Interrogating the architecture of protein assemblies and protein interaction networks by cross-linking mass spectrometry

Current Opinion in Structural Biology

Volumn 35, Issue , 2015, Pages 100-108

  Liu, Fan ^a,b   Heck, Albert J R ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY PURIFICATION; BINDING AFFINITY; CROSS LINKING MASS SPECTROMETRY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; FRACTIONATION; HUMAN; MACROMOLECULE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEOMICS; REVIEW; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; AFFINITY CHROMATOGRAPHY; CHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; PROCEDURES; PROTEIN ANALYSIS;

PROTEIN;

CHROMATOGRAPHY, AFFINITY; HUMANS; MASS SPECTROMETRY; PROTEIN INTERACTION MAPPING; PROTEINS; PROTEOMICS;

EID: 84947770886     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.10.006     Document Type: Review

References (55)

1. Sinz A. The advancement of chemical cross-linking and mass spectrometry for structural proteomics: from single proteins to protein interaction networks. Expert Rev Proteomics 2014, 11:733-743.
2. 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.
3. Walzthoeni T., Leitner A., Stengel F., Aebersold R. Mass spectrometry supported determination of protein complex structure. Curr Opin Struct Biol 2013, 23:252-260.
4. Rappsilber J. The beginning of a beautiful friendship: cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. J Struct Biol 2011, 173:530-540.
5. 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, 9:1634-1649.
6. Arlt C., Ihling C.H., Sinz A. Structure of full-length p53 tumor suppressor probed by chemical cross-linking and mass spectrometry. Proteomics 2015, 10.1002/pmic.201400549.
7. 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, 6:2200-2211.
8. Lössl P., Kölbel K., Tänzler D., Nannemann D., Ihling C.H., Keller M.V., Schneider M., Zaucke F., Meiler J., Sinz A. Analysis of nidogen-1/laminin γ1 interaction by cross-linking, mass spectrometry, and computational modeling reveals multiple binding modes. PLoS One 2014, 9:e112886.
9. Fu C., Uetrecht C., Kang S., Morais M.C., Heck A.J.R., Walter M.R., Prevelige P.E. A docking model based on mass spectrometric and biochemical data describes phage packaging motor incorporation. Mol Cell Proteomics 2010, 9:1764-1773.
10. Chen Z.A., Jawhari A., Fischer L., Buchen C., Tahir S., Kamenski T., Rasmussen M., Lariviere L., Bukowski-Wills J.-C., Nilges M., et al. Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J 2010, 29:717-726.
11. Bohn S., Beck F., Sakata E., Walzthoeni T., Beck M., Aebersold R., Förster F., Baumeister W., Nickell S. Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc Natl Acad Sci U S A 2010, 107:20992-20997.
12. 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.
13. Kao A., Randall A., Yang Y., Patel V.R., Kandur W., Guan S., Rychnovsky S.D., Baldi P., Huang L. Mapping the structural topology of the yeast 19S proteasomal regulatory particle using chemical cross-linking and probabilistic modeling. Mol Cell Proteomics 2012, 10.1074/mcp.M112.018374.
14. Leitner A., Joachimiak L.A., Bracher A., Mönkemeyer L., Walzthoeni T., Chen B., Pechmann S., Holmes S., Cong Y., Ma B., et al. The molecular architecture of the eukaryotic chaperonin TRiC/CCT. Structure 2012, 20:814-825.
15. Kalisman N., Adams C.M., Levitt M. Subunit order of eukaryotic TRiC/CCT chaperonin by cross-linking, mass spectrometry, and combinatorial homology modeling. Proc Natl Acad Sci 2012, 109:2884-2889.
16. Lasker K., Forster F., Bohn S., Walzthoeni T., Villa E., Unverdorben P., Beck F., Aebersold R., Sali A., Baumeister W. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci 2012, 109:1380-1387.
