Selective enrichment and identification of cross-linked peptides to study 3-D structures of protein complexes by mass spectrometry

Journal of Proteomics

Volumn 75, Issue 7, 2012, Pages 2205-2215

  Buncherd, Hansuk ^a   Nessen, Merel A ^a   Nouse, Niels ^a   Stelder, Sacha K ^a   Roseboom, Winfried ^a   Dekker, Henk L ^a   Arents, Jos C ^a   Smeenk, Linde E ^b   Wanner, Martin J ^b   van Maarseveen, Jan H ^b   Yang, Xiao ^c   Lewis, Peter J ^c   de Koning, Leo J ^a   de Koster, Chris G ^a   de Jong, Luitzen ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Click chemistry; Mass spectrometry; Protein cross linking; RNA polymerase

Indexed keywords

AZIDE; BIS(SUCCINIMIDYL) 3 AZIDOMETHYL GLUTARATE; CYCLOOCTYNE; RESIN; RNA POLYMERASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CHEMICAL REACTION; CONJUGATION; FRAGMENTATION REACTION; ION EXCHANGE CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TANDEM MASS SPECTROMETRY; THREE DIMENSIONAL IMAGING;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CROSS-LINKING REAGENTS; DATABASES, PROTEIN; DNA-DIRECTED RNA POLYMERASES; MASS SPECTROMETRY; MODELS, MOLECULAR; PEPTIDES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN;

BACILLUS SUBTILIS;

EID: 84862782006     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.01.025     Document Type: Article

References (55)

