Catch me if you can: Challenges and applications of cross-linking approaches

European Journal of Mass Spectrometry

Volumn 20, Issue 1, 2014, Pages 99-116

  Tinnefeld, Verena ^a   Sickmann, Albert ^a,b   Ahrends, Robert ^a  

^a LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Analysis software; Chemical cross linking; Cross linking; Cross linking reagents; Mass spectrometry; Metabolic cross linking; Protein interaction; Structural proteomics

Indexed keywords

APPLICATION PROGRAMS; BIOCHEMISTRY; CELL SIGNALING; CHEMICAL ANALYSIS; CROSSLINKING; ENERGY TRANSFER; MASS SPECTROMETRY; METABOLISM; MOLECULAR BIOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS;

ANALYSIS SOFTWARES; CHEMICAL CROSS-LINKING; CROSS-LINKING REAGENTS; PROTEIN INTERACTION; PROTEOMICS;

X RAY CRYSTALLOGRAPHY;

CROSS LINKING REAGENT; PROTEIN; RNA;

ARTICLE; CHEMISTRY; HUMAN; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; PROTEIN BINDING; PROTEOMICS;

CROSS-LINKING REAGENTS; HUMANS; MASS SPECTROMETRY; PROTEIN BINDING; PROTEINS; PROTEOMICS; RNA;

EID: 84902350024     PISSN: None     EISSN: 17516838     Source Type: Journal    
DOI: 10.1255/ejms.1259     Document Type: Article

References (131)

1. M. Karas and F. Hillenkamp, "Laser desorption ionization of proteins with molecular masses exceeding 10, 000 Daltons", Anal. Chem. 60, 2299 (1988). http://dx.doi.org/10.1021/ac00171a028
2. J.B. Fenn, M. Mann, C.K. Meng, S.F. Wong and C.M. Whitehouse, "Electrospray ionization for mass spectrometryof large biomolecules", Science 246, 64-71 (1989). http://dx.doi.org/10.1126/science.2675315
3. G.E. Davies and G.R. Stark, "Use of dimethyl suberimidate, a cross-linking reagent, in studying the subunit structure of oligomeric proteins", Proc. Natl Acad. Sci. USA 66, 651 (1970). http://dx.doi.org/10. 1073/pnas.66.3.651
4. B. Schilling, R.H. Row, B.W. Gibson, X. Guo and M.M. Young, "MS2Assign, automated assignment and nomenclature of tandem mass spectra of chemically crosslinked peptides", J. Am. Soc. Mass Spectrom. 14, 834 (2003). http://dx.doi.org/10.1016/S1044- 0305(03)00327-1
5. M. Fioramonte, A.M. dos Santos, S. McIlwain, W.S. Noble, K.G. Franchini and F.C. Gozzo, "Analysis of secondarystructure in proteins by chemical cross?linking coupled to MS", Proteomics 12, 2746 (2012). http://dx.doi.org/10.1002/pmic.201200040
6. P. Friedhoff, "Mapping protein-protein interactions by bioinformatics and cross-linking", Anal. Bioanal. Chem. 381, 78 (2005). http://dx.doi.org/10.1007/s00216-004- 2892-7
7. X. Du, S.M. Chowdhury, N.P. Manes, S. Wu, M.U. Mayer, J.N. Adkins, G.A. Anderson and R.D. Smith, "Xlinkidentifier: an automated data analysis platformfor confidentidentifications of chemically cross-linked peptides using tandem mass spectrometry", J. Proteome Res. 10, 923 (2011). http://dx.doi.org/10.1021/pr100848a
8. P. Singh, A. Panchaud and D.R. Goodlett, "Chemical cross-linking and mass spectrometry as a lowresolutionprotein structure determination technique", Anal. Chem. 82, 2636 (2010). http://dx.doi.org/10.1021/ ac1000724
9. R. Ahrends, J. Kosinski, D. Kirsch, L. Manelyte, L. Giron-Monzon, L. Hummerich, O. Schulz, B. Spengler and P. Friedhoff, "Identifying an interaction site between MutH and the C-terminal domain of MutL by crosslinking, affinity purification, chemical coding and mass spectrometry", Nucleic Acids Res. 34, 3169 (2006). http://dx.doi.org/10.1093/nar/gkl407
10. The pyMol Molecular Graphics System, Version 1.5.0.4, Schrödinger, LLC.
11. A. Kahraman, L. Malmstrom and R. Aebersold, "Xwalk: computing and visualizing distances in cross-linking experiments", Bioinformatics 27, 2163 (2011). http://dx.doi.org/10.1093/bioinformatics/btr348
12. L. Giron-Monzon, L. Manelyte, R. Ahrends, D. Kirsch, B. Spengler and P. Friedhoff, "Mapping protein-proteininteractions between MutL and MutH by crosslinking", J. Biol. Chem. 278, 49338 (2004). http://dx.doi.org/10.1074/ jbc.M409307200
13. J.E. Bruce, "In vivo protein complex topologies: sights through a cross-linking lens", Proteomics 12, 1565 (2012). http://dx.doi.org/10.1002/ pmic.201100516
14. D. Fabris and E.T. Yu, "Elucidating the higher-order structure of biopolymers by structural probing and mass spectrometry: MS3D", J. Mass Spectrom. 45, 841 (2010). http://dx.doi.org/10.1002/jms.1762
15. J. Vasilescu, X. Guo and J. Kast, "Identification of protein- protein interactions using in vivo cross-linking and mass spectrometry", Proteomics 4, 3845 (2004). http://dx.doi.org/10.1002/pmic.200400856
16. C. Zheng, L. Xang, M.R. Hoopmann, J.K. Eng, X. Tang, C.R. Weisbrod and J.E. Bruce, "Cross-linking measurementsof in vivo protein complex topologies", Mol. Cell. Proteomics 10 M 110.0068M(2001).
