Biological insights from hydrogen exchange mass spectrometry

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 6, 2013, Pages 1188-1201

  Jaswal, Sheila S ^a  

^a AMHERST COLLEGE   (United States)

Author keywords

Folding landscape; Hydrogen exchange mass spectrometry; Protein dynamics; Protein interaction; Protein stability; Protein structure

Indexed keywords

COMPLEX FORMATION; CONFORMATION; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; REVIEW; THERMODYNAMICS;

DEUTERIUM; DEUTERIUM EXCHANGE MEASUREMENT; HYDROGEN; KINETICS; MASS SPECTROMETRY; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 84878109818     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.10.011     Document Type: Review

References (152)

1. V. Katta, and B.T. Chait Conformational changes in proteins probed by hydrogen-exchange electrospray-ionization mass spectrometry Rapid Commun. Mass Spectrom. 5 1991 214 217
2. Z. Zhang, and D.L. Smith Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation Protein Sci. 2 1993 522 531
3. A. Miranker, C.V. Robinson, S.E. Radford, R.T. Aplin, and C.M. Dobson Detection of transient protein folding populations by mass spectrometry Science 262 1993 896 900
4. D.S. Wagner, and R.J. Anderegg Conformation of cytochrome c studied by deuterium exchange-electrospray ionization mass spectrometry Anal. Chem. 66 1994 706 711
5. M.J. Chalmers, S.A. Busby, B.D. Pascal, G.M. West, and P.R. Griffin Differential hydrogen/deuterium exchange mass spectrometry analysis of protein-ligand interactions Expert Rev. Proteomics 8 2011 43 59
6. G.M. West, E.Y.T. Chien, V. Katritch, J. Gatchalian, M.J. Chalmers, R.C. Stevens, and P.R. Griffin Ligand-dependent perturbation of the conformational ensemble for the GPCR β2 adrenergic receptor revealed by HDX Structure 19 2011 1424 1432
7. P.D. DeArmond, G.M. West, V. Anbalagan, M.J. Campa, E.F. Patz, and M.C. Fitzgerald Discovery of novel cyclophilin A ligands using an H/D exchange- and mass spectrometry-based strategy J. Biomol. Screen. 15 2010 1051 1062
8. K.J. Pacholarz, R.A. Garlish, R.J. Taylor, and P.E. Barran Mass spectrometry based tools to investigate protein-ligand interactions for drug discovery Chem. Soc. Rev. 41 2012 4335 4355
9. A.N. Hoofnagle, K.A. Resing, and N.G. Ahn Protein analysis by hydrogen exchange mass spectrometry Annu. Rev. Biophys. Biomol. Struct. 32 2003 1 25
10. E.D. Hopper, A.M.C. Pittman, C.L. Tucker, M.J. Campa, E.F. Patz, and M.C. Fitzgerald Hydrogen/deuterium exchange- and protease digestion-based screening assay for protein-ligand binding detection Anal. Chem. 81 2009 6860 6867
11. S.W. Englander Hydrogen exchange and mass spectrometry: A historical perspective J. Am. Soc. Mass Spectrom. 17 2006 1481 1489
12. D. Pandit, S.J. Tuske, S.J. Coales, E. Sy, A. Liu, J.E. Lee, J.A. Morrow, J.F. Nemeth, and Y. Hamuro Mapping of discontinuous conformational epitopes by amide hydrogen/deuterium exchange mass spectrometry and computational docking J. Mol. Recognit. 25 2012 114 124
13. L. Konermann, J. Pan, and Y.-H. Liu Hydrogen exchange mass spectrometry for studying protein structure and dynamics Chem. Soc. Rev. 40 2011 1224
14. J.M.L. Ling, L. Silva, D.C. Schriemer, and A.B. Schryvers Hydrogen-deuterium exchange coupled to mass spectrometry to investigate ligand-receptor interactions Meth. Mol. Biol. 799 2012 237 252
15. R.E. Iacob, and J.R. Engen Hydrogen exchange mass spectrometry: Are we out of the quicksand? J. Am. Soc. Mass Spectrom. 23 2012 1003 1010
