Joining forces: Integrating proteomics and cross-linking with the mass spectrometry of intact complexes

Molecular and Cellular Proteomics

Volumn 11, Issue 3, 2012, Pages

  Stengel, Florian ^a,b   Aebersold, Ruedi ^b,c   Robinson, Carol V ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE; PROTEIN;

CHEMISTRY; DIMERIZATION; HUMAN; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEOMICS; REVIEW;

CHEMISTRY; HUMANS; MASS SPECTROMETRY; METABOLISM; METHODS; PROTEIN INTERACTION MAPPING; PROTEINS; PROTEOMICS;

EID: 84857938427     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.R111.014027     Document Type: Review

References (122)

1. Aebersold, R., and Mann, M. (2003) Mass spectrometry-based proteomics. Nature 422, 198-207 (Pubitemid 36362757)
2. Gstaiger, M., and Aebersold, R. (2009) Applying mass spectrometry-based proteomics to genetics, genomics and network biology. Nat. Rev. 10, 617-627
3. Walther, T. C., and Mann, M. (2010) Mass spectrometry-based proteomics in cell biology. J. Cell Biol. 190, 491-500
4. Cox, J., and Mann, M. (2011) Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 80, 273-299
5. 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 (Pubitemid 47106612)
6. Seebacher, J., and Gavin, A. C. (2011) SnapShot: Protein-protein interaction networks. Cell 144, 1000, 1000 e1001
7. Gavin, A. C., Maeda, K., and Kühner, S. (2011) Recent advances in charting protein-protein interaction: Mass spectrometry-based approaches. Curr. Opin. Biotechnol. 22, 42-49
8. Kaake, R. M., Wang, X., and Huang, L. (2010) Profiling of protein interaction networks of protein complexes using affinity purification and quantitative mass spectrometry. Mol. Cell. Proteomics 9, 1650-1665
9. Köcher, T., and Superti-Furga, G. (2007) Mass spectrometry-based functional proteomics: From molecular machines to protein networks. Nat. Methods 4, 807-815 (Pubitemid 350055577)
10. Sharon, M., and Robinson, C. V. (2007) The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem. 76, 167-193
11. Benesch, J. L., Ruotolo, B. T., Simmons, D. A., and Robinson, C. V. (2007) Protein complexes in the gas phase: Technology for structural genomics and proteomics. Chem. Rev. 107, 3544-3567 (Pubitemid 47322744)
12. Wyttenbach, T., and Bowers, M. T. (2007) Intermolecular interactions in biomolecular systems examined by mass spectrometry. Annu. Rev. Phys. Chem. 58, 511-533 (Pubitemid 46877600)
13. Heck, A. J. (2008) Native mass spectrometry: A bridge between interactomics and structural biology. Nat. Methods 5, 927-933
14. Domon, B., and Aebersold, R. (2006) Mass spectrometry and protein analysis. Science 312, 212-217
15. Ganem, B., Li, Y. T., and Henion, J. D. (1991) Detection of noncovalent receptor ligand complexes by mass spectrometry. J. Am. Chem. Soc. 113, 6294-6296
16. Sobott, F., Hernández, H., McCammon, M. G., Tito, M. A., and Robinson, C. V. (2002) A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 74, 1402-1407 (Pubitemid 34233333)
17. Hernández, H., and Robinson, C. V. (2007) Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2, 715-726 (Pubitemid 47040033)
18. Barrera, N. P., and Robinson, C. V. (2011) Advances in the mass spectrometry of membrane proteins: From individual proteins to intact complexes. Annu. Rev. Biochem. 80, 247-271
19. Chernushevich, I. V., and Thomson, B. A. (2004) Collisional cooling of large ions in electrospray mass spectrometry. Anal. Chem. 76, 1754-1760 (Pubitemid 38338425)
