Extending the capabilities of intact-mass analyses to monoclonal immunoglobulins of the E-isotype (IgE)

References

• Kaltashov IA, Bobst CE, Abzalimov RR, Wang G, Baykal B, Wang S. Advances and challenges in analytical characterization of biotechnology products: mass spectrometry-based approaches to study properties and behavior of protein therapeutics. Biotechnol Adv. 2012;30:210–10. doi:10.1016/j.biotechadv.2011.05.006
   PubMed Web of Science ®Google Scholar
• Jin Y, Lin Z, Xu Q, Fu C, Zhang Z, Zhang Q, Pritts WA, Ge Y. Comprehensive characterization of monoclonal antibody by Fourier transform ion cyclotron resonance mass spectrometry. MAbs. 2019;11:106–15. doi:10.1080/19420862.2018.1525253
   PubMed Web of Science ®Google Scholar
• Dillon TM, Bondarenko PV, Rehder DS, Pipes GD, Kleemann GR, Ricci MS. Optimization of a reversed-phase high-performance liquid chromatography/mass spectrometry method for characterizing recombinant antibody heterogeneity and stability. J Chromatogr A. 2006;1120:112–20. doi:10.1016/j.chroma.2006.01.016
   PubMed Web of Science ®Google Scholar
• Bailey AO, Han G, Phung W, Gazis P, Sutton J, Josephs JL, Sandoval W. Charge variant native mass spectrometry benefits mass precision and dynamic range of monoclonal antibody intact mass analysis. MAbs. 2018;10:1214–25. doi:10.1080/19420862.2018.1521131
   PubMed Web of Science ®Google Scholar
• Valliere-Douglass JF, McFee WA, Salas-Solano O. Native intact mass determination of antibodies conjugated with monomethyl auristatin E and F at interchain cysteine residues. Anal Chem. 2012;84:2843–49. doi:10.1021/ac203346c
   PubMed Web of Science ®Google Scholar
• Wang G, Bondarenko PV, Kaltashov IA. Multi-step conformational transitions in heat-treated protein therapeutics can be monitored in real time with temperature-controlled electrospray ionization mass spectrometry. Analyst. 2018;143:670–77. doi:10.1039/C7AN01655G
   PubMed Web of Science ®Google Scholar
• Atmanene C, Wagner-Rousset E, Malissard M, Chol B, Robert A, Corvaia N, Dorsselaer AV, Beck A, Sanglier-Cianférani S. Extending mass spectrometry contribution to therapeutic monoclonal antibody lead optimization: characterization of immune complexes using noncovalent ESI-MS. Anal Chem. 2009;81:6364–73. doi:10.1021/ac9007557
   PubMed Web of Science ®Google Scholar
• Jian W, Kang L, Burton L, Weng N. A workflow for absolute quantitation of large therapeutic proteins in biological samples at intact level using LC-HRMS. Bioanalysis. 2016;8:1679–91. doi:10.4155/bio-2016-0096
   PubMed Web of Science ®Google Scholar
• Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol. 2007;25:21–50. doi:10.1146/annurev.immunol.25.022106.141702
   PubMed Web of Science ®Google Scholar
• Pawlowski JW, Bajardi-Taccioli A, Houde D, Feschenko M, Carlage T, Kaltashov IA. Influence of glycan modification on IgG1 biochemical and biophysical properties. J Pharm Biomed Anal. 2018;151:133–44. doi:10.1016/j.jpba.2017.12.061
   PubMed Web of Science ®Google Scholar
• Kang SH, Lee CH. Development of therapeutic antibodies and modulating the characteristics of therapeutic antibodies to maximize the therapeutic efficacy. Biotechnol Bioprocess Eng. 2021;2021:1–17.