16. B.D. Pascal, M.J. Chalmers, S.A. Busby, C.C. Mader, M.R. Southern, N.F. Tsinoremas, and P.R. Griffin The Deuterator: Software for the determination of backbone amide deuterium levels from H/D exchange MS data BMC Bioinformatics 8 2007 156
17. A. Brock Fragmentation hydrogen exchange mass spectrometry: A review of methodology and applications Protein Expr. Purif. 84 2012 19 37
18. A.J. Percy, M. Rey, K.M. Burns, and D.C. Schriemer Probing protein interactions with hydrogen/deuterium exchange and mass spectrometry - a review Anal. Chim. Acta 721 2012 7 21
19. A.H. Wani, and J.B. Udgaonkar Mass spectrometry studies of protein folding Curr. Sci. India 102 2012 245 265
20. D. Beckett Hydrogen-deuterium exchange study of an allosteric energy cycle Meth. Mol. Biol. 796 2012 261 278
21. S.J. Eyles, and I.A. Kaltashov Methods to study protein dynamics and folding by mass spectrometry Methods 34 2004 88 99
22. I. Kheterpal, and R. Wetzel Hydrogen/deuterium exchange mass spectrometry - a window into amyloid structure Acc. Chem. Res. 39 2006 584 593
23. S.S. Jaswal, and A.D. Miranker Scope and utility of hydrogen exchange as a tool for mapping landscapes Protein Sci. 16 2007 2378 2390
24. E. Van Duijn Current limitations in native mass spectrometry based structural biology J. Am. Soc. Mass Spectrom. 21 2010 971 978
25. R. Liyanage, N. Devarapalli, L.M. Puckett, N.H. Phan, J. Gidden, W.E. Stites, and J.O.J. Lay Comparison of two ESI-MS based H/D exchange methods for extracting protein folding energies Int. J. Mass Spectrom. 287 2009 96 104
26. S. Dai, M. Gardner, and M. Fitzgerald Protocol for the thermodynamic analysis of some proteins using an H/D exchange- and mass spectrometry based technique Anal. Chem. 77 2005 693 697
27. I.A. Kaltashov, C.E. Bobst, R.R. Abzalimov, G. Wang, B. Baykal, and S. Wang Advances and challenges in analytical characterization of biotechnology products: Mass spectrometry-based approaches to study properties and behavior of protein therapeutics Biotechnol. Adv. 30 2012 210 222
28. D. Houde, S.A. Berkowitz, and J.R. Engen The utility of hydrogen/deuterium exchange mass spectrometry in biopharmaceutical comparability studies J. Pharm. Sci. 100 2011 2071 2086
29. R.L. Baldwin Early days of protein hydrogen exchange: 1954-1972 Proteins 79 2011 2021 2026
30. A. Hvidt A discussion of the pH dependence of the hydrogen-deuterium exchange of proteins C. R. Trav. Lab. Carlsberg 34 1964 299 317
31. S.W. Englander, L. Mayne, Y. Bai, and T.R. Sosnick Hydrogen exchange: The modern legacy of Linderstrøm-Lang Protein Sci. 6 1997 1101 1109
32. G.P. Connelly, Y. Bai, M.F. Jeng, and S.W. Englander Isotope effects in peptide group hydrogen exchange Proteins 17 1993 87 92
33. R.S. Molday, S.W. Englander, and R.G. Kallen Primary structure effects on peptide group hydrogen exchange Biochemistry 11 1972 150 158
34. Y. Bai, J.S. Milne, L. Mayne, and S.W. Englander Primary structure effects on peptide group hydrogen exchange Proteins 17 1993 75 86
35. H. Roder, G. Wagner, and K. Wüthrich Individual amide proton exchange rates in thermally unfolded basic pancreatic trypsin inhibitor Biochemistry 24 1985 7407 7411
36. A.D. Robertson, and R.L. Baldwin Hydrogen exchange in thermally denatured ribonuclease A Biochemistry 30 1991 9907 9914
37. J.J. Skinner, W.K. Lim, S. Bédard, B.E. Black, and S.W. Englander Protein hydrogen exchange: Testing current models Protein Sci. 21 2012 987 995
38. K. Dharmasiri, and D.L. Smith Mass spectrometric determination of isotopic exchange rates of amide hydrogens located on the surfaces of proteins Anal. Chem. 68 1996 2340 2344