17. Schmidt C., Zhou M., Marriott H., Morgner N., Politis A., Robinson C.V. Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation. Nat Commun 2013, 4:1985.
18. Benda C., Ebert J., Scheltema R.A., Schiller H.B., Baumgärtner M., Bonneau F., Mann M., Conti E. Structural model of a CRISPR RNA-silencing complex reveals the RNA-target cleavage activity in Cmr4. Mol Cell 2014, 10.1016/j.molcel.2014.09.002.
19. Leitner A., Joachimiak L.A., Unverdorben P., Walzthoeni T., Frydman J., Förster F., Aebersold R. Chemical cross-linking/mass spectrometry targeting acidic residues in proteins and protein complexes. Proc Natl Acad Sci U S A 2014, 111:9455-9460.
20. Erzberger J.P., Stengel F., Pellarin R., Zhang S., Schaefer T., Aylett C.H.S., Cimermančič P., Boehringer D., Sali A., Aebersold R., et al. Molecular architecture of the 40S eIF1 eIF3 translation initiation complex. Cell 2014, 158:1123-1135.
21. Shi Y., Fernandez-Martinez J., Tjioe E., Pellarin R., Kim S.J., Williams R., Schneidman-Duhovny D., Sali a., Rout M.P., Chait B.T. Structural characterization by cross-linking reveals the detailed architecture of a coatomer-related heptameric module from the nuclear pore complex. Mol Cell Proteomics 2014, 13:2927-2943.
22. Plaschka C., Larivière L., Wenzeck L., Seizl M., Hemann M., Tegunov D., Petrotchenko E.V., Borchers C.H., Baumeister W., Herzog F., et al. Architecture of the RNA polymerase II-mediator core initiation complex. Nature 2015, 10.1038/nature14229.
23. Thierbach K., von Appen A., Thoms M., Beck M., Flemming D., Hurt E. Protein interfaces of the conserved Nup84 complex from Chaetomium thermophilum shown by crosslinking mass spectrometry and electron microscopy. Structure 2013, 21:1672-1682.
24. Bui K.H., Von Appen A., Diguilio A.L., Ori A., Sparks L., Mackmull M.T., Bock T., Hagen W., Andrés-Pons A., Glavy J.S., et al. Integrated structural analysis of the human nuclear pore complex scaffold. Cell 2013, 155:1233-1243.
25. Herzog F., Kahraman A., Boehringer D., Mak R., Bracher A., Walzthoeni T., Leitner A., Beck M., Hartl F.-U., Ban N., et al. Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 2012, 337:1348-1352.
26. Liu H., Zhang H., Weisz D.a., Vidavsky I., Gross M.L., Pakrasi H.B. MS-based cross-linking analysis reveals the location of the PsbQ protein in cyanobacterial photosystem II. Proc Natl Acad Sci USA 2014, 2014:1-6.
27. Liu H., Zhang H., Niedzwiedzki D.M., Prado M., He G., Gross M.L., Blankenship R.E. Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 2013, 342:1104-1107.
28. Tang X., Bruce J.E. A new cross-linking strategy: protein interaction reporter (PIR) technology for protein-protein interaction studies. Mol Biosyst 2010, 6:939-947.
29. 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, 5:315-318.
30. Yang B., Wu Y.-J., Zhu M., Fan S.-B., Lin J., Zhang K., Li S., Chi H., Li Y.-X., Chen H.-F., et al. Identification of cross-linked peptides from complex samples. Nat Methods 2012, 9:904-906.
31. Walzthoeni T., Claassen M., Leitner A., Herzog F., Bohn S., Förster F., Beck M., Aebersold R. False discovery rate estimation for cross-linked peptides identified by mass spectrometry. Nat Methods 2012, 9:901-903.
32. Chavez J.D., Weisbrod C.R., Zheng C., Eng J.K., Bruce J.E. Protein interactions, post-translational modifications and topologies in human cells. Mol Cell Proteomics 2013, 12:1451-1467.
33. Buncherd H., Roseboom W., de Koning L.J., de Koster C.G., De Jong L. A gas phase cleavage reaction of cross-linked peptides for protein complex topology studies by peptide fragment fingerprinting from large sequence database. J Proteomics 2014, 108:65-77.
34. Kaake R.M., Wang X., Burke A., Yu C., Kandur W., Yang Y., Novtisky E.J., Second T., Duan J., Kao A., et al. A new in vivo cross-linking mass spectrometry platform to define protein-protein interactions in living cells. Mol Cell Proteomics 2014, 13:3533-3543.
