Integrating mass spectrometry of intact protein complexes into structural proteomics

Proteomics

Volumn 12, Issue 10, 2012, Pages 1547-1564

  Hyung, Suk Joon ^a   Ruotolo, Brandon T ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

High throughput; Noncovalent complexes; Protein ligand screening; Structural genomics; Systems biology; Technology

Indexed keywords

PROTEIN;

AMINO ACID SEQUENCE; CHEMICAL LABELING; CROSS LINKING; DEUTERIUM HYDROGEN EXCHANGE; HUMAN; MASS SPECTROMETRY; MOLECULAR INTERACTION; MOLECULAR MODEL; OXIDATIVE FOOT PRINTING MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; REVIEW; SPECTROMETRY; STRUCTURAL PROTEOMICS; TANDEM MASS SPECTROMETRY;

ANIMALS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MASS SPECTROMETRY; MULTIPROTEIN COMPLEXES; PROTEOMICS; SYSTEMS BIOLOGY;

EID: 84862663706     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100520     Document Type: Review

References (193)

1. Kuhner, S., van Noort, V., Betts, M. J., Leo-Macias, A. et al., Proteome organization in a genome-reduced bacterium. Science 2009, 326, 1235-1240.
2. Tarassov, K., Messier, V., Landry, C. R., Radinovic, S. et al., An in vivo map of the yeast protein interactome. Science 2008, 320, 1465-1470.
3. Rix, U., Superti-Furga, G., Target profiling of small molecules by chemical proteomics. Nat. Chem. Biol. 2009, 5, 616-624.
4. Shi, W., Chance, M. R., Metalloproteomics: forward and reverse approaches in metalloprotein structural and functional characterization. Curr. Opin. Chem. Biol. 2011, 15, 144-148.
5. Young, N. L., Plazas-Mayorca, M. D., Garcia, B. A., Systems-wide proteomic characterization of combinatorial post-translational modification patterns. Expert Rev. Proteomics 2010, 7, 79-92.
6. Yang, Z., Progress and challenges in protein structure prediction. Curr. Opin. Struct. Biol. 2008, 18, 342-348.
7. Alber, F., Dokudovskaya, S., Veenhoff, L. M., Zhang, W. et al., The molecular architecture of the nuclear pore complex. Nature 2007, 450, 695-701.
8. 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.
9. Englander, S. W., Hydrogen exchange and mass spectrometry: a historical perspective. J. Am. Soc. Mass Spectrom. 2006, 17, 1481-1489.
10. Engen, J. R., Analysis of protein conformation and dynamics by hydrogen/deuterium exchange MS. Anal. Chem. 2009, 81, 7870-7875.
11. Kaltashov, I. A., Bobst, C. E., Abzalimov, R. R., H/D exchange and mass spectrometry in the studies of protein conformation and dynamics: is there a need for a top-down approach? Anal. Chem. 2009, 81, 7892-7899.
12. Chalmers, M. J., Busby, S. A., Pascal, B. D., West, G. M. et al., Differential hydrogen/deuterium exchange mass spectrometry analysis of protein-ligand interactions. Expert Rev. Proteomics 2011, 8, 43-59.
13. Konermann, L., Pan, J., Liu, Y. H., Hydrogen exchange mass spectrometry for studying protein structure and dynamics. Chem. Soc. Rev. 2011, 40, 1224-1234.
14. Jin Lee, Y., Mass spectrometric analysis of cross-linking sites for the structure of proteins and protein complexes. Mol. Biosyst. 2008, 4, 816-823.
15. Leitner, A., Walzthoeni, T., Kahraman, A., Herzog, F. et al., Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics. Mol. Cell. Proteomics 2010, 9, 1634-1649.
16. Petrotchenko, E. V., Borchers, C. H., Crosslinking combined with mass spectrometry for structural proteomics. Mass Spectrom. Rev. 2010, 29, 862-876.
17. Konermann, L., Stocks, B. B., Pan, Y., Tong, X., Mass spectrometry combined with oxidative labeling for exploring protein structure and folding. Mass Spectrom. Rev. 2010, 29, 651-667.
18. Kiselar, J. G., Chance, M. R., Future directions of structural mass spectrometry using hydroxyl radical footprinting. J. Mass Spectrom. 2010, 45, 1373-1382.
19. Simon, J. H., The structural aspects of limited proteolysis of native proteins. BBA-Protein Struct. M. 1998, 1382, 191-206.
20. Fontana, A., de Laureto, P. P., Spolaore, B., Frare, E. et al., Probing protein structure by limited proteolysis. Acta. Biochim. Pol. 2004, 51, 299-321.
21. Yates, J. R., Ruse, C. I., Nakorchevsky, A., Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng. 2009, 11, 49-79.
22. Uetrecht, C., Rose, R. J., van Duijn, E., Lorenzen, K. et al., Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 2010, 39, 1633-1655.
23. Kanu, A. B., Dwivedi, P., Tam, M., Matz, L. et al., Ion mobility-mass spectrometry. J. Mass Spectrom. 2008, 43, 1-22.