20. Rostom, A. A., and Robinson, C. V. (1999) Detection of the intact GroEL chaperonin assembly by mass spectrometry. J. Am. Chem. Soc. 121, 4718-4719 (Pubitemid 29239513)
21. Tahallah, N., Pinkse, M., Maier, C. S., and Heck, A. J. (2001) The effect of the source pressure on the abundance of ions of noncovalent protein assemblies in an electrospray ionization orthogonal time-of-flight instrument. Rapid Commun. Mass Spectrom. 15, 596-601 (Pubitemid 32391094)
22. van Duijn, E., Simmons, D. A., van den Heuvel, R. H., Bakkes, P. J., van Heerikhuizen, H., Heeren, R. M., Robinson, C. V., van der Vies, S. M., and Heck, A. J. (2006) Tandem mass spectrometry of intact GroEL-substrate complexes reveals substrate-specific conformational changes in the trans ring. J. Am. Chem. Soc. 128, 4694-4702
23. Benesch, J. L. (2009) Collisional activation of protein complexes: Picking up the pieces. J. Am. Soc. Mass Spectrom. 20, 341-348
24. Benesch, J. L., Ruotolo, B. T., Sobott, F., Wildgoose, J., Gilbert, A., Bateman, R., and Robinson, C. V. (2009) Quadrupole-time-of-flight mass spectrometer modified for higher-energy dissociation reduces protein assemblies to peptide fragments. Anal. Chem. 81, 1270-1274
25. Jurchen, J. C., Garcia, D. E., and Williams, E. R. (2003) Gas-phase dissociation pathways of multiply charged peptide clusters. J. Am. Soc. Mass Spectrom. 14, 1373-1386 (Pubitemid 37491042)
26. Pagel, K., Hyung, S. J., Ruotolo, B. T., and Robinson, C. V. (2010) Alternate dissociation pathways identified in charge-reduced protein complex ions. Anal. Chem. 82, 5363-5372
27. Felitsyn, N., Kitova, E. N., and Klassen, J. S. (2002) Thermal dissociation of the protein homodimer ecotin in the gas phase. J. Am. Soc. Mass Spectrom. 13, 1432-1442 (Pubitemid 36871594)
28. de la Mora, J. F. (2000) Electrospray ionization of large multiply charged species proceeds via Dole's charged residue mechanism. Anal. Chim. Acta 406, 93-104
29. Hernández, H., Dziembowski, A., Taverner, T., Séraphin, B., and Robinson, C. V. (2006) Subunit architecture of multimeric complexes isolated directly from cells. EMBO Reports 7, 605-610 (Pubitemid 43827327)
30. Sharon, M., Mao, H., Boeri Erba, E., Stephens, E., Zheng, N., and Robinson, C. V. (2009) Symmetrical modularity of the COP9 signalosome complex suggests its multifunctionality. Structure 17, 31-40
31. Zhou, M., Sandercock, A. M., Fraser, C. S., Ridlova, G., Stephens, E., Schenauer, M. R., Yokoi-Fong, T., Barsky, D., Leary, J. A., Hershey, J. W., Doudna, J. A., and Robinson, C. V. (2008) Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl. Acad. Sci. U.S.A. 105, 18139-18144
32. Lane, L. A., Fernández-Tornero, C., Zhou, M., Morgner, N., Ptchelkine, D., Steuerwald, U., Politis, A., Lindner, D., Gvozdenovic, J., Gavin, A. C., Müller, C. W., and Robinson, C. V. (2011) Mass spectrometry reveals stable modules in holo and apo RNA polymerases I and III. Structure 19, 90-100
33. Stengel, F., Baldwin, A. J., Painter, A. J., Jaya, N., Basha, E., Kay, L. E., Vierling, E., Robinson, C. V., and Benesch, J. L. (2010) Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. Proc. Natl. Acad. Sci. U.S.A. 107, 2007-2012