39. S.M.E. Truhlar, C.H. Croy, J.W. Torpey, J.R. Koeppe, and E.A. Komives Solvent accessibility of protein surfaces by amide H/2H exchange MALDI-TOF mass spectrometry J. Am. Soc. Mass Spectrom. 17 2006 1490 1497
40. G. Gemmecker, W. Jahnke, and H. Kessler Isotopically labeled compounds J. Am. Chem. Soc. 115 1993 11620 11621
41. S. Koide, W. Jahnke, and P. Wright Measurement of intrinsic exchange rates of amide protons in a 15N-labeled peptide J. Biomol. NMR 6 1995
42. J.J. Skinner, W.K. Lim, S. Bédard, B.E. Black, and S.W. Englander Protein dynamics viewed by hydrogen exchange Protein Sci. 21 2012 996 1005
43. H. Qian, S.L. Mayo, and A. Morton Protein hydrogen exchange in denaturant: Quantitative analysis by a two-process model Biochemistry 33 1994 8167 8171
44. Y. Bai, T.R. Sosnick, L. Mayne, and S.W. Englander Protein folding intermediates: Native-state hydrogen exchange Science 269 1995 192 197
45. A.K. Chamberlain, T.M. Handel, and S. Marqusee Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH Nat. Struct. Biol. 3 1996 782 787
46. C. Woodward, N. Carulla, and G. Barany Native state hydrogen-exchange analysis of protein folding and protein motional domains Meth. Enzymol. 380 2004 379 400
47. A. Hvidt, and S.O. Nielsen Hydrogen exchange in proteins Adv. Protein Chem. 21 1966 287 386
48. Q. Yi, and D. Baker Direct evidence for a two-state protein unfolding transition from hydrogen-deuterium exchange, mass spectrometry, and NMR Protein Sci. 5 1996 1060 1066
49. T. Sivaraman, C.B. Arrington, and A.D. Robertson Kinetics of unfolding and folding from amide hydrogen exchange in native ubiquitin Nat. Struct. Biol. 8 2001 331 333
50. C.B. Arrington, and A.D. Robertson Microsecond protein folding kinetics from native-state hydrogen exchange Biochemistry 36 1997 8686 8691
51. L. Hoang, S. Bédard, M.M.G. Krishna, Y. Lin, and S.W. Englander Cytochrome c folding pathway: Kinetic native-state hydrogen exchange Proc. Natl. Acad. Sci. U. S. A. 99 2002 12173 12178
52. M. Cliff Beyond the EX1 limit: Probing the structure of high-energy states in protein unfolding J. Mol. Biol. 336 2004 497 508
53. S. Yan Thermodynamic and kinetic exploration of the energy landscape of Borrelia burgdorferi OspA by native-state hydrogen exchange J. Mol. Biol. 323 2002 363 375
54. R.L. Baldwin, and H. Roder Characterizing protein folding intermediates Curr. Biol. 1 1991 218 220
55. W.A. Houry, J.M. Sauder, H. Roder, and H.A. Scheraga Definition of amide protection factors for early kinetic intermediates in protein folding Proc. Natl. Acad. Sci. U. S. A. 95 1998 4299 4302
56. B.M. Huyghues-Despointes, J.M. Scholtz, and C.N. Pace Protein conformational stabilities can be determined from hydrogen exchange rates Nat. Struct. Biol. 6 1999 910 912
57. Y. Bai Protein folding pathways studied by pulsed- and native-state hydrogen exchange Chem. Rev. 106 2006 1757 1768
58. A.K. Chamberlain, and S. Marqusee Touring the landscapes: Partially folded proteins examined by hydrogen exchange Structure 5 1997 859 863
59. C.B. Arrington, and A.D. Robertson Kinetics and thermodynamics of conformational equilibria in native proteins by hydrogen exchange Meth. Enzymol. 323 2000 104 124
60. K.L. Maxwell, D. Wildes, A. Zarrine-Afsar, M.A. De Los Rios, A.G. Brown, C.T. Friel, L. Hedberg, J.-C. Horng, D. Bona, E.J. Miller, A. Vallée-Bélisle, E.R.G. Main, F. Bemporad, L. Qiu, K. Teilum, N.-D. Vu, A.M. Edwards, I. Ruczinski, F.M. Poulsen, and B.B. Kragelund Protein folding: Defining a "standard" set of experimental conditions and a preliminary kinetic data set of two-state proteins Protein Sci. 14 2005 602 616
