Distance restraints from crosslinking mass spectrometry: Mining a molecular dynamics simulation database to evaluate lysine-lysine distances

Protein Science

Volumn 23, Issue 6, 2014, Pages 747-759

  Merkley, Eric D ^a   Rysavy, Steven ^b   Kahraman, Abdullah ^c   Hafen, Ryan P ^a   Daggett, Valerie ^b,d   Adkins, Joshua N ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d University of Washington   (United States)

Author keywords

Chemical crosslinking mass spectrometry; Distance restraints; Hybrid modeling; Integrative structural biology; Molecular dynamics simulations

Indexed keywords

AMINO ACID; CYTOCHROME C; LYSINE; N HYDROXYSUCCINIMIDE; CROSS LINKING REAGENT; DISUCCINIMIDYL SUBERATE; N-HYDROXYSUCCINIMIDE; PROTEIN; SUCCINIMIDE DERIVATIVE;

ARTICLE; ATOM; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COVALENT BOND; CROSS LINKING; CRYSTAL STRUCTURE; DATA MINING; HEART; HORSE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; TANDEM MASS SPECTROMETRY; TEMPERATURE; CHEMISTRY; PROCEDURES;

CROSS-LINKING REAGENTS; LYSINE; MASS SPECTROMETRY; MOLECULAR DYNAMICS SIMULATION; PROTEINS; SUCCINIMIDES;

EID: 84903715767     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2458     Document Type: Article

References (47)