34. Uetrecht, C., Versluis, C., Watts, N. R., Roos, W. H., Wuite, G. J., Wingfield, P. T., Steven, A. C., and Heck, A. J. (2008) High-resolution mass spectrometry of viral assemblies: Molecular composition and stability of dimorphic hepatitis B virus capsids. Proc. Natl. Acad. Sci. U.S.A. 105, 9216-9220
35. Barrera, N. P., Di Bartolo, N., Booth, P. J., and Robinson, C. V. (2008) Micelles protect membrane complexes from solution to vacuum. Science 321, 243-246 (Pubitemid 351989094)
36. Barrera, N. P., Isaacson, S. C., Zhou, M., Bavro, V. N., Welch, A., Schaedler, T. A., Seeger, M. A., Miguel, R. N., Korkhov, V. M., van Veen, H. W., Venter, H., Walmsley, A. R., Tate, C. G., and Robinson, C. V. (2009) Mass spectrometry of membrane transporters reveals subunit stoichiometry and interactions. Nat. Methods 6, 585-587
37. Park, A. Y., Jergic, S., Politis, A., Ruotolo, B. T., Hirshberg, D., Jessop, L. L., Beck, J. L., Barsky, D., O'Donnell, M., Dixon, N. E., and Robinson, C. V. (2010) A single subunit directs the assembly of the Escherichia coli DNA sliding clamp loader. Structure 18, 285-292
38. Rostom, A. A., Fucini, P., Benjamin, D. R., Juenemann, R., Nierhaus, K. H., Hartl, F. U., Dobson, C. M., and Robinson, C. V. (2000) Detection and selective dissociation of intact ribosomes in a mass spectrometer. Proc. Natl. Acad. Sci. U. S. A. 97, 5185-5190 (Pubitemid 30313693)
39. Gordiyenko, Y., Deroo, S., Zhou, M., Videler, H., and Robinson, C. V. (2008) Acetylation of L12 increases interactions in the Escherichia coli ribosomal stalk complex. J. Mol. Biol. 380, 404-414
40. Hernández, H., Makarova, O. V., Makarov, E. M., Morgner, N., Muto, Y., Krummel, D. P., and Robinson, C. V. (2009) Isoforms of U1-70k control subunit dynamics in the human spliceosomal U1 snRNP. PLoS One 4, e7202
41. Lorenzen, K., Vannini, A., Cramer, P., and Heck, A. J. (2007) Structural biology of RNA polymerase III: Mass spectrometry elucidates subcomplex architecture. Structure 15, 1237-1245 (Pubitemid 47539158)
42. Schreiber, A., Stengel, F., Zhang, Z., Enchev, R. I., Kong, E. H., Morris, E. P., Robinson, C. V., da Fonseca, P. C., and Barford, D. (2011) Structural basis for the subunit assembly of the anaphase-promoting complex. Nature 470, 227-232
43. Sakata, E., Stengel, F., Fukunaga, K., Zhou, M., Saeki, Y., Förster, F., Baumeister, W., Tanaka, K., and Robinson, C. V. (2011) The catalytic activity of ubp6 enhances maturation of the proteasomal regulatory particle. Mol. Cell 42, 637-649
44. Taverner, T., Hernández, H., Sharon, M., Ruotolo, B. T., Matak-Vinković, D., Devos, D., Russell, R. B., and Robinson, C. V. (2008) Subunit architecture of intact protein complexes from mass spectrometry and homology modeling. Acc. Chem. Res. 41, 617-627
45. Park, A. Y., and Robinson, C. V. (2011) Protein-nucleic acid complexes and the role of mass spectrometry in their structure determination. Crit. Rev. Biochem. Mol. Biol. 46, 152-164
46. Uetrecht, C., Rose, R. J., van Duijn, E., Lorenzen, K., and Heck, A. J. (2010) Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 39, 1633-1655
47. Ruotolo, B. T., Giles, K., Campuzano, I., Sandercock, A. M., Bateman, R. H., and Robinson, C. V. (2005) Evidence for macromolecular protein rings in the absence of bulk water. Science 310, 1658-1661 (Pubitemid 41780783)
48. Pukala, T. L., Ruotolo, B. T., Zhou, M., Politis, A., Stefanescu, R., Leary, J. A., and Robinson, C. V. (2009) Subunit architecture of multiprotein assemblies determined using restraints from gas-phase measurements. Structure 17, 1235-1243
