Getting to the core of protein pharmaceuticals - Comprehensive structure analysis by mass spectrometry

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 93, Issue , 2015, Pages 95-109

  Leurs, Ulrike ^a   Mistarz, Ulrik H ^a   Rand, Kasper D ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Biopharmaceuticals; Hydrogen deuterium exchange mass spectrometry; Mass spectrometry; Pharmaceutical analysis; Protein pharmaceuticals; Protein structure analysis

Indexed keywords

CORE PROTEIN; DRUG; PROTEIN;

ARTICLE; DEUTERIUM HYDROGEN EXCHANGE; MASS SPECTROMETRY; PHARMACEUTICS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG STABILITY; PROCEDURES; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION;

DRUG STABILITY; MASS SPECTROMETRY; MODELS, MOLECULAR; PHARMACEUTICAL PREPARATIONS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEINS; PROTEOLYSIS; STRUCTURE-ACTIVITY RELATIONSHIP; TECHNOLOGY, PHARMACEUTICAL;

EID: 84926283147     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2015.03.012     Document Type: Review

References (155)

1. Ronald R. Rader (Ed.), Biosimilars/Biobetters Pipeline Review, 2014. < www.biopharma.com >.
2. D.J. Crommelin, G. Storm, R. Verrijk, L. de Leede, W. Jiskoot, and W.E. Hennink Shifting paradigms: biopharmaceuticals versus low molecular weight drugs Int. J. Pharm. 266 2003 3 16
3. L. Tao, M. Ackerman, W. Wu, P. Liu, and R. Russell Characterization of impurities and degradants in protein therapeutics by mass spectrometry B.N. Pramanik, H.-N. Lee, S.K. Kim, G. Chen, Characterization of Impurities and Degradants using Mass Spectrometry 2011 John Wiley & Sons, Inc.
4. S. Hermeling, D.J. Crommelin, H. Schellekens, and W. Jiskoot Structure-immunogenicity relationships of therapeutic proteins Pharm. Res. 21 2004 897 903
5. F. Hillenkamp, and M. Karas Mass spectrometry of peptides and proteins by matrix-assisted ultraviolet laser desorption/ionization Methods Enzymol. 193 1990 280 295
6. F. Hillenkamp, M. Karas, R.C. Beavis, and B.T. Chait Matrix-assisted laser desorption/ionization mass spectrometry of biopolymers Anal. Chem. 63 1991 1193A 1203A
7. M. Karas, and F. Hillenkamp Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons Anal. Chem. 60 1988 2299 2301
8. J.B. Fenn, M. Mann, C.K. Meng, S.F. Wong, and C.M. Whitehouse Electrospray ionization for mass spectrometry of large biomolecules Science 246 1989 64 71
9. K. Tanaka The origin of macromolecule ionization by laser irradiation (Nobel lecture) Angew. Chem. Int. Ed. 42 2003 3860 3870
10. M.L. Gross, G. Chen, and B.N. Pramanik Protein and Peptide Mass Spectrometry in Drug Discovery 2012 Wiley Hoboken, NJ
11. G. Chen Characterization of Protein Therapeutics using Mass Spectrometry first ed. 2013 Springer US
12. F. Lanucara, S.W. Holman, C.J. Gray, and C.E. Eyers The power of ion mobility-mass spectrometry for structural characterization and the study of conformational dynamics Nat. Chem. 6 2014 281 294
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 1234
14. 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
15. D.P. Marciano, V. Dharmarajan, and P.R. Griffin HDX-MS guided drug discovery: small molecules and biopharmaceuticals Curr. Opin. Struct. Biol. 28C 2014 105 111
16. R. Majumdar, C.R. Middaugh, D.D. Weis, and D.B. Volkin Hydrogen-deuterium exchange mass spectrometry as an emerging analytical tool for stabilization and formulation development of therapeutic monoclonal antibodies J. Pharm. Sci. 104 2014 327 345
17. H. Wei, J. Mo, L. Tao, R.J. Russell, A.A. Tymiak, G. Chen, R.E. Iacob, and J.R. Engen Hydrogen/deuterium exchange mass spectrometry for probing higher order structure of protein therapeutics: methodology and applications Drug Discov. Today 19 2014 95 102
