Mass spectrometry coupled experiments and protein structure modeling methods

International Journal of Molecular Sciences

Volumn 14, Issue 10, 2013, Pages 20635-20657

  Pi, Jaewoo ^a,b   Sael, Lee ^a,b  

^a Stony Brook University   (United States)

^b State University of New York   (South Korea)

Author keywords

Constraint base structure prediction; Integrative structure prediction; Mass spectrometry; Protein dynamics; Sequence variants

Indexed keywords

ACCURACY; AMINO ACID SEQUENCE; COMPUTER ANALYSIS; CONSTRAINT BASE STRUCTURE PREDICTION; DISEASES; DYNAMICS; HUMAN; HYDROGEN BOND; INTEGRATIVE STRUCTURE PREDICTION; MASS SPECTROMETRY; MOLECULAR BIOLOGY; MOLECULAR MODEL; NONHUMAN; PREDICTION; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEOMICS; REVIEW; SENSITIVITY ANALYSIS; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE;

COMPUTER SIMULATION; HUMANS; MASS SPECTROMETRY; MOLECULAR STRUCTURE; PROTEINS;

EID: 84885908505     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141020635     Document Type: Review

References (107)

1. Apweiler, R.; Bairoch, A.; Wu, C.H. Protein sequence databases. Curr. Opin. Chem. Biol. 2004, 8, 76-80.
2. Gao, X. Towards Automating Protein Structure Determination from NMR Data. Ph.D. Thesis, University of Waterloo, Waterloo, ON, Canada, 2009.
3. Skolnick, J.; Zhang, Y.; Arakaki, A.K.; Kolinski, A.; Boniecki, M.; Szilágyi, A.; Kihara, D. TOUCHSTONE: A unified approach to protein structure prediction. Proteins 2003, 53, 469-479.
4. Xu, D.; Zhang, Y. Ab initio protein structure assembly using continuous structure fragments and optimized knowledge-based force field. Proteins 2012, 80, 1715-1735.
5. Venkatraman, V.; Yang, Y.D.; Sael, L.; Kihara, D. Protein-protein docking using region-based 3D Zernike descriptors. BMC Bioinf. 2009, 10, 407.
6. Kihara, D.; Sael, L.; Chikhi, R.; Esquivel-Rodriguez, J. Molecular surface representation using 3D Zernike descriptors for protein shape comparison and docking. Curr. Protein Pept. Sci. 2011, 12, 520-530.
7. Sael, L.; Chitale, M.; Kihara, D. Structure-and sequence-based function prediction for non-homologous proteins. J. Struct. Funct. Genomics 2012, 13, 111-123.
8. Sael, L.; Kihara, D. Binding ligand prediction for proteins using partial matching of local surface patches. Int. J. Mol. Sci. 2010, 11, 5009-5026.
9. Benesch, J.L.P.; Ruotolo, B.T. Mass spectrometry: Come of age for structural and dynamical biology. Curr. Opin. Struct. Biol. 2011, 21, 641-649.
10. Kaur, P.; Chance, M. The Utility of Mass Spectrometry Based Structural Proteomics in Biopharmaceutical Biologics Development. In Integrative Proteomics; Leung, H.-C., Ed.; InTech: Cleveland, OH, USA, 2012; pp. 340-412.
11. Dobson, C.M. Protein folding and misfolding. Nature 2003, 426, 884-890.
12. Glish, G.L.; Vachet, R.W. The basics of mass spectrometry in the twenty-first century. Nat. Rev. Drug Discovery 2003, 2, 140-150.
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. Kiselar, J.G.; Chance, M.R. Future directions of structural mass spectrometry using hydroxyl radical footprinting. J. Mass Spectrom. 2010, 45, 1373-1382.
15. Fioramonte, M.; dos Santos, A.M.; McIlwain, S.; Noble, W.S.; Franchini, K.G.; Gozzo, F.C. Analysis of secondary structure in proteins by chemical cross-linking coupled to MS. Proteomics 2012, 12, 2746-2752.
16. Uetrecht, C.; Rose, R.J.; van Duijn, E.; Lorenzen, K.; Heck, A.J.R. Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 2010, 39, 1633-1655.
17. Trible, R.P.; Emert-Sedlak, L.; Wales, T.E.; Ayyavoo, V.; Engen, J.R.; Smithgall, T.E. Allosteric loss-of-function mutations in HIV-1 Nef from a long-term non-progressor. J. Mol. Biol. 2007, 374, 121-129.