49. van Duijn, E., Barendregt, A., Synowsky, S., Versluis, C., and Heck, A. J. (2009) Chaperonin complexes monitored by ion mobility mass spectrometry. J. Am. Chem. Soc. 131, 1452-1459
50. Zhou, M., and Robinson, C. V. (2010) When proteomics meets structural biology. Trends Biochem. Sci. 35, 522-529
51. Damoc, E., Fraser, C. S., Zhou, M., Videler, H., Mayeur, G. L., Hershey, J. W., Doudna, J. A., Robinson, C. V., and Leary, J. A. (2007) Structural characterization of the human eukaryotic initiation factor 3 protein complex by mass spectrometry. Mol. Cell. Proteomics 6, 1135-1146 (Pubitemid 47099225)
52. Hinnebusch, A. G. (2006) eIF3: A versatile scaffold for translation initiation complexes. Trends Biochem. Sci. 31, 553-562
53. Masutani, M., Sonenberg, N., Yokoyama, S., and Imataka, H. (2007) Reconstitution reveals the functional core of mammalian eIF3. EMBO J. 26, 3373-3383 (Pubitemid 47123530)
54. Glickman, M. H., and Ciechanover, A. (2002) The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 82, 373-428 (Pubitemid 34654457)
55. Murata, S., Yashiroda, H., and Tanaka, K. (2009) Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 10, 104-115
56. Lander, G. C., Estrin, E., Matyskiela, M. E., Bashore, C., Nogales, E., and Martin, A. (2012) Complete subunit architecture of the proteasome regulatory particle. Nature Jan 11; 482(7384), 186-91. doi: 10.1038/nature10774
57. da Fonseca, P. C., and Morris, E. P. (2008) Structure of the human 26S proteasome: Subunit radial displacements open the gate into the proteolytic core. J. Biol. Chem. 283, 23305-23314
58. Bohn, S., Beck, F., Sakata, E., Walzthoeni, T., Beck, M., Aebersold, R., Förster, F., Baumeister, W., and Nickell, S. (2010) Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc. Natl. Acad. Sci. U.S.A. 107, 20992-20997
59. Saeki, Y., Toh-E., A., Kudo, T., Kawamura, H., and Tanaka, K. (2009) Multiple proteasome-interacting proteins assist the assembly of the yeast 19S regulatory particle. Cell 137, 900-913
60. Roelofs, J., Park, S., Haas, W., Tian, G., McAllister, F. E., Huo, Y., Lee, B. H., Zhang, F., Shi, Y., Gygi, S. P., and Finley, D. (2009) Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459, 861-865
61. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A. P., Punna, T., Peregrín-Alvarez, J. M., Shales, M., Zhang, X., Davey, M., Robinson, M. D., Paccanaro, A., Bray, J. E., Sheung, A., Beattie, B., Richards, D. P., Canadien, V., Lalev, A., Mena, F., Wong, P., Starostine, A., Canete, M. M., Vlasblom, J., Wu, S., Orsi, C., Collins, S. R., Chandran, S., Haw, R., Rilstone, J. J., Gandi, K., Thompson, N. J., Musso, G., St Onge, P., Ghanny, S., Lam, M. H., Butland, G., Altaf-Ul, A. M., Kanaya, S., Shilatifard, A., O'Shea, E., Weissman, J. S., Ingles, C. J., Hughes, T. R., Parkinson, J., Gerstein, M., Wodak, S. J., Emili, A., and Greenblatt, J. F. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643
62. Gavin, A. C., Aloy, P., Grandi, P., Krause, R., Boesche, M., Marzioch, M., Rau, C., Jensen, L. J., Bastuck, S., Dümpelfeld, B., Edelmann, A., Heurtier, M. A., Hoffman, V., Hoefert, C., Klein, K., Hudak, M., Michon, A. M., Schelder, M., Schirle, M., Remor, M., Rudi, T., Hooper, S., Bauer, A., Bouwmeester, T., Casari, G., Drewes, G., Neubauer, G., Rick, J. M., Kuster, B., Bork, P., Russell, R. B., and Superti-Furga, G. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636