24. Bohrer, B. C., Merenbloom, S. I., Koeniger, S. L., Hilderbrand, A. E. et al., Biomolecule analysis by ion mobility spectrometry. Annu. Rev. Anal. Chem. 2008, 1, 293-327.
25. Chernushevich, I. V., Thomson, B. A., Collisional cooling of large ions in electrospray mass spectrometry. Anal. Chem. 2004, 76, 1754-1760.
26. Sobott, F., Hernandez, H., McCammon, M. G., Tito, M. A. et al., A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 2002, 74, 1402-1407.
27. van den Heuvel, R. H., van Duijn, E., Mazon, H., Synowsky, S. A. et al., Improving the performance of a quadrupole time-of-flight instrument for macromolecular mass spectrometry. Anal. Chem. 2006, 78, 7473-7483.
28. Benesch, J. L., Ruotolo, B. T., Simmons, D. A., Robinson, C. V., Protein complexes in the gas phase: technology for structural genomics and proteomics. Chem. Rev. 2007, 107, 3544-3567.
29. Heck, A. J. R., Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 2008, 5, 927-933.
30. Zhou, M., Robinson, C. V., When proteomics meets structural biology. Trends Biochem. Sci. 2010, 35, 522-529.
31. Kelleher, N. L., Top-down proteomics. Anal. Chem. 2004, 76, 197A-203A.
32. Cui, W., Rohrs, H. W., Gross, M. L., Top-down mass spectrometry: recent developments, applications and perspectives. Analyst 2011, 136, 3854-3864.
33. Paizs, B., Suhai, S., Fragmentation pathways of protonated peptides. Mass Spectrom. Rev. 2005, 24, 508-548.
34. Cooper, H. J., Hakansson, K., Marshall, A. G., The role of electron capture dissociation in biomolecular analysis. Mass Spectrom. Rev. 2005, 24, 201-222.
35. Mann, M., Hendrickson, R. C., Pandey, A., Analysis of proteins and proteomes by mass spectrometry. Annu. Rev. Biochem. 2001, 70, 437-473.
36. Counterman, A. E., Clemmer, D. E., Large anhydrous polyalanine ions: evidence for extended helices and onset of a more compact state. J. Am. Chem. Soc. 2001, 123, 1490-1498.
37. Jarrold, M. F., Helices and sheets in vacuo. Phys. Chem. Chem. Phys. 2007, 9, 1659-1671.
38. Ruotolo, B. T., Tate, C. C., Russell, D. H., Ion mobility-mass spectrometry applied to cyclic peptide analysis: conformational preferences of gramicidin S and linear analogs in the gas phase. J. Am. Soc. Mass Spectrom. 2004, 15, 870-878.
39. Ruotolo, B. T., Gillig, K. J., Woods, A. S., Egan, T. F. et al., Analysis of phosphorylated peptides by ion mobility-mass spectrometry. Anal. Chem. 2004, 76, 6727-6733.
40. Ruotolo, B. T., Verbeck, G. F., Thomson, L. M., Woods, A. S. et al., Distinguishing between phosphorylated and nonphosphorylated peptides with ion mobility-mass spectrometry. J. Proteome Res. 2002, 1, 303-306.
41. McLean, J. A., The mass-mobility correlation redux: the conformational landscape of anhydrous biomolecules. J. Am. Soc. Mass Spectrom. 2009, 20, 1775-1781.
42. Baumketner, A., Bernstein, S. L., Wyttenbach, T., Bitan, G. et al., Amyloid beta-protein monomer structure: a computational and experimental study. Protein Sci. 2006, 15, 420-428.
43. Wyttenbach, T., Bowers, M. T., Intermolecular interactions in biomolecular systems examined by mass spectrometry. Annu. Rev. Phys. Chem. 2007, 58, 511-533.
44. Jurneczko, E., Barran, P. E., How useful is ion mobility mass spectrometry for structural biology? The relationship between protein crystal structures and their collision cross sections in the gas phase. Analyst 2011, 136, 20-28.
45. Rizzo, T. R., Stearns, J. A., Boyarkin, O. V., Spectroscopic studies of cold, gas-phase biomolecular ions. Int. Rev. Phys. Chem. 2009, 28, 481-515.
46. Fabris, D., Yu, E. T., Elucidating the higher-order structure of biopolymers by structural probing and mass spectrometry: MS3D. J. Mass Spectrom. 2010, 45, 841-860.
47. Sinz, A., Investigation of protein-protein interactions in living cells by chemical crosslinking and mass spectrometry. Anal. Bioanal. Chem. 2010, 397, 3433-3440.
48. Sharon, M., Robinson, C. V., The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem. 2007, 76, 167-193.
49. Rand, K. D., Adams, C. M., Zubarev, R. A., Jorgensen, T. J., Electron capture dissociation proceeds with a low degree of intramolecular migration of peptide amide hydrogens. J. Am. Chem. Soc. 2008, 130, 1341-1349.
50. Pan, J., Han, J., Borchers, C. H., Konermann, L., Hydrogen/deuterium exchange mass spectrometry with top-down electron capture dissociation for characterizing structural transitions of a 17 kDa protein. J. Am. Chem. Soc. 2009, 131, 12801-12808.