18. L. Konermann, S. Vahidi, and M.A. Sowole Mass spectrometry methods for studying structure and dynamics of biological macromolecules Anal. Chem. 86 2014 213 232
19. S.A. Berkowitz, J.R. Engen, J.R. Mazzeo, and G.B. Jones Analytical tools for characterizing biopharmaceuticals and the implications for biosimilars Nat. Rev. Drug Discov. 11 2012 527 540
20. J.H. Moon, S. Yoon, Y.J. Bae, and M.S. Kim Formation of gas-phase peptide ions and their dissociation in MALDI: insights from kinetic and ion yield studies Mass Spectrom. Rev. 34 2014 94 115
21. P. Kebarle, and M. Peschke On the mechanisms by which the charged droplets produced by electrospray lead to gas phase ions Anal. Chim. Acta 406 2000 11 35
22. P. Roepstorff, and J. Fohlman Proposal for a common nomenclature for sequence ions in mass spectra of peptides Biomed. Mass Spectrom. 11 1984 601
23. B. Paizs, and S. Suhai Fragmentation pathways of protonated peptides Mass Spectrom. Rev. 24 2005 508 548
24. J.E. Syka, J.J. Coon, M.J. Schroeder, J. Shabanowitz, and D.F. Hunt Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry Proc. Natl. Acad. Sci. U.S.A. 101 2004 9528 9533
25. R.A. Zubarev, D.M. Horn, E.K. Fridriksson, N.L. Kelleher, N.A. Kruger, M.A. Lewis, B.K. Carpenter, and F.W. McLafferty Electron capture dissociation for structural characterization of multiply charged protein cations Anal. Chem. 72 2000 563 573
26. K.R. Jennings Collision-induced decompositions of aromatic molecular ions Int. J. Mass Spectrom. Ion Phys. 1 1968 227 235
27. L. Quan, and M. Liu CID, ETD and HCD fragmentation to study protein post-translational modifications Mod. Chem. Appl. 1 2013 e102
28. J. Wiesner, T. Premsler, and A. Sickmann Application of electron transfer dissociation (ETD) for the analysis of posttranslational modifications Proteomics 8 2008 4466 4483
29. F. Kjeldsen, K.F. Haselmann, B.A. Budnik, E.S. Sørensen, and R.A. Zubarev Complete characterization of posttranslational modification sites in the bovine milk protein PP3 by tandem mass spectrometry with electron capture dissociation as the last stage Anal. Chem. 75 2003 2355 2361
30. J.R. Yates, C.I. Ruse, and A. Nakorchevsky Proteomics by mass spectrometry: approaches, advances, and applications Annu. Rev. Biomed. Eng. 11 2009 49 79
31. M. Holcapek, R. Jirasko, and M. Lisa Recent developments in liquid chromatography-mass spectrometry and related techniques J. Chromatogr. A 1259 2012 3 15
32. J.F. Nemeth-Cawley, B.S. Tangarone, and J.C. Rouse "Top Down" characterization is a complementary technique to peptide sequencing for identifying protein species in complex mixtures J. Proteome Res. 2 2003 495 505
33. E. Wagner-Rousset, M.C. Janin-Bussat, O. Colas, M. Excoffier, D. Ayoub, J.F. Haeuw, I. Rilatt, M. Perez, N. Corvaia, and A. Beck Antibody-drug conjugate model fast characterization by LC-MS following IdeS proteolytic digestion MAbs 6 2014 273 285
34. M. Mann, and O.N. Jensen Proteomic analysis of post-translational modifications Nat. Biotechnol. 21 2003 255 261
35. B. Thiede, W. Höhenwarter, A. Krah, J. Mattow, M. Schmid, F. Schmidt, and P.R. Jungblut Peptide mass fingerprinting Methods 35 2005 237 247
36. N. Takahashi, and T. Isobe Proteomic Biology using LC-MS: Large Scale Analysis of Cellular Dynamics and Function 2008 Wiley-Interscience, John Wiley Chichester, Hoboken, NJ
37. M.A. Gillette, and S.A. Carr Quantitative analysis of peptides and proteins in biomedicine by targeted mass spectrometry Nat. Methods 10 2013 28 34
38. D.C. Liebler, and L.J. Zimmerman Targeted quantitation of proteins by mass spectrometry Biochemistry 52 2013 3797 3806
39. E. Ezan, M. Dubois, and F. Becher Bioanalysis of recombinant proteins and antibodies by mass spectrometry Analyst 134 2009 825 834