63. Gavin, A. C., Bösche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J. M., Michon, A. M., Cruciat, C. M., Remor, M., Höfert, C., Schelder, M., Brajenovic, M., Ruffner, H., Merino, A., Klein, K., Hudak, M., Dickson, D., Rudi, T., Gnau, V., Bauch, A., Bastuck, S., Huhse, B., Leutwein, C., Heurtier, M. A., Copley, R. R., Edelmann, A., Querfurth, E., Rybin, V., Drewes, G., Raida, M., Bouwmeester, T., Bork, P., Seraphin, B., Kuster, B., Neubauer, G., and Superti-Furga, G. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147 (Pubitemid 34059510)
64. Malovannaya, A., Lanz, R. B., Jung, S. Y., Bulynko, Y., Le, N. T., Chan, D. W., Ding, C., Shi, Y., Yucer, N., Krenciute, G., Kim, B. J., Li, C., Chen, R., Li, W., Wang, Y., O'Malley, B. W., and Qin, J. (2011) Analysis of the human endogenous coregulator complexome. Cell 145, 787-799
65. Kühner, S., van Noort, V., Betts, M. J., Leo-Macias, A., Batisse, C., Rode, M., Yamada, T., Maier, T., Bader, S., Beltran-Alvarez, P., Castaño-Diez, D., Chen, W. H., Devos, D., Güell, M., Norambuena, T., Racke, I., Rybin, V., Schmidt, A., Yus, E., Aebersold, R., Herrmann, R., Böttcher, B., Frangakis, A. S., Russell, R. B., Serrano, L., Bork, P., and Gavin, A. C. (2009) Proteome organization in a genome-reduced bacterium. Science 326, 1235-1240
66. Bennett, E. J., Rush, J., Gygi, S. P., and Harper, J. W. (2010) Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 143, 951-965
67. Breitkreutz, A., Choi, H., Sharom, J. R., Boucher, L., Neduva, V., Larsen, B., Lin, Z. Y., Breitkreutz, B. J., Stark, C., Liu, G., Ahn, J., Dewar-Darch, D., Reguly, T., Tang, X., Almeida, R., Qin, Z. S., Pawson, T., Gingras, A. C., Nesvizhskii, A. I., and Tyers, M. (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328, 1043-1046
68. Guerrero, C., Tagwerker, C., Kaiser, P., and Huang, L. (2006) An integrated mass spectrometry-based proteomic approach: Quantitative analysis of tandem affinity-purified in vivo cross-linked protein complexes (QTAX) to decipher the 26 S proteasome-interacting network. Mol. Cell. Proteomics 5, 366-378 (Pubitemid 43329314)
69. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Séraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032 (Pubitemid 29474865)
70. Glatter, T., Wepf, A., Aebersold, R., and Gstaiger, M. (2009) An integrated workflow for charting the human interaction proteome: Insights into the PP2A system. Mol. Syst Biol. 5, 237
71. 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. Nat. Methods 5, 409-415 (Pubitemid 351619099)
72. Sowa, M. E., Bennett, E. J., Gygi, S. P., and Harper, J. W. (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403
73. Wepf, A., Glatter, T., Schmidt, A., Aebersold, R., and Gstaiger, M. (2009) Quantitative interaction proteomics using mass spectrometry. Nat. Methods 6, 203-205
74. 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
75. Pflieger, D., Jünger, M. A., Müller, M., Rinner, O., Lee, H., Gehrig, P. M., Gstaiger, M., and Aebersold, R. (2008) Quantitative proteomic analysis of protein complexes: Concurrent identification of interactors and their state of phosphorylation. Mol. Cell. Proteomics 7, 326-346 (Pubitemid 351298447)
76. Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W., and Gygi, S. P. (2003) Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. U.S.A. 100, 6940-6945 (Pubitemid 36706372)
