Cross-linking immunoprecipitation-MS (xIP-MS): Topological analysis of chromatinassociated protein complexes using single affinity purification

Molecular and Cellular Proteomics

Volumn 15, Issue 3, 2016, Pages 854-865

  Makowski, Matthew M ^a   Willems, Esther ^a   Jansen, Pascal W T C ^a   Vermeulen, Michiel ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN ASSOCIATED PROTEIN COMPLEX; COHESIN; KU ANTIGEN; PROTEIN; RIBOSEPHOSPHATE PYROPHOSPHOKINASE; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CHROMATIN; CROSS LINKING REAGENT; MINICHROMOSOME MAINTENANCE PROTEIN; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN;

ARTICLE; CELL LYSATE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS LINKING; CROSS LINKING IMMUNOPRECIPITATION MASS SPECTROMETRY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MAMMAL CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PURIFICATION; QUALITY CONTROL; SINGLE AFFINITY PURIFICATION; TANDEM MASS SPECTROMETRY; WHOLE CELL; CHEMISTRY; CHROMATIN; COMPARATIVE STUDY; HELA CELL LINE; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR MODEL; PROCEDURES; PROTEIN QUATERNARY STRUCTURE;

CELL CYCLE PROTEINS; CHROMATIN; CHROMATOGRAPHY, LIQUID; CHROMOSOMAL PROTEINS, NON-HISTONE; CROSS-LINKING REAGENTS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MINICHROMOSOME MAINTENANCE PROTEINS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN STRUCTURE, QUATERNARY; RIBOSE-PHOSPHATE PYROPHOSPHOKINASE;

EID: 84962576477     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.053082     Document Type: Article

References (63)