17. H. Baruah, S. Puthenveetil, Y.-A. Choi, S. Shah and A.Y. Ting, "An engineered aryl azide ligase for site-specific mapping of protein-protein interactions trough photocross- linking", Angew. Chem. Int. Ed. 47, 7018 (2008). http://dx.doi.org/10.1002/anie.200802088
18. Y.J. Lee, "Mass spectrometric analysis of crosslinking sites for the structure of proteins and proteincomplexes", Mol. BioSyst. 4, 816 (2008). http://dx.doi.org/10.1039/b801810c
19. G.H. Kruppa, J. Schoeniger and M.M. Young, "A top down approach to protein structural studies using chemical cross-linking and Fourier transform mass spectrometry", Rapid Commun. Mass Spectrom. 17, 155 (2003). http://dx.doi.org/10.1002/rcm.885
20. J.M. Burkhart, C. Schumbrutzki, S. Wortelkamp, A. Sickmann and R.P. Zahedi, "Systematic and quantitative comparison of digest efficiency and specificity reveals the impact of trypsin quality on MS-based proteomics", J. Proteomics 75, 1454 (2012). http://dx.doi.org/10.1016/j.jprot.2011.11.016
21. M.J. Raftery and C.L. Geczy, "Electrospray low energy CID and MALDI PSD fragmentations of protonated sulfinamide cross-linked peptides", J. Am. Soc. Mass Spectrom. 13, 709 (2002). http://dx.doi.org/10.1016/S1044-0305(02) 00359-8
22. M.D. Person, K.C. Brown, S. Mahrus, C.S. Craik, and A.L. Burlingame, "Novel inter-protein cross-link identifiedin the GGH-ecotin D137Y dimer", Protein Sci. 10, 1549 (2001). http://dx.doi.org/10.1110/ps.ps.46601
23. J.V. Staros and B.P. Kakkad, "Cross-linking and chymotryptic digestion of the extracytoplasmic domain of the anion exchange channel in intact human erythrocytes", J. Membr. Biol. 74, 247 (1983). http://dx.doi.org/10. 1007/BF02332127
24. D.T. Cheung and M.E. Nimni, "Mechanism of crosslinking of proteins by glutaraldehyde II. Reaction with monomeric and polymeric collagen", Connect Tissue Res. 10, 201 (1982). http://dx.doi.org/10.3109/03008208209034419
25. M. Trester-Zedlitz, K. Kamada, S.K. Burley, D., Fenyö, B.T. Chait, B.T. and T.W. Muir, "A modular cross-linking approach for exploring protein interactions", J. Am. Chem. Soc. 125, 2416 (2003). http://dx.doi.org/10. 1021/ja026917a
26. M.M. Young, N. Tang, J.C. Hempel, C.M. Oshiro, E.W. Taylor, I.D. Kuntz, B.W. Gibson and G. Dollinger, "High throughput protein fold identification by using experimental constraints derived from intramolecular cross-links and mass spectrometry", Proc. Natl Acad. Sci. USA 97, 5802 (2000). http://dx.doi.org/10.1073/pnas.090099097
27. R. Fritzsche, C.H. Ihling, M. Gotze and A. Sinz, "Optimizing the enrichment of cross-linked productsfor mass spectrometric protein analysis", Rapid Commun. Mass Spectrom. 26, 653 (2012). http://dx.doi.org/10.1002/rcm.6150
28. J.J. Serpa, A.P. Patterson, J. Pan, J. Han, D.S. Wishart, E.V. Petrotchenko and C.H. Borchers, "Using multiple structural proteomics approaches for the characterization of prion proteins", J. Proteomics 81, 31 (2013). http://dx.doi.org/10.1016/j.jprot.2012.10.008
29. M. Liu, Z. Zhang, T. Zang, C. Spahr, J. Cheetham, D. Ren and Z.S. Zhou, "Discovery of undefined protein cross-linking chemistry: a comprehensive methodology utilizing 18O-labeling and mass spectrometry", Anal. Chem. 85, 5900 (2013). http://dx.doi.org/10.1021/ac400666p
30. H. Zhang and Y. Ge, "Comprehensive analysis of proteinmodifications by top-down mass spectrometry", Circ. Cardiovasc. Genet. 4, 711 (2011). http://dx.doi.org/10.1161/CIRCGENETICS.110.957829
31. H. Hernández and C.V. Robinson, "Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry", Nature Protocols 2, 715 (2007). http://dx.doi.org/10.1038/ nprot.2007.73
32. K.R. Durbin, J.C. Tran, L. Zamdborg, S.M. Sweet, A.D. Catherman, J.E. Lee, M. Li, J.F. Kellie and N.L. Kelleher, "Intact mass detection, interpretation, and visualization to automate top-down proteomics on a large scale", Proteomics 10, 3589 (2010). http://dx.doi.org/10.1002/pmic. 201000177