40. I. van den Broek, W.M. Niessen, and W.D. van Dongen Bioanalytical LC-MS/MS of protein-based biopharmaceuticals J. Chromatogr. B 929 2013 161 179
41. S. Zhang, and W. Jian Recent advances in absolute quantification of peptides and proteins using LC-MS Rev. Anal. Chem. 33 2014 31 47
42. Z. Zhang, H. Pan, and X. Chen Mass Spectrom. Rev. 28 2009 147 176
43. H. Xie, A. Chakraborty, J. Ahn, Y.Q. Yu, D.P. Dakshinamoorthy, M. Gilar, W. Chen, and J.R. Mazzeo Rapid comparison of a candidate biosimilar to an innovator monoclonal antibody with advanced liquid chromatography and mass spectrometry technologies MAbs 2 2010 379 394
44. Y.O. Tsybin, L. Fornelli, C. Stoermer, M. Luebeck, J. Parra, S. Nallet, F.M. Wurm, and R. Hartmer Structural analysis of intact monoclonal antibodies by electron transfer dissociation mass spectrometry Anal. Chem. 83 2011 8919 8927
45. Y. Mao, S.G. Valeja, J.C. Rouse, C.L. Hendrickson, and A.G. Marshall Top-down structural analysis of an intact monoclonal antibody by electron capture dissociation-Fourier transform ion cyclotron resonance-mass spectrometry Anal. Chem. 85 2013 4239 4246
46. F.G. Hanisch Top-down sequencing of O-glycoproteins by in-source decay matrix-assisted laser desorption ionization mass spectrometry for glycosylation site analysis Anal. Chem. 83 2011 4829 4837
47. J.C. Rouse, J.E. McClellan, H.K. Patel, M.A. Jankowski, and T.J. Porter Top-down characterization of protein pharmaceuticals by liquid chromatography/mass spectrometry: application to recombinant factor IX comparability - a case study Methods Mol. Biol. 308 2005 435 460
48. C.A.S. Barnes, and A. Lim Applications of mass spectrometry for the structural characterization of recombinant protein pharmaceuticals Mass Spectrom. Rev. 26 2007 370 388
49. G.M. Edelman, B.A. Cunningham, W.E. Gall, P.D. Gottlieb, U. Rutishauser, and M.J. Waxdal The covalent structure of an entire gammaG immunoglobulin molecule Proc. Natl. Acad. Sci. U.S.A. 63 1969 78 85
50. J.W. Ellison, B.J. Berson, and L.E. Hood The nucleotide sequence of a human immunoglobulin C gamma1 gene Nucleic Acids Res. 10 1982 4071 4079
51. C.E. Eyers, and S.J. Gaskell Wiley Encyclopedia Chem. Biol. 2008
52. H. Tong, D. Bell, K. Tabei, and M.M. Siegel Automated data massaging, interpretation, and e-mailing modules for high throughput open access mass spectrometry J. Am. Soc. Mass Spectrom. 10 1999 1174 1187
53. E. Stadtman, and R. Levine Free radical-mediated oxidation of free amino acids and amino acid residues in proteins Amino Acids 25 2003 207 218
54. E. Shacter Quantification and significance of protein oxidation in biological samples 1∗ Drug Metab. Rev. 32 2000 307 326
55. M.C. Manning, D.K. Chou, B.M. Murphy, R.W. Payne, and D.S. Katayama Stability of protein pharmaceuticals: an update Pharm. Res. 27 2010 544 575
56. S. Li, C. Schoneich, and R.T. Borchardt Chemical instability of protein pharmaceuticals: mechanisms of oxidation and strategies for stabilization Biotechnol. Bioeng. 48 1995 490 500
57. L.A. Sluyterman Photo-oxidation, sensitized by proflavine, of a number of protein constituents Biochim. Biophys. Acta 60 1962 557 561
58. M.C. Manning, K. Patel, and R.T. Borchardt Stability of protein pharmaceuticals Pharm. Res. 6 1989 903 918
59. S. Hermeling, H. Schellekens, C. Maas, M.F. Gebbink, D.J. Crommelin, and W. Jiskoot Antibody response to aggregated human interferon alpha2b in wild-type and transgenic immune tolerant mice depends on type and level of aggregation J. Pharm. Sci. 95 2006 1084 1096
60. T. Geiger, and S. Clarke Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation J. Biol. Chem. 262 1987 785 794