1. Mann, M., Hendrickson, R. C., and Pandey, A. (2001) Analysis of proteins and proteomes by mass spectrometry. Ann. Rev. Biochem. 70, 437-473
2. Gingras, A. C., Gstaiger, M., Raught, B., and Aebersold, R. (2007) Analysis of protein complexes using mass spectrometry. Nat. Rev. Mol. Cell Biol. 8, 645-654
3. Dunham, W. H., Mullin, M., and Gingras, A. C. (2012) Affinity-purification coupled to mass spectrometry: basic principles and strategies. Proteomics 12, 1576-1590
4. Rappsilber, J. (2011) The beginning of a beautiful friendship: cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. J. Structural Biol. 173, 530-540
5. Sinz, A. (2006) Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions. Mass Spectrometry Rev. 25, 663-682
6. 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
7. Nguyen, V. Q., Ranjan, A., Stengel, F., Wei, D., Aebersold, R., Wu, C., and Leschziner, A. E. (2013) Molecular architecture of the ATP-dependent chromatin-remodeling complex SWR1. Cell 154, 1220-1231
8. Tosi, A., Haas, C., Herzog, F., Gilmozzi, A., Berninghausen, O., Ungewickell, C., Gerhold, C. B., Lakomek, K., Aebersold, R., Beckmann, R., and Hopfner, K. P. (2013) Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell 154, 1207-1219
9. Ciferri, C., Lander, G. C., Maiolica, A., Herzog, F., Aebersold, R., and Nogales, E. (2012) Molecular architecture of human polycomb repressive complex 2. Elife 1, e00005
10. Han, Y., Luo, J., Ranish, J., and Hahn, S. (2014) Architecture of the Saccharomyces cerevisiae SAGA transcription coactivator complex. EMBO J. 33, 2534-2546
11. Huisin't Veld, P. J., Herzog, F., Ladurner, R., Davidson, I. F., Piric, S., Kreidl, E., Bhaskara, V., Aebersold, R., and Peters, J. M. (2014) Characterization of a DNA exit gate in the human cohesin ring. Science 346, 968-972
12. Barysz, H., Kim, J. H., Chen, Z. A., Hudson, D. F., Rappsilber, J., Gerloff, D. L., and Earnshaw, W. C. (2015) Three-dimensional topology of the SMC2/SMC4 subcomplex from chicken condensin I revealed by crosslinking and molecular modelling. Open Biol. 5, 150005
13. Kloet, S. L., Baymaz, H. I., Makowski, M., Groenewold, V., Jansen, P. W., Berendsen, M., Niazi, H., Kops, G. J., and Vermeulen, M. (2015) Towards elucidating the stability, dynamics and architecture of the nucleosome remodeling and deacetylase complex by using quantitative interaction proteomics. FEBS J. 282, 1774-1785
14. Nguyen-Huynh, N. T., Sharov, G., Potel, C., Fichter, P., Trowitzsch, S., Berger, I., Lamour, V., Schultz, P., Potier, N., and Leize-Wagner, E. (2015) Chemical cross-linking and mass spectrometry to determine the subunit interaction network in a recombinant human SAGA HAT subcomplex. Protein Sci. 24, 1232-1246
15. Herzog, F., Kahraman, A., Boehringer, D., Mak, R., Bracher, A., Walzthoeni, T., Leitner, A., Beck, M., Hartl, F. U., Ban, N., Malmstrom, L., and Aebersold, R. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry, Science 337, 1348-1352
16. Kaake, R. M., Wang, X., Burke, A., Yu, C., Kandur, W., Yang, Y., Novtisky, E. J., Second, T., Duan, J., Kao, A., Guan, S., Vellucci, D., Rychnovsky, S. D., and Huang, L. (2014) A new in vivo cross-linking mass spectrometry platform to define protein-protein interactions in living cells. Mol. Cell. Proteomics 13, 3533-3543
17. Fritzsche, R., Ihling, C. H., Gotze, M., and Sinz, A. (2012) Optimizing the enrichment of cross-linked products for mass spectrometric protein analysis. Rapid Commun. Mass Spectrom. 26, 653-658
18. Leitner, A., Reischl, R., Walzthoeni, T., Herzog, F., Bohn, S., Forster, F., and Aebersold, R. (2012) Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol. Cell. Proteomics 11, M111 014126
19. Leitner, A., Joachimiak, L. A., Unverdorben, P., Walzthoeni, T., Frydman, J., Forster, F., and Aebersold, R. (2014) Chemical cross-linking/mass spectrometry targeting acidic residues in proteins and protein complexes. Proc Natl Acad Sci U. S. A. 111, 9455-9460
20. Liu, F., Rijkers, D. T., Post, H., and Heck, A. J. (2015) Proteome-wide profiling of protein assemblies by cross-linking mass spectrometry. Nature Methods 12, 1179-1184
21. Eberl, H. C., Mann, M., and Vermeulen, M. (2011) Quantitative proteomics for epigenetics. Chembiochem 12, 224-234
22. Smits, A. H., Jansen, P. W., Poser, I., Hyman, A. A., and Vermeulen, M. (2012) Stoichiometry of chromatin-associated protein complexes revealed by label-free quantitative mass spectrometry-based proteomics. Nucleic Acids Res. gks941