77. Beynon, R. J., Doherty, M. K., Pratt, J. M., and Gaskell, S. J. (2005) Multiplexed absolute quantification in proteomics using artificial QCAT proteins of concatenated signature peptides. Nat. Methods 2, 587-589 (Pubitemid 41086849)
78. Rinner, O., Mueller, L. N., Hubálek, M., Müller, M., Gstaiger, M., and Aebersold, R. (2007) An integrated mass spectrometric and computational framework for the analysis of protein interaction networks. Nat. Biotechnol. 25, 345-352 (Pubitemid 46398770)
79. Vermeulen, M., Hubner, N. C., and Mann, M. (2008) High confidence determination of specific protein-protein interactions using quantitative mass spectrometry. Curr. Opin. Biotechnol. 19, 331-337
80. Ranish, J. A., Yi, E. C., Leslie, D. M., Purvine, S. O., Goodlett, D. R., Eng, J., and Aebersold, R. (2003) The study of macromolecular complexes by quantitative proteomics. Nat. Genet. 33, 349-355 (Pubitemid 36278851)
81. Clegg, C., and Hayes, D. (1974) Identification of neighbouring proteins in the ribosomes of Escherichia coli: A topographical study with the cross-linking reagent dimethyl suberimidate. Eur. J. Biochem. 42, 21-28
82. Young, M. M., Tang, N., Hempel, J. C., Oshiro, C. M., Taylor, E. W., Kuntz, I. D., Gibson, B. W., and Dollinger, G. (2000) High throughput protein fold identification by using experimental constraints derived from intramolecular cross-links and mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 97, 5802-5806 (Pubitemid 30367479)
83. Leitner, A., Reischl, R., Walzthoeni, T., Herzog, F., Bohn, S., Förster, 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
84. 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
85. Sinz, A. (2006) Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions. Mass Spectrom. Rev. 25, 663-682
86. Jin Lee, Y. (2008) Mass spectrometric analysis of cross-linking sites for the structure of proteins and protein complexes. Mol. Biosyst. 4, 816-823
87. Tang, X., and Bruce, J. E. (2009) Chemical cross-linking for protein-protein interaction studies. Methods Mol. Biol. 492, 283-293
88. Mouradov, D., King, G., Ross, I. L., Forwood, J. K., Hume, D. A., Sinz, A., Martin, J. L., Kobe, B., and Huber, T. (2008) Protein structure determination using a combination of cross-linking, mass spectrometry, and molecular modeling. Methods Mol. Biol. 426, 459-474
89. Singh, P., Panchaud, A., and Goodlett, D. R. (2010) Chemical cross-linking and mass spectrometry as a low-resolution protein structure determination technique. Anal. Chem. 82, 2636-2642
90. Sinz, A. (2007) Investigation of protein-ligand interactions by mass spectrometry. ChemMedChem 2, 425-431
91. Maiolica, A., Cittaro, D., Borsotti, D., Sennels, L., Ciferri, C., Tarricone, C., Musacchio, A., and Rappsilber, J. (2007) Structural analysis of multi-protein complexes by cross-linking, mass spectrometry, and database searching. Mol. Cell. Proteomics 6, 2200-2211
92. Ciferri, C., Pasqualato, S., Screpanti, E., Varetti, G., Santaguida, S., Dos Reis, G., Maiolica, A., Polka, J., De Luca, J. G., De Wulf, P., Salek, M., Rappsilber, J., Moores, C. A., Salmon, E. D., and Musacchio, A. (2008) Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133, 427-439 (Pubitemid 351622013)