51. Rand, K. D., Zehl, M., Jensen, O. N., Jorgensen, T. J., Protein hydrogen exchange measured at single-residue resolution by electron transfer dissociation mass spectrometry. Anal. Chem. 2009, 81, 5577-5584.
52. Zhang, J., Chalmers, M. J., Stayrook, K. R., Burris, L. L. et al., Hydrogen/deuterium exchange reveals distinct agonist/partial agonist receptor dynamics within vitamin D receptor/retinoid X receptor heterodimer. Structure 2010, 18, 1332-1341.
53. West, G. M., Chien, E. Y., Katritch, V., Gatchalian, J. et al., Ligand-dependent perturbation of the conformational ensemble for the GPCR beta(2) adrenergic receptor revealed by HDX. Structure 2011, 19, 1424-1432.
54. Marcsisin, S. R., Narute, P. S., Emert-Sedlak, L. A., Kloczewiak, M. et al., On the solution conformation and dynamics of the HIV-1 viral infectivity factor. J. Mol. Biol. 2011, 410, 1008-1022.
55. Morgan, C. R., Hebling, C. M., Rand, K. D., Stafford, D. W. et al., Conformational transitions in the membrane scaffold protein of phospholipid bilayer nanodiscs. Mol. Cell Proteomics 2011, 10, M111. 010876.
56. Pan, J., Han, J., Borchers, C. H., Konermann, L., Characterizing short-lived protein folding intermediates by top-down hydrogen exchange mass spectrometry. Anal. Chem. 2010, 82, 8591-8597.
57. Choi, J. H., Banks, A. S., Kamenecka, T. M., Busby, S. A. et al., Antidiabetic actions of a non-agonist PPARgamma ligand blocking Cdk5-mediated phosphorylation. Nature 2011, 477, 477-481.
58. Wang, L., Lane, L. C., Smith, D. L., Detecting structural changes in viral capsids by hydrogen exchange and mass spectrometry. Protein Sci. 2001, 10, 1234-1243.
59. Zhang, X., Chien, E. Y., Chalmers, M. J., Pascal, B. D. et al., Dynamics of the beta2-adrenergic G-protein coupled receptor revealed by hydrogen-deuterium exchange. Anal. Chem. 2010, 82, 1100-1108.
60. Hebling, C. M., Morgan, C. R., Stafford, D. W., Jorgenson, J. W. et al., Conformational analysis of membrane proteins in phospholipid bilayer nanodiscs by hydrogen exchange mass spectrometry. Anal. Chem. 2010, 82, 5415-5419.
61. Toyama, B. H., Kelly, M. J., Gross, J. D., Weissman, J. S., The structural basis of yeast prion strain variants. Nature 2007, 449, 233-237.
62. Smirnovas, V., Baron, G. S., Offerdahl, D. K., Raymond, G. J. et al., Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 2011, 18, 504-506.
63. Carulla, N., Zhou, M., Giralt, E., Robinson, C. V. et al., Structure and intermolecular dynamics of aggregates populated during amyloid fibril formation studied by hydrogen/deuterium exchange. Acc. Chem. Res. 2010, 43, 1072-1079.
64. Williams, A. D., Sega, M., Chen, M., Kheterpal, I. et al., Structural properties of Abeta protofibrils stabilized by a small molecule. Proc. Natl. Acad. Sci. USA 2005, 102, 7115-7120.
65. Mendoza, V. L., Vachet, R. W., Probing protein structure by amino acid-specific covalent labeling and mass spectrometry. Mass Spectrom. Rev. 2009, 28, 785-815.
66. Hambly, D. M., Gross, M. L., Laser flash photolysis of hydrogen peroxide to oxidize protein solvent-accessible residues on the microsecond timescale. J. Am. Soc. Mass Spectrom. 2005, 16, 2057-2063.
67. Stocks, B. B., Konermann, L., Structural characterization of short-lived protein unfolding intermediates by laser-induced oxidative labeling and mass spectrometry. Anal. Chem. 2009, 81, 20-27.
68. Chen, J., Rempel, D. L., Gross, M. L., Temperature jump and fast photochemical oxidation probe submillisecond protein folding. J. Am. Chem. Soc. 2010, 132, 15502-15504.
69. Stocks, B. B., Rezvanpour, A., Shaw, G. S., Konermann, L., Temporal development of protein structure during S100A11 folding and dimerization probed by oxidative labeling and mass spectrometry. J. Mol. Biol. 2011, 409, 669-679.
70. Wang, L., Qin, Y., Ilchenko, S., Bohon, J. et al., Structural analysis of a highly glycosylated and unliganded gp120-based antigen using mass spectrometry. Biochemistry 2010, 49, 9032-9045.
71. Angel, T. E., Gupta, S., Jastrzebska, B., Palczewski, K. et al., Structural waters define a functional channel mediating activation of the GPCR, rhodopsin. Proc. Natl. Acad. Sci. USA 2009, 106, 14367-14372.
72. Gavin, A. C., Bosche, M., Krause, R., Grandi, P. et al., Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415, 141-147.