18. Morgan, C.R.; Hebling, C.M.; Rand, K.D.; Stafford, D.W.; Jorgenson, J.W.; Engen, J.R. Conformational transitions in the membrane scaffold protein of phospholipid bilayer nanodiscs. Mol. Cell. Proteomics 2011, 10, doi:10.1074/mcp.M111.010876.
19. Zhang, J.; Chalmers, M.J.; Stayrook, K.R.; Burris, L.L.; Garcia-Ordonez, R.D.; Pascal, B.D.; Burris, T.P.; Dodge, J.A.; Griffin, P.R. Hydrogen/deuterium exchange reveals distinct agonist/partial agonist receptor dynamics within vitamin D receptor/retinoid X receptor heterodimer. Structure 2010, 18, 1332-1341.
20. Charvátová, O.; Foley, B.L.; Bern, M.W.; Sharp, J.S.; Orlando, R.; Woods, R.J. Quantifying protein interface footprinting by hydroxyl radical oxidation and molecular dynamics simulation: Application to galectin-1. J. Am. Soc. Mass Spectrom. 2008, 19, 1692-1705.
21. Xu, G.; Chance, M.R. Radiolytic modification and reactivity of amino acid residues serving as structural probes for protein footprinting. Anal. Chem. 2005, 77, 4549-4555.
22. Takamoto, K.; Chance, M.R. Radiolytic protein footprinting with mass spectrometry to probe the structure of macromolecular complexes. Annu. Rev. Biophys. Biomol. Struct. 2006, 35, 251-276.
23. Wang, L.; Qin, Y.; Ilchenko, S.; Bohon, J.; Shi, W.; Cho, M.W.; Takamoto, K.; Chance, M.R. Structural analysis of a highly glycosylated and unliganded gp120-based antigen using mass spectrometry. Biochemistry 2010, 49, 9032-9045.
24. Schmitz, A.; Galas, D.J. Sequence-specific interactions of the tight-binding I12-X86 lac repressor with non-operator DNA. Nucleic Acids Res. 1980, 8, 487-506.
25. Angel, T.E.; Chance, M.R.; Palczewski, K. Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors. Proc. Natl. Acad. Sci. USA 2009, 106, 8555-8560.
26. 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.
27. 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.
28. Sharon, M.; Taverner, T.; Ambroggio, X.I.; Deshaies, R.J.; Robinson, C.V. Structural organization of the 19S proteasome lid: Insights from MS of intact complexes. PLoS Biol. 2006, 4, e267.
29. Kang, S.; Hawkridge, A.M.; Johnson, K.L.; Muddiman, D.C.; Prevelige, P.E. Identification of subunit-subunit interactions in bacteriophage P22 procapsids by chemical cross-linking and mass spectrometry. J. Proteome Res. 2006, 5, 370-377.
30. Pacholarz, K.J.; Garlish, R. A; Taylor, R.J.; Barran, P.E. Mass spectrometry based tools to investigate protein-ligand interactions for drug discovery. Chem. Soc. Rev. 2012, 41, 4335-4355.
31. 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.
32. Calvo, F.; Chirot, F.; Albrieux, F.; Lemoine, J.; Tsybin, Y.O.; Pernot, P.; Dugourd, P. Statistical analysis of ion mobility spectrometry. II. Adaptively biased methods and shape correlations. J. Am. Soc. Mass Spectrom. 2012, 23, 1279-1288.
33. Ruotolo, B.T.; Giles, K.; Campuzano, I.; Sandercock, A.M.; Bateman, R.H.; Robinson, C.V. Evidence for macromolecular protein rings in the absence of bulk water. Science 2005, 310, 1658-1661.
34. Bernstein, S.L.; Wyttenbach, T.; Baumketner, A.; Shea, J.-E.; Bitan, G.; Teplow, D.B.; Bowers, M.T. Amyloid beta-protein: Monomer structure and early aggregation states of Abeta42 and its Pro19 alloform. J. Am. Chem. Soc. 2005, 127, 2075-2084.
35. Smith, D.P.; Woods, L.A.; Radford, S.E.; Ashcroft, A.E. Structure and dynamics of oligomeric intermediates in β2-microglobulin self-assembly. Biophys. J. 2011, 101, 1238-1247.
36. Kanu, A.B.; Dwivedi, P.; Tam, M.; Matz, L.; Hill, H.H. Ion mobility-mass spectrometry. J. Mass Spectrom. 2008, 43, 1-22.
37. Van den Heuvel, R.H.H.; Heck, A.J.R. Native protein mass spectrometry: From intact oligomers to functional machineries. Curr. Opin. Chem. Biol. 2004, 8, 519-526.
38. Heck, A.J.R. Native mass spectrometry: A bridge between interactomics and structural biology. Nat. Methods 2008, 5, 927-933.