1. Schneidman-Duhovny D, Rossi A, Avila-Sakar A, Kim SJ, Velázquez-Muriel J, Strop P, Liang H, Krukenberg KA, Liao M, Kim HM, Sobhanifar S, Dötsch V, Rajpal A, Pons J, Agard DA, Cheng Y, Sali A (2012) A method for integrative structure determination of proteinprotein complexes. Bioinformatics 28:3282-3289
2. Ward AB, Sali A, Wilson IA (2013) Integrative structural biology. Science 339:913-915
3. Sinz A (2006) Chemical crosslinking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions. Mass Spectrom Rev 25:663-682
4. Fabris D, Yu ET (2010) Elucidating the higher-order structure of biopolymers by structural probing and mass spectrometry: MS3D. J Mass Spectrom 45:841-860
5. Rappsilber J (2011) The beginning of a beautiful friendship: Crosslinking/mass spectrometry and modelling of proteins and multi-protein complexes. J Struct Biol 173:530-540
6. Merkley ED, Cort JR, Adkins JN (2013) Crosslinking and mass spectrometry methodologies to facilitate structural biology: finding a path through the maze. J Struct Funct Genomics 14:77-90
7. Kalkhof S, Sinz A (2008) Chances and pitfalls of chemical crosslinking with amine-reactive N-hydroxysuccinimide esters. Analyt Bioanalyt Chem 392:305-312
8. Muadler S, Bich C, Touboul D, Zenobi R (2009) Chemical crosslinking with NHS esters: A systematic study on amino acid reactivities. J Mass Spectrom 44:694-706
9. Young MM, Tang N, Hempel JC, Oshiro CM, Taylor EW, Kuntz ID, Gibson BW, Dollinger G (2000) High throughput protein fold identification by using experimental constraints derived from intramolecular crosslinks and mass spectrometry. Proc Natl Acad Sci USA 97:5802-5806
10. Zheng CX, Yang L, Hoopmann MR, Eng JK, Tang XT, Weisbrod CR, Bruce JE (2011) Crosslinking measurements of in vivo protein complex topologies. Mol Cell Proteomics 10:M110.006841
11. Weisbrod CR, Chavez JD, Eng JK, Yang L, Zheng C, Bruce JE (2013) In vivo protein interaction network identified with a novel teal-time crosslinked peptide identification strategy. J Proteome Res 12:1569-1579
12. Chen ZA, Jawhari A, Fischer L, Buchen C, Tahir S, Kamenski T, Rasmussen M, Lariviere L, Bukowski- Wills J-C, Nilges M, Cramer P, Rappsilber J (2010) Architecture of the RNA polymerase II-TFIIF complex revealed by crosslinking and mass spectrometry. EMBO J 29:717-726
13. Sanowar S, Singh P, Pfuetzner RA, Andre I, Zheng HJ, Spreter T, Strynadka NCJ, Gonen T, Baker D, Goodlett DR, Miller SI (2010) Interactions of the transmembrane polymeric rings of the Salmonella enterica serovar typhimurium type III secretion system.MBio 1.pii: e00158-10
14. Herzog F, Kahraman A, Boehringer D, Mak R, Bracher A, Walzthoeni T, Leitner A, Beck M, Hartl F-U, Ban N, Malmström L, Aebersold R (2012) Structural probing of a protein phosphatase 2A network by chemical crosslinking and mass spectrometry. Science 337:1348-1352
15. Lasker K, Forster F, Bohn S, Walzthoeni T, Villa E, Unverdorben P, Beck F, Aebersold R, Sali A, Baumeister W (2012) Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci USA 109:1380-1387
16. Walzthoeni T, Claassen M, Leitner A, Herzog F, Bohn S, Forster F, Beck M, Aebersold R (2012) False discovery rate estimation for crosslinked peptides identified by mass spectrometry. Nat Meth 9:901-903
17. Green NS, Reisler E, Houk KN (2001) Quantitative evaluation of the lengths of homobifunctional protein crosslinking reagents used as molecular rulers. Protein Sci 10:1293-1304
18. Jacobsen RB, Sale KL, Ayson MJ, Novak P, Hong JH, Lane P, Wood NL, Kruppa GH, Young MM, Schoeniger JS (2006) Structure and dynamics of dark-state bovine rhodopsin revealed by chemical crosslinking and highresolution mass spectrometry. Protein Sci 15:1303-1317
19. Zelter A, Hoopmann MR, Vernon R, Baker D, MacCoss MJ, Davis TN (2010) Isotope signatures allow identification of chemically crosslinked peptides by mass spectrometry: A novel method to determine inter-residue distances in protein structures through crosslinking. J Proteome Res 9:3583-3589
20. Li H, Wells SA, Jimenez-Roldan JE, Römer RA, Zhao Y, Sadler PJ, O'Connor PB (2012) Protein flexibility is key to cisplatin crosslinking in calmodulin. Protein Sci 21:1269-1279
21. Pettelkau J, Schroder T, Ihling CH, Olausson BES, Kolbel K, Lange C, Sinz A (2012) Structural insights into retinal guanylylcyclase-GCAP-2 interaction determined by crosslinking and mass spectrometry. Biochemistry 51:4932-4949