93. Trnka, M. J., and Burlingame, A. L. (2010) Topographic studies of the GroEL-GroES chaperonin complex by chemical cross-linking using diformyl ethynylbenzene: The power of high resolution electron transfer dissociation for determination of both peptide sequences and their attachment sites. Mol. Cell. Proteomics 9, 2306-2317
94. 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., and Rappsilber, J. (2010) Architecture of the RNA polymerase IITFIIF complex revealed by cross-linking and mass spectrometry. EMBO J. 29, 717-726
95. Rinner, O., Seebacher, J., Walzthoeni, T., Mueller, L. N., Beck, M., Schmidt, A., Mueller, M., and Aebersold, R. (2008) Identification of cross-linked peptides from large sequence databases. Nat. Methods 5, 315-318 (Pubitemid 351455158)
96. Xu, H., Hsu, P. H., Zhang, L., Tsai, M. D., and Freitas, M. A. (2010) Database search algorithm for identification of intact cross-links in proteins and peptides using tandem mass spectrometry. J. Proteome Res. 9, 3384-3393
97. Singh, P., Shaffer, S. A., Scherl, A., Holman, C., Pfuetzner, R. A., Larson Freeman, T. J., Miller, S. I., Hernandez, P., Appel, R. D., and Goodlett, D. R. (2008) Characterization of protein cross-links via mass spectrometry and an open-modification search strategy. Anal. Chem. 80, 8799-8806
98. Petrotchenko, E. V., and Borchers, C. H. (2010) ICC-CLASS: Isotopically-coded cleavable cross-linking analysis software suite. BMC Bioinformatics 11, 64
99. McIlwain, S., Draghicescu, P., Singh, P., Goodlett, D. R., and Noble, W. S. (2010) Detecting cross-linked peptides by searching against a database of cross-linked peptide pairs. J. Proteome Res. 9, 2488-2495
100. Chu, F., Baker, P. R., Burlingame, A. L., and Chalkley, R. J. (2010) Finding chimeras: A bioinformatics strategy for identification of cross-linked peptides. Mol. Cell. Proteomics 9, 25-31
101. Rappsilber, J. (2011) The beginning of a beautiful friendship: Cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. J. Struct. Biol. 173, 530-540
102. Tang, X., Munske, G. R., Siems, W. F., and Bruce, J. E. (2005) Mass spectrometry identifiable cross-linking strategy for studying protein-protein interactions. Anal. Chem. 77, 311-318 (Pubitemid 40096700)
103. Zheng, C., Yang, L., Hoopmann, M. R., Eng, J. K., Tang, X., Weisbrod, C. R., and Bruce, J. E. (2011) Cross-linking measurements of in vivo protein complex topologies. Mol. Cell. Proteomics 10.1074/mcp.M110.006841
104. Gold, M. G., Stengel, F., Nygren, P. J., Weisbrod, C. R., Bruce, J. E., Robinson, C. V., Barford, D., and Scott, J. D. (2011) Architecture and dynamics of an A-kinase anchoring protein 79 (AKAP79) signaling complex. Proc. Natl. Acad. Sci. U.S.A. 108, 6426-6431
105. Ruotolo, B. T., and Robinson, C. V. (2006) Aspects of native proteins are retained in vacuum. Curr. Opin. Chem. Biol. 10, 402-408 (Pubitemid 44375072)
106. von Helden, G., Wyttenbach, T., and Bowers, M. T. (1995) Conformation of macromolecules in the gas phase: Use of matrix-assisted laser desorption methods in ion chromatography. Science 267, 1483-1485
107. Ruotolo, B. T., Benesch, J. L., Sandercock, A. M., Hyung, S. J., and Robinson, C. V. (2008) Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc. 3, 1139-1152
108. Bush, M. F., Hall, Z., Giles, K., Hoyes, J., Robinson, C. V., and Ruotolo, B. T. (2010) Collision cross sections of proteins and their complexes: A calibration framework and database for gas-phase structural biology. Anal. Chem. 82, 9557-9565