39. Van Duijn, E. Current limitations in native mass spectrometry based structural biology. J. Am. Soc. Mass Spectrom. 2010, 21, 971-978.
40. Konijnenberg, A; Butterer, A.; Sobott, F. Native ion mobility-mass spectrometry and related methods in structural biology. Biochim. Biophys. Acta 2012, 1834, 1239-1256.
41. Kebarle, P.; Verkerk, U.H. Electrospray: From ions in solution to ions in the gas phase, what we know now. Mass Spectrom. Rev. 2009, 28, 898-917.
42. Taverner, T.; Hernández, H.; Sharon, M.; Ruotolo, B.T.; Matak-Vinković, D.; Devos, D.; Russell, R.B.; Robinson, C.V. Subunit architecture of intact protein complexes from mass spectrometry and homology modeling. Acc. Chem. Res. 2008, 41, 617-627.
43. Loo, J.A.; Berhane, B.; Kaddis, C.S.; Wooding, K.M.; Xie, Y.; Kaufman, S.L.; Chernushevich, I.V. Electrospray ionization mass spectrometry and ion mobility analysis of the 20S proteasome complex. J. Am. Soc. Mass Spectrom. 2005, 16, 998-1008.
44. Sharon, M.; Witt, S.; Felderer, K.; Rockel, B.; Baumeister, W.; Robinson, C.V. 20S proteasomes have the potential to keep substrates in store for continual degradation. J. Biol. Chem. 2006, 281, 9569-9575.
45. Lorenzen, K.; Vannini, A.; Cramer, P.; Heck, A.J.R. Structural biology of RNA polymerase III: Mass spectrometry elucidates subcomplex architecture. Structure 2007, 15, 1237-1245.
46. Synowsky, S.A.; van den Heuvel, R.H.H.; Mohammed, S.; Pijnappel, P.W.W.M.; Heck, A.J.R. Probing genuine strong interactions and post-translational modifications in the heterogeneous yeast exosome protein complex. Mol. Cell. Proteomics 2006, 5, 1581-1592.
47. Zhang, Y. Protein structure prediction: When is it useful? Curr. Opin. Struct. Biol. 2009, 19, 145-155.
48. Sali, A.; Blundell, T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234, 779-815.
49. Arnold, K.; Bordoli, L.; Kopp, J.; Schwede, T. The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling. Bioinformatics 2006, 22, 195-201.
50. Söding, J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005, 21, 951-960.
51. Peng, J.; Xu, J. RaptorX: Exploiting structure information for protein alignment by statistical inference. Proteins 2011, 79, 161-171.
52. Wu, S.; Zhang, Y. MUSTER: Improving protein sequence profile-profile alignments by using multiple sources of structure information. Proteins 2008, 72, 547-556.
53. Yang, Y.; Faraggi, E.; Zhao, H.; Zhou, Y. Improving protein fold recognition and template-based modeling by employing probabilistic-based matching between predicted one-dimensional structural properties of query and corresponding native properties of templates. Bioinformatics 2011, 27, 2076-2082.
54. Das, R.; Qian, B.; Raman, S.; Vernon, R.; Thompson, J.; Bradley, P.; Khare, S.; Tyka, M.D.; Bhat, D.; Chivian, D.; et al. Structure prediction for CASP7 targets using extensive all-atom refinement with Rosetta@home. Proteins 2007, 69, 118-128.
55. Roy, A.; Kucukural, A.; Zhang, Y. I-TASSER: A unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5, 725-738.
56. Fujitsuka, Y.; Chikenji, G.; Takada, S. SimFold energy function for de novo protein structure prediction: Consensus with Rosetta. Proteins 2006, 62, 381-398.
57. Takada, S. Protein folding simulation with solvent-induced force field: Folding pathway ensemble of three-helix-bundle proteins. Proteins 2001, 42, 85-98.
58. Kolinski, A. Protein modeling and structure prediction with a reduced representation. Acta Biochim. 2004, 51, 349-371.
59. Martí-Renom, M.A.; Stuart, A.C.; Fiser, A.; Sánchez, R.; Melo, F.; Sali, A. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 291-325.
60. Roy, A.; Zhang, Y. Protein Structure Prediction. eLS; John Wiley & Sons, Ltd: Chichester, UK, 2007.