61. D.M. Ferraro, N.D. Lazo, and A.D. Robertson EX1 hydrogen exchange and protein folding Biochemistry 43 2004 587 594
62. H. Roder, G. Wagner, and K. Wüthrich Amide proton exchange in proteins by EX1 kinetics: Studies of the basic pancreatic trypsin inhibitor at variable p2H and temperature Biochemistry 24 1985 7396 7407
63. G. Wagner, and K. Wüthrich Observation of internal motility of proteins by nuclear magnetic resonance in solution Meth. Enzymol. 131 1986 307 326
64. A. Miranker, C.V. Robinson, S.E. Radford, and C.M. Dobson Investigation of protein folding by mass spectrometry FASEB J. 10 1996 93 101
65. R. Heuvel, and A.J.R. Heck Native protein mass spectrometry: From intact oligomers to functional machineries Curr. Opin. Chem. Biol. 8 2004 519 526
66. A.J.R. Heck Native mass spectrometry: A bridge between interactomics and structural biology Nat. Meth. 5 2008 927 933
67. S.R. Marcsisin, and J.R. Engen Hydrogen exchange mass spectrometry: What is it and what can it tell us? Anal. Bioanal. Chem. 397 2010 967 972
68. T. Rob, and D.J. Wilson Time-resolved mass spectrometry for monitoring millisecond time-scale solution-phase processes Eur. J. Mass Spectrom. 18 2012 205 214
69. H.J. Sterling, and E.R. Williams Real-time hydrogen/deuterium exchange kinetics via supercharged electrospray ionization tandem mass spectrometry Anal. Chem. 82 2010 9050 9057
70. S. Ghaemmaghami, and T.G. Oas Quantitative protein stability measurement in vivo Nat. Struct. Biol. 8 2001 879 882
71. H. Zhai, P.C. Dorrestein, A. Chatterjee, T.P. Begley, and F.W. Mclafferty Simultaneous kinetic characterization of multiple protein forms by top down mass spectrometry J. Am. Soc. Mass Spectrom. 16 2005 1052 1059
72. J. Pan, J. Han, C.H. Borchers, and L. Konermann Structure and dynamics of small soluble Aβ(1-40) oligomers studied by top-down hydrogen exchange mass spectrometry Biochemistry 51 2012 3694 3703
73. N. Carulla, M. Zhou, M. Arimon, M. Gairí, E. Giralt, C.V. Robinson, and C.M. Dobson Experimental characterization of disordered and ordered aggregates populated during the process of amyloid fibril formation Proc. Natl. Acad. Sci. U. S. A. 106 2009 7828 7833
74. V.L. Woods, and Y. Hamuro High resolution, high-throughput amide deuterium exchange-mass spectrometry (DXMS) determination of protein binding site structure and dynamics: Utility in pharmaceutical design J. Cell. Biochem. 84 2002 89 98
75. S. Ghaemmaghami, M.C. Fitzgerald, and T.G. Oas A quantitative, high-throughput screen for protein stability Proc. Natl. Acad. Sci. U. S. A. 97 2000 8296 8301
76. M.C. Fitzgerald, and G.M. West Painting proteins with covalent labels: What's in the picture? J. Am. Soc. Mass Spectrom. 20 2009 1193 1206
77. L. Tang, E.D. Hopper, Y. Tong, J.D. Sadowsky, K.J. Peterson, S.H. Gellman, and M.C. Fitzgerald H/D exchange- and mass spectrometry-based strategy for the thermodynamic analysis of protein-ligand binding Anal. Chem. 79 2007 5869 5877
78. D.D. Weis, T.E. Wales, J.R. Engen, M. Hotchko, and L.F. Ten Eyck Identification and characterization of EX1 kinetics in H/D exchange mass spectrometry by peak width analysis J. Am. Soc. Mass Spectrom. 2006 1498 1509
79. H. Xiao, J.K. Hoerner, S.J. Eyles, A. Dobo, E. Voigtman, A.I. Mel'cuk, and I.A. Kaltashov Mapping protein energy landscapes with amide hydrogen exchange and mass spectrometry: I A generalized model for a two-state protein and comparison with experiment Protein Sci. 14 2005 543 557