73. Butland, G., Peregrin-Alvarez, J. M., Li, J., Yang, W. et al., Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005, 433, 531-537.
74. Gavin, A. C., Aloy, P., Grandi, P., Krause, R. et al., Proteome survey reveals modularity of the yeast cell machinery. Nature 2006, 440, 631-636.
75. Krogan, N. J., Cagney, G., Yu, H., Zhong, G. et al., Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440, 637-643.
76. Gavin, A. C., Maeda, K., Kuhner, S., Recent advances in charting protein-protein interaction: mass spectrometry-based approaches. Curr. Opin. Biotechnol. 2011, 22, 42-49.
77. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M. et al., A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17, 1030-1032.
78. Einhauer, A., Jungbauer, A., The FLAG peptide, a versatile fusion tag for the purification of recombinant proteins. J. Biochem. Biophys. Methods 2001, 49, 455-465.
79. Blagoev, B., Kratchmarova, I., Ong, S. E., Nielsen, M. et al., A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat Biotechnol 2003, 21, 315-318.
80. Ross, P. L., Huang, Y. N., Marchese, J. N., Williamson, B. et al., Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell Proteomics 2004, 3, 1154-1169.
81. Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F. et al., Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 1999, 17, 994-999.
82. Bouwmeester, T., Bauch, A., Ruffner, H., Angrand, P. O. et al., A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat. Cell Biol. 2004, 6, 97-105.
83. Jeronimo, C., Forget, D., Bouchard, A., Li, Q. et al., Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol. Cell 2007, 27, 262-274.
84. Behrends, C., Sowa, M. E., Gygi, S. P., Harper, J. W., Network organization of the human autophagy system. Nature 2010, 466, 68-76.
85. Sowa, M. E., Bennett, E. J., Gygi, S. P., Harper, J. W., Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138, 389-403.
86. Jao, D. L., Chen, K. Y., Tandem affinity purification revealed the hypusine-dependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. J. Cell Biochem. 2006, 97, 583-598.
87. Behzadnia, N., Golas, M. M., Hartmuth, K., Sander, B. et al., Composition and three-dimensional EM structure of double affinity-purified, human prespliceosomal A complexes. EMBO J. 2007, 26, 1737-1748.
88. de Wulf, P., McAinsh, A. D., Sorger, P. K., Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev. 2003, 17, 2902-2921.
89. 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.
90. Lee, Y. J., Lackner, L. L., Nunnari, J. M., Phinney, B. S., Shotgun cross-linking analysis for studying quaternary and tertiary protein structures. J. Proteome Res. 2007, 6, 3908-3917.
91. Vasilescu, J., Guo, X. C., Kast, J., Identification of protein-protein interactions using in vivo cross-linking and mass spectrometry. Proteomics 2004, 4, 3845-3854.
92. Chu, F., Shan, S. O., Moustakas, D. T., Alber, F. et al., Unraveling the interface of signal recognition particle and its receptor by using chemical cross-linking and tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 2004, 101, 16454-16459.
93. Chu, F., Maynard, J. C., Chiosis, G., Nicchitta, C. V. et al., Identification of novel quaternary domain interactions in the Hsp90 chaperone, GRP94. Protein Sci. 2006, 15, 1260-1269.
94. Maiolica, A., Cittaro, D., Borsotti, D., Sennels, L. et al., Structural analysis of multiprotein complexes by cross-linking, mass spectrometry, and database searching. Mol. Cell Proteomics 2007, 6, 2200-2211.
95. Schulz, D. M., Kalkhof, S., Schmidt, A., Ihling, C. et al., Annexin A2/P11 interaction: new insights into annexin A2 tetramer structure by chemical crosslinking, high-resolution mass spectrometry, and computational modeling. Proteins 2007, 69, 254-269.
96. Pimenova, T., Nazabal, A., Roschitzki, B., Seebacher, J. et al., Epitope mapping on bovine prion protein using chemical cross-linking and mass spectrometry. J. Mass Spectrom. 2008, 43, 185-195.
97. Dimova, K., Kalkhof, S., Pottratz, I., Ihling, C. et al., Structural insights into the calmodulin-Munc13 interaction obtained by cross-linking and mass spectrometry. Biochemistry 2009, 48, 5908-5921.
98. Trnka, M. J., Burlingame, A. L., 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 2010, 9, 2306-2317.
99. Chen, Z. A., Jawhari, A., Fischer, L., Buchen, C. et al., Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J. 2010, 29, 717-726.
100. Sinz, A., Chemical cross-linking and mass spectrometry for mapping three-dimensional structures of proteins and protein complexes. J. Mass Spectrom. 2003, 38, 1225-1237.
101. 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.
102. Petrotchenko, E. V., Xiao, K., Cable, J., Chen, Y. et al., BiPS, a photocleavable, isotopically coded, fluorescent cross-linker for structural proteomics. Mol. Cell Proteomics 2009, 8, 273-286.
103. Novak, P., Giannakopulos, A. E., Chemical cross-linking and mass spectrometry as structure determination tools. Eur. J. Mass Spectrom. (Chichester, Eng.) 2007, 13, 105-113.