23. Keilhauer, E. C., Hein, M. Y., and Mann, M. (2015) Accurate protein complex retrieval by affinity enrichment mass spectrometry (AE-MS) rather than affinity purification mass spectrometry (AP-MS). Mol. Cell. Proteomics 14, 120-135
24. Poser, I., Sarov, M., Hutchins, J. R., Hériché, J.-K., Toyoda, Y., Pozniakovsky, A., Weigl, D., Nitzsche, A., Hegemann, B., Bird, A. W., Pelletier, L., Kittler, R., Hua, S., Naumann, R., Augsburg, M., Sykora, M. M., Hofemeister, H., Zhang, Y., Nasmyth, K., White, K. P., Dietzel, S., Mechtler, K., Durbin, R., Stewart, A. F., Peters, J. M., Buchholz, F., and Hyman, A. A. (2008) BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nature Methods 5, 409-415
25. Hubner, N. C., Bird, A. W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., Hyman, A., and Mann, M. (2010) Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189, 739-754
26. Baymaz, H. I., Spruijt, C. G., and Vermeulen, M. (2014) Identifying Nuclear Protein-Protein Interactions Using GFP Affinity Purification and SILAC-Based Quantitative Mass Spectrometry in Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) pp. 207-226, Springer.
27. Shi, Y., Pellarin, R., Fridy, P. C., Fernandez-Martinez, J., Thompson, M. K., Li, Y., Wang, Q. J., Sali, A., Rout, M. P., and Chait, B. T. (2015) A strategy for dissecting the architectures of native macromolecular assemblies. Nature Methods 12, 1135-1138
28. Walzthoeni, T., Claassen, M., Leitner, A., Herzog, F., Bohn, S., Forster, F., Beck, M., and Aebersold, R. (2012) False discovery rate estimation for cross-linked peptides identified by mass spectrometry. Nature Methods 9, 901-903
29. Trnka, M. J., Baker, P. R., Robinson, P. J., Burlingame, A., and Chalkley, R. J. (2014) Matching cross-linked peptide spectra: only as good as the worse identification. Mol. Cell. Proteomics 13, 420-434
30. Yang, B., Wu, Y.-J., Zhu, M., Fan, S.-B., Lin, J., Zhang, K., Li, S., Chi, H., Li, Y.-X., and Chen, H.-F. (2012) Identification of cross-linked peptides from complex samples, Nature Methods 9, 904-906
31. Li, S., Lu, Y., Peng, B., and Ding, J. (2007) Crystal structure of human phosphoribosylpyrophosphate synthetase 1 reveals a novel allosteric site. Biochem. J. 401, 39-47
32. Walker, J. R., Corpina, R. A., and Goldberg, J. (2001) Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412, 607-614
33. Rivera-Calzada, A., Spagnolo, L., Pearl, L. H., and Llorca, O. (2007) Structural model of full-length human Ku70-Ku80 heterodimer and its recognition of DNA and DNA-PKcs. EMBO Rep. 8, 56-62
34. Coué, M., Amariglio, F., Maiorano, D., Bocquet, S., and Méchali, M. (1998) Evidence for Different MCM Subcomplexes with Differential Binding to Chromatin inXenopus. Exp. Cell Res. 245, 282-289
35. Maiorano, D., Lemaitre, J.-M., and Méchali, M. (2000) Stepwise regulated chromatin assembly of MCM2-7 proteins. J. Biol. Chem. 275, 8426-8431
36. Prokhorova, T. A., and Blow, J. J. (2000) Sequential MCM/P1 subcomplex assembly is required to form a heterohexamer with replication licensing activity. J. Biol. Chem. 275, 2491-2498
37. Moyer, S. E., Lewis, P. W., and Botchan, M. R. (2006) Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl. Acad. Sci. U. S. A. 103, 10236-10241
38. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
39. Cox, J., Hein, M. Y., Luber, C. A., Paron, I., Nagaraj, N., and Mann, M. (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics 13, 2513-2526
40. Chambers, M. C., Maclean, B., Burke, R., Amodei, D., Ruderman, D. L., Neumann, S., Gatto, L., Fischer, B., Pratt, B., Egertson, J., Hoff, K., Kessner, D., Tasman, N., Shulman, N., Frewen, B., Baker, T. A., Brusniak, M. Y., Paulse, C., Creasy, D., Flashner, L., Kani, K., Moulding, C., Seymour, S. L., Nuwaysir, L. M., Lefebvre, B., Kuhlmann, F., Roark, J., Rainer, P., Detlev, S., Hemenway, T., Huhmer, A., Langridge, J., Connolly, B., Chadick, T., Holly, K., Eckels, J., Deutsch, E. W., Moritz, R. L., Katz, J. E., Agus, D. B., MacCoss, M., Tabb, D. L., and Mallick, P. (2012) A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 30, 918-920
41. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Computational Chem. 25, 1605-1612
42. Combe, C. W., Fischer, L., and Rappsilber, J. (2015) xiNET: cross-link network maps with residue resolution. Mol. Cell. Proteomics 14, 1137-1147