61. Apostolico, A.; Giancarlo, R. Sequence alignment in molecular biology. J. Comput. Biol. 1998, 5, 173-196.
62. Pearson, W.R.; Lipman, D.J. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 1988, 85, 2444-2448.
63. Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403-410.
64. Lipman, D.J.; Altschul, S.F.; Kececioglu, J.D. A tool for multiple sequence alignment. Proc. Natl. Acad. Sci. USA 1989, 86, 4412-4415.
65. Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792-1797.
66. Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R.; et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23, 2947-2948.
67. Altschul, S.F.; Madden, T.L.; Schäffer, A. A; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997, 25, 3389-3402.
68. Blundell, T.L.; Sibanda, B.L.; Sternberg, M.J.E.; Thornton, J.M. Knowledge-based prediction of protein structures and the design of novel molecules. Nature 1987, 326, 347-352.
69. Baker, D.; Sali, A. Protein structure prediction and structural genomics. Science 2001, 294, 93-96.
70. Wallner, B.; Elofsson, A. All are not equal: A benchmark of different homology modeling programs. Protein Sci. 2005, 14, 1315-1327.
71. Unger, R.; Harel, D.; Wherland, S.; Sussman, J. A 3D building blocks approach to analyzing and predicting structure of proteins. Proteins 1989, 5, 355-373.
72. Levitt, M. Accurate modeling of protein conformation by automatic segment matching. J. Mol. Biol. 1992, 226, 507-533.
73. Bowie, J., Clarke, N., Pabo, C., Sauer, R. Identification of protein folds: Matching hydrophobicity patterns of sequence sets with solvent accessibility patterns of known structures. Proteins 1990, 7, 257-264.
74. Bowie, J.; Luthy, R.; Eisenberg, D. A method to identify protein sequences that fold into a known three-dimensional structure. Science 1991, 253, 164-170.
75. Xu, Y.; Xu, D. Protein threading using PROSPECT: Design and evaluation. Proteins: Struct, Funct, Bioinf. 2000, 354, 343-354.
76. Xu, Y.; Xu, D.; Uberbacher, E.C. An efficient computational method for globally optimal threading. J. Comput. Biol. 1998, 5, 597-614.
77. Zhou, H.; Zhou, Y. Fold recognition by combining sequence profiles derived from evolution and from depth-dependent structural alignment of fragments. Proteins 2005, 58, 321-328.
78. Chakravarty, S.; Varadarajan, R. Residue depth: A novel parameter for the analysis of protein structure and stability. Structure 1999, 7, 723-732.
79. Frishman, D.; Argos, P. Knowledge-based protein secondary structure assignment. Proteins 1995, 23, 566-579.
80. Brooks, B.; Bruccoleri, R. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 1983, 4, 187-217.
81. Weiner, S.J.; Kollman, P.A.; Case, D.A.; Singh, U.C.; Ghio, C.; Alagona, G.; Profeta, S.; Weiner, P. A new force field for molecular mechanical simulation of nucleic acids and proteins. J. Am. Chem. Soc. 1984, 106, 765-784.
82. Jorgensen, W.; Tirado-Rives, J. The OPLS potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 1988, 110, 1657-1666.
83. Liwo, A.; Pincus, M.R.; Wawak, R.J.; Rackovsky, S.; Scheraga, H.A. Calculation of protein backbone geometry from alpha-carbon coordinates based on peptide-group dipole alignment. Protein Sci. 1993, 2, 1697-1714.
84. Lazaridis, T.; Karplus, M. Effective energy function for proteins in solution. Proteins 1999, 35, 133-152.
85. Durham, E.; Dorr, B.; Woetzel, N.; Staritzbichler, R.; Meiler, J. Solvent accessible surface area approximations for rapid and accurate protein structure prediction. J. Mol. Model. 2009, 15, 1093-1108.
86. Bradley, P.; Misura, K.M.S.; Baker, D. Toward high-resolution de novo structure prediction for small proteins. Science 2005, 309, 1868-1871.