   Google Scholar
• Kretschmer A, Schwanbeck R, Valerius T, Rösner T. Antibody isotypes for tumor immunotherapy. Transfus Med Hemother. 2017;44:320–26. doi:10.1159/000479240
   PubMed Web of Science ®Google Scholar
• Ejemel M, Li Q, Hou S, Schiller ZA, Tree JA, Wallace A, Amcheslavsky A, Kurt Yilmaz N, Buttigieg KR, Elmore MJ, et al. A cross-reactive human IgA monoclonal antibody blocks SARS-CoV-2 spike-ACE2 interaction. Nat Commun. 2020;11:4198. doi:10.1038/s41467-020-18058-8
   PubMed Web of Science ®Google Scholar
• Josephs DH, Spicer JF, Karagiannis P, Gould HJ, Karagiannis SN. IgE immunotherapy: a novel concept with promise for the treatment of cancer. MAbs. 2014;6:54–72. doi:10.4161/mabs.27029
   PubMed Web of Science ®Google Scholar
• Chauhan J, McCraw AJ, Nakamura M, Osborn G, Sow HS, Cox VF, Stavraka C, Josephs DH, Spicer JF, Karagiannis SN, et al. IgE antibodies against cancer: efficacy and safety. Antibodies. 2020;9. doi:10.3390/antib9040055
   Web of Science ®Google Scholar
• Fazekas-Singer J, Singer J, Jensen-Jarolim E. Precision medicine in clinical oncology: the journey from IgG antibody to IgE. Curr Opin Allergy Clin Immunol. 2020;20:282–89. doi:10.1097/ACI.0000000000000637
   PubMed Web of Science ®Google Scholar
• Sutton BJ, Davies AM, Bax HJ, Karagiannis SN. IgE antibodies: from structure to function and clinical translation. Antibodies. 2019;8:41. doi:10.3390/antib8010019
   Web of Science ®Google Scholar
• Bobst CE, Sperry J, Friese OV, Kaltashov IA. Simultaneous evaluation of a vaccine component microheterogeneity and conformational integrity using native mass spectrometry and limited charge reduction. J Am Soc Mass Spectrom. 2021;32:1631–37. doi:10.1021/jasms.1c00091
   PubMed Web of Science ®Google Scholar
• Muneeruddin K, Thomas JJ, Salinas PA, Kaltashov IA. Characterization of small protein aggregates and oligomers using size exclusion chromatography with on-line detection by native electrospray ionization mass spectrometry. Anal Chem. 2014;86:10692–99. doi:10.1021/ac502590h
   PubMed Web of Science ®Google Scholar
• Muneeruddin K, Nazzaro M, Kaltashov IA. Characterization of intact protein conjugates and biopharmaceuticals using ion-exchange chromatography with online detection by native electrospray ionization mass spectrometry and top-down tandem mass spectrometry. Anal Chem. 2015;87:10138–45. doi:10.1021/acs.analchem.5b02982
   PubMed Web of Science ®Google Scholar
• Domínguez-Vega E, Tengattini S, Peintner C, van Angeren J, Temporini C, Haselberg R, Massolini G, Somsen GW. High-resolution glycoform profiling of intact therapeutic proteins by hydrophilic interaction chromatography-mass spectrometry. Talanta. 2018;184:375–81. doi:10.1016/j.talanta.2018.03.015
   PubMed Web of Science ®Google Scholar
• Belov AM, Viner R, Santos MR, Horn DM, Bern M, Karger BL, Ivanov AR. Analysis of proteins, protein complexes, and organellar proteomes using sheathless capillary zone electrophoresis - native mass spectrometry. J Am Soc Mass Spectrom. 2017;28:2614–34. doi:10.1007/s13361-017-1781-1
   PubMed Web of Science ®Google Scholar
• Muneeruddin K, Bobst CE, Frenkel R, Houde D, Turyan I, Sosic Z, Kaltashov, IA. Characterization of a PEGylated protein therapeutic by ion exchange chromatography with on-line detection by native ESI MS and MS/MS. Analyst. 2017;142:336–44. doi:10.1039/C6AN02041K
   PubMed Web of Science ®Google Scholar
• Fuerstenau SD, Benner WH. Molecular weight determination of megadalton DNA electrospray ions using charge detection time-of-flight mass spectrometry. Rapid Commun Mass Spectrom. 1995;9:1528–38. doi:10.1002/rcm.1290091513
   PubMed Web of Science ®Google Scholar
• den Boer MA, Lai SH, Xue X, van Kampen MD, Bleijlevens B, Heck AJR. Comparative analysis of antibodies and heavily glycosylated macromolecular immune complexes by size-exclusion chromatography multi-angle light scattering, native charge detection mass spectrometry, and mass photometry. Anal Chem. 2022;94:892–900. doi:10.1021/acs.analchem.1c03656
