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Non-targeted characterization of attributes affecting antibody-FcγRIIIa V158 (CD16a) binding via online affinity chromatography-mass spectrometry

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Article: 2004982 | Received 20 Jul 2021, Accepted 08 Nov 2021, Published online: 03 Jan 2022

References

  • Kim JM, Ashkenazi A. Fcγ receptors enable anticancer action of proapoptotic and immune-modulatory antibodies. J Exp Med. 2013;210(9):1647–17. doi:10.1084/jem.20131625.
  • Nimmerjahn F, Ravetch JV. Fcγ receptors as regulators of immune responses. Nat Rev Immunol. 2008;8(1):34–47. doi:10.1038/nri2206. 2008/01/01.
  • Nimmerjahn F, Gordan S, Lux A. FcγR dependent mechanisms of cytotoxic, agonistic, and neutralizing antibody activities. Trends Immunol. 2015 Jun;36(6):325–36. doi:10.1016/j.it.2015.04.005. PMID: 25981969.
  • Bruhns P, Iannascoli B, England P, Mancardi DA, Fernandez N, Jorieux S, Daëron M. Specificity and affinity of human Fcγ receptors and their polymorphic variants for human IgG subclasses. Blood. 2009;113(16):3716–25. doi:10.1182/blood-2008-09-179754.
  • Rascu A, Repp R, Westerdaal NA, Kalden, JR, and van de Winkel, JG, et al. Clinical relevance of Fc gamma receptor polymorphisms. AAnn NY Acad Sci. 1997 Apr 5;815:282–95. doi:10.1111/j.1749-6632.1997.tb52070.x. PMID: 9186665.
  • Sugita N, Yamamoto K, Kobayashi T, Der Pol V, De Winkel V. Relevance of Fc gamma RIIIa-158V-F polymorphism to recurrence of adult periodontitis in Japanese patients. Clin.Exp.Immunol. 1999;117(2):350–54. doi:10.1046/j.1365-2249.1999.00984.x. PMID: 10444269.
  • Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol. 2008;8:713–25. doi:10.1038/nri2381.
  • Kaplon H, Muralidharan M, Schneider Z, Reichert JM. Antibodies to watch in 2020. mAbs. 2020;12(1):1703531. doi:10.1080/19420862.2019.1703531. 2020/01/01.
  • Kiyoshi M, Caaveiro JMM, Tada M, Tamura H, Tanaka T, Terao Y, Morante, K, Harazono, A, Hashii, N, Shibata, H, et al. Assessing the heterogeneity of the Fc-Glycan of a therapeutic antibody using an engineered FcγReceptor IIIa-immobilized column. Sci Rep. 2018;8:3955. doi:10.1038/s41598-018-22199-8.
  • Jefferis R. Glycosylation of recombinant antibody therapeutics. Biotechnol Progr. 2005;21:11–16. doi:10.1021/bp040016j.
  • Jefferis R. Recombinant antibody therapeutics: the impact of glycosylation on mechanisms of action. Trends Pharm Sci. 2009;30:356–62. doi:10.1016/j.tips.2009.04.007.
  • Russell A, Adua E, Ugrina I, Laws S, Unravelling Immunoglobulin WW. G Fc N-glycosylation: a dynamic marker potentiating predictive, preventive and personalised medicine. Int J Mol Sci. 2018;19:390. doi:10.3390/ijms19020390.
  • Liu L. Antibody glycosylation and its impact on the pharmacokinetics and pharmacodynamics of monoclonal antibodies and Fc-fusion proteins. J Pharm Sci. 2015;104:1866–84. doi:10.1002/jps.24444.
  • Zhang Z, Shah B. Prediction of collision-induced dissociation spectra of common N-Glycopeptides for glycoform identification. Anal, Chem. 2010;82(24):10194–202. doi:10.1021/ac102359u. 2010/12/15.
  • Houde D, Peng Y, Berkowitz SA, Engen JR. Post-translational modifications differentially affect IgG1 conformation and receptor binding. Mol Cell Proteomics. 2010;9:1716. doi:10.1074/mcp.M900540-MCP200.
  • Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Bio. 2003;325:979–89. doi:10.1016/s0022-2836(02)01250-0.