61. G.C. Chu, D. Chelius, G. Xiao, H.K. Khor, S. Coulibaly, and P.V. Bondarenko Accumulation of succinimide in a recombinant monoclonal antibody in mildly acidic buffers under elevated temperatures Pharm. Res. 24 2007 1145 1156
62. P.B. O'Connor, J.J. Cournoyer, S.J. Pitteri, P.A. Chrisman, and S.A. McLuckey Differentiation of aspartic and isoaspartic acids using electron transfer dissociation J. Am. Soc. Mass Spectrom. 17 2006 15 19
63. J.J. Cournoyer, J.L. Pittman, V.B. Ivleva, E. Fallows, L. Waskell, C.E. Costello, and P.B. O'Connor Deamidation: differentiation of aspartyl from isoaspartyl products in peptides by electron capture dissociation Protein Sci. 14 2005 452 463
64. D. Chelius, D.S. Rehder, and P.V. Bondarenko Identification and characterization of deamidation sites in the conserved regions of human immunoglobulin gamma antibodies Anal. Chem. 77 2005 6004 6011
65. U.J. Lewis, E.V. Cheever, and W.C. Hopkins Kinetic study of the deamidation of growth hormone and prolactin Biochim. Biophys. Acta 214 1970 498 508
66. B.V. Fisher, and P.B. Porter Stability of bovine insulin J. Pharm. Pharmacol. 33 1981 203 206
67. W. Wang, A.R. Meeler, L.T. Bergerud, M. Hesselberg, M. Byrne, and Z. Wu Quantification and characterization of antibody deamidation by peptide mapping with mass spectrometry Int. J. Mass Spectrom. 312 2012 107 113
68. D. Bagal, J.F. Valliere-Douglass, A. Balland, and P.D. Schnier Resolving disulfide structural isoforms of IgG2 monoclonal antibodies by ion mobility mass spectrometry Anal. Chem. 82 2010 6751 6755
69. D.S. Zhao, Z.R. Gregorich, and Y. Ge High throughput screening of disulfide-containing proteins in a complex mixture Proteomics 13 2013 3256 3260
70. A. Kraj, H.J. Brouwer, N. Reinhoud, and J.P. Chervet A novel electrochemical method for efficient reduction of disulfide bonds in peptides and proteins prior to MS detection Anal. Bioanal. Chem. 405 2013 9311 9320
71. S. Mysling, R. Salbo, M. Ploug, and T.J. Jorgensen Electrochemical reduction of disulfide-containing proteins for hydrogen/deuterium exchange monitored by mass spectrometry Anal. Chem. 86 2014 340 345
72. H. Lis, and N. Sharon Protein glycosylation. Structural and functional aspects. FEBS J. 218 1993 1 27
73. M.v.d. Weert, and E.H. Møller Immunogenicity of Biopharmaceuticals 2008 Springer, AAPS Press Arlington, VA, New York
74. H. Schellekens Bioequivalence and the immunogenicity of biopharmaceuticals Nat. Rev. Drug Discov. 1 2002 457 462
75. R.G. Spiro Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds Glycobiology 12 2002 43R 56R
76. J.C. Bigge, T.P. Patel, J.A. Bruce, P.N. Goulding, S.M. Charles, and R.B. Parekh Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid Anal. Biochem. 230 1995 229 238
77. R. Montesino, L. Calvo, A. Vallin, P.M. Rudd, D.J. Harvey, and J.A. Cremata Structural characterization of N-linked oligosaccharides on monoclonal antibody Nimotuzumab through process development Biologicals 40 2012 288 298
78. 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
79. K. Håkansson, H.J. Cooper, M.R. Emmett, C.E. Costello, A.G. Marshall, and C.L. Nilsson Electron capture dissociation and infrared multiphoton dissociation MS/MS of an N-glycosylated tryptic peptide to yield complementary sequence information Anal. Chem. 73 2001 4530 4536
80. D.A. Lewis, A.W. Guzzetta, W.S. Hancock, and M. Costello Characterization of humanized anti-TAC, an antibody directed against the interleukin 2 receptor, using electrospray ionization mass spectrometry by direct infusion, LC/MS, and MS/MS Anal. Chem. 66 1994 585 595
81. Y. Mechref, Use of CID/ETD mass spectrometry to analyze glycopeptides, Current Protocols in Protein Science, 2012, Unit 12.11.1-11 (Chapter 12).