43. Kosinski, J., von Appen, A., Ori, A., Karius, K., Müller, C. W., and Beck, M. (2015) Xlink Analyzer: Software for analysis and visualization of crosslinking data in the context of three-dimensional structures. J. Structural Biol. 189, 177-183
44. Yang, Z., Lasker, K., Schneidman-Duhovny, D., Webb, B., Huang, C. C., Pettersen, E. F., Goddard, T. D., Meng, E. C., Sali, A., and Ferrin, T. E. (2012) UCSF Chimera, MODELLER, and IMP: an integrated modeling system. J. Structural Biol. 179, 269-278
45. Meng, E. C., Pettersen, E. F., Couch, G. S., Huang, C. C., and Ferrin, T. E. (2006) Tools for integrated sequence-structure analysis with UCSF Chimera. BMC Bioinformatics 7, 339
46. Rice, P., Longden, I., and Bleasby, A. (2000) EMBOSS: the European molecular biology open software suite. Trends Genetics 16, 276-277
47. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385
48. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., and Bordoli, L. (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res., 42, W252-W258
49. Bakan, A., Meireles, L. M., and Bahar, I. (2011) ProDy: protein dynamics inferred from theory and experiments. Bioinformatics 27, 1575-1577
50. Humphrey, W., Dalke, A., and Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-8:27-8, 1996
51. Vizcaino, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Rios, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P. A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H. J., Albar, J. P., Martinez-Bartolome, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) Proteome-Xchange provides globally coordinated proteomics data submission and dissemination. Nature Biotechnol. 32, 223-226
52. Kita, K., Ishizuka, T., Ishijima, S., Sonoda, T., and Tatibana, M. (1994) A novel 39-kDa phosphoribosylpyrophosphate synthetase-associated protein of rat liver. Cloning, high sequence similarity to the catalytic subunits, and a negative regulatory role. J. Biol. Chem. 269, 8334-8340
53. Haering, C. H., Schoffnegger, D., Nishino, T., Helmhart, W., Nasmyth, K., and Löwe, J. (2004) Structure and stability of cohesin's Smc1-kleisin interaction. Mol. Cell. 15, 951-964
54. Gligoris, T. G., Scheinost, J. C., Bürmann, F., Petela, N., Chan, K.-L., Uluocak, P., Beckouët, F., Gruber, S., Nasmyth, K., and Löwe, J. (2014) Closing the cohesin ring: Structure and function of its Smc3-kleisin interface. Science 346, 963-967
55. Kurze, A., Michie, K. A., Dixon, S. E., Mishra, A., Itoh, T., Khalid, S., Strmecki, L., Shirahige, K., Haering, C. H., Löwe, J., and Nasmyth, K. (2011) A positively charged channel within the Smc1/Smc3 hinge required for sister chromatid cohesion. EMBO J. 30, 364-378
56. Burmann, F., Shin, H. C., Basquin, J., Soh, Y. M., Gimenez-Oya, V., Kim, Y. G., Oh, B. H., and Gruber, S. (2013) An asymmetric SMC-kleisin bridge in prokaryotic condensing. Nat. Struct. Mol. Biol. 20, 371-379
57. Belsom, A., Schneider, M., Fischer, L., Brock, O., and Rappsilber, J. (2015) Serum albumin domain structures in human blood serum by mass spectrometry and computational biology. Mol. Cell. Proteomics ePub article 10.1074/mcp. M115.048504
58. Dimova, K., Kalkhof, S., Pottratz, I., Ihling, C., Rodriguez-Castaneda, F., Liepold, T., Griesinger, C., Brose, N., Sinz, A., and Jahn, O. (2009) Structural insights into the calmodulin-Munc13 interaction obtained by cross-linking and mass spectrometry. Biochemistry 48, 5908-5921
59. Schmidt, C., and Robinson, C. V. (2014) A comparative cross-linking strategy to probe conformational changes in protein complexes. Nature Protocols 9, 2224-2236
60. Schmidt, C., Zhou, M., Marriott, H., Morgner, N., Politis, A., and Robinson, C. V. (2013) Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation. Nat. Commun. 4, 1985
61. Fischer, L., Chen, Z. A., and Rappsilber, J. (2013) Quantitative crosslinking/mass spectrometry using isotope-labelled cross-linkers. J. Proteomics 88, 120-128
62. Fridy, P. C., Li, Y., Keegan, S., Thompson, M. K., Nudelman, I., Scheid, J. F., Oeffinger, M., Nussenzweig, M. C., Fenyö, D., and Chait, B. T. (2014) A robust pipeline for rapid production of versatile nanobody repertoires. Nature Methods 11, 1253-1260
63. Petrotchenko, E. V., Serpa, J. J., and Borchers, C. H. (2011) An isotopically coded CID-cleavable biotinylated cross-linker for structural proteomics. Mol. Cell. Proteomics 10, M110.001420