35. 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.
36. Fritzsche R., Ihling C.H., Götze M., Sinz A. Optimizing the enrichment of cross-linked products for mass spectrometric protein analysis. Rapid Commun Mass Spectrom 2012, 26:653-658.
37. 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. M111.014126-M111.014126.
38. 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.
39. Nessen M.A., Kramer G., Back J., Baskin J.M., Smeenk L.E.J., De Koning L.J., Van Maarseveen J.H., De Jong L., Bertozzi C.R., Hiemstra H., et al. Selective enrichment of azide-containing peptides from complex mixtures. J Proteome Res 2009, 8:3702-3711.
40. Chowdhury S.M., Du X., Tolić N., Wu S., Moore R.J., Mayer M.U., Smith R.D., Adkins J.N. 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.
41. Trnka M.J., Baker P.R., Robinson P.J.J., Burlingame A.L., Chalkley R.J. Matching cross-linked peptide spectra: only as good as the worse identification. Mol Cell Proteomics 2014, 13:420-434.
42. Wang J., Anania V.G., Knott J., Rush J., Lill J.R., Bourne P.E., Bandeira N. Combinatorial approach for large-scale identification of linked-peptides from MS/MS spectra. Mol Cell Proteomics 2014, 10.1074/mcp.M113.035758.
43. Müller M.Q., Dreiocker F., Ihling C.H., Schäfer M., Sinz A. Cleavable cross-linker for protein structure analysis: reliable identification of cross-linking products by tandem MS. Anal Chem 2010, 82:6958-6968.
44. Soderblom E.J., Goshe M.B. Collision-induced dissociative chemical cross-linking reagents and methodology: applications to protein structural characterization using tandem mass spectrometry analysis. Anal Chem 2006, 78:8059-8068.
45. Kao A., Chiu C., Vellucci D., Yang Y., Patel V.R., Guan S., Randall A., Baldi P., Rychnovsky S.D., Huang L. Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes. Mol Cell Proteomics 2011, 10. M110.002212.
46. Liu F., Rijkers D.T.S., Post H., Heck A.J.R. Proteome-wide profiling of protein assemblies by cross-linking mass spectrometry. Nat Methods 2015, 10.1038/nmeth.3603.
47. Beck F., Unverdorben P., Bohn S., Schweitzer A., Pfeifer G., Sakata E., Nickell S., Plitzko J.M., Villa E., Baumeister W., et al. Near-atomic resolution structural model of the yeast 26S proteasome. Proc Natl Acad Sci 2012, 109:14870-14875.
48. Greber B.J., Boehringer D., Leitner A., Bieri P., Voigts-Hoffmann F., Erzberger J.P., Leibundgut M., Aebersold R., Ban N. Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature 2014, 505:515-519.
49. Greber B.J., Bieri P., Leibundgut M. The complete structure of the 55 S mammalian mitochondrial ribosome. Science 2015, 348:303-308.
50. Staals R.H.J., Zhu Y., Taylor D.W., Kornfeld J.E., Sharma K., Barendregt A., Koehorst J.J., Vlot M., Neupane N., Varossieau K., et al. RNA targeting by the Type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol Cell 2014, 56:518-530.
51. Martinez-Rucobo F.W., Kohler R., van de Waterbeemd M., Heck A.J.R., Hemann M., Herzog F., Stark H., Cramer P. Molecular basis of transcription-coupled pre-mRNA capping. Mol Cell 2015, 10.1016/j.molcel.2015.04.004.
52. Gingras A.-C., Gstaiger M., Raught B., Aebersold R. Analysis of protein complexes using mass spectrometry. Nat Rev Mol Cell Biol 2007, 8:645-654.
53. 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:M110. 006841-M110.006841.
54. 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, 8:409-420.
55. Navare A.T., Chavez J.D., Zheng C., Weisbrod C.R., Eng J.K., Siehnel R., Singh P.K., Manoil C., Bruce J.E. Probing the protein interaction network of Pseudomonas aeruginosa cells by chemical cross-linking mass spectrometry. Structure 2015, 23:762-773.