82. P.F. Jensen, V. Larraillet, T. Schlothauer, H. Kettenberger, M. Hilger, and K.D. Rand Investigating the interaction between the neonatal Fc receptor and monoclonal antibody variants by hydrogen/deuterium exchange mass spectrometry Mol. Cell. Proteomics 14 2015 148 161
83. A. Harazono, N. Hashii, R. Kuribayashi, S. Nakazawa, and N. Kawasaki Mass spectrometric glycoform profiling of the innovator and biosimilar erythropoietin and darbepoetin by LC/ESI-MS J. Pharm. Biomed. Anal. 83 2013 65 74
84. Z. Lin, and D.M. Lubman Permethylated N-glycan analysis with mass spectrometry Methods Mol. Biol. 1007 2013 289 300
85. V. Tretter, F. Altmann, and L. Marz Peptide-N4-(N-acetyl-beta-glucosaminyl)asparagine amidase F cannot release glycans with fucose attached alpha 1-3 to the asparagine-linked N-acetylglucosamine residue FEBS J. 199 1991 647 652
86. W. Morelle, and J.-C. Michalski Analysis of protein glycosylation by mass spectrometry Nat. Protoc. 2 2007 1585 1602
87. J.E. Schiel, N.J. Smith, and K.W. Phinney Universal proteolysis and MSn for N- and O-glycan branching analysis J. Mass Spectrom. 48 2013 533 538
88. K. Marino, J. Bones, J.J. Kattla, and P.M. Rudd A systematic approach to protein glycosylation analysis: a path through the maze Nat. Chem. Biol. 6 2010 713 723
89. D.E. Clemmer, and M.F. Jarrold Ion mobility measurements and their applications to clusters and biomolecules J. Mass Spectrom. 32 1997 577 592
90. A.B. Kanu, P. Dwivedi, M. Tam, L. Matz, and H.H. Hill Jr. Ion mobility-mass spectrometry J. Mass Spectrom. 43 2008 1 22
91. B.C. Bohrer, S.I. Merenbloom, S.L. Koeniger, A.E. Hilderbrand, and D.E. Clemmer Biomolecule analysis by ion mobility spectrometry Annu. Rev. Anal. Chem. 1 2008 293 327
92. W. Chen, Characterizing biotherapeutic protein 3D structures by electrospray ion-mobility mass spectrometry: biological significance and comparison with X-ray crystallography and NMR measurements, in: 58th ASMS Conference on Mass Spectrometry and Allied Topics, Salt Lake City, UT, USA, 2010.
93. E.R. Badman, C.S. Hoaglund-Hyzer, and D.E. Clemmer Monitoring structural changes of proteins in an ion trap over 10-200 ms: unfolding transitions in cytochrome c ions Anal. Chem. 73 2001 6000 6007
94. K. Breuker, and F.W. McLafferty Stepwise evolution of protein native structure with electrospray into the gas phase, 10(-12) to 10(2) s Proc. Natl. Acad. Sci. U.S.A. 105 2008 18145 18152
95. T. Wyttenbach, and M.T. Bowers Structural stability from solution to the gas phase: native solution structure of ubiquitin survives analysis in a solvent-free ion mobility-mass spectrometry environment J. Phys. Chem. B 115 2011 12266 12275
96. F. Debaene, E. Wagner-Rousset, O. Colas, D. Ayoub, N. Corvaia, A. Van Dorsselaer, A. Beck, and S. Cianferani Time resolved native ion-mobility mass spectrometry to monitor dynamics of IgG4 Fab arm exchange and "bispecific" monoclonal antibody formation Anal. Chem. 85 2013 9785 9792
97. C.W. Damen, W. Chen, A.B. Chakraborty, M. van Oosterhout, J.R. Mazzeo, J.C. Gebler, J.H. Schellens, H. Rosing, and J.H. Beijnen Electrospray ionization quadrupole ion-mobility time-of-flight mass spectrometry as a tool to distinguish the lot-to-lot heterogeneity in N-glycosylation profile of the therapeutic monoclonal antibody trastuzumab J. Am. Soc. Mass Spectrom. 20 2009 2021 2033
98. R. Salbo, M.F. Bush, H. Naver, I. Campuzano, C.V. Robinson, I. Pettersson, T.J. Jorgensen, and K.F. Haselmann Traveling-wave ion mobility mass spectrometry of protein complexes: accurate calibrated collision cross-sections of human insulin oligomers Rapid Commun. Mass Spectrom. 26 2012 1181 1193