80. X. Lou, M. Kirchner, B.Y. Renard, U. Köthe, S. Boppel, C. Graf, C.-T. Lee, J.A.J. Steen, H. Steen, M.P. Mayer, and F.A. Hamprecht Deuteration distribution estimation with improved sequence coverage for HX/MS experiments Bioinformatics 26 2010 1535 1541
81. M. Hotchko, G.S. Anand, E.A. Komives, and L.F. Ten Eyck Automated extraction of backbone deuteration levels from amide H/2H mass spectrometry experiments Protein Sci. 15 2006 583 601
82. E.W. Chung, E.J. Nettleton, C.J. Morgan, M. Gross, A. Miranker, S.E. Radford, C.M. Dobson, and C.V. Robinson Hydrogen exchange properties of proteins in native and denatured states monitored by mass spectrometry and NMR Protein Sci. 6 1997 1316 1324
83. G.W. Slysz, A.J. Percy, and D.C. Schriemer Restraining expansion of the peak envelope in H/D exchange-MS and its application in detecting perturbations of protein structure/dynamics Anal. Chem. 80 2008 7004 7011
84. A. Hamid Wani, and J.B. Udgaonkar HX-ESI-MS and optical studies of the unfolding of thioredoxin indicate stabilization of a partially unfolded, aggregation-competent intermediate at low pH Biochemistry 45 2006 11226 11238
85. A.H. Wani, and J.B. Udgaonkar Native state dynamics drive the unfolding of the SH3 domain of PI3 kinase at high denaturant concentration Proc. Natl. Acad. Sci. U. S. A. 106 2009 20711 20716
86. I.A. Kaltashov, C.E. Bobst, and R.R. Abzalimov 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. 81 2009 7892 7899
87. Z. Zhang, C.B. Post, and D.L. Smith Amide hydrogen exchange determined by mass spectrometry: Application to rabbit muscle aldolase Biochemistry 35 1996 779 791
88. J.J. Rosa, and F.M. Richards An experimental procedure for increasing the structural resolution of chemical hydrogen-exchange measurements on proteins: Application to ribonuclease S peptide J. Mol. Biol. 133 1979 399 416
89. J.J. Englander, J.R. Rogero, and S.W. Englander Protein hydrogen exchange studied by the fragment separation method Anal. Biochem. 147 1985 234 244
90. Z. Zhang, and D.L. Smith Thermal-induced unfolding domains in aldolase identified by amide hydrogen exchange and mass spectrometry Protein Sci. 5 1996 1282 1289
91. Y. Liu, and D.L. Smith Probing high order structure of proteins by fast-atom bombardment mass spectrometry J. Am. Soc. Mass Spectrom. 5 1994 19 28
92. R.R. Landgraf, M.J. Chalmers, and P.R. Griffin Automated hydrogen/deuterium exchange electron transfer dissociation high resolution mass spectrometry measured at single-amide resolution J. Am. Soc. Mass Spectrom. 23 2012 301 309
93. K.D. Rand, S.D. Pringle, M. Morris, J.R. Engen, and J.M. Brown ETD in a traveling wave ion guide at tuned Z-spray ion source conditions allows for site-specific hydrogen/deuterium exchange measurements J. Am. Soc. Mass Spectrom. 22 2011 1784 1793
94. J.J. Englander, C. Del Mar, W. Li, S.W. Englander, J.S. Kim, D.D. Stranz, Y. Hamuro, and V.L. Woods Protein structure change studied by hydrogen-deuterium exchange, functional labeling, and mass spectrometry Proc. Natl. Acad. Sci. U. S. A. 100 2003 7057 7062
95. E. Althaus, S. Canzar, C. Ehrler, M.R. Emmett, A. Karrenbauer, A.G. Marshall, A. Meyer-Bäse, J.D. Tipton, and H.-M. Zhang Computing H/D-exchange rates of single residues from data of proteolytic fragments BMC Bioinformatics 11 2010 424
96. P.G. Fajer, G.M. Bou-Assaf, and A.G. Marshall Improved sequence resolution by global analysis of overlapped peptides in hydrogen/deuterium exchange mass spectrometry J. Am. Soc. Mass Spectrom. 23 2012 1202 1208
