In vivo protein interaction network identified with a novel real-time cross-linked peptide identification strategy

Journal of Proteome Research

Volumn 12, Issue 4, 2013, Pages 1569-1579

  Weisbrod, Chad R ^a   Chavez, Juan D ^a   Eng, Jimmy K ^a   Yang, Li ^a   Zheng, Chunxiang ^a   Bruce, James E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cross linking; FTICR MS; in vivo protein interactions; PIR; protein interaction reporter; protein interaction topologies; real time MS strategy; XL MS

Indexed keywords

ARTICLE; BACTERIAL CELL; ESCHERICHIA COLI; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REAL TIME ANLYSIS FOR CROSS LINKED PEPTIDE TECHNOLOGY;

ALGORITHMS; AMINO ACID SEQUENCE; CROSS-LINKING REAGENTS; ESCHERICHIA COLI; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN INTERACTION MAPPING;

EID: 84875913034     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3011638     Document Type: Article

References (41)

1. Ellis, R. J. Macromolecular crowding: obvious but underappreciated Trends Biochem. Sci. 2001, 26 (10) 597-604
2. Dedmon, M. M.; Patel, C. N.; Young, G. B.; Pielak, G. J. FlgM gains structure in living cells Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (20) 12681-4
3. Ikeya, T.; Sasaki, A.; Sakakibara, D.; Shigemitsu, Y.; Hamatsu, J.; Hanashima, T.; Mishima, M.; Yoshimasu, M.; Hayashi, N.; Mikawa, T.; Nietlispach, D.; Walchli, M.; Smith, B. O.; Shirakawa, M.; Guntert, P.; Ito, Y. NMR protein structure determination in living E. coli cells using nonlinear sampling Nat. Protoc. 2010, 5 (6) 1051-60
4. Robinson, K. E.; Reardon, P. N.; Spicer, L. D. In-cell NMR spectroscopy in Escherichia coli Methods Mol. Biol. 2012, 831, 261-77
5. Sugase, K.; Dyson, H. J.; Wright, P. E. Mechanism of coupled folding and binding of an intrinsically disordered protein Nature 2007, 447 (7147) 1021-5
6. Tompa, P.; Fuxreiter, M. Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions Trends Biochem. Sci. 2008, 33 (1) 2-8
7. Chavez, J. D.; Liu, N. L.; Bruce, J. E. Quantification of protein-protein interactions with chemical cross-linking and mass spectrometry J. Proteome Res. 2011, 10 (4) 1528-37
8. Leitner, A.; Walzthoeni, T.; Kahraman, A.; Herzog, F.; Rinner, O.; Beck, M.; Aebersold, R. Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics Mol. Cell. Proteomics 2010, 9 (8) 1634-49
9. Rappsilber, J.; Siniossoglou, S.; Hurt, E. C.; Mann, M. A generic strategy to analyze the spatial organization of multi-protein complexes by cross-linking and mass spectrometry Anal. Chem. 2000, 72 (2) 267-75
10. Rinner, O.; Seebacher, J.; Walzthoeni, T.; Mueller, L. N.; Beck, M.; Schmidt, A.; Mueller, M.; Aebersold, R. Identification of cross-linked peptides from large sequence databases Nat. Methods 2008, 5 (4) 315-8
11. Singh, P.; Shaffer, S. A.; Scherl, A.; Holman, C.; Pfuetzner, R. A.; Larson Freeman, T. J.; Miller, S. I.; Hernandez, P.; Appel, R. D.; Goodlett, D. R. Characterization of protein cross-links via mass spectrometry and an open-modification search strategy Anal. Chem. 2008, 80 (22) 8799-806
12. Tang, X.; Bruce, J. E. Chemical cross-linking for protein-protein interaction studies Methods Mol. Biol. 2009, 492, 283-93
13. Tang, X.; Bruce, J. E. A new cross-linking strategy: protein interaction reporter (PIR) technology for protein-protein interaction studies Mol. Biosyst. 2011, 6 (6) 939-47
14. 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 (1) 311-8
15. 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.; Rappsilber, J. Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry EMBO J. 2010, 29 (4) 717-26
16. Herzog, F.; Kahraman, A.; Boehringer, D.; Mak, R.; Bracher, A.; Walzthoeni, T.; Leitner, A.; Beck, M.; Hartl, F. U.; Ban, N.; Malmstrom, L.; Aebersold, R. Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry Science 2012, 337 (6100) 1348-52
17. Karadzic, I.; Maupin-Furlow, J.; Humbard, M.; Prunetti, L.; Singh, P.; Goodlett, D. R. Chemical cross-linking, mass spectrometry, and in silico modeling of proteasomal 20S core particles of the haloarchaeon Haloferax volcanii Proteomics 2012, 12 (11) 1806-14
18. Maiolica, A.; Cittaro, D.; Borsotti, D.; Sennels, L.; Ciferri, C.; Tarricone, C.; Musacchio, A.; Rappsilber, J. Structural analysis of multiprotein complexes by cross-linking, mass spectrometry, and database searching Mol. Cell. Proteomics 2007, 6 (12) 2200-11
19. Zhang, H.; Tang, X.; Munske, G. R.; Tolic, N.; Anderson, G. A.; Bruce, J. E. Identification of protein-protein interactions and topologies in living cells with chemical cross-linking and mass spectrometry Mol. Cell. Proteomics 2009, 8 (3) 409-20