99. C. Uetrecht, R.J. Rose, E. van Duijn, K. Lorenzen, and A.J. Heck Ion mobility mass spectrometry of proteins and protein assemblies Chem. Soc. Rev. 39 2010 1633 1655
100. 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
101. 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
102. K.D. Rand, C.M. Adams, R.A. Zubarev, and T.J.D. Jørgensen Electron capture dissociation proceeds with a low degree of intramolecular migration of peptide amide hydrogens J. Am. Chem. Soc. 130 2008 1341 1349
103. K.D. Rand, M. Zehl, O.N. Jensen, and T.J.D. Jørgensen Loss of ammonia during electron-transfer dissociation of deuterated peptides as an inherent gauge of gas-phase hydrogen scrambling Anal. Chem. 82 2010 9755 9762
104. K.D. Rand, M. Zehl, O.N. Jensen, and T.J.D. Jørgensen Protein hydrogen exchange measured at single-residue resolution by electron transfer dissociation mass spectrometry Anal. Chem. 81 2009 5577 5584
105. 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
106. J. Pan, J. Han, C.H. Borchers, and L. Konermann Electron capture dissociation of electrosprayed protein ions for spatially resolved hydrogen exchange measurements JACS 2008
107. R.R. Abzalimov, C.E. Bobst, and I.A. Kaltashov A new approach to measuring protein backbone protection with high spatial resolution using H/D exchange and electron capture dissociation Anal. Chem. 85 2013 9173 9180
108. T.E. Wales, K.E. Fadgen, G.C. Gerhardt, and J.R. Engen High-speed and high-resolution UPLC separation at zero degrees Celsius Anal. Chem. 80 2008 6815 6820
109. R. Plumb, J. Castro-Perez, J. Granger, I. Beattie, K. Joncour, and A. Wright Ultra-performance liquid chromatography coupled to quadrupole-orthogonal time-of-flight mass spectrometry Rapid Commun. Mass Spectrom. 18 2004 2331 2337
110. S.J. Geromanos, J.P. Vissers, J.C. Silva, C.A. Dorschel, G.Z. Li, M.V. Gorenstein, R.H. Bateman, and J.I. Langridge The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LC-MS/MS Proteomics 9 2009 1683 1695
111. G.Z. Li, J.P. Vissers, J.C. Silva, D. Golick, M.V. Gorenstein, and S.J. Geromanos Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures Proteomics 9 2009 1696 1719
112. M.J. Chalmers, S.A. Busby, B.D. Pascal, Y. He, C.L. Hendrickson, A.G. Marshall, and P.R. Griffin Probing protein ligand interactions by automated hydrogen/deuterium exchange mass spectrometry Anal. Chem. 78 2006 1005 1014
113. M.J. Bennett, K. Barakat, J.T. Huzil, J. Tuszynski, and D.C. Schriemer Discovery and characterization of the laulimalide-microtubule binding mode by mass shift perturbation mapping Chem. Biol. 17 2010 725 734
114. J.R. Engen, W.H. Gmeiner, T.E. Smithgall, and D.L. Smith Hydrogen exchange shows peptide binding stabilizes motions in Hck SH2 Biochemistry 38 1999 8926 8935
115. R.E. Iacob, J.M. Zhang, N.S. Gray, and J.R. Engen Allosteric interactions between the myristate- and ATP-site of the Abl kinase PLOS ONE 6 2011
116. D. Pandit, S.J. Tuske, S.J. Coales, S.Y. E, 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
117. J. Lu, D.R. Witcher, M.A. White, X. Wang, L. Huang, R. Rathnachalam, J.M. Beals, and S. Kuhstoss IL-1beta epitope mapping using site-directed mutagenesis and hydrogen-deuterium exchange mass spectrometry analysis Biochemistry 44 2005 11106 11114
118. Q. Zhang, L.N. Willison, P. Tripathi, S.K. Sathe, K.H. Roux, M.R. Emmett, G.T. Blakney, H.M. Zhang, and A.G. Marshall Epitope mapping of a 95 kDa antigen in complex with antibody by solution-phase amide backbone hydrogen/deuterium exchange monitored by Fourier transform ion cyclotron resonance mass spectrometry Anal. Chem. 83 2011 7129 7136
119. V.H. Obungu, V. Gelfanova, and L. Huang Epitope mapping of antibodies by mass spectroscopy: a case study Methods Mol. Biol. 988 2013 291 302