  • Zhang Z, Shah B, Richardson J. Impact of Fc N-glycan sialylation on IgG structure. mAbs. 2019 Nov-Dec;11(8):1381–90. doi:10.1080/19420862.2019.1655377. PMID: 31411531.
  • Higel F, Seidl A, Sörgel F, Friess W. N-glycosylation heterogeneity and the influence on structure, function and pharmacokinetics of monoclonal antibodies and Fc fusion proteins. Eur J Pharm Biopharm. 2016;100:94–100. doi:10.1016/j.ejpb.2016.01.005.
  • Zheng K, Bantog C, Bayer R. The impact of glycosylation on monoclonal antibody conformation and stability. mAbs. 2011;3:568–76. doi:10.4161/mabs.3.6.17922.
  • Jefferis R, Lund J. Interaction sites on human IgG-Fc for FcgammaR: current models. Immunol Lett. 2002;82:57–65. doi:10.1016/s0165-2478(02)00019-6.
  • Tao MH, Morrison SL. Studies of aglycosylated chimeric mouse-human IgG. Role of carbohydrate in the structure and effector functions mediated by the human IgG constant region. J Immunol. 1989;143(8):2595–601. PMID: 2507634.
  • Jefferis R, Lund J, Pound JD. IgG-Fc-mediated effector functions: molecular definition of interaction sites for effector ligands and the role of glycosylation. Immunol Rev. 1998;163:59–76. doi:10.1111/j.1600-065x.1998.tb01188.x. PMID: 9700502.
  • Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Ann Rev Immunol. 2007;25:21–50. doi:10.1146/annurev.immunol.25.022106.141702.
  • Barb AW, Prestegard JH. NMR analysis demonstrates immunoglobulin G N-glycans are accessible and dynamic. Nat Chem Bio. 2011;7(3):147–53. doi:10.1038/nchembio.511. PMID: 21258329.
  • Shields RL, Lai J, Keck R, O’Connell LY, Hong K, Meng YG, Weikert SHA, Presta LG. Lack of Fucose on Human IgG1 N-Linked Oligosaccharide Improves Binding to Human FcγRIII and Antibody-dependent Cellular Toxicity. J Biol Chem. 2002;277:26733–40. doi:10.1074/jbc.M202069200. PMID: 11986321.
  • Kanda Y, Yamada T, Mori K, Okazaki A, Inoue M, Kitajima-Miyama K, Kuni-Kamochi R, Nakano R, Yano K, Kakita S, et al. Comparison of biological activity among nonfucosylated therapeutic IgG1 antibodies with three different N-linked Fc oligosaccharides: the high-mannose, hybrid, and complex types. Glycobiology. 2007;17:104–18. doi:10.1093/glycob/cwl057.
  • Junttila TT, Parsons K, Olsson C, Lu Y, Xin Y, Theriault J, Crocker L, Pabonan O, Baginski T, Meng G, et al. Superior In vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res. 2010;70:4481. doi:10.1158/0008-5472.CAN-09-3704.
  • Niwa R, Natsume A, Uehara A, Wakitani M, Iida S, Uchida K, Satoh M, Shitara K. IgG subclass-independent improvement of antibody-dependent cellular cytotoxicity by fucose removal from Asn297-linked oligosaccharides. J Immunol Meth. 2005;306:151–60. doi:10.1016/j.jim.2005.08.009.
  • Ferrara C, Grau S, Jäger C, Sondermann P, Brünker P, Waldhauer I, Hennig M, Ruf A, Rufer AC, Stihle M, et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Nat Acad Sci. 2011;108:12669–74. doi:10.1073/pnas.1108455108.
  • Mizushima T, Yagi H, Takemoto E, Shibata-Koyama M, Isoda Y, Iida S, Masuda K, Satoh M, Kato K. Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans. Genes Cells. 2011;16:1071–80. doi:10.1111/j.1365-2443.2011.01552.x.
  • Shatz W, Chung S, Li B, Marshall B, Tejada M, Phung W, Sandoval W, Kelley RF, Scheer JM. Knobs-into-holes antibody production in mammalian cell lines reveals that asymmetric afucosylation is sufficient for full antibody-dependent cellular cytotoxicity. mAbs. 2013;5:872–81. doi:10.4161/mabs.26307.