104. Panchaud, A., Singh, P., Shaffer, S. A., Goodlett, D. R., xComb: a cross-linked peptide database approach to protein-protein interaction analysis. J. Proteome Res. 2010, 9, 2508-2515.
105. Gao, Q. X., Xue, S., Doneanu, C. E., Shaffer, S. A. et al., Pro-CrossLink. software tool for protein cross-linking and mass spectrometry. Anal. Chem. 2006, 78, 2145-2149.
106. Muller, M. Q., Dreiocker, F., Ihling, C. H., Schafer, M. et al., Cleavable cross-linker for protein structure analysis: reliable identification of cross-linking products by tandem MS. Anal. Chem. 2010, 82, 6958-6968.
107. Dreiocker, F., Muller, M. Q., Sinz, A., Schafer, M., Collision-induced dissociative chemical cross-linking reagent for protein structure characterization: applied Edman chemistry in the gas phase. J. Mass Spectrom. 2010, 45, 178-189.
108. Lu, Y. L., Tanasova, M., Borhan, B., Reid, G. E., Ionic reagent for controlling the gas-phase fragmentation reactions of cross-linked peptides. Anal. Chem. 2008, 80, 9279-9287.
109. Soderblom, E. J., Bobay, B. G., Cavanagh, J., Goshe, M. B., Tandem mass spectrometry acquisition approaches to enhance identification of protein-protein interactions using low-energy collision-induced dissociative chemical crosslinking reagents. Rapid Commun. Mass Spectrom. 2007, 21, 3395-3408.
110. Hoopmann, M. R., Weisbrod, C. R., Bruce, J. E., Improved strategies for rapid identification of chemically cross-linked peptides using protein interaction reporter technology. J. Proteome Res. 2010, 9, 6323-6333.
111. Jaya, N., Garcia, V., Vierling, E., Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc. Natl. Acad. Sci. USA 2009, 106, 15604-15609.
112. Andreasson, C., Fiaux, J., Rampelt, H., Druffel-Augustin, S. et al., Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity. Proc. Natl. Acad. Sci. USA 2008, 105, 16519-16524.
113. Sharon, M., Taverner, T., Ambroggio, X. I., Deshaies, R. J. et al., Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biol 2006, 4, 1314-1323.
114. Scaloni, A., Miraglia, N., Orru, S., Amodeo, P. et al., Topology of the calmodulin-melittin complex. J. Mol. Biol. 1998, 277, 945-958.
115. Schulz, D. M., Ihling, C., Clore, G. M., Sinz, A., Mapping the topology and determination of a low-resolution three-dimensional structure of the calmodulin-melittin complex by chemical cross-linking and high-resolution FTICRMS: direct demonstration of multiple binding modes. Biochemistry 2004, 43, 4703-4715.
116. Kang, S., Hawkridge, A. M., Johnson, K. L., Muddiman, D. C. et al., Identification of subunit-subunit interactions in bacteriophage P22 procapsids by chemical cross-linking and mass spectrometry. J. Proteome Res. 2006, 5, 370-377.
117. Cai, K., Itoh, Y., Khorana, H. G., Mapping of contact sites in complex formation between transducin and light-activated rhodopsin by covalent crosslinking: use of a photoactivatable reagent. Proc. Natl. Acad. Sci. USA 2001, 98, 4877-4882.
118. Itoh, Y., Cai, K., Khorana, H. G., Mapping of contact sites in complex formation between light-activated rhodopsin and transducin by covalent crosslinking: use of a chemically preactivated reagent. Proc. Natl. Acad. Sci. USA 2001, 98, 4883-4887.
119. Back, J. W., Sanz, M. A., de Jong, L., de Koning, L. J. et al., A structure for the yeast prohibitin complex: structure prediction and evidence from chemical crosslinking and mass spectrometry. Protein Sci. 2002, 11, 2471-2478.
120. Felitsyn, N., Kitova, E. N., Klassen, J. S., Thermal decomposition of a gaseous multiprotein complex studied by blackbody infrared radiative dissociation. Investigating the origin of the asymmetric dissociation behavior. Anal. Chem. 2001, 73, 4647-4661.
121. Kitova, E. N., Kitov, P. I., Bundle, D. R., Klassen, J. S., The observation of multivalent complexes of Shiga-like toxin with globotriaoside and the determination of their stoichiometry by nanoelectrospray Fourier-transform ion cyclotron resonance mass spectrometry. Glycobiology 2001, 11, 605-611.
122. Jurchen, J. C., Garcia, D. E., Williams, E. R., Further studies on the origins of asymmetric charge partitioning in protein homodimers. J. Am. Soc. Mass Spectrom. 2004, 15, 1408-1415.
123. Jurchen, J. C., Williams, E. R., Origin of asymmetric charge partitioning in the dissociation of gas-phase protein homodimers. J. Am. Chem. Soc. 2003, 125, 2817-2826.
124. Versluis, C., van der Staaij, A., Stokvis, E., Heck, A. J. et al., Metastable ion formation and disparate charge separation in the gas-phase dissection of protein assemblies studied by orthogonal time-of-flight mass spectrometry. J. Am. Soc. Mass Spectrom. 2001, 12, 329-336.