120. U. Leurs, B. Lohse, S.A. Ming, P.A. Cole, R.P. Clausen, J.L. Kristensen, and K.D. Rand Dissecting the binding mode of low affinity phage display peptide ligands to protein targets by hydrogen/deuterium exchange coupled to mass spectrometry Anal. Chem. 86 2014 11734 11741
121. 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
122. H. Wei, J. Ahn, Y.Q. Yu, A. Tymiak, J.R. Engen, and G. Chen Using hydrogen/deuterium exchange mass spectrometry to study conformational changes in granulocyte colony stimulating factor upon PEGylation J. Am. Soc. Mass Spectrom. 23 2012 498 504
123. C.E. Bobst, R.R. Abzalimov, D. Houde, M. Kloczewiak, R. Mhatre, S.A. Berkowitz, and I.A. Kaltashov Detection and characterization of altered conformations of protein pharmaceuticals using complementary mass spectrometry-based approaches Anal. Chem. 80 2008 7473 7481
124. D. Houde, J. Arndt, W. Domeier, S. Berkowitz, and J.R. Engen Characterization of IgG1 conformation and conformational dynamics by hydrogen/deuterium exchange mass spectrometry Anal. Chem. 81 2009 2644 2651
125. W. Burkitt, P. Domann, and G. O'Connor Conformational changes in oxidatively stressed monoclonal antibodies studied by hydrogen exchange mass spectrometry Protein Sci. 19 2010 826 835
126. J. Visser, I. Feuerstein, T. Stangler, T. Schmiederer, C. Fritsch, and M. Schiestl Physicochemical and functional comparability between the proposed biosimilar rituximab GP2013 and originator rituximab BioDrugs 27 2013 495 507
127. K.D. Rand, M.D. Andersen, O.H. Olsen, T.J.D. Jørgensen, H. Ostergaard, O.N. Jensen, H.R. Stennicke, and E. Persson The origins of enhanced activity in factor VIIa analogs and the interplay between key allosteric sites revealed by hydrogen exchange mass spectrometry J. Biol. Chem. 283 2008 13378 13387
128. D. Houde, J. Arndt, W. Domeier, S. Berkowitz, and J.R. Engen Characterization of IgG1 conformation and conformational dynamics by hydrogen/deuterium exchange mass spectrometry Anal. Chem. 81 2009 5966
129. D. Houde, Y. Peng, S.A. Berkowitz, and J.R. Engen Post-translational modifications differentially affect IgG1 conformation and receptor binding Mol. Cell. Proteomics 9 2010 1716 1728
130. L. Tang, S. Sundaram, J. Zhang, P. Carlson, A. Matathia, B. Parekh, Q. Zhou, and M.C. Hsieh Conformational characterization of the charge variants of a human IgG1 monoclonal antibody using H/D exchange mass spectrometry MAbs 5 2013 114 125
131. R.J. Rose, P.H. van Berkel, E.T. van den Bremer, A.F. Labrijn, T. Vink, J. Schuurman, A.J. Heck, and P.W. Parren Mutation of Y407 in the CH3 domain dramatically alters glycosylation and structure of human IgG MAbs 5 2013 219 228
132. R. Majumdar, P. Manikwar, J.M. Hickey, H.S. Samra, H.A. Sathish, S.M. Bishop, C.R. Middaugh, D.B. Volkin, and D.D. Weis Effects of salts from the Hofmeister series on the conformational stability, aggregation propensity, and local flexibility of an IgG1 monoclonal antibody Biochemistry 52 2013 3376 3389
133. P. Manikwar, R. Majumdar, J.M. Hickey, S.V. Thakkar, H.S. Samra, H.A. Sathish, S.M. Bishop, C.R. Middaugh, D.D. Weis, and D.B. Volkin Correlating excipient effects on conformational and storage stability of an IgG1 monoclonal antibody with local dynamics as measured by hydrogen/deuterium-exchange mass spectrometry J. Pharm. Sci. 102 2013 2136 2151
134. Y. Bai, J.S. Milne, L. Mayne, and S.W. Englander Primary structure effects on peptide group hydrogen exchange Proteins 17 1993 75 86
135. J.J. Skinner, W.K. Lim, S. Bedard, B.E. Black, and S.W. Englander Protein hydrogen exchange: testing current models Protein Sci. 21 2012 987 995