  • Yu M, Brown D, Reed C, Chung S, Lutman J, Stefanich E, Wong A, Stephan JP, Bayer R. Production, characterization, and pharmacokinetic properties of antibodies with N-linked mannose-5 glycans. MAbs. 2012;4(4):475–87. doi:10.4161/mabs.20737. PMID: 22699308.
  • Reusch D, Tejada ML. Fc glycans of therapeutic antibodies as critical quality attributes. Glycobiology. 2015;25:1325–34. doi:10.1093/glycob/cwv065.
  • Dekkers G, Treffers L, Plomp R, Bentlage AEH, de Boer M, Koeleman CAM, Lissenberg-Thunnissen SN, Visser R, Brouwer M, Mok JY, et al. Decoding the human immunoglobulin G-glycan repertoire reveals a spectrum of Fc-Receptor- and complement-mediated-effector activities. Front Immunol. 2017;8:877. doi:10.3389/fimmu.2017.00877.
  • Subedi GP, Barb AW. The immunoglobulin G1 N-glycan composition affects binding to each low affinity Fc γ receptor. mAbs. 2016;8:1512–24. doi:10.1080/19420862.2016.1218586.
  • Chung CH, Mirakhur B, Chan E, Le Q-T, Berlin J, Morse M, Murphy BA, Satinover SM, Hosen J, Mauro D, et al. Cetuximab-induced anaphylaxis and IgE specific for galactose-α-1, 3-galactose. N Engl J Med. 2008;358:1109–17. doi:10.1056/NEJMoa074943.
  • Chitnavis M, Stein DJ, Commins S, Schuyler AJ, Behm B. First-dose anaphylaxis to infliximab: a case of mammalian meat allergy. J Allerg Cl Imm-Prac. 2017;5:1425–26. doi:10.1016/j.jaip.2017.04.044.
  • Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-Inflammatory activity of immunoglobulin G resulting from Fc Sialylation. Science. 2006;313:670. doi:10.1126/science.1129594.
  • Jones MB, Oswald DM, Joshi S, Whiteheart SW, Orlando R, Cobb BA. B-cell–independent sialylation of IgG. Proc Nat Acad of Sci. 2016;113:7207. doi:10.1073/pnas.1523968113.
  • Washburn N, Schwab I, Ortiz D, Bhatnagar N, Lansing JC, Medeiros A, Tyler S, Mekala D, Cochran E, Sarvaiya H, et al. Controlled tetra-Fc sialylation of IVIg results in a drug candidate with consistent enhanced anti-inflammatory activity. Proc Nat Acad of Sci. 2015;112:E1297. doi:10.1073/pnas.1422481112.
  • Kuhne F, Bonnington L, Malik S, Thomann M, Avenal C, Cymer F, Wegele H, Reusch D, Mormann M, Bulau P. The impact of immunoglobulin G1 Fc sialylation on backbone amide H/D exchange. Antibodies (Basel). 2019;8:49. doi:10.3390/antib8040049.
  • Parekh RB, Dwek RA, Sutton BJ, Fernandes DL, Leung A, Stanworth D, Rademacher TW, Mizuochi T, Taniguchi T, Matsuta K, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature. 1985;316(6027):452–57. doi:10.1038/316452a0. 1985/08/01.
  • Wong AHY, Fukami Y, Sudo M, Kokubun N, Hamada S, Yuki N. Sialylated IgG-Fc: a novel biomarker of chronic inflammatory demyelinating polyneuropathy. J Neurol Neurosur Ps. 2016;87:275. doi:10.1136/jnnp-2014-309964.
  • Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol. 2007;44:1524–34. doi:10.1016/j.molimm.2006.09.005.
  • Vidarsson G, Dekkers G, Rispens T. IgG subclasses and allotypes: from structure to effector functions. Front Immunol. 2014:5. doi:10.3389/fimmu.2014.00520.
  • Lippold S, Nicolardi S, Domínguez-Vega E, Heidenreich A-K, Vidarsson G, Reusch D, Haberger M, Wuhrer M, Falck D. Glycoform-resolved FcɣRIIIa affinity chromatography–mass spectrometry. mAbs. 2019;11:1191–96. doi:10.1080/19420862.2019.1636602.
  • Sondermann P, Huber R, Oosthuizen V, Jacob U. The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex. Nature. 2000;406:267–73. doi:10.1038/35018508.