97. L. Mayne, Z.-Y. Kan, P. Sevugan Chetty, A. Ricciuti, B.T. Walters, and S.W. Englander Many overlapping peptides for protein hydrogen exchange experiments by the fragment separation-mass spectrometry method J. Am. Soc. Mass Spectrom. 22 2011 1898 1905
98. T.R. Keppel, M.E. Jacques, R.W. Young, K.L. Ratzlaff, and D.D. Weis An efficient and inexpensive refrigerated LC system for H/D exchange mass spectrometry J. Am. Soc. Mass Spectrom. 22 2011 1472 1476
99. R. Zenobi, and R. Knochenmuss Ion formation in MALDI mass spectrometry Mass Spectrom. Rev. 17 1998 337 366
100. J.G. Mandell, A. Baerga-Ortiz, A.M. Falick, and E.A. Komives Measurement of solvent accessibility at protein-protein interfaces Meth. Mol. Biol. 305 2005 65 80
101. J. Pan, J. Han, C.H. Borchers, and L. Konermann Hydrogen/deuterium exchange mass spectrometry with top-down electron capture dissociation for characterizing structural transitions of a 17 kDa protein J. Am. Chem. Soc. 131 2009 12801 12808
102. K. Breuker, M. Jin, X. Han, H. Jiang, and F.W. Mclafferty Top-down identification and characterization of biomolecules by mass spectrometry J. Am. Soc. Mass Spectrom. 19 2008 1045 1053
103. M. Zehl, K.D. Rand, O.N. Jensen, and T.J.D. Jørgensen Electron transfer dissociation facilitates the measurement of deuterium incorporation into selectively labeled peptides with single residue resolution J. Am. Chem. Soc. 130 2008 17453 17459
104. P.D. Compton, L. Zamdborg, P.M. Thomas, and N.L. Kelleher On the scalability and requirements of whole protein mass spectrometry Anal. Chem. 83 2011 6868 6874
105. S. Sharma, H. Zheng, Y.J. Huang, A. Ertekin, Y. Hamuro, P. Rossi, R. Tejero, T.B. Acton, R. Xiao, M. Jiang, L. Zhao, L.C. Ma, G.V.T. Swapna, J.M. Aramini, and G.T. Montelione Construct optimization for protein NMR structure analysis using amide hydrogen/deuterium exchange mass spectrometry Proteins 76 2009 882 894
106. D. Pantazatos, J.S. Kim, H.E. Klock, R.C. Stevens, I.A. Wilson, S.A. Lesley, and V.L. Woods Rapid refinement of crystallographic protein construct definition employing enhanced hydrogen/deuterium exchange MS Proc. Natl. Acad. Sci. U. S. A. 101 2004 751 756
107. G. Spraggon, D. Pantazatos, H.E. Klock, I.A. Wilson, V.L. Woods, and S.A. Lesley On the use of DXMS to produce more crystallizable proteins: Structures of the T maritima proteins TM0160 and TM1171 Protein Sci. 13 2004 3187 3199
108. T. Liu, D. Pantazatos, S. Li, Y. Hamuro, V.J. Hilser, and V.L. Woods Quantitative assessment of protein structural models by comparison of H/D exchange MS data with exchange behavior accurately predicted by DXCOREX J. Am. Soc. Mass Spectrom. 23 2012 43 56
109. P.O. Craig, J. Lätzer, P. Weinkam, R.M.B. Hoffman, D.U. Ferreiro, E.A. Komives, and P.G. Wolynes Prediction of native-state hydrogen exchange from perfectly funneled energy landscapes J. Am. Chem. Soc. 133 2011 17463 17472
110. G.G. Tartaglia, A. Cavalli, and M. Vendruscolo Prediction of local structural stabilities of proteins from their amino acid sequences Structure 15 2007 139 143
111. N.V. Dovidchenko, M.Y. Lobanov, S.O. Garbuzynskiy, and O.V. Galzitskaya Prediction of amino acid residues protected from hydrogen-deuterium exchange in a protein chain Biochemistry (Mosc.) 74 2009 888 897
112. D.M. LeMaster, J.S. Anderson, and G. Hernández Peptide conformer acidity analysis of protein flexibility monitored by hydrogen exchange Biochemistry 48 2009 9256 9265