33. Hermanson, Bioconjugate Techniques 2nd edn. Elsevier, San Diego (2008).
34. A. Sinz, "Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions", Mass Spectrom. Rev. 25, 663 (2006). http://dx.doi.org/10.1002/mas.20082
35. C. Tagwerker, K. Flick, M. Cui, C. Guerro, Y. Dou, B. Auer, P. Baldi, L. Huang and P.A. Kaiser, "A tandemaffinity tag for two-step purification under fully denaturingconditions: application in ubiquitin profilingand protein complex identification combined with in vivo cross-linking", Mol. Cell. Proteomics 5, 737 (2006). http://dx.doi.org/10.1074/mcp.M500368- MCP200
36. B.L. Simons, M.C. King, T. Cyr, M.A. Hefford H. and H. Kaplan, "Covalent cross-linking of proteins without chemical reagents", Protein Sci. 11, 1558 (2002). http://dx.doi.org/10.1110/ps.4390102
37. D. Li, H.Y. Tang and D.W. Speicher, "A structural model of the erythrocyte spectrin homodimer initiation site determined using homology modeling and chemical cross-linking", J. Biol. Chem. 283, 1553 (2008). http://dx.doi.org/10.1074/jbc.M706981200
38. H. Zhang, X. Tang, G.R. Munske, N. Tolic, G.S. Anderson and J.E. Bruce, "Identification of protein-protein interactions and topologies in living cells with chemicalcross- linking and mass spectrometry", Mol. Cell. Proteomics 8, 409 (2009). http//dx.doi.org/10.1074/mcp. M800232-MCP200
39. N.S. Green, E. Reisler and K.N. Houk, "Quantitative evaluation of the lengths of homobifunctional protein cross-linking reagents used as molecular rulers", Protein Sci. 10, 1293 (2001). http://dx.doi.org/10.1110/ps.51201
40. D. Paramelle, G. Miralles, G. Subra and J. Martinez, "Chemical cross-linkers for protein structure studies by mass spectrometry", Proteomics 13, 438 (2013). http://dx.doi.org/10.1002/pmic.201200305
41. E.V. Petrotchenko and C.H. Borchers, "Crosslinking combined with mass spectrometry for structural proteomics", Mass Spectrom. Rev. 29, 862 (2010). http://dx.doi.org/10.1002/mas.20293
42. P. Novak, M.M. Young, J.S. Schoeniger and G. Kruppa, "A top-down approach to protein structure studies using chemical cross-linking and Fourier transform mass spectrometry", Eur. J. Mass Spectrom. 9, 623 (2003). http://dx.doi.org/10.1255/ejms.590
43. E.V. Petrotchenko, V.K. Olkhovic and C.H. Borchers, "Isotopically coded cleavable cross-linker for studying protein-protein interaction and protein complexes", Mol. Cell. Proteomics 4, 1167 (2005). http://dx.doi.org/10.1074/mcp.T400016-MCP200
44. L. Yang, N. Tang, C.R. Weisbrod, G.R. Munske, J.K. Eng, P.D. van Haller, N.K. Kaiser and J.E. Bruce, "A photocleavableand mass spectrometry identifiable cross-linker for protein interaction studies", Anal. Chem. 82, 3556 (2010). http://dx.doi.org/10.1021/ac902615g
45. E.V. Petrotchenko, K. Xiao, J. Cable, Y. Chen, N.V. Dokholyan and C.H. Borchers, "BiPS, a photocleavable, isotopically coded, fluorescent cross-linker for structural proteomics", Mol. Cell. Proteomics 8, 273 (2009). http://dx.doi.org/10.1074/mcp.M800265-MCP200
46. E.V. Petrotchenko, J.J. Serpa and C.H. Borchers, "An isotopically coded CID-cleavable biotinylated crosslinker for structural proteomics", Mol. Cell. Proteomics 10, 1 (2011). http://dx.doi.org/10.1074/mcp.M110.001420
47. J.A. Madsen, M.W. Gardner, S.I. Smith, A.R. Ledvina, J.J. Coon, J.C. Schwartz, G.C.J. Stafford and J.S. Brodbelt, "Top-down protein fragmentation by infrared multiphoton dissociation in a dual pressure linear ion trap", Anal. Chem. 81, 8677 (2009). http://dx.doi.org/10.1021/ac901554z
48. Y. Tanaka and J.J. Kohler, "Photoactivatable crosslinking sugars for capturing glycoprotein interactions", J. Am. Chem. Soc. 130, 3278 (2008). http://dx.doi.org/10.1021/ja7109772
49. I. Pe'er, C.E. Felder, O. Man, I. Silman, J.L. Sussmann and J.S. Beckmann, "Proteomic signatures: amino acid and oligopeptide composition differentiate among phyle", Proteins 54, 20 (2004). http://dx.doi.org/10. 1002/prot.10559
50. 2+- activated adenosine triphosphatases of Escherichia coli and Salmonella typhimurium", Arch. Biochem. Biophys. 167, 311 (1975). http://dx.doi.org/10.1016/0003- 9861(75)90467-1
51. F.C. Hartmann and F. Wold, "Bifunctional reagents. Cross-linking of pancreatic ribonuclease with diimido ester", J. Am. Chem. Soc. 88, 1390 (1966). http://dx.doi.org/10.1021/ja00968a058
52. S. Kalkhof and A. Sinz, "Chances and pitfalls of chemical cross-linking with amine-reactive N-hydroxysuccinimide esters", Anal. Bioanal. Chem. 392, 305 (2008). http://dx.doi.org/10.1007/s00216-008- 2231-5