22. Beck DA, Jonsson AL, Schaeffer RD, Scott KA, Day R, Toofanny RD, Alonso DO, Daggett V (2008) Dynameomics: mass annotation of protein dynamics and unfolding in water by high-throughput atomistic molecular dynamics simulations. Protein Eng Des Sel 21:353-368
23. Kehl C, Simms AM, Toofanny RD, Daggett V (2008) Dynameomics: A multi-dimensional analysis-optimized database for dynamic protein data. Protein Eng Des Sel 21:379-386
24. Simms AM, Toofanny RD, Kehl C, Benson NC, Daggett V (2008) Dynameomics: design of a computational lab workflow and scientific data repository for protein simulations. Protein Eng Des Sel 21:369-377
25. van der Kamp MW, Schaeffer RD, Jonsson AL, Scouras AD, Simms AM, Toofanny RD, Benson NC, Anderson PC, Merkley ED, Rysavy S, Bromley D, Beck DAC, Daggett V (2010) Dynameomics: A comprehensive database of protein dynamics. Structure 18:423-435
26. Schaeffer RD, Jonsson AL, Simms AM, Daggett V (2011) Generation of a consensus protein domain dictionary. Bioinformatics 27:46-54
27. Rinner O, Seebacher J, Walzthoeni T, Mueller L, Beck M, Schmidt A, Mueller M, Aebersold R (2008) Identification of crosslinked peptides from large sequence databases. Nat Meth 5:315-318
28. Xu H, Hsu P-H, Zhang L, Tsai M-D, Freitas MA (2010) Database search algorithm for identification of intact crosslinks in proteins and peptides using tandem mass spectrometry. J Proteome Res 9:3384-3393
29. Fritzsche R, Ihling CH, Gotze M, Sinz A (2012) Optimizing the enrichment of crosslinked products for mass spectrometric protein analysis. Rapid Commun Mass Spectrom 26:653-658
30. Kahraman A, Herzog F, Leitner A, Rosenberger G, Aebersold R, Malmström L (2013) CrossLink guided molecular modeling with ROSETTA. Plos One 8:e73411
31. Lee YJ, Lackner LL, Nunnari JM, Phinney BS (2007) Shotgun crosslinking analysis for studying quaternary and tertiary protein structures. J Proteome Res 6: 3908-3917
32. Guo X, Bandyopadhyay P, Schilling B, Young MM, Fujii N, Aynechi T, Guy RK, Kuntz ID, Gibson BW (2008) Partial acetylation of lysine residues improves intraprotein crosslinking. Anal Chem 80:951-960
33. Mendoza VL, Vachet RW (2009) Probing protein structure by amino acid-specific covalent labeling and mass spectrometry. Mass Spectrom Rev 28:785-815
34. Liu F, Goshe MB (2010) Combinatorial electrostatic collision-induced dissociative chemical crosslinking reagents for probing protein surface topology. Anal Chem 82:6215-6223
35. Scouras AD, Daggett V (2011) The dynameomics rotamer library: Amino acid side chain conformations and dynamics from comprehensive molecular dynamics simulations in water. Protein Sci 20:341-352
36. Clifford-Nunn B, Showalter HDH, Andrews PC (2012) Quaternary diamines as mass spectrometry cleavable crosslinkers for protein interactions. J Am Soc Mass Spectrom 23:201-212
37. Merkley ED, Baker ES, Crowell KL, Orton DJ, Taverner T, Ansong C, Ibrahim YM, Burnet MC, Cort JR, Anderson GA, Smith RD, Adkins JN (2013) Mixedisotope labeling with LC-IMS-MS for characterization of protein-protein interactions by chemical crosslinking. J Am Soc Mass Spectrom 24:444-449
38. Kahraman A, Malmström L, Aebersold R (2011) Xwalk: Computing and visualizing distances in crosslinking experiments. Bioinformatics 27:2163-2164
39. Leitner A, Reischl R, Walzthoeni T, Herzog F, Bohn S, Förster F, Aebersold R (2012) Expanding the chemical crosslinking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol Cell Proteomics 11:M111.014126
40. Fischer L, Chen ZA, Rappsilber J (2013) Quantitative crosslinking/mass spectrometry using isotope-labelled crosslinkers. J Proteomics 88:120-128.
41. Henzler-Wildman K, Kern D (2007) Dynamic personalities of proteins. Nature 450:964-972
42. Leitner A, Walzthoeni T, Kahraman A, Herzog F, Rinner O, Beck M, Aebersold R (2010) Probing native protein structures by chemical crosslinking, mass spectrometry, and bioinformatics. Mol Cell Proteomics 9: 1634-1649
43. ilmm, in lucem molecular mechanics, Seattle: Beck DA, Alonso DOV, Daggett V; 2000-2008
44. Levitt M, Hirshberg M, Sharon R, Daggett V (1995) Potential energy function and parameters for simulations of the molecular dynamics of proteins and nucleic acids in solution. Comput Phys Commun 91:215-231
45. Levitt M, Hirshberg M, Sharon R, Laidig KE, Daggett V (1997) Calibration and testing of a water model for simulation of the molecular dynamics of proteins and nucleic acids in solution. J Phys Chem B 101:5051-5061
46. Beck DAC, Daggett V (2004) Methods for molecular dynamics simulations of protein folding/unfolding in solution. Methods 34:112-120
47. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012