113. H.J. Dyson Expanding the proteome: Disordered and alternatively folded proteins Q. Rev. Biophys. 44 2011 467 518
114. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
115. C.E. Bobst, and I.A. Kaltashov Localizing flexible regions in proteins using hydrogen-deuterium exchange mass spectrometry Meth. Mol. Biol. 896 2012 375 385
116. J.G. Mandell, A.M. Falick, and E.A. Komives Identification of protein-protein interfaces by decreased amide proton solvent accessibility Proc. Natl. Acad. Sci. U. S. A. 95 1998 14705 14710
117. J.G. Mandell, A. Baerga-Ortiz, S. Akashi, K. Takio, and E.A. Komives Solvent accessibility of the thrombin-thrombomodulin interface J. Mol. Biol. 306 2001 575 589
118. K.M. Sours, S.C. Kwok, T. Rachidi, T. Lee, A. Ring, A.N. Hoofnagle, K.A. Resing, and N.G. Ahn Hydrogen-exchange mass spectrometry reveals activation-induced changes in the conformational mobility of p38alpha MAP kinase J. Mol. Biol. 379 2008 1075 1093
119. T. Tu, M. Drǎguşanu, B.-A. Petre, D.L. Rempel, M. Przybylski, and M.L. Gross Protein-peptide affinity determination using an h/d exchange dilution strategy: Application to antigen-antibody interactions J. Am. Soc. Mass Spectrom. 21 2010 1660 1667
120. C.V. Robinson, M. Gross, S.J. Eyles, J.J. Ewbank, M. Mayhew, F.U. Hartl, C.M. Dobson, and S.E. Radford Conformation of GroEL-bound alpha-lactalbumin probed by mass spectrometry Nature 372 1994 646 651
121. G. Cheng, E. Basha, V.H. Wysocki, and E. Vierling Insights into small heat shock protein and substrate structure during chaperone action derived from hydrogen/deuterium exchange and mass spectrometry J. Biol. Chem. 283 2008 26634 26642
122. W. Rist, C. Graf, B. Bukau, and M. Mayer Amide hydrogen exchange reveals conformational changes in Hsp70 chaperones important for allosteric regulation J. Biol. Chem. 281 2006 16493 16501
123. C. Andreasson, J. Fiaux, H. Rampelt, S. Druffel-Augustin, and B. Bukau Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity Proc. Natl. Acad. Sci. U. S. A. 105 2008 16519 16524
124. J. Fiaux, J. Horst, A. Scior, S. Preissler, A. Koplin, B. Bukau, and E. Deuerling Structural analysis of the ribosome-associated complex (RAC) reveals an unusual Hsp70/Hsp40 interaction J. Biol. Chem. 285 2010 3227 3234
125. E.U. Weber-Ban, B.G. Reid, A.D. Miranker, and A.L. Horwich Global unfolding of a substrate protein by the Hsp100 chaperone ClpA Nature 401 1999 90 93
126. B.S. Moorthy, and G.S. Anand Multistate allostery in response regulators: Phosphorylation and mutagenesis activate RegA via alternate modes J. Mol. Biol. 417 2012 468 487
127. J. Swain, and L.M. Gierasch The changing landscape of protein allostery Curr. Opin. Struct. Biol. 16 2006 102 108
128. Z. Shi, K.A. Resing, and N.G. Ahn Networks for the allosteric control of protein kinases Curr. Opin. Struct. Biol. 16 2006 686 692
129. P. Sevugan Chetty, L. Mayne, Z.-Y. Kan, S. Lund-Katz, S.W. Englander, and M.C. Phillips Apolipoprotein A-I helical structure and stability in discoidal high-density lipoprotein (HDL) particles by hydrogen exchange and mass spectrometry Proc. Natl. Acad. Sci. U. S. A. 109 2012 11687 11692
130. X. Mei, and D. Atkinson Crystal structure of C-terminal truncated apolipoprotein A-I reveals the assembly of high density lipoprotein (HDL) by dimerization J. Biol. Chem. 286 2011 38570 38582
131. O. Gursky, X. Mei, and D. Atkinson The crystal structure of the C-terminal truncated apolipoprotein A-I sheds new light on amyloid formation by the N-terminal fragment Biochemistry 51 2012 10 18