53. M.D. Leavell, P., Novak C.R. Behrens, J.S. Schoeniger and G.H. Kruppa, "Strategy for selective chemical cross-linking of tyrosine and lysine residues", J. Am. Soc. Mass. Spectrom. 15, 1604 (2004). http://dx.doi.org/10.1016/j.jasms.2004.07.018
54. J.V. Staros, "N-Hydroxysulfosuccinimide active esters: bis(N-hydroxysulfosuccinimide) esters of two dicarboxylic acids are hydrophilic, membrane-impermeant, protein cross-linkers", Biochemistry 21, 3951 (1982). http://dx.doi.org/10.1021/bi00260a008
55. R.E. Hansen, D. Roth and J.R. Winther, "Quantifying the global cellular thiol-disulfide status", Proc. Natl Acad. Sci. USA 106, 422 (2009). http://dx.doi.org/10.1073/pnas.0812149106
56. C. Salaun, J. Greaves and L.H. Chamberlain, "The intracellular dynamic of protein palmitoylation", J. Cell Biol. 191, 1229 (2010). http://dx.doi.org/10.1083/jcb.201008160
57. R.J. Roskoski, "Protein prenylation: a pivotal posttranslational process", Biochem. Biophys. Res. Commun. 303, 1 (2003). http://dx.doi.org/10.1016/S0006- 291X(03)00323-1
58. J.J. Mieyal and P.B. Chock, "Posttranslational modification of cysteine in redox signaling and oxidative stress: focus on S- glutathionylation", Antioxid. Redox Signal. 16, 471 (2012). http://dx.doi.org/10.1089/ars.2011.4454
59. F.S. Groothuizen, A. Fish, M.V. Petoukhov, A. Reumer, L. Manelyte, H.H. Winterwerp, M.G. Marinus, J.H. Lebbink, D.I. Svergun, P. Friedhoff and T.K. Sixma, "Using stable MutS dimers and tetramers to quantitatively analyze DNA mismatch recognition and sliding clamp formation", Nucleic Acids Res. 41, 8166 (2013). http://dx.doi.org/10.1093/nar/gkt582
60. G.W. Preston and A.J. Wilson, "Photo-induced covalent cross-linking for the analysis of biomolecular interactions", Chem. Soc. Rev. 42, 3289 (2013). http://dx.doi.org/10.1039/c3cs35459h
61. R.V. Lewis, M.F. Roberts, E.A. Dennis and W.S. Allison, "Photoactivated heterobifunctional cross-linking reagentswhich demonstrate the aggregate state of phospholipase A2", Biochemistry 16, 5650 (1977). http://dx.doi.org/10.1021/bi00644a041
62. A.F. Gomes and F.C. Gozzo, "Chemical cross-linking with a diazirine photoactivatable cross-linker investigated by MALDI- and ESI-MS/MS", J. Mass Spectrom. 45, 892 (2010). http://dx.doi.org/10.1002/jms.1776
63. A. Sinz, S. Kalkhof and C. Ihling, "Mapping protein interfaces by a trifunctional cross-linker combined with MALDI-TOF and ESI-FTICR mass spectrometry", J. Am. Soc. Mass Spectrom. 16, 1921 (2005). http://dx.doi.org/10.1016/j.jasms.2005.07.020
64. J. Xie and P.G. Schultz, "A chemical toolkit for proteins - an expanded genetic code", Nature Rev. Mol. Cell Biol. 7, 775-782 (2006). http://dx.doi.org/10.1038/nrm2005
65. M. Suchanek, A. Radzikowska and C. Thiele, "Photoleucine and photo-methionine allow identification of protein-protein interactions in living cells, Nature Methods 2, 261 (2005). http://dx.doi.org/10.1038/nmeth752
66. P. Yan, T. Wang, G.J. Newton, T.V. Knyushko, Y. Xiong, D.J. Bigelow, T.C. Squier and M.U. Mayer, "A targeted releasable affinity probe (TRAP) for in vivo photocrosslinking", Chem. Biochem. 10, 1507 (2009). http://dx.doi.org/10.1002/cbic.200900029
67. C. Uttamapinant, K.A. White, H. Baruah, S. Thompson, M. Fernández-Suárez, S. Puthenveetil and A.Y. Ting, "A fluorophore ligase for site-specific protein labeling inside living cells", Proc. Natl Acad. Sci. USA 107, 10914 (2010). http://dx.doi.org/10.1073/pnas. 0914067107
68. J. Gubbens, P. Vader, J.M.A. Damen, M.C. O'Flaherty, M. Slijper, B. de Kruijff and A.I.P.M. de Kroon, "Probing the membrane interface-interacting proteome using photoactivatable lipid cross-linkers", J. Proteome Res. 6, 1951 (2007). http://dx.doi.org/10.1021/pr060561a
69. J. Gubbens, E. Ruijter, L.E. de Fays, J.M. Damen, B. de Kruijff, M. Slijper, D.T. Rijkers, R.M. Liskamp and A.I. de Kroon, "Photocrosslinking and click chemistry enable the specific detection of proteins interacting with phospholipids at the membrane interface", Chem. Biol. 16, 3 (2009). http://dx.doi.org/10.1016/j.chembiol.2008.11.009
70. C. Schmidt, K. Kramer and H. Urlaub, "Investigation of protein-RNA interactions by mass spectrometry- techniques and applications", J. Proteomics 75, 3478 (2012). http://dx.doi.org/10.1016/j.jprot.2012.04.030
71. R.S. Greenfield, T. Kaneko, A. Daues, M.A. Edson, K.A. Fitzgerald, L.J. Olech, J.A. Grattan, G.L. Spitalny and G.R. Braslwasky, "Evaluation in vitro of adriamycin immunoconjugates synthesized using an acid-sensitive hydrazone linker", Cancer Res. 50, 6600 (1990).