20. Zheng, C.; Yang, L.; Hoopmann, M. R.; Eng, J. K.; Tang, X.; Weisbrod, C. R.; Bruce, J. E. Cross-linking measurements of in vivo protein complex topologies Mol. Cell. Proteomics 2011, 10 (10) M110.006841
21. Yang, L.; Zheng, C.; Weisbrod, C. R.; Tang, X.; Munske, G. R.; Hoopmann, M. R.; Eng, J. K.; Bruce, J. E. In vivo application of photocleavable protein interaction reporter technology J. Proteome Res. 2012, 11 (2) 1027-41
22. Anderson, G. A.; Tolic, N.; Tang, X.; Zheng, C.; Bruce, J. E. Informatics strategies for large-scale novel cross-linking analysis J. Proteome Res. 2007, 6 (9) 3412-21
23. Hoopmann, M. R.; Weisbrod, C. R.; Bruce, J. E. Improved strategies for rapid identification of chemically cross-linked peptides using protein interaction reporter technology J. Proteome Res. 2010, 9 (12) 6323-33
24. Merrifield, R. B. Solid-phase peptide synthesis. 3. An improved synthesis of bradykinin Biochemistry 1964, 3, 1385-90
25. Sieber, P. A new acid-labile anchor group for the solid-phase synthesis of C-terminal peptide amides by the Fmoc method Tetrahedron Lett. 1987, 28 (19) 2107-2110
26. Katritzky, A. R.; Yang, B.; Qiu, G.; Zhang, Z. ChemInform abstract: A convenient trifluoroacetylation reagent: N-(Trifluoroacetyl)succinimide ChemInform 1999, 30 (19) no-no
27. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4 (3) 207-14
28. Swaney, D. L.; McAlister, G. C.; Coon, J. J. Decision tree-driven tandem mass spectrometry for shotgun proteomics Nat. Methods 2008, 5 (11) 959-64
29. Graumann, J.; Scheltema, R. A.; Zhang, Y.; Cox, J.; Mann, M. A framework for intelligent data acquisition and real-time database searching for shotgun proteomics Mol. Cell. Proteomics 2012, 11 (3) M111 013185
30. Paramelle, D.; Miralles, G.; Subra, G.; Martinez, J. Chemical cross-linkers for protein structure studies by mass spectrometry Proteomics 2012, 13, 438-56
31. Liu, F.; Wu, C.; Sweedler, J. V.; Goshe, M. B. An enhanced protein crosslink identification strategy using CID-cleavable chemical crosslinkers and LC/MS(n) analysis Proteomics 2012, 12 (3) 401-5
32. Tabb, D. L.; Vega-Montoto, L.; Rudnick, P. A.; Variyath, A. M.; Ham, A. J.; Bunk, D. M.; Kilpatrick, L. E.; Billheimer, D. D.; Blackman, R. K.; Cardasis, H. L.; Carr, S. A.; Clauser, K. R.; Jaffe, J. D.; Kowalski, K. A.; Neubert, T. A.; Regnier, F. E.; Schilling, B.; Tegeler, T. J.; Wang, M.; Wang, P.; Whiteaker, J. R.; Zimmerman, L. J.; Fisher, S. J.; Gibson, B. W.; Kinsinger, C. R.; Mesri, M.; Rodriguez, H.; Stein, S. E.; Tempst, P.; Paulovich, A. G.; Liebler, D. C.; Spiegelman, C. Repeatability and reproducibility in proteomic identifications by liquid chromatography-tandem mass spectrometry J. Proteome Res. 2010, 9 (2) 761-76
33. Zheng, C.; Weisbrod, C. R.; Chavez, J. D.; Eng, J. K.; Sharma, V.; Wu, X.; Bruce, J. E. CrossLink-DB: Database and software tools for storing and visualizing protein interaction topology data. J. Proteome Res. 2012, in press.
34. Yu, N. Y.; Wagner, J. R.; Laird, M. R.; Melli, G.; Rey, S.; Lo, R.; Dao, P.; Sahinalp, S. C.; Ester, M.; Foster, L. J.; Brinkman, F. S. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes Bioinformatics 2010, 26 (13) 1608-15
35. Walzthoeni, T.; Claassen, M.; Leitner, A.; Herzog, F.; Bohn, S.; Forster, F.; Beck, M.; Aebersold, R. False discovery rate estimation for cross-linked peptides identified by mass spectrometry Nat. Methods 2012, 9, 901-3
36. Yang, B.; Wu, Y. J.; Zhu, M.; Fan, S. B.; Lin, J.; Zhang, K.; Li, S.; Chi, H.; Li, Y. X.; Chen, H. F.; Luo, S. K.; Ding, Y. H.; Wang, L. H.; Hao, Z.; Xiu, L. Y.; Chen, S.; Ye, K.; He, S. M.; Dong, M. Q. Identification of cross-linked peptides from complex samples Nat. Methods 2012, 9, 904-6
37. Chavez, J. D.; Cilia, M.; Weisbrod, C. R.; Ju, H. J.; Eng, J. K.; Gray, S. M.; Bruce, J. E. Cross-linking measurements of the Potato leafroll virus reveal protein interaction topologies required for virion stability, aphid transmission, and virus-plant interactions J. Proteome Res. 2012, 11, 2968-81
38. Ban, N.; Nissen, P.; Hansen, J.; Moore, P. B.; Steitz, T. A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution Science 2000, 289 (5481) 905-20
39. Voorhees, R. M.; Weixlbaumer, A.; Loakes, D.; Kelley, A. C.; Ramakrishnan, V. Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome Nat. Struct. Mol. Biol. 2009, 16 (5) 528-33
40. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-58
41. Leitner, A.; Reischl, R.; Walzthoeni, T.; Herzog, F.; Bohn, S.; Forster, F.; Aebersold, R. Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography Mol. Cell. Proteomics 2012, 11 (3) M111.014126