136. Y. Li, T.D. Williams, R.L. Schowen, and E.M. Topp Characterizing protein structure in amorphous solids using hydrogen/deuterium exchange with mass spectrometry Anal. Biochem. 366 2007 18 28
137. A. Zhang, W. Qi, S.K. Singh, and E.J. Fernandez A new approach to explore the impact of freeze-thaw cycling on protein structure: hydrogen/deuterium exchange mass spectrometry (HX-MS) Pharm. Res. 28 2011 1179 1193
138. Y. Li, T.D. Williams, and E.M. Topp Effects of excipients on protein conformation in lyophilized solids by hydrogen/deuterium exchange mass spectrometry Pharm. Res. 25 2008 259 267
139. A. Zhang, S.K. Singh, M.R. Shirts, S. Kumar, and E.J. Fernandez Distinct aggregation mechanisms of monoclonal antibody under thermal and freeze-thaw stresses revealed by hydrogen exchange Pharm. Res. 29 2012 236 250
140. J. Ring, W. Stephan, and W. Brendel Anaphylactoid reactions to infusions of plasma protein and human serum albumin. Role of aggregated proteins and of stabilizers added during production J. Clin. Allergy Clin. Immunol. 9 1979 89 97
141. W. Wang Instability, stabilization, and formulation of liquid protein pharmaceuticals Int. J. Pharm. 185 1999 129 188
142. A.J.S. Jones Analysis of polypeptides and proteins Adv. Drug Deliv. Rev. 10 1993 29 90
143. T. Arakawa, J.S. Philo, D. Ejima, K. Tsumoto, and F. Arisaka Aggregation analysis of therapeutic proteins, Part 2 BioProcess Int. 5 2007 8
144. B. Kukrer, V. Filipe, E. van Duijn, P.T. Kasper, R.J. Vreeken, A.J. Heck, and W. Jiskoot Mass spectrometric analysis of intact human monoclonal antibody aggregates fractionated by size-exclusion chromatography Pharm. Res. 27 2010 2197 2204
145. D.R. Himanshu Gadgil, Paul Rainville, Bill Warren, Mark Baynham, Claude Mallet, Jeff Mazzeo, and Reb Russell SEC-MS analysis of aggregates in protein mixtures The Applications Book - Biotechnol. 2 9 2003
146. Y. Wang, Q. Lu, S.-L. Wu, B.L. Karger, and W.S. Hancock Characterization and comparison of disulfide linkages and scrambling patterns in therapeutic monoclonal antibodies: using LC-MS with electron transfer dissociation Anal. Chem. 83 2011 3133 3140
147. I. Kheterpal, K.D. Cook, and R. Wetzel Hydrogen/deuterium exchange mass spectrometry analysis of protein aggregates Methods Enzymol. 413 2006 140 166
148. R.E. Iacob, G.M. Bou-Assaf, L. Makowski, J.R. Engen, S.A. Berkowitz, and D. Houde Investigating monoclonal antibody aggregation using a combination of H/DX-MS and other biophysical measurements J. Pharm. Sci. 102 2013 4315 4329
149. J.K. Eng, A.L. McCormack, and J.R. Yates An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database J. Am. Soc. Mass Spectrom. 5 1994 976 989
150. D.N. Perkins, D.J. Pappin, D.M. Creasy, and J.S. Cottrell Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 20 1999 3551 3567
151. J.C. Silva, R. Denny, C.A. Dorschel, M. Gorenstein, I.J. Kass, G.Z. Li, T. McKenna, M.J. Nold, K. Richardson, P. Young, and S. Geromanos Quantitative proteomic analysis by accurate mass retention time pairs Anal. Chem. 77 2005 2187 2200
152. D.D. Weis, J.R. Engen, and I.J. Kass Semi-automated data processing of hydrogen exchange mass spectra using HX-Express J. Am. Soc. Mass Spectrom. 17 2006 1700 1703
153. R. Lindner, X. Lou, J. Reinstein, R.L. Shoeman, F.A. Hamprecht, and A. Winkler Hexicon 2: automated processing of hydrogen-deuterium exchange mass spectrometry data with improved deuteration distribution estimation J. Am. Soc. Mass Spectrom. 25 2014 1018 1028
154. B.D. Pascal, S. Willis, J.L. Lauer, R.R. Landgraf, G.M. West, D. Marciano, S. Novick, D. Goswami, M.J. Chalmers, and P.R. Griffin HDX workbench: software for the analysis of H/D exchange MS data J. Am. Soc. Mass Spectrom. 23 2012 1512 1521
155. 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. 17 2006 1498 1509