72. J.J. Zara, R.D. Wood, P. Boon, C.-H. Kim, N. Pomato, R. Bredehorst and C.-W. Vogel, "A carbohydrate-directed heterobifunctional cross-linking reagent for the synthesis of immunoconjugates", Anal. Biochem. 194, 156 (1991). http://dx.doi.org/10.1016/0003-2697(91)90163-N
73. M.R. Wenk, "Lipidomics: new tools and applications", Cell 143, 888 (2010). http://dx.doi.org/10.1016/j. cell.2010.11.033
74. M. Knobloch, S.M. Braun, L. Zurkirchen, C. von Schoultz, N. Zamboni, M.J. Arauzo-Bravo, W.J. Kovacs, O. Karalay, U. Suter, R.A. Machado, M. Roccio, M.P. Lutolf, C.F. Semenkovich and S. Jessberger, "Metabolomic control of adult neural stem cell activity by Fasn-dependent lipogenesis", Nature 493, 226 (2013). http://dx.doi.org/10.1038/nature11689
75. Z.A. Chen, A. Jawhari, L. Fischer, C. Buchen, S. Tahir, T. Kamenski, M. Rasmussen, L. Lariviere, J.C. Bukowski- Wills, M. Nilges, P. Cramer and J. Rappsilber, "Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry", EMBO J. 29, 717 (2010). http://dx.doi.org/10.1038/emboj.2009.401
76. A. Leitner, R. Reischl, T. Walzthoeni, F. Herzog, S. Bohn, F. Forster and R. Aebersold, "Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography", Mol. Cell. Proteomics 11, http://dx.doi.org/10.1074/mcp. M111.014126 (2012).
77. D.P Smith, J. Anderson, J. Plante, A.E. Ashcroft, S.E. Radford, A.J. Wilson and M.J. Parker, "Trifluoromethyldiazirine: an effective photo-induced cross-linking probe for exploring amyloid formation", Chem. Commun., 5728 (2008). http://dx.doi.org/10.1039/b813504e
78. S.D. Pringle, K. Giles, J.L. Wildgoose, J.P. Williams, S.E. Slade, K. Thalassinos, R.H. Bateman, M.T. Bowers and J.H. Scrivens, "An investigation of the mobility separation of some peptide and protein ions using a new hybrid quadrupole/travelling wave IMS/oa-ToF instrument", Int. J. Mass Spectrom. 261, 1 (2007). http://dx.doi.org/10.1016/j.ijms.2006.07.021
79. D.R. Müller, P. Schindler, H. Towbin, U. Wirth, H. Voshol, S. Hoving and M.O. Steinmetz, "Isotope-tagged crosslinking reagents: a new tool in mass spectrometric protein interaction analysis", Anal. Chem. 73, 1927 (2001). http://dx.doi.org/10.1021/ac001379a
80. J.W. Back, V. Notenboom, L.J. de Koning, A.O. Muijsers, T.K. Sixma, C.G. de Koster and L. de Jong, "Identification of cross-linked peptides for protein interaction studies using mass spectrometry and 18O labeling", Anal. Chem. 74, 4417 (2002). http://dx.doi.org/10.1021/ac0257492
81. E.V. Petrotchenko, J.J. Serpa and C.H. Borchers, "Use of a combination of isotopically coded cross-linkers and isotopically coded N-terminal modification reagentsfor selective identification on inter-peptide crosslinks", Anal. Chem. 82, 817 (2010). http://dx.doi.org/10.1021/ ac901637v
82. X. Tang, G.R. Munske, W.F. Siems and J.E. Bruce, "Mass spectrometry identifiable cross-linking strategy for studying protein-protein interactions", Anal. Chem. 77, 311 (2005). http://dx.doi.org/10.1021/ ac0488762
83. B. Clifford-Nunn, H.D. Showalter and P.C. Andrews, "Quaternary diamines as mass spectrometry cleavable crosslinkers for protein interactions", J. Am. Soc. Mass Spectrom. 23, 201 (2012). http://dx.doi.org/10.1007/s13361-011-0288-4
84. R.J. Rose, E. Damoc, E. Denisov, A. Makarov and A.J. Heck, "High-sensitivity Orbitrap mass analysis of intact macromolecular assemblies", Nature Methods 9, 1084 (2012). http://dx.doi.org/10.1038/ nmeth.2208
85. M. Mentinova and S.A. McLuckey, "Intra- and intermolecular cross-linking of peptide ions in the gas phase: reagents and conditions", J. Am. Soc. Mass Spectrom. 22, 912 (2011). http://dx.doi.org/10.1007/s13361-011- 0103-2