125. Rostom, A. A., Sunde, M., Richardson, S. J., Schreiber, G. et al., Dissection of multi-protein complexes using mass spectrometry: subunit interactions in transthyretin and retinol-binding protein complexes. Proteins 1998, 33, 3-11.
126. Benesch, J. L., Aquilina, J. A., Ruotolo, B. T., Sobott, F. et al., Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies. Chem. Biol. 2006, 13, 597-605.
127. Ruotolo, B. T., Hyung, S. J., Robinson, P. M., Giles, K. et al., Ion mobility-mass spectrometry reveals long-lived, unfolded intermediates in the dissociation of protein complexes. Angew Chem. Int. Ed. Engl. 2007, 46, 8001-8004.
128. Ruotolo, B. T., Giles, K., Campuzano, I., Sandercock, A. M. et al., Evidence for macromolecular protein rings in the absence of bulk water. Science 2005, 310, 1658-1661.
129. Duijn, E. V., Barendregt, A., Synowsky, S., Versluis, C. et al., Chaperonin complexes monitored by ion mobility mass spectrometry. J Am Chem Soc 2009, 131, 1452-1459.
130. Benesch, J. L., Ruotolo, B. T., Sobott, F., Wildgoose, J. et al., Quadrupole-time-of-flight mass spectrometer modified for higher-energy dissociation reduces protein assemblies to peptide fragments. Anal. Chem. 2009, 81, 1270-1274.
131. Pagel, K., Hyung, S. J., Ruotolo, B. T., Robinson, C. V., Alternate dissociation pathways identified in charge-reduced protein complex ions. Anal. Chem. 2010, 82, 5363-5372.
132. Ge, Y., Lawhorn, B. G., ElNaggar, M., Strauss, E. et al., Top down characterization of larger proteins (45 kDa) by electron capture dissociation mass spectrometry. J. Am. Chem. Soc. 2002, 124, 672-678.
133. Horn, D. M., Zubarev, R. A., McLafferty, F. W., Automated de novo sequencing of proteins by tandem high-resolution mass spectrometry. Proc. Natl. Acad. Sci. USA 2000, 97, 10313-10317.
134. Wysocki, V. H., Joyce, K. E., Jones, C. M., Beardsley, R. L., Surface-induced dissociation of small molecules, peptides, and non-covalent protein complexes. J. Am. Soc. Mass Spectrom. 2008, 19, 190-208.
135. Jones, C. M., Beardsley, R. L., Galhena, A. S., Dagan, S. et al., Symmetrical gas-phase dissociation of noncovalent protein complexes via surface collisions. J. Am. Chem. Soc. 2006, 128, 15044-15045.
136. Galhena, A. S., Dagan, S., Jones, C. M., Beardsley, R. L. et al., Surface-induced dissociation of peptides and protein complexes in a quadrupole/time-of-flight mass spectrometer. Anal. Chem. 2008, 80, 1425-1436.
137. Beardsley, R. L., Jones, C. M., Galhena, A. S., Wysocki, V. H., Noncovalent protein tetramers and pentamers with "n" charges yield monomers with n/4 and n/5 charges. Anal. Chem. 2009, 81, 1347-1356.
138. Blackwell, A. E., Dodds, E. D., Bandarian, V., Wysocki, V. H., Revealing the quaternary structure of a heterogeneous noncovalent protein complex through surface-induced dissociation. Anal. Chem. 2011, 83, 2862-2865.
139. Hernandez, H., Robinson, C. V., Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2007, 2, 715-726.
140. Zhou, M., Sandercock, A. M., Fraser, C. S., Ridlova, G. et al., Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl. Acad. Sci. USA 2008, 105, 18139-18144.
141. Taverner, T., Hernandez, H., Sharon, M., Ruotolo, B. T. et al., Subunit architecture of intact protein complexes from mass spectrometry and homology modeling. Acc. Chem. Res. 2008, 41, 617-627.
142. Jore, M. M., Lundgren, M., van Duijn, E., Bultema, J. B. et al., Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 2011, 18, 529-536.
143. Tian, Y., Simanshu, D. K., Ascano, M., Diaz-Avalos, R. et al., Multimeric assembly and biochemical characterization of the Trax-translin endonuclease complex. Nat. Struct. Mol. Biol. 2011, 18, 658-664.
144. Lane, L. A., Fernandez-Tornero, C., Zhou, M., Morgner, N. et al., Mass spectrometry reveals stable modules in holo and apo RNA polymerases I and III. Structure 2011, 19, 90-100.
145. Park, A. Y., Jergic, S., Politis, A., Ruotolo, B. T. et al., A single subunit directs the assembly of the Escherichia coli DNA sliding clamp loader. Structure 2010, 18, 285-292.
146. Munoz, I. G., Yebenes, H., Zhou, M., Mesa, P. et al., Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin. Nat. Struct. Mol. Biol. 2011, 18, 14-19.
147. Ganem, B., Li, Y. T., Henion, J. D., Observation of noncovalent enzyme substrate and enzyme product complexes by ion-spray mass-spectrometry. J. Am. Chem. Soc. 1991, 113, 7818-7819.