  • Houel S, Hilliard M, Yu YQ, McLoughlin N, Martin SM, Rudd PM, Williams JP, N- CW. and O-glycosylation analysis of etanercept using liquid chromatography and quadrupole time-of-flight mass spectrometry equipped with electron-transfer dissociation functionality. Anal Chem. 2014;86:576–84. doi:10.1021/ac402726h.
  • Kleemann GR, Beierle J, Nichols AC, Dillon TM, Pipes GD, Bondarenko PV. Characterization of IgG1 Immunoglobulins and Peptide−Fc fusion proteins by limited proteolysis in conjunction with LC−MS. Anal Chem. 2008;80:2001–09. doi:10.1021/ac701629v.
  • Gadgil HS, Bondarenko PV, Pipes GD, Dillon TM, Banks D, Abel J, Kleemann GR, Treuheit MJ. Identification of cysteinylation of a free cysteine in the Fab region of a recombinant monoclonal IgG1 antibody using Lys-C limited proteolysis coupled with LC/MS analysis. Anal Biochem. 2006;355:165–74. doi:10.1016/j.ab.2006.05.037. PMID: 16828048.
  • Fang J, Richardson J, Du Z, Zhang Z. Effect of Fc-Glycan structure on the conformational stability of IgG revealed by hydrogen/deuterium exchange and limited proteolysis. Biochemistry. 2016;55:860–68. doi:10.1021/acs.biochem.5b01323. PMID: 26812426.
  • de Taeye SW, Bentlage AEH, Mebius MM, Meesters JI, Lissenberg-Thunnissen S, Falck D, Sénard T, Salehi N, Wuhrer M, and Schuurman J, et al. FcγR binding and ADCC activity of human IgG allotypes Front Immunol . 2020 2020-May-06;11(740). doi:10.3389/fimmu.2020.00740.
  • Edelman GM, Cunningham BA, Gall WE, Gottlieb PD, Rutishauser U, Waxdal MJ. The covalent structure of an entire gammaG immunoglobulin molecule. Proc Natl Acad Sci. 1969;63(1):78–85. doi:10.1073/pnas.63.1.78. PMID: 5257969.
  • Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, Briggs J, Xie D, Lai J, Stadlen A, Li B, et al. High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J Biol Chem. 2001;276:6591–604. doi:10.1074/jbc.M009483200. PMID: 11096108.
  • Jacobsen FW, Stevenson R, Li C, Salimi-Moosavi H, Liu L, Luo WJ, Quanzhou DK, Buck L, Miller S, Miller S, et al. Engineering an IgG scaffold lacking effector function with optimized developability. J Biol Chem. 2017;292:1865–75. doi:10.1074/jbc.M116.748525. PMID: 27994062.
  • Liu L, Jacobsen FW, Everds N, Zhuang Y, Yu YB, Li N, Clark D, Nguyen MP, Fort M, Narayanan P, et al. Biological characterization of a stable effector functionless (SEFL) monoclonal antibody scaffold in vitro. J Biol Chem. 2017;292(5):1876–83. doi:10.1074/jbc.M116.748707. PMID: 27994063.
  • Yu J, Song Y, Tian W. How to select IgG subclasses in developing anti-tumor therapeutic antibodies. J Hematol Oncol. 2020;13(1):45. doi:10.1186/s13045-020-00876-4. PMID: 32370812.
  • Schneider-Merck T, Lammerts van Bueren JJ, Berger S, Rossen K, van Berkel PH, Derer S, Beyer T, Lohse S, Wk B, Peipp M, et al. Human IgG2 antibodies against epidermal growth factor receptor effectively trigger antibody-dependent cellular cytotoxicity but, in contrast to IgG1, only by cells of myeloid lineage. J Immunol. 2010;184:512–20. doi:10.4049/jimmunol.0900847. PMID: 19949082.
  • Wypych J, Li M, Guo A, Zhang Z, Martinez T, Allen MJ, Fodor S, Kelner DN, Flynn GC, Liu YD, et al. Human IgG2 antibodies display disulfide-mediated structural isoforms. J Biol Chem. 2008;283:16194–205. doi:10.1074/jbc.M709987200. PMID: 18339624.
  • Dillon TM, Ricci MS, Vezina C, Flynn GC, Liu YD, Rehder DS, Plant M, Henkle B, Li Y, Deechongkit S, et al. Structural