86. I.K. Webb, M. Mentinova, W.M. McGee and S.A. McLuckey, "Gas-phase intramolecular protein crosslinking via ion/ion reactions: ubiquitin and a homobifunctional sulfo-NHS ester", J. Am. Soc. Mass Spectrom. 24, 733 (2013). http://dx.doi.org/10.1007/s13361-013-0590-4
87. A. Armirotti and G. Damonte, "Achievements and perspectives of top-down proteomics", Proteomics 10, 3566 (2010). http://dx.doi.org/10. 1002/pmic.201000245
88. S.L. Mayne and H.G. Patterton, "Bioinformatics tools for the structural elucidation of multi-subunit protein complexes by mass spectrometric analysis of proteinprotein cross-links", Brief. Bioinform. 12, 660 (2011). http://dx.doi.org/10.1093/bib/bbq087
89. B. Yang, Y.J. Wu, M. Zhu, S.B. Fan, J. Lin, K. Zhang, S. Li, H. Chi, Y.X. Li, H.F. Chen, S.K. Luo, Y.H. Ding, L.H. Wang, Z. Hao, L.Y. Xiu, S., Chen, K. Ye, S.M. He and M.Q. Dong, "Identification of cross-linked peptides from complex samples", Nature Methods 9, 904 (2012). http://dx.doi.org/10.1038/ nmeth.2099
90. D.J. Lipman and W.R. Pearson, "Rapid and sensitive protein similarity searches", Science 227, 1435 (1985). http://dx.doi.org/10.1126/ science.2983426
91. M.I. Rasmussen, J.C. Refsgaard, L. Peng, G. Houen and P. Hojrup, "CrossWork: software-assisted identification of cross-linked peptides", J. Proteomics 74, 1871 (2011). http://dx.doi.org/10.1016/j. jprot.2011.04.019
92. H. Xu, P.-H. Hsu, L. Zhang, M.-D. Tsai and M.A. Freitags, "Database search algorithm for identification of intact cross-links in proteins and peptides using tandem mass spectrometry", J. Proteome Res. 9, 3384 (2010). http://dx.doi.org/10.1021/pr100369y
93. P.G. Pedrioli, J.K. Eng, R. Hubley, M. Vogelzang, E.W. Deutsch, B. Raught, B. Pratt, E. Nilsson, R.H. Angeletti, R. Apweiler, K. Cheung, C.E. Costello, H. Hermjakob, S. Huang, R.K. Julian, E. Kapp, M.E. McComb, S.G. Oliver, G. Omenn, N.W. Paton, R.J. Simpson, R. Smith, C.F. Taylor, W. Zhu and R. Aebersold, "A common open representationof mass spectrometry data and its application to proteomics research", Nature Biotechnol. 22, 1459 (2004). http://dx.doi.org/10.1038/nbt1031
94. O. Rinner, J. Seebacher, T. Walzthoeni, L.N. Mueller, M. Beck, A. Schmidt, M. Mueller and R. Aebersold, "Identification of cross-linked peptides from large sequence databases", Nature Methods 5, 315 (2008). http://dx.doi.org/10.1038/nmeth0808-748a
95. J.E. Elias and S.P. Gygi, "Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry", Nature Methods 4, 207 (2007). http://dx.doi.org/10.1038/ nmeth1019
96. J.E. Elias and S.P. Gygi, "Target-decoy search strategy for mass spectrometry-based proteomics", Methods Mol. Biol. 604, 55 (2010). http://dx.doi.org/10.1007/978-1-60761-444-9-5
97. T. Walzthoeni, M. Claassen, A. Leitner, F. Herzog, S. Bohn, F. Forster, M. Beck and R. Aebersold, "False discovery rate estimation for cross-linked peptides identified by mass spectrometry", Nature Methods 9, 901 (2012). http://dx.doi.org/10.1038/nmeth.2103
98. S. Peri, H. Steen and A. Pandey, "GPMAW - a software tool for analyzing proteins and peptides", Trends Biochem. Sci. 26, 687 (2001). http://dx.doi.org/10.1016/S0968-0004(01)01954-5
99. Y. Tang, Y. Chen, C.F. Lichti, R.A. Hall, K.D. Raney and S.F. Jennings, "CLPM: a cross-linked peptide mappingalgorithm for mass spectrometric analysis", BMC Bioinformatics 6 (Suppl 2), S9 (2005). http://dx.doi.org/10. 1186/1471-2105-6-S2-S9
100. D. Fenyö, "A software tool for the analysis of mass spectrometric disulfide mapping experiments", Comput. Appl. Biosci. 13, 617-618 (1997).
