Pubitemid 32140361)
20. FU Hartl A Bracher M Hayer-Hartl 2011 Molecular chaperones in protein folding and proteostasis Nature 475 324 332 21776078 10.1038/nature10317 1:CAS:528:DC%2BC3MXpt1aqsb8%3D
21. M Haslbeck T Franzmann D Weinfurtner J Buchner 2005 Some like it hot: the structure and function of small heat-shock proteins Nat Struct Mol Biol 12 842 846 16205709 10.1038/nsmb993 1:CAS:528:DC%2BD2MXhtVKnsrjF (Pubitemid 41486706)
22. N Jaya V Garcia E Vierling 2009 Substrate binding site flexibility of the small heat shock protein molecular chaperones Proc Natl Acad Sci U S A 106 15604 15609 19717454 10.1073/pnas.0902177106 1:CAS:528:DC%2BD1MXhtFyjsLvJ
23. KK Kim R Kim SH Kim 1998 Crystal structure of a small heat-shock protein Nature 394 595 599 9707123 10.1038/29106 1:CAS:528:DyaK1cXltlyrs70%3D (Pubitemid 28366837)
24. A Laganowsky D Eisenberg 2010 Non-3D domain swapped crystal structure of truncated zebrafish alphaA crystallin Protein Sci 19 1978 1984 20669149 10.1002/pro.471 1:CAS:528:DC%2BC3cXhsFCntbrP
25. A Laganowsky JL Benesch M Landau L Ding MR Sawaya D Cascio Q Huang CV Robinson J Horwitz D Eisenberg 2010 Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function Protein Sci 19 1031 1043 20440841 10.1002/pro.380 1:CAS:528:DC%2BC3cXlsFSgtrw%3D
26. W Lambert PJ Koeck E Ahrman P Purhonen K Cheng D Elmlund H Hebert C Emanuelsson 2011 Subunit arrangement in the dodecameric chloroplast small heat shock protein Hsp21 Protein Sci 20 291 301 21280121 10.1002/pro.560 1:CAS:528:DC%2BC3MXjvFWntb8%3D
27. W Lambert CA Soderberg G Rutsdottir WC Boelens C Emanuelsson 2011 Thiol-exchange in DTSSP crosslinked peptides is proportional to cysteine content and precisely controlled in crosslink detection by two-step LC-MALDI MSMS Protein Sci 20 1682 1691 21780214 10.1002/pro.699 1:CAS:528:DC%2BC3MXhtF2isrjI
28. Lawrence AM, Besir HU (2009) Staining of proteins in gels with Coomassie G-250 without organic solvent and acetic acid. J Vis Exp pii: 1350
29. A Leitner T Walzthoeni A Kahraman F Herzog O Rinner M Beck R Aebersold 2010 Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics Mol Cell Proteomics 9 1634 1649 20360032 10.1074/mcp.R000001-MCP201 1:CAS:528:DC%2BC3cXhtlWgtLrN
30. Leitner A, Reischl R, Walzthoeni T, Herzog F, Bohn S, Foerster F, Aebersold R (2012) Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol Cell Proteomics 11(3):M111.014126
31. RA Lindner TM Treweek JA Carver 2001 The molecular chaperone alpha-crystallin is in kinetic competition with aggregation to stabilize a monomeric molten-globule form of alpha-lactalbumin Biochem J 354 79 87 11171082 10.1042/0264-6021:3540079 1:CAS:528:DC%2BD3MXhslSju78%3D (Pubitemid 32183447)
32. HS McHaourab JA Godar PL Stewart 2009 Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins Biochemistry 48 3828 3837 19323523 10.1021/bi900212j 1:CAS:528:DC%2BD1MXkt1Olsrg%3D
33. EV Mymrikov AS Seit-Nebi NB Gusev 2012 Heterooligomeric complexes of human small heat shock proteins Cell Stress Chaperones 17 157 169 22002549 10.1007/s12192-011-0296-0 1:CAS:528:DC%2BC38XitFGgsLw%3D
34. H Nakamoto L Vigh 2007 The small heat shock proteins and their clients Cell Mol Life Sci 64 294 306 17187175 10.1007/s00018-006-6321-2 1:CAS:528:DC%2BD2sXjtlSrsrY%3D
35. AJ Painter N Jaya E Basha E Vierling CV Robinson JL Benesch 2008 Real-time monitoring of protein complexes reveals their quaternary organization and dynamics Chem Biol 15 246 253 18355724 10.1016/j.chembiol.2008.01.009 1:CAS:528:DC%2BD1cXjs1Klsrg%3D (Pubitemid 351381986)
36. S Peri H Steen A Pandey 2001 GPMAW-a software tool for analyzing proteins and peptides Trends Biochem Sci 26 687 689 11701329 10.1016/S0968-0004(01) 01954-5 1:CAS:528:DC%2BD3MXotFSms78%3D
37. P Poulain JC Gelly D Flatters 2010 Detection and architecture of small heat shock protein monomers PLoS One 5 e9990 20383329 10.1371/journal.pone. 0009990
38. KK Sharma RS Kumar GS Kumar PT Quinn 2000 Synthesis and characterization of a peptide identified as a functional element in alphaA-crystallin J Biol Chem 275 3767 3771 10660525 10.1074/jbc.275.6.3767 1:CAS:528:DC%2BD3cXht12hu7o%3D (Pubitemid 30094597)
39. P Singh A Panchaud DR Goodlett 2010 Chemical cross-linking and mass spectrometry as a low-resolution protein structure determination technique Anal Chem 82 2636 2642 20210330 10.1021/ac1000724 1:CAS:528:DC%2BC3cXivV2mu7c%3D
40. A Sinz 2006 Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions Mass Spectrom Rev 25 663 682 16477643 10.1002/mas.20082 1:CAS:528: DC%2BD28XmslOqurs%3D (Pubitemid 44014105)
41. Söderberg CAG, Lambert W, Kjellström S, Wiegandt A, Peterson-Wulff R, Månsson C, Rutsdottir G, Emanuelsson C (2012) Detection of crosslinks within and between proteins by LC-MALDI-TOFTOF and the software FINDX to reduce the MSMS-data to acquire for validation. PLoS ONE 7(6):e38927
42. F Stengel AJ Baldwin AJ Painter N Jaya E Basha LE Kay E Vierling CV Robinson JL Benesch 2010 Quaternary dynamics and plasticity underlie small heat shock protein chaperone function Proc Natl Acad Sci USA 107 2007 2012 20133845 10.1073/pnas.0910126107 1:CAS:528:DC%2BC3cXhvFSnsbs%3D
43. CM Stoscheck 1990 Quantitation of protein Methods Enzymol 182 50 68 2314256 10.1016/0076-6879(90)82008-P 1:CAS:528:DyaK3MXitValsLw%3D (Pubitemid 20154379)
44. Y Sun TH MacRae 2005 The small heat shock proteins and their role in human disease FEBS J 272 2613 2627 15943797 10.1111/j.1742-4658.2005.04708.x 1:CAS:528:DC%2BD2MXlt1Cnur8%3D (Pubitemid 40825410)
45. J Tyedmers A Mogk B Bukau 2010 Cellular strategies for controlling protein aggregation Nat Rev Mol Cell Biol 11 777 788 20944667 10.1038/nrm2993 1:CAS:528:DC%2BC3cXht1yjsL3K
46. RL Van Montfort E Basha KL Friedrich C Slingsby E Vierling 2001 Crystal structure and assembly of a eukaryotic small heat shock protein Nat Struct Biol 8 1025 1030 11702068 10.1038/nsb722 (Pubitemid 33101621)