109. Politis, A., Park, A. Y., Hyung, S. J., Barsky, D., Ruotolo, B. T., and Robinson, C. V. (2010) Integrating ion mobility mass spectrometry with molecular modelling to determine the architecture of multiprotein complexes. PLoS One 5, e12080
110. Wang, S. C., Politis, A., Di Bartolo, N., Bavro, V. N., Tucker, S. J., Booth, P. J., Barrera, N. P., and Robinson, C. V. (2010) Ion mobility mass spectrometry of two tetrameric membrane protein complexes reveals compact structures and differences in stability and packing. J. Am. Chem. Soc. 132, 15468-15470
111. Loo, J. A., Berhane, B., Kaddis, C. S., Wooding, K. M., Xie, Y., Kaufman, S. L., and Chernushevich, I. V. (2005) Electrospray ionization mass spectrometry and ion mobility analysis of the 20S proteasome complex. J. Am. Soc. Mass Spectrom. 16, 998-1008 (Pubitemid 40828781)
112. Ekeowa, U. I., Freeke, J., Miranda, E., Gooptu, B., Bush, M. F., Pérez, J., Teckman, J., Robinson, C. V., and Lomas, D. A. (2010) Defining the mechanism of polymerization in the serpinopathies. Proc. Natl. Acad. Sci. U.S.A. 107, 17146-17151
113. Koschubs, T., Lorenzen, K., Baumli, S., Sandström, S., Heck, A. J., and Cramer, P. (2010) Preparation and topology of the mediator middle module. Nucleic Acids Res. 38, 3186-3195
114. Siridechadilok, B., Fraser, C. S., Hall, R. J., Doudna, J. A., and Nogales, E. (2005) Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310, 1513-1515 (Pubitemid 41746350)
115. Barford, D. (2011) Structure, function and mechanism of the anaphase promoting complex (APC/C). Q Rev. Biophys. 44, 153-190
116. Herzog, F., Primorac, I., Dube, P., Lenart, P., Sander, B., Mechtler, K., Stark, H., and Peters, J. M. (2009) Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex. Science 323, 1477-1481
117. da Fonseca, P. C., Kong, E. H., Zhang, Z., Schreiber, A., Williams, M. A., Morris, E. P., and Barford, D. (2011) Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 470, 274-278
118. Muñoz, I. G., Yébenes, H., Zhou, M., Mesa, P., Serna, M., Park, A. Y., Bragado-Nilsson, E., Beloso, A., de Cárcer, G., Malumbres, M., Robinson, C. V., Valpuesta, J. M., and Montoya, G. (2011) Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin. Nat. Struct. Mol. Biol. 18, 14-19
119. de Godoy, L. M., Olsen, J. V., Cox, J., Nielsen, M. L., Hubner, N. C., Fröhlich, F., Walther, T. C., and Mann, M. (2008) Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455, 1251-1254
120. Kisko, K., Brozzo, M. S., Missimer, J., Schleier, T., Menzel, A., Leppänen, V. M., Alitalo, K., Walzthoeni, T., Aebersold, R., and Ballmer-Hofer, K. (2011) Structural analysis of vascular endothelial growth factor receptor-2/ligand complexes by small-angle X-ray solution scattering. FASEB J. 25, 2980-2986
121. Buey, R. M., Mohan, R., Leslie, K., Walzthoeni, T., Missimer, J. H., Menzel, A., Bjelic, S., Bargsten, K., Grigoriev, I., Smal, I., Meijering, E., Aebersold, R., Akhmanova, A., and Steinmetz, M. O. (2011) Insights into EB structure and the role of its C-terminal domain in discriminating microtubule tips from lattice. Mol. Biol. Cell 22, 2912-2923
122. Lasker, K., Förster, F., Bohn, S., Walzthoeni, T., Villa, E., Unverdorben, P., Beck, F., Aebersold, R., Sali, A., and Baumeister, W. (2012) Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl. Acad. Sci. U.S.A. Jan 31; 109(5), 1380-1387