132. D.W. Borhani, D.P. Rogers, J.A. Engler, and C.G. Brouillette Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation Proc. Natl. Acad. Sci. U. S. A. 94 1997 12291 12296
133. C.-T. Lee, C. Graf, F.J. Mayer, S.M. Richter, and M.P. Mayer Dynamics of the regulation of Hsp90 by the co-chaperone Sti1 EMBO J. 31 2012 1518 1528
134. C. Ratzke, M. Mickler, B. Hellenkamp, J. Buchner, and T. Hugel Dynamics of heat shock protein 90 C-terminal dimerization is an important part of its conformational cycle Proc. Natl. Acad. Sci. U. S. A. 107 2010 16101 16106
135. D. Wildes, and S. Marqusee Hydrogen exchange and ligand binding: Ligand-dependent and ligand-independent protection in the Src SH3 domain Protein Sci. 14 2005 81 88
136. C. Graf, M. Stankiewicz, G. Kramer, and M.P. Mayer Spatially and kinetically resolved changes in the conformational dynamics of the Hsp90 chaperone machine EMBO J. 28 2009 602 613
137. S. Cavagnero, Y. Thériault, S.S. Narula, H.J. Dyson, and P.E. Wright Amide proton hydrogen exchange rates for sperm whale myoglobin obtained from 15N-1H NMR spectra Protein Sci. 9 2000 186 193
138. Y. Tsutsui, R. Dela Cruz, and P.L. Wintrode Folding mechanism of the metastable serpin α1-antitrypsin Proc. Natl. Acad. Sci. U. S. A. 109 2012 4467 4472
139. B. Gooptu, and D.A. Lomas Conformational pathology of the serpins: Themes, variations, and therapeutic strategies Annu. Rev. Biochem. 78 2009 147 176
140. B. Krishnan, and L.M. Gierasch Dynamic local unfolding in the serpin α-1 antitrypsin provides a mechanism for loop insertion and polymerization Nat. Struct. Mol. Biol. 18 2011 222 226
141. J.-H. Baek, W.S. Yang, C. Lee, and M.-H. Yu Functional unfolding of alpha1-antitrypsin probed by hydrogen-deuterium exchange coupled with mass spectrometry Mol. Cell. Proteomics 8 2009 1072 1081
142. D. Kim, and M.H. Yu Folding pathway of human alpha 1-antitrypsin: Characterization of an intermediate that is active but prone to aggregation Biochem. Biophys. Res. Commun. 226 1996 378 384
143. E.L. James, J.C. Whisstock, M.G. Gore, and S.P. Bottomley Probing the unfolding pathway of alpha1-antitrypsin J. Biol. Chem. 274 1999 9482 9488
144. H. Im, M.-S. Woo, K.Y. Hwang, and M.-H. Yu Interactions causing the kinetic trap in serpin protein folding J. Biol. Chem. 277 2002 46347 46354
145. C.-H. Jung, Y.-R. Na, and H. Im Retarded protein folding of deficient human alpha 1-antitrypsin D256V and L41P variants Protein Sci. 13 2004 694 702
146. P.E. Stein, and R.W. Carrell What do dysfunctional serpins tell us about molecular mobility and disease Nat. Struct. Biol. 2 1995 96 113
147. Y. Pan, L. Brown, and L. Konermann Hydrogen exchange mass spectrometry of bacteriorhodopsin reveals light-induced changes in the structural dynamics of a biomolecular machine J. Am. Chem. Soc. 133 2011 20237 20244
148. J.P. Schlebach, Z. Cao, J.U. Bowie, and C. Park Revisiting the folding kinetics of bacteriorhodopsin Protein Sci. 21 2012 97 106
149. S.E. Jackson How do small single-domain proteins fold? Fold. Des. 3 1998 R81 R91
150. R.B. Best, and M. Vendruscolo Structural interpretation of hydrogen exchange protection factors in proteins: Characterization of the native state fluctuations of CI2 Structure 14 2006 97 106
151. I.A. Kaltashov Probing protein dynamics and function under native and mildly denaturing conditions with hydrogen exchange and mass spectrometry Int. J. Mass Spectrom. 240 2005 249 259
152. L. Konermann, X. Tong, and Y. Pan Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches J. Mass Spectrom. 43 2008 1021 1036