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

Molecular and Cellular Proteomics

Volumn 9, Issue 10, 2010, Pages 2306-2317

  Trnka, Michael J ^a   Burlingame, A L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 DIFORMYL 5 ETHYNYLBENZENE; ADENOSINE DIPHOSPHATE; BENZENE DERIVATIVE; CHAPERONIN; DIFORMYL ETHYNYLBENZENE; ION; PEPTIDE; PROTEIN SUBUNIT; REAGENT; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL BOND; COMPLEX FORMATION; CROSS LINKING; DISSOCIATION; ELECTRON TRANSPORT; ENERGY; GAS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTON TRANSPORT; TOPOGRAPHY;

ALKYNES; AMINO ACID SEQUENCE; BENZALDEHYDES; CHAPERONIN 10; CHAPERONIN 60; CHROMATOGRAPHY, LIQUID; CROSS-LINKING REAGENTS; ELECTRONS; MOLECULAR SEQUENCE DATA; TANDEM MASS SPECTROMETRY;

EID: 77957975473     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.003764     Document Type: Article

References (52)

1. Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F., and Yonath, A. (2000) Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102, 615-623
2. Wimberly, B. T., Brodersen, D. E., Clemons, W. M., Jr., Morgan-Warren, R. J., Carter, A. P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. (2000) Structure of the 30S ribosomal subunit. Nature 407, 327-339
3. Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000) The Complete Atomic Structure of the Large Ribosomal Subunit at 2.4 A Resolution. Science 289, 905-920
4. Robinson, C. V., Sali, A., and Baumeister, W. (2007) The molecular sociology of the cell. Nature 450, 973-982
5. 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
6. Jin Lee, Y. (2008) Mass spectrometric analysis of cross-linking sites for the structure of proteins and protein complexes. Mol. Biosyst. 4, 816-823
7. Leitner, A., Walzthoeni, T., Kahraman, A., Herzog, F., Rinner, O., Beck, M., and Aebersold, R. (2010) Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics. Mol. Cell. Proteomics 9, 1634-1649
8. Chu, F., Shan, S. O., Moustakas, D. T., Alber, F., Egea, P. F., Stroud, R. M., Walter, P., and Burlingame, A. L. (2004) Unraveling the interface of signal recognition particle and its receptor by using chemical cross-linking and tandem mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 101, 16454-16459
9. Chen, Z. A., Jawhari, A., Fischer, L., Buchen, C., Tahir, S., Kamenski, T., Rasmussen, M., Lariviere, L., Bukowski-Wills, J. C., Nilges, M., Cramer, P., and Rappsilber, J. (2010) Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J. 29, 717-726
10. Syka, J. E., Coon, J. J., Schroeder, M. J., Shabanowitz, J., and Hunt, D. F. (2004) Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 101, 9528-9533
11. Zubarev, R. A. (2004) Electron-capture dissociation tandem mass spectrometry. Curr. Opin. Biotechnol. 15, 12-16
12. Good, D. M., Wirtala, M., McAlister, G. C., and Coon, J. J. (2007) Performance characteristics of electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics 6, 1942-1951
13. Rinner, O., Seebacher, J., Walzthoeni, T., Mueller, L. N., Beck, M., Schmidt, A., Mueller, M., and Aebersold, R. (2008) Identification of cross-linked peptides from large sequence databases. Nat. Methods 5, 315-318
14. Müller, D. R., Schindler, P., Towbin, H., Wirth, U., Voshol, H., Hoving, S., and Steinmetz, M. O. (2001) Isotope-tagged cross-linking reagents. A new tool in mass spectrometric protein interaction analysis. Anal. Chem. 73, 1927-1934
15. Back, J. W., Notenboom, V., de Koning, L. J., Muijsers, A. O., Sixma, T. K., de Koster, C. G., and de Jong, L. (2002) Identification of cross-linked peptides for protein interaction studies using mass spectrometry and 18O labeling. Anal. Chem. 74, 4417-4422
16. Pearson, K. M., Pannell, L. K., and Fales, H. M. (2002) Intramolecular cross-linking experiments on cytochrome c and ribonuclease A using an isotope multiplet method. Rapid Commun. Mass Spectrom. 16, 149-159
17. Collins, C. J., Schilling, B., Young, M., Dollinger, G., and Guy, R. K. (2003) Isotopically labeled crosslinking reagents: resolution of mass degeneracy in the identification of crosslinked peptides. Bioorg. Med. Chem. Lett. 13, 4023-4026
18. Petrotchenko, E. V., Olkhovik, V. K., and Borchers, C. H. (2005) Isotopically coded cleavable cross-linker for studying protein-protein interaction and protein complexes. Mol. Cell. Proteomics 4, 1167-1179