   PubMed Web of Science ®Google Scholar
• Jarrold MF. Applications of charge detection mass spectrometry in molecular biology and biotechnology. Chem Rev. 2021;122:7415–41. doi:10.1021/acs.chemrev.1c00377
   PubMed Web of Science ®Google Scholar
• Foreman DJ, McLuckey SA. Recent developments in gas-phase ion/ion reactions for analytical mass spectrometry. Anal Chem. 2020;92:252–66. doi:10.1021/acs.analchem.9b05014
   PubMed Web of Science ®Google Scholar
• Abzalimov RR, Kaltashov IA. Electrospray ionization mass spectrometry of highly heterogeneous protein systems: protein ion charge state assignment via incomplete charge reduction. Anal Chem. 2010;82:7523–26. doi:10.1021/ac101848z
   PubMed Web of Science ®Google Scholar
• Kaltashov IA, Bobst CE, Pawlowski J, Wang G. Mass spectrometry-based methods in characterization of the higher order structure of protein therapeutics. J Pharm Biomed Anal. 2020;184:113169. doi:10.1016/j.jpba.2020.113169
   PubMed Web of Science ®Google Scholar
• Kaltashov IA, Abzalimov RR. Do ionic charges in ESI MS provide useful information on macromolecular structure? J Am Soc Mass Spectrom. 2008;19:1239–46. doi:10.1016/j.jasms.2008.05.018
   PubMed Web of Science ®Google Scholar
• Marty MT, Baldwin AJ, Marklund EG, Hochberg GK, Benesch JL, Robinson CV. Bayesian deconvolution of mass and ion mobility spectra: from binary interactions to polydisperse ensembles. Anal Chem. 2015;87:4370–76. doi:10.1021/acs.analchem.5b00140
   PubMed Web of Science ®Google Scholar
• Dawson P. 1976. Quadrupole mass spectrometry and its applications. Amsterdam: Elsevier Scientific Pub. Co.
   Google Scholar
• Cech NB, Enke CG. Practical implications of some recent studies in electrospray ionization fundamentals. Mass Spectrom Rev. 2001;20:362–87. doi:10.1002/mas.10008
   PubMed Web of Science ®Google Scholar
• Wang G, Johnson AJ, Kaltashov IA. Evaluation of electrospray ionization mass spectrometry as a tool for characterization of small soluble protein aggregates. Anal Chem. 2012;84:1718–24. doi:10.1021/ac203017x
   PubMed Web of Science ®Google Scholar
• Kaltashov IA, Wang S, and Wang G. 2021. Mass Spectrometry in Biopharmaceutical Analysis. Berlin, Germany/Boston, MA, USA: De Gruyter. doi:10.1515/9783110546187
   Google Scholar
• Hernandez-Alba O, Wagner-Rousset E, Beck A, Cianférani S. Native mass spectrometry, ion mobility, and collision-induced unfolding for conformational characterization of igg4 monoclonal antibodies. Anal Chem. 2018;90:8865–72. doi:10.1021/acs.analchem.8b00912
   PubMed Web of Science ®Google Scholar
• Pomés A, Mueller GA, Chruszcz M. Structural aspects of the allergen-antibody Interaction. Front Immunol. 2020;11:2067. doi:10.3389/fimmu.2020.02067
   PubMed Web of Science ®Google Scholar
• Senko MW, Beu SC, McLafferty FW. Determination of monoisotopic masses and ion populations for large biomolecules from resolved isotopic distributions. J Am Soc Mass Spectrom. 1995;6:229–33. doi:10.1016/1044-0305(95)00017-8
   PubMed Web of Science ®Google Scholar
• Barnidge DR, Dasari S, Ramirez-Alvarado M, Fontan A, Willrich MA, Tschumper RC, Jelinek DF, Snyder MR, Dispenzieri A, Katzmann JA, et al. Phenotyping polyclonal kappa and lambda light chain molecular mass distributions in patient serum using mass spectrometry. J Proteome Res. 2014;13:5198–205. doi:10.1021/pr5005967
   PubMed Web of Science ®Google Scholar
• Shade KT, Platzer B, Washburn N, Mani V, Bartsch YC, Conroy M, Pagan JD, Bosques C, Mempel TR, Fiebiger E, et al. A single glycan on IgE is indispensable for initiation of anaphylaxis. J Exp Med. 2015;212:457–67. doi:10.1084/jem.20142182
   PubMed Web of Science ®Google Scholar
• Tong W, Wang G. How can native mass spectrometry contribute to characterization of biomacromolecular higher-order structure and interactions? Methods (San Diego. Calif). 2018;144:3–13.