1. Back J.W., de Jong L., Muijsers A.O., de Koster C.G. Chemical cross-linking and mass spectrometry for protein structural modeling. J Mol Biol 2003, 331:303-313.
2. Back J.W., Sanz M.A., De Jong L., De Koning L.J., Nijtmans L.G., De Koster C.G., et al. A structure for the yeast prohibitin complex: Structure prediction and evidence from chemical crosslinking and mass spectrometry. Protein Sci 2002, 11:2471-2478.
3. Lee Y.J. Mass spectrometric analysis of cross-linking sites for the structure of proteins and protein complexes. Mol Biosyst 2008, 4:816-823.
4. Leitner A., Walzthoeni T., Kahraman A., Herzog F., Rinner O., Beck M., et al. Probing native protein structures by chemical cross-linking, mass spectrometry and bioinformatics. Mol Cell Proteomics 2010, 9:1634-1649.
5. Rappsilber J. The beginning of a beautiful friendship: cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. J Struct Biol 2010, 173:530-540.
6. Sinz A. Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions. Mass Spectrom Rev 2006, 25:663-682.
7. Petrotchenko E.V., Borchers C.H. Crosslinking combined with mass spectrometry for structural proteomics. Mass Spectrom Rev 2010, 29:862-876.
8. Fabris D., Yu E.T. Elucidating the higher-order structure of biopolymers by structural probing and mass spectrometry: MS3D. J Mass Spectrom 2010, 45:841-860.
9. van Dijk A.D., Boelens R., Bonvin A.M. Data-driven docking for the study of biomolecular complexes. FEBS J 2005, 272:293-312.
10. Schilling B., Row R.H., Gibson B.W., Guo X., Young M.M. MS2Assign, automated assignment and nomenclature of tandem mass spectra of chemically crosslinked peptides. J Am Soc Mass Spectrom 2003, 14:834-850.
11. Rinner O., Seebacher J., Walzthoeni T., Mueller L., Beck M., Schmidt A., et al. Identification of cross-linked peptides from large sequence databases. Nat Methods 2008, 5:315-318.
12. Crimmins D.L. Strong cation-exchange high-performance liquid chromatography as a versatile tool for the characterization and purification of peptides. Anal Chim Acta 1997, 352:21-30.
13. Lauber M.A., Reilly J.P. Novel amidinating cross-linker for facilitating analyses of protein structures and interactions. Anal Chem 2011, 82:7736-7743.
14. Lauber M.A., Reilly J.P. Structural analysis of a prokaryotic ribosome using a novel amidinating cross-linker and mass spectrometry. J Proteome Res 2011, 10:3604-3616.
15. Yan F., Che F.Y., Nieves E., Weiss L.M., Angeletti R.H., Fiser A. Photo-assisted peptide enrichment in protein complex cross-linking analysis of a model homodimeric protein using mass spectrometry. Proteomics 2011, 11:4109-4115.
16. Chowdhury S.M., Du X., Tolic N., Wu S., Moore R.J., Mayer M.U., et al. Identification of cross-linked peptides after click-based enrichment using sequential collision-induced dissociation and electron transfer dissociation tandem mass spectrometry. Anal Chem 2009, 81:5524-5532.
17. Kang S., Mou L., Lanman J., Velu S., Brouillette W.J., Prevelige P.E. Synthesis of biotin-tagged chemical cross-linkers and their applications for mass spectrometry. Rapid Commun Mass Spectrom 2009, 23:1719-1726.
18. Sinz A., Kalkhof S., Ihling C. Mapping protein interfaces by a trifunctional cross-linker combined with MALDI-TOF and ESI-FTICR mass spectrometry. J Am Soc Mass Spectrom 2005, 16:1921-1931.
19. Trester-Zedlitz M., Kamada K., Burley S.K., Fenyo D., Chait B.T., Muir T.W. A modular cross-linking approach for exploring protein interactions. J Am Chem Soc 2003, 125:2416-2425.
20. Vellucci D., Kao A., Kaake R.M., Rychnovsky S.D., Huang L. Selective enrichment and identification of azide-tagged cross-linked peptides using chemical ligation and mass spectrometry. J Am Soc Mass Spectrom 2010, 21:1432-1445.
21. Petrotchenko E.V., Serpa J.J., Borchers C.H. An isotopically coded CID-cleavable biotinylated cross-linker for structural proteomics. Mol Cell Proteomics 2010, 10. M110.001420.
22. Kasper P.T., Back J.W., Vitale M., Hartog A.F., Roseboom W., de Koning L.J., et al. An aptly positioned azido group in the spacer of a protein cross-linker for facile mapping of lysines in close proximity. Chembiochem 2007, 8:1281-1292.
23. Tang X., Munske G.R., Siems W.F., Bruce J.E. Mass spectrometry identifiable cross-linking strategy for studying protein-protein interactions. Anal Chem 2005, 77:311-318.
24. Zheng C., Yang L., Hoopmann M.R., Eng J.K., Tang X., Weisbrod C.R., et al. Cross-linking measurements of in vivo protein complex topologies. Mol Cell Proteomics 2011, 10. M110.006841.
25. Nessen M.A., Kramer G., Back J., Baskin J.M., Smeenk L.E., de Koning L.J., et al. Selective Enrichment of Azide-Containing Peptides from Complex Mixtures. J Proteome Res 2009, 8:3702-3711.
26. Schultz M.K., Parameswarappa S.G., Pigge F.C. Synthesis of a DOTA-biotin conjugate for radionuclide chelation via Cu-free click chemistry. Org Lett 2010, 12:2398-2401.
27. Sletten E.M., Bertozzi C.R. A hydrophilic azacyclooctyne for Cu-free click chemistry. Org Lett 2008, 10:3097-3099.
28. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985, 150:76-85.
29. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