19. Chu, F., Mahrus, S., Craik, C. S., and Burlingame, A. L. (2006) Isotope-coded and affinity-tagged cross-linking (ICATXL): an efficient strategy to probe protein interaction surfaces. J. Am. Chem. Soc. 128, 10362-10363
20. Seebacher, J., Mallick, P., Zhang, N., Eddes, J. S., Aebersold, R., and Gelb, M. H. (2006) Protein cross-linking analysis using mass spectrometry, isotope-coded cross-linkers, and integrated computational data processing. J. Proteome Res. 5, 2270-2282
21. Petrotchenko, E. V., Serpa, J. J., and Borchers, C. H. (July 9, 2010) An isotopically coded CID-cleavable biotinylated cross-linker for structural proteomics. Mol. Cell. Proteomics 10.1074/mcp.M110.001420
22. Chowdhury, S. M., Du, X., Toliæ, N., Wu, S., Moore, R. J., Mayer, M. U., Smith, R. D., and Adkins, J. N. (2009) Identification of cross-linked peptides after click-based enrichment using sequential collision-induced dissociation and electron transfer dissociation tandem mass spectrometry. Anal. Chem. 81, 5524-5532
23. Nessen, M. A., Kramer, G., Back, J., Baskin, J. M., Smeenk, L. E., de Koning, L. J., van Maarseveen, J. H., de Jong, L., Bertozzi, C. R., Hiemstra, H., and de Koster, C. G. (2009) Selective enrichment of azide-containing peptides from complex mixtures. J. Proteome Res. 8, 3702-3711
24. Yan, F., Che, F. Y., Rykunov, D., Nieves, E., Fiser, A., Weiss, L. M., and Hogue Angeletti, R. (2009) Nonprotein based enrichment method to analyze peptide cross-linking in protein complexes. Anal. Chem. 81, 7149-7159
25. Vellucci, D., Kao, A., Kaake, R. M., Rychnovsky, S. D., and Huang, L. (2010) Selective enrichment and identification of azide-tagged cross-linked peptides using chemical ligation and mass spectrometry. J. Am. Soc. Mass Spectrom. 21, 1432-1445
26. Chowdhury, S. M., Munske, G. R., Tang, X., and Bruce, J. E. (2006) Collisionally activated dissociation and electron capture dissociation of several mass spectrometry-identifiable chemical cross-linkers. Anal. Chem. 78, 8183-8193
27. Lu, Y., Tanasova, M., Borhan, B., and Reid, G. E. (2008) Ionic reagent for controlling the gas-phase fragmentation reactions of cross-linked peptides. Anal. Chem. 80, 9279-9287
28. Gardner, M. W., Vasicek, L. A., Shabbir, S., Anslyn, E. V., and Brodbelt, J. S. (2008) Chromogenic cross-linker for the characterization of protein structure by infrared multiphoton dissociation mass spectrometry. Anal. Chem. 80, 4807-4819
29. Yang, L., Tang, X., Weisbrod, C. R., Munske, G. R., Eng, J. K., von Haller, P. D., Kaiser, N. K., and Bruce, J. E. (2010) A photocleavable and mass spectrometry identifiable cross-Linker for protein interaction studies. Anal. Chem. 82, 3556-3566
30. Gardner, M. W., and Brodbelt, J. S. (2010) Preferential cleavage of N-N hydrazone bonds for sequencing bis-arylhydrazone conjugated peptides by electron transfer dissociation. Anal. Chem. 82, 5751-5759
31. Kao, A., Chiu, C., Vellucci, D., Yang, Y., Patel, V. R., Guan, S., Randall, A., Baldi, P., Rychnovsky, S. D., and Huang, L. (August 24, 2010) Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes. Mol. Cell. Proteomics 10.1074/mcp.M110.002212
32. Soderblom, E. J., Bobay, B. G., Cavanagh, J., and Goshe, M. B. (2007) Tandem mass spectrometry acquisition approaches to enhance identification of protein-protein interactions using low-energy collision-induced dissociative chemical crosslinking reagents. Rapid Commun. Mass Spectrom. 21, 3395-3408
33. Chaudhry, C., Farr, G. W., Todd, M. J., Rye, H. S., Brunger, A. T., Adams, P. D., Horwich, A. L., and Sigler, P. B. (2003) Role of the [gamma]-phosphate of ATP in triggering protein folding by GroEL-GroES: function, structure and energetics. EMBO J. 22, 4877-4887
34. Tyagi, N. K., Fenton, W. A., and Horwich, A. L. (2009) GroEL/GroES cycling: ATP binds to an open ring before substrate protein favoring protein binding and production of the native state. Proc. Natl. Acad. Sci. U.S.A. 106, 20264-20269
35. Krishna, K. A., Rao, G. V., and Rao, K. R. (2007) Chaperonin GroEL: structure and reaction cycle. Curr. Protein Pept. Sci. 8, 418-425
36. Bhagwat, S. S., Roland, D. M., Main, A. J., Gude, C., Grim, K., Goldstein, R., Cohen, D. S., Dotson, R., Mathis, J., and Lee, W. (1992) Thromboxane receptor antagonism combined with thromboxane synthase inhibition. 7. Pyridinylalkyl-substituted arylsulfonylamino arylalkanoic acids. Bioorg. Med. Chem. Lett. 2, 1623-1626 (Pubitemid 23008904)