87. Xu, D.; Zhang, J.; Roy, A.; Zhang, Y. Automated protein structure modeling in CASP9 by I-TASSER pipeline combined with QUARK-based ab initio folding and FG-MD-based structure refinement. Proteins 2011, 79, 147-160.
88. Gront, D.; Kulp, D.W.; Vernon, R.M.; Strauss, C.E.M.; Baker, D. Generalized fragment picking in Rosetta: Design, protocols and applications. PLoS One 2011, 6, e23294.
89. Topf, M.; Sali, A. Combining electron microscopy and comparative protein structure modeling. Curr. Opin. Struct. Biol. 2005, 15, 578-585.
90. Schneidman-Duhovny, D.; Kim, S.J.; Sali, A. Integrative structural modeling with small angle X-ray scattering profiles. BMC Struct. Biol. 2012, 12, 17.
91. Young, M.M.; Tang, N.; Hempel, J.C.; Oshiro, C.M.; Taylor, E.W.; Kuntz, I.D.; Gibson, B.W.; Dollinger, G. High throughput protein fold identification by using experimental constraints derived from intramolecular cross-links and mass spectrometry. Proc. Natl. Acad. Sci. USA 2000, 97, 5802-5806.
92. 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.
93. Stengel, F.; Aebersold, R.; Robinson, C.V. Joining forces: Integrating proteomics and cross-linking with the mass spectrometry of intact complexes. Mol. Cell. Proteomics 2012, 11, doi:10.1074/mcp.R1111.014027
94. Petrotchenko, E.V.; Borchers, C.H. Crosslinking combined with mass spectrometry for structural proteomics. Mass Spectrom. Rev. 2010, 29, 862-876.
95. Bereszczak, J.Z.; Barbu, I.M.; Tan, M.; Xia, M.; Jiang, X.; van Duijn, E.; Heck, A.J.R. Structure, stability and dynamics of norovirus P domain derived protein complexes studied by native mass spectrometry. J. Struct. Biol. 2012, 177, 273-282.
96. Hernández, H.; Dziembowski, A.; Taverner, T.; Séraphin, B.; Robinson, C.V. Subunit architecture of multimeric complexes isolated directly from cells. EMBO Rep. 2006, 7, 605-610.
97. Ilag, L.L.; Westblade, L.F.; Deshayes, C.; Kolb, A.; Busby, S.J.W.; Robinson, C.V. Mass spectrometry of Escherichia coli RNA polymerase: Interactions of the core enzyme with sigma70 and Rsd protein. Structure 2004, 12, 269-275.
98. Thompson, N.J.; Rosati, S.; Heck, A.J.R. Performing native mass spectrometry analysis on therapeutic antibodies. Methods 2013, doi:10.1016/j.ymeth.2013.05.003.
99. Levy, E.D.; Boeri Erba, E.; Robinson, C.V.; Teichmann, S.A. Assembly reflects evolution of protein complexes. Nature 2008, 453, 1262-1265.
100. Walzthoeni, T.; Leitner, A.; Stengel F.; Aebersold, R. Mass spectrometry supported determination of protein complex structure. Curr. Opin. Struct. Biol. 2013, 23, 252-260.
101. Lasker, K.; Phillips, J.L.; Russel, D.; Velázquez-Muriel, J.; Schneidman-Duhovny, D.; Tjioe, E.; Webb, B.; Schlessinger, A.; Sali, A. Integrative structure modeling of macromolecular assemblies from proteomics data. Mol. Cell. Proteomics 2010, 9, 1689-1702.
102. Pieper, U.; Webb, B.M.; Barkan, D.T.; Schneidman-Duhovny, D.; Schlessinger, A.; Braberg, H.; Yang, Z.; Meng, E.C.; Pettersen, E.F.; Huang, C.C.; et al. MODBASE, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res. 2011, 39, D465-D474.
103. Stark, C.; Breitkreutz, B.-J.; Reguly, T.; Boucher, L.; Breitkreutz, A.; Tyers, M. BioGRID: A general repository for interaction datasets. Nucleic Acids Res. 2006, 34, D535-D539.
104. Lawson, C.L.; Baker, M.L.; Best, C.; Bi, C.; Dougherty, M.; Feng, P.; van Ginkel, G.; Devkota, B.; Lagerstedt, I.; Ludtke, S.J.; et al. EMDataBank. org: Unified data resource for CryoEM. Nucleic Acids Res. 2011, 39, D456-D464.
105. Zhou, M.; Robinson, C.V. When proteomics meets structural biology. Trends Biochem. Sci. 2010, 35, 522-529.
106. Benesch, J.L.P.; 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.
107. Hyung, S.-J.; Ruotolo, B.T. Integrating mass spectrometry of intact protein complexes into structural proteomics. Proteomics 2012, 12, 1547-1564.