30. Yang X., Lewis P.J. Overproduction and purification of recombinant Bacillus subtilis RNA polymerase. Protein Expr Purif 2008, 59:86-93.
31. Zagorski M.G., Yang J., Shao H., Ma K., Zeng H., Hong A. Methodological and chemical factors affecting amyloid beta peptide amyloidogenicity. Methods Enzymol 1999, 309:189-204.
32. Maiolica A., Cittaro D., Borsotti D., Sennels L., Ciferri C., Tarricone C., et al. Structural analysis of multiprotein complexes by cross-linking, mass spectrometry, and database searching. Mol Cell Proteomics 2007, 6:2200-2211.
33. Panchaud A., Singh P., Shaffer S.A., Goodlett D.R. xComb: a cross-linked peptide database approach to protein-protein interaction analysis. J Proteome Res 2010, 9:2508-2515.
34. MacDougall I.J., Lewis P.J., Griffith R. Homology modelling of RNA polymerase and associated transcription factors from Bacillus subtilis. J Mol Graph Model 2005, 23:297-303.
35. Zhang G., Campbell E.A., Minakhin L., Richter C., Severinov K., Darst S.A. Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 A resolution. Cell 1999, 98:811-824.
36. Back J.W., David O., Kramer G., Masson G., Kasper P.T., de Koning L.J., et al. Mild and chemoselective peptide-bond cleavage of peptides and proteins at azido homoalanine. Angew Chem Int Ed Engl 2005, 44:7946-7950.
37. Madler S., Bich C., Touboul D., Zenobi R. Chemical cross-linking with NHS esters: a systematic study on amino acid reactivities. J Mass Spectrom 2009, 44:694-706.
38. Davis C.A., Bingman C.A., Landick R., Record M.T., Saecker R.M. Real-time footprinting of DNA in the first kinetically significant intermediate in open complex formation by Escherichia coli RNA polymerase. Proc Natl Acad Sci U S A 2007, 104:7833-7838.
39. Darst S.A., Opalka N., Chacon P., Polyakov A., Richter C., Zhang G., et al. Conformational flexibility of bacterial RNA polymerase. Proc Natl Acad Sci U S A 2002, 99:4296-4301.
40. Yang X., Molimau S., Doherty G.P., Johnston E.B., Marles-Wright J., Rothnagel R., et al. The structure of bacterial RNA polymerase in complex with the essential transcription elongation factor NusA. EMBO Rep 2009, 10:997-1002.
41. Kontur W.S., Saecker R.M., Davis C.A., Capp M.W., Record M.T. Solute probes of conformational changes in open complex (RPo) formation by Escherichia coli RNA polymerase at the lambdaPR promoter: evidence for unmasking of the active site in the isomerization step and for large-scale coupled folding in the subsequent conversion to RPo. Biochemistry 2006, 45:2161-2177.
42. Chen Z.A., Jawhari A., Fischer L., Buchen C., Tahir S., Kamenski T., et al. Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J 2010, 29:717-726.
43. Bohn S., Beck F., Sakata E., Walzthoeni T., Beck M., Aebersold R., et al. Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc Natl Acad Sci U S A 2010, 107:20992-20997.
44. Kao A., Chiu C.L., Vellucci D., Yang Y., Patel V.R., Guan S., et al. Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes. Mol Cell Proteomics 2010, 10. M110.002212.
45. Trnka M.J., Burlingame A.L. Topographic studies of the GroEL-GroES chaperonin complex by chemical cross-linking using diformyl ethynylbenzene: the power of high resolution electron transfer dissociation for determination of both peptide sequences and their attachment sites. Mol Cell Proteomics 2010, 9:2306-2317.
46. Arshady R. Development of new hydrophilic polymer supports based on dimethylacrylamide. Colloid Polym Sci 1990, 268:948-958.
47. Back J.W., Notenboom V., de Koning L.J., Muijsers A.O., Sixma T.K., de Koster C.G., et al. Identification of cross-linked peptides for protein interaction studies using mass spectrometry and 18O labeling. Anal Chem 2002, 74:4417-4422.
48. Mirgorodskaya O.A., Kozmin Y.P., Titov M.I., Korner R., Sonksen C.P., Roepstorff P. Quantitation of peptides and proteins by matrix-assisted laser desorption/ionization mass spectrometry using (18)O-labeled internal standards. Rapid Commun Mass Spectrom 2000, 14:1226-1232.
49. Wang Y.K., Ma Z., Quinn D.F., Fu E.W. Inverse 18O labeling mass spectrometry for the rapid identification of marker/target proteins. Anal Chem 2001, 73:3742-3750.
50. Yao X., Freas A., Ramirez J., Demirev P.A., Fenselau C. Proteolytic 18O labeling for comparative proteomics: model studies with two serotypes of adenovirus. Anal Chem 2001, 73:2836-2842.
51. Yang X., Lewis P.J. The interaction between bacterial transcription factors and RNA polymerase during the transition from initiation to elongation. Transcription 2011, 1:66-69.
52. Syka J.E., Coon J.J., Schroeder M.J., Shabanowitz J., Hunt D.F. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc Natl Acad Sci U S A 2004, 101:9528-9533.
53. Santos L.F., Eberlin M.N., Gozzo F.C. IRMPD and ECD fragmentation of intermolecular cross-linked peptides. J Mass Spectrom 2011, 46:262-268.
54. Zubarev R.A., Kelleher N.L., McLafferty F.W. Electron capture dissociation of multiply charged protein cations. A nonergodic process. J Am Chem Soc 1998, 120:3265-3266.
55. Little D.P., Speir J.P., Senko M.W., O'Connor P.B., McLafferty F.W. Infrared multiphoton dissociation of large multiply charged ions for biomolecule sequencing. Anal Chem 1994, 66:2809-2815.