37. Lynn, A. J., Chalkley, R. J., Baker, P. R., Medzihradszky, K. F., Guan, S., and Burlingame, A. L. (2008) The effect of peaklist generation software on database search results, in 56th ASMS Conference, Denver, June 1-5, 2008, American Society for Mass Spectrometry, Santa Fe, NM
38. Baker, P. R., Medzihradszky, K. F., and Chalkley, R. J. (2010) Improving software performance for peptide ETD data analysis by implementation of charge-state and sequence-dependent scoring. Mol. Cell. Proteomics 9, 1795-1803
39. Schilling, B., Row, R. H., Gibson, B. W., Guo, X., and Young, M. M. (2003) MS2Assign, automated assignment and nomenclature of tandem mass spectra of chemically crosslinked peptides. J. Am. Soc. Mass Spectrom. 14, 834-850
40. Chu, F., Baker, P. R., Burlingame, A. L., and Chalkley, R. J. (2010) Finding chimeras: a bioinformatics strategy for identification of cross-linked peptides. Mol. Cell. Proteomics 9, 25-31
41. Xu, Z., Horwich, A. L., and Sigler, P. B. (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388, 741-750
42. Azem, A., Weiss, C., and Goloubinoff, P. (1998) Structural analysis of GroE chaperonin complexes using chemical cross-linking. Methods Enzymol. 290, 253-268
43. Shewmaker, F., Maskos, K., Simmerling, C., and Landry, S. J. (2001) The disordered mobile loop of GroES folds into a defined β-hairpin upon binding GroEL. J. Biol. Chem. 276, 31257-31264
44. Fiaux, J., Bertelsen, E. B., Horwich, A. L., and Wüthrich, K. (2002) NMR analysis of a 900K GroEL-GroES complex. Nature 418, 207-211
45. Tang, X., and Bruce, J. E. (2010) A new cross-linking strategy: protein interaction reporter (PIR) technology for protein-protein interaction studies. Mol. Biosyst. 6, 939-947
46. Anderson, G. A., Tolic, N., Tang, X., Zheng, C., and Bruce, J. E. (2007) Informatics strategies for large-scale novel cross-linking analysis. J. Proteome Res. 6, 3412-3421
47. Zhang, H., Tang, X., Munske, G. R., Tolic, N., Anderson, G. A., and Bruce, J. E. (2009) Identification of protein-protein interactions and topologies in living cells with chemical cross-linking and mass spectrometry. Mol. Cell. Proteomics 8, 409-420
48. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A. P., Punna, T., Peregrín-Alvarez, J. M., Shales, M., Zhang, X., Davey, M., Robinson, M. D., Paccanaro, A., Bray, J. E., Sheung, A., Beattie, B., Richards, D. P., Canadien, V., Lalev, A., Mena, F., Wong, P., Starostine, A., Canete, M. M., Vlasblom, J., Wu, S., Orsi, C., Collins, S. R., Chandran, S., Haw, R., Rilstone, J. J., Gandi, K., Thompson, N. J., Musso, G., St Onge, P., Ghanny, S., Lam, M. H., Butland, G., Altaf-Ul, A. M., Kanaya, S., Shilatifard, A., O'Shea, E., Weissman, J. S., Ingles, C. J., Hughes, T. R., Parkinson, J., Gerstein, M., Wodak, S. J., Emili, A., and Greenblatt, J. F. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643
49. Hutchins, J. R., Toyoda, Y., Hegemann, B., Poser, I., Hériché, J. K., Sykora, M. M., Augsburg, M., Hudecz, O., Buschhorn, B. A., Bulkescher, J., Conrad, C., Comartin, D., Schleiffer, A., Sarov, M., Pozniakovsky, A., Slabicki, M. M., Schloissnig, S., Steinmacher, I., Leuschner, M., Ssykor, A., Lawo, S., Pelletier, L., Stark, H., Nasmyth, K., Ellenberg, J., Durbin, R., Buchholz, F., Mechtler, K., Hyman, A. A., and Peters, J. M. (2010) Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 328, 593-599
50. Scott, J. D., and Pawson, T. (2009) Cell signaling in space and time: where proteins come together and when they're apart. Science 326, 1220-1224
51. Ewing, R. M., Chu, P., Elisma, F., Li, H., Taylor, P., Climie, S., McBroom-Cerajewski, L., Robinson, M. D., O'Connor, L., Li, M., Taylor, R., Dharsee, M., Ho, Y., Heilbut, A., Moore, L., Zhang, S., Ornatsky, O., Bukhman, Y. V., Ethier, M., Sheng, Y., Vasilescu, J., Abu-Farha, M., Lambert, J. P., Duewel, H. S., Stewart, I. I., Kuehl, B., Hogue, K., Colwill, K., Gladwish, K., Muskat, B., Kinach, R., Adams, S. L., Moran, M. F., Morin, G. B., Topaloglou, T., and Figeys, D. (2007) Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol. Syst. Biol. 3, 89
52. Wells, J. A., and McClendon, C. L. (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450, 1001-1009