   Google Scholar
• Bailey AO, Huguet R, Mullen C, Syka JEP, Russell WK. Ion–ion charge reduction addresses multiple challenges common to denaturing intact mass analysis. Anal Chem. 2022;94:3930–38. doi:10.1021/acs.analchem.1c04973
   PubMed Web of Science ®Google Scholar
• Abzalimov RR, Bobst CE, Salinas PA, Savickas P, Thomas JJ, Kaltashov IA. Studies of pH-dependent self-association of a recombinant form of arylsulfatase A with electrospray ionization mass spectrometry and size-exclusion chromatography. Anal Chem. 2013;85:1591–96. doi:10.1021/ac302829k
   PubMed Web of Science ®Google Scholar
• Frimpong AK, Abzalimov RR, Eyles SJ, Kaltashov IA. Gas-phase interference-free analysis of protein ion charge-state distributions: detection of small-scale conformational transitions accompanying pepsin inactivation. Anal Chem. 2007;79:4154–61. doi:10.1021/ac0704098
   PubMed Web of Science ®Google Scholar
• Zhang H, Cui W, Gross ML. Mass spectrometry for the biophysical characterization of therapeutic monoclonal antibodies. FEBS Lett. 2014;588:308–17. doi:10.1016/j.febslet.2013.11.027
   PubMed Web of Science ®Google Scholar
• Thangaraj SK, Arola H, Tullila A, Nevanen TK, Rouvinen J, Jänis J. Quantitation of thyroid hormone binding to anti-thyroxine antibody fab fragment by native mass spectrometry. ACS Omega. 2019;4:18718–24. doi:10.1021/acsomega.9b02659
   PubMed Web of Science ®Google Scholar
• Plomp R, Hensbergen PJ, Rombouts Y, Zauner G, Dragan I, Koeleman CA, Deelder AM, Wuhrer M. Site-specific N-glycosylation analysis of human immunoglobulin e. J Proteome Res. 2014;13:536–46. doi:10.1021/pr400714w
   PubMed Web of Science ®Google Scholar
• Wu G, Hitchen PG, Panico M, North SJ, Barbouche MR, Binet D, Morris HR, Dell A, Haslam SM. Glycoproteomic studies of IgE from a novel hyper IgE syndrome linked to PGM3 mutation. Glycoconj J. 2016;33:447–56. doi:10.1007/s10719-015-9638-y
   PubMed Web of Science ®Google Scholar
• Greisch JF, den Boer MA, Beurskens F, Schuurman J, Tamara S, Bondt A, Heck AJR. Generating informative sequence tags from antigen-binding regions of heavily glycosylated IgA1 antibodies by native top-down electron capture dissociation. J Am Soc Mass Spectrom. 2021;32:1326–35. doi:10.1021/jasms.0c00461
   PubMed Web of Science ®Google Scholar
• Greisch JF, den Boer MA, Lai SH, Gallagher K, Bondt A, Commandeur J, Heck AJR. Extending native top-down electron capture dissociation to MDa Immunoglobulin complexes provides useful sequence tags covering their critical variable complementarity-determining regions. Anal Chem. 2021;93:16068–75. doi:10.1021/acs.analchem.1c03740
   PubMed Web of Science ®Google Scholar
• Lupinek C, Roux KH, Laffer S, Rauter I, Reginald K, Kneidinger M, Blatt K, Ball T, Pree I, Jahn-Schmid B, et al. Trimolecular complex formation of IgE, Fc epsilon RI, and a recombinant nonanaphylactic single-chain antibody fragment with high affinity for IgE. J Immunol. 2009;182:4817–29. doi:10.4049/jimmunol.0800726
   PubMed Web of Science ®Google Scholar
• Leverence R, Mason AB, Kaltashov IA. Noncanonical interactions between serum transferrin and transferrin receptor evaluated with electrospray ionization mass spectrometry. Proc Natl Acad Sci USA. 2010;107:8123–28. doi:10.1073/pnas.0914898107
   PubMed Web of Science ®Google Scholar
• Balbino B, Conde E, Marichal T, Starkl P, Reber LL. Approaches to target IgE antibodies in allergic diseases. Pharmacol Ther. 2018;191:50–64. doi:10.1016/j.pharmthera.2018.05.015
   PubMed Web of Science ®Google Scholar
• Yang Y, Niu C, Bobst CE, Kaltashov IA. Charge manipulation using solution and gas-phase chemistry to facilitate analysis of highly heterogeneous protein complexes in native mass spectrometry. Anal Chem. 2021;93:3337–42. doi:10.1021/acs.analchem.0c05249
   PubMed Web of Science ®Google Scholar
• Yang W, Tu Z, McClements DJ, Kaltashov IA. A systematic assessment of structural heterogeneity and IgG/IgE-binding of ovalbumin. Food & Function. 2021;12:8130–40. doi:10.1039/D0FO02980G
   PubMed Web of Science ®Google Scholar