101. S. Wefing, V. Schnaible and D. Hoffmann, "SearchXLinks - a program for the Identification of disulfide bonds in proteins from mass spectra", Anal. Chem. 78, 1235 (2006). http://dx.doi.org/10.1021/ac051634x
102. O. Nadeau, G.J. Wyckoff, J.E. Paschall, A. Artigues, J. Sage, M.T. Villar and G.M. Carlson, "CrossSearch - a user friendly search engine for detecting chemically cross-linked peptides and conjugated proteins", Mol. Cell. Proteomics 7, 739 (2008). http://dx.doi.org/10.1074/mcp.M800020-MCP200
103. J. Seebacher, P. Mallick, N. Zhang, J.S. Eddes, R. Aebersold and M.H. Gelb, "Protein cross-linking analysisusing mass spectrometry isotope-coded cross-linkers and integrated computational data processing", J. Proteome Res. 5, 2270 (2006). http://dx.doi.org/10.1021/pr060154z
104. Q. Gao, S. Xue, C.E. Doneanu, S.A. Shaffer, D.R. Goodlett and S.D. Nelson, "Pro-CrossLink. software tool for protein cross-linking and mass spectrometry", Anal. Chem. 78, 2145-2149 (2006). http://dx.doi.org/10.1021/ ac051339c
105. T. Taverner, N.E. Hall, R.A. O'Hair and R.J. Simpson, "Characterization of an antagonist interleukin-6 dimer by stable isotope labeling, cross-linking, and mass spectrometry", J. Biol. Chem. 277, 46487 (2002). http://dx.doi.org/10.1074/jbc.M207370200
106. G.A. Anderson, N. Tolic, X. Tang, C. Zheng and J.E. Bruce, "Informatic strategies for large-scale novel cross-linking analysis", J. Proteome Res. 6, 3412 (2007). http://dx.doi.org/10.1021/pr070035z
107. M. Heymann, D. Paramelle, G. Subra, E. Forest, J. Martinez, C. Geourjon and G. Deleage, "MSX-3D: a tool to validate 3D protein models using mass spectrometry, Bioinformatics 24, 2782 (2008). http://dx.doi.org/10.1093/ bioinformatics/btn510
108. L.J. de Koning, P.T. Kasper, J.W. Back, M.A. Nessen, F. Vanrobaeys, J. Van Beeumen, E. Gherardi, C.G. de Koster and L. de Jong, "Computer-assisted mass spectrometric analysis of naturally occurring and artificiallyintroduced cross-links in proteins and proteincomplexes", FEBS J. 273, 281 (2006). http://dx.doi.org/10.1111/j.1742-4658.2005.05053.x
109. C.Y. Park, A.A. Klammer, L. Kall, M.J. MacCoss and W.S. Noble, "Rapid and accurate peptide identification from tandem mass spectra", J. Proteome Res. 7, 3022 (2008). http://dx.doi.org/10.1021/pr800127y
110. C.H. Sohn, H.D. Agnew, J.E. Lee, M.J. Sweredoski, R.L. Graham, G.T. Smith, S. Hess, G. Czerwieniec, J.A. Loo, J.R. Heath, R.J. Deshaies and J.L. Beauchamp, "Designer reagents for mass spectrometry-based proteomics: clickable cross-linkers for elucidation of protein structures and interactions", Anal. Chem. 84, 2662 (2012). http://dx.doi.org/10.1021/ ac202637n
111. K.A. Kellersberger, E. Yu, G.H. Kruppa, M.M. Young and Fabris, "Top-down characterization of nucleic acids modified by structural probes using high-resolution tandem mass spectrometry and automated data interpretation", Anal. Chem. 76, 2438 (2004). http://dx.doi.org/10.1021/ ac0355045
112. A. Panchaud, P. Singh, S.A. Shaffer and D. Goodlett, "xComb - a cross-linked peptide database approach to protein-protein interaction analysis", J. Proteome Res. 9, 2508 (2010). http://dx.doi.org/10.1021/ pr9011816
113. M. Gotze, J. Pettelkau, S. Schaks, K. Bosse, C.H. Ihling, F. Krauth, R. Fritzsche, U. Kuhn and A. Sinz, "StavroX-a software for analyzing crosslinked productsin protein interaction studies", J. Am. Soc. Mass. Spectrom. 23, 76 (2012). http://dx.doi.org/10.1007/s13361-011-0261-2
114. K.J. Riley and J.A. Steitz, "The 'Observer Effect' in genome-wide surveys of protein-RNA interactions", Mol. Cell 49, 601 (2013). http://dx.doi.org/10.1016/j.molcel. 2013.01.030
115. P. Haberkant, R. Raijmakers, M. Wildwater, T. Sachsenheimer, B. Brügger, K. Maeda, M. Houwelig, A.C., Gavin, C. Schultz, G. Van Meer, A.J.R., Heck and J.C.M. Holthuis, "In vivo profiling and visualization of cellular protein-lipid interactions using bifunctional fatty acids", Angew. Chem. Int. Ed. 52, 4033 (2013). http://dx.doi.org/10.1002/anie.201210178