148. Katta, V., Chait, B. T., Observation of the heme globin complex in native myoglobin by electrospray-ionization mass-spectrometry. J. Am. Chem. Soc. 1991, 113, 8534-8535.
149. Hu, P. F., Loo, J. A., Determining calcium-binding stoichiometry and cooperativity of parvalbumin and calmodulin by mass-spectrometry. J. Mass Spectrom. 1995, 30, 1076-1082.
150. McCammon, M. G., Scott, D. J., Keetch, C. A., Greene, L. H. et al., Screening transthyretin amyloid fibril inhibitors: characterization of novel multiprotein, multiligand complexes by mass spectrometry. Structure 2002, 10, 851-863.
151. Kitova, E. N., Seo, M., Roy, P. N., Klassen, J. S., Elucidating the intermolecular interactions within a desolvated protein-ligand complex. An experimental and computational study. J. Am. Chem. Soc. 2008, 130, 1214-1226.
152. Robinson, C. V., Chung, E. W., Kragelund, B. B., Knudsen, J. et al., Probing the nature of noncovalent interactions by mass spectrometry. A study of protein-CoA Ligand Binding and Assembly. J. Am. Chem. Soc. 1996, 118, 8646-8653.
153. Loo, J. A., Studying noncovalent protein complexes by electrospray ionization mass spectrometry. Mass Spectrom. Rev. 1997, 16, 1-23.
154. Bovet, C., Wortmann, A., Eiler, S., Granger, F. et al., Estrogen receptor-ligand complexes measured by chip-based nanoelectrospray mass spectrometry: an approach for the screening of endocrine disruptors. Protein Sci 2007, 16, 938-946.
155. Wortmann, A., Jecklin, M. C., Touboul, D., Badertscher, M. et al. Binding constant determination of high-affinity protein-ligand complexes by electrospray ionization mass spectrometry and ligand competition. J. Mass Spectrom 2008, 43, 600-608.
156. Liu, J., Konermann, L., Protein-protein binding affinities in solution determined by electrospray mass spectrometry. J. Am. Soc. Mass Spectrom. 2011, 22, 408-417.
157. Kitova, E. N., Soya, N., Klassen, J. S., Identifying specific small-molecule interactions using electrospray ionization mass spectrometry. Anal. Chem. 2011, 83, 5160-5167.
158. Hyung, S. J., Robinson, C. V., Ruotolo, B. T., Gas-phase unfolding and disassembly reveals stability differences in ligand-bound multiprotein complexes. Chem. Biol. 2009, 16, 382-390.
159. Ghaemmaghami, S., Fitzgerald, M. C., Oas, T. G., A quantitative, high-throughput screen for protein stability. Proc. Natl. Acad. Sci. USA 2000, 97, 8296-8301.
160. Zhu, M. M., Rempel, D. L., Du, Z., Gross, M. L., Quantification of protein-ligand interactions by mass spectrometry, titration, and H/D exchange: PLIMSTEX. J. Am. Chem. Soc. 2003, 125, 5252-5253.
161. West, G. M., Tang, L., Fitzgerald, M. C., Thermodynamic analysis of protein stability and ligand binding using a chemical modification- and mass spectrometry-based strategy. Anal. Chem. 2008, 80, 4175-4185.
162. Dearmond, P. D., Xu, Y., Strickland, E. C., Daniels, K. G. et al., Thermodynamic analysis of protein-ligand interactions in complex biological mixtures using a Shotgun Proteomics Approach. J. Proteome Res. 2011, 10, 4948-4958.
163. Ruotolo, B. T., Robinson, C. V., Aspects of native proteins are retained in vacuum. Curr. Opin. Chem. Biol. 2006, 10, 402-408.
164. Loo, J. A., Berhane, B., Kaddis, C. S., Wooding, K. M. et al., Electrospray ionization mass spectrometry and ion mobility analysis of the 20S proteasome complex. J. Am. Soc. Mass Spectrom. 2005, 16, 998-1008.
165. Bernstein, S. L., Wyttenbach, T., Baumketner, A., Shea, J. E. et al., Amyloid beta-protein: monomer structure and early aggregation states of Abeta42 and its Pro19 alloform. J. Am. Chem. Soc. 2005, 127, 2075-2084.
166. Bowers, M. T., Kemper, P. R., von Helden, G., van Koppen, P. A., Gas-phase ion chromatography: transition metal state selection and carbon cluster formation. Science 1993, 260, 1446-1451.
167. Kemper, P. R., Bowers, M. T., Electronic-state chromatography: application to first-row transition-metal ions. J. Phys. Chem. 1991, 95, 5134-5146.
168. Jarrold, M. F., Drift tube studies of atomic clusters. J. Phys. Chem. 1995, 99, 11-21.
169. Eiceman, G. A., Advances in ion mobility spectrometry: 1980-1990. Cr. Rev. Anal. Chem. 1991, 22, 471-490.
170. Baumbach, J. I., Eiceman, G. A., Ion mobility spectrometry: arriving on site and moving beyond a low profile. Appl. Spectrosc. 1999, 53, 338A-355A.