116. S. Kalkhof, C. Ihling, K. Mechtler and A. Sinz, "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 (2005). http://dx.doi.org/10.1021/ac0487294
117. C. Ciferri, G.C. Lander, A. Maiolica, F. Herzog, R. Aebersold and E. Nogales, "Molecular architecture of human polycomb repressive complex 2", eLife 1, 1 (2012). http://dx.doi.org/10.7554/eLife.00005
118. P. Singh, E. Nakatani, D.R. Goodlett and C.E. Catalano, "A pseudo-atomic model for the capsid shell of bacteriophage lambda using chemical cross-linking/mass spectrometry and molecular modeling", J. Mol. Biol. 425, 3378 (2013). http://dx.doi.org/10.1016/j. jmb.2013.06.026
119. F. Herzog, A. Kahraman, D. Boehringer, R. Mak, A. Bracher, T. Walzthoeni, A. Leitner, M. Beck, F.U. Hartl, N. Ban, L. Malmstrom and R. Aebersold, "Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry", Science 337, 1348 (2012). http://dx.doi.org/10.1126/science.1221483
120. R. Schwarz, D. Tanzler, C.H. Ihling, M.Q. Muller, K. Kolbel and A. Sinz, "Monitoring conformational changes in peroxisome proliferator-activated receptor alpha by a genetically encoded photoamino acid, crosslinking, and mass spectrometry", J. Med. Chem. 56, 4252 (2013). http://dx.doi.org/10.1021/ jm400446b
121. A. Castello, B. Fischer, K. Eichelbaum, R. Horos, B.M. Beckmann, C. Strein, N.E. Davey, D.T. Humphreys, T. Preiss, L.M. Steinmetz, J. Krijgsveld and M.W. Hentze, "Insights into RNA biology from an atlas of mammalian mRNA-binding proteins", Cell 149, 1393 (2012). http://dx.doi.org/10.1016/j. cell.2012.04.031
122. K. Kramer, P. Hummel, H.-H. Hsiao, X. Luo, M. Wahl and H. Urlaub, "Mass-spectrometric analysis of proteins cross-linked to 4-thio-uracil- and 5-bromouracil- substituted RNA", Int. J. Mass Spectrom. 304, 184 (2011). http://dx.doi.org/10.1016/j.ijms.2010.10.009
123. P. Haberkant and G. van Meer, "Protein-lipid interactions: paparazzi hunting for snap-shots", Biol. Chem. 390, 795 (2009). http://dx.doi.org/ 10.1515/BC.2009.074
124. N.P. Barrera, M. Zhou and C.V. Robinson, "The role of lipids in defining membrane protein interactions: insights from mass spectrometry", Trends Cell Biol. 23, 1 (2013). http://dx.doi.org/10.1016/j.tcb.2012.08.007
125. S.H. Yu, M. Boyce, A.M. Wands, M.R. Bond, C.R. Bertozzi and J.J. Kohler, "Metabolic labeling enables selective photocrosslinking of O-GlcNAc-modified proteins to their binding partners", Proc. Natl Acad. Sci. USA 109, 4834 (2012). http://dx.doi.org/10.1073/pnas.1114356109
126. L. Sleno, "The use of mass defect in modern mass spectrometry", J. Mass Spectrom. 47, 226 (2012). http://dx.doi.org/10.1002/jms.2953
127. A.S. Hebert, A.E. Merrill, D.J. Bailey, A.J. Still, M.S. Westphall, E.R. Strieter, D.J. Pagliarini and J.J. Coon, "Neutron-encoded mass signatures for multiplexed proteome quantification", Nature Methods 10, 332 (2013). http://dx.doi.org/10.1038/nmeth.2378
128. S.M. Chowdhury, X. Du, N. Tolic, S. Wu, R.J. Moore, M.U. Mayer, R.D. Smith and J.N. Adkins, "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 (2009). http://dx.doi.org/10.1021/ac900853k
129. E.D. Merkley, E.S. Baker, K.L. Crowell, D.J. Orton, T. Taverner, C. Ansong, Y.M. Ibrahim, M.C. Burnet, J.R. Cort, G.A. Anderson, R.D. Smith and J.N. Adkins, "Mixed-isotope labeling with LC-IMS-MS for characterization of protein-protein interactions by chemical cross-linking", J. Am. Soc. Mass Spectrom. 24, 444 (2013). http://dx.doi.org/10.1007/s13361-012-0565-x
130. A. Kahraman, F. Herzog, A. Leitner, G. Rosenberger, R. Aebersold and L. Malmstrom, "Cross-link guided molecular modeling with ROSETTA", PloS One 8, e73411 (2013). http://dx.doi.org/10.1371/journal.pone.0073411
131. F.M. Richter, H.H. Hsiao, H. Plessmann and H. Urlaub, "Enrichment of protein-RNA crosslinks from crude UV-irradiated mixtures for MS analysis by on-line chromatography using titanium dioxide columns", Biopolymers 91, 297-309. http://dx.doi.org/10.1002/bip.21139