171. von Helden, G., Wyttenbach, T., Bowers, M. T., Conformation of macromolecules in the gas phase: use of matrix-assisted laser desorption methods in ion chromatography. Science 1995, 267, 1483-1485.
172. Clemmer, D. E., Jarrold, M. F., Ion mobility measurements and their applications to clusters and biomolecules. J. Mass Spectrom. 1997, 32, 577-592.
173. Valentine, S. J., Liu, X., Plasencia, M. D., Hilderbrand, A. E. et al., Developing liquid chromatography ion mobility mass spectometry techniques. Expert Rev. Proteomics 2005, 2, 553-565.
174. McLean, J. A., Ruotolo, B. T., Gillig, K. J., Russell, D. H., Ion mobility-mass spectrometry: a new paradigm for proteomics. Int. J. Mass Spectrom. 2005, 240, 301-315.
175. Tao, L., Dahl, D., Pérez, L., Russell, D., The contributions of molecular framework to IMS collision cross-sections of gas-phase peptide ions. J. Am. Soc. Mass Spectrom. 2009, 20, 1593-1602.
176. Politis, A., Park, A. Y., Hyung, S. J., Barsky, D. et al., Integrating ion mobility mass spectrometry with molecular modelling to determine the architecture of multiprotein complexes. PLoS One 2010, 5, e12080.
177. Uetrecht, C., Barbu, I. M., Shoemaker, G. K., van Duijn, E. et al., Interrogating viral capsid assembly with ion mobility-mass spectrometry. Nat. Chem. 2011, 3, 126-132.
178. Bernstein, S. L., Dupuis, N. F., Lazo, N. D., Wyttenbach, T. et al., Amyloid-beta protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat. Chem. 2009, 1, 326-331.
179. Dupuis, N. F., Wu, C., Shea, J. E., Bowers, M. T., The amyloid formation mechanism in human IAPP: dimers have beta-strand monomer-monomer interfaces. J. Am. Chem. Soc. 2011, 133, 7240-7243.
180. Smith, D. P., Radford, S. E., Ashcroft, A. E., Elongated oligomers in beta2-microglobulin amyloid assembly revealed by ion mobility spectrometry-mass spectrometry. Proc. Natl. Acad. Sci. USA 2010, 107, 6794-6798.
181. Smith, D. P., Woods, L. A., Radford, S. E., Ashcroft, A. E., Structure and dynamics of oligomeric intermediates in beta(2)-microglobulin self-assembly. Biophys J. 2011, 101, 1238-1247.
182. Hernandez, H., Dziembowski, A., Taverner, T., Seraphin, B. et al., Subunit architecture of multimeric complexes isolated directly from cells. EMBO Rep. 2006, 7, 605-610.
183. Liu, Q., Greimann, J. C., Lima, C. D., Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 2006, 127, 1223-1237.
184. Breuker, K., McLafferty, F. W., Native electron capture dissociation for the structural characterization of noncovalent interactions in native cytochrome c. Angew Chem. Int. Edit. 2003, 42, 4900-4904.
185. Breuker, K., McLafferty, F. W., The thermal unfolding of native cytochrome c in the transition from solution to gas phase probed by native electron capture dissociation. Angew Chem. Int. Edit. 2005, 44, 4911-4914.
186. Polfer, N. C., Oomens, J., Vibrational spectroscopy of bare and solvated ionic complexes of biological relevance. Mass Spectrom. Rev. 2009, 28, 468-494.
187. Oomens, J., Polfer, N., Moore, D. T., van der Meer, L. et al., Charge-state resolved mid-infrared spectroscopy of a gas-phase protein. Phys. Chem. Chem. Phys. 2005, 7, 1345-1348.
188. Bian, Q. Z., Forbes, M. W., Talbot, F. O., Jockusch, R. A., Gas-phase fluorescence excitation and emission spectroscopy of mass-selected trapped molecular ions. Phys. Chem. Chem. Phys. 2010, 12, 2590-2598.
189. Benesch, J. L. P., Ruotolo, B. T., Simmons, D. A., Barrera, N. P. et al., Separating and visualisiing protein assemblies by means of preparative mass spectrometry and microscopy. J. Struct. Biol. 2010, 172, 161-168.
190. Kim, J., Kim, K. H., Lee, J. H., Ihee, H., Ultrafast X-ray diffraction in liquid, solution and gas: present status and future prospects. Acta. Crystallogr. A 2010, 66, 270-280.
191. Aquilina, J. A., The major toxin from the Australian Common Brown Snake is a hexamer with unusual gas-phase dissociation properties. Proteins 2009, 75, 478-485.
192. Zhang, H., Cui, W. D., Wen, J. Z., Blankenship, R. E. et al., Native electrospray and electron-capture dissociation in FTICR mass spectrometry provide top-down sequencing of a protein component in an intact protein assembly. J. Am. Soc. Mass Spectrom. 2010, 21, 1966-1968.
193. Boeri Erba, E., Ruotolo, B. T., Barsky, D., Robinson, C. V., Ion mobility-mass spectrometry reveals the influence of subunit packing and charge on the dissociation of multiprotein complexes. Anal. Chem. 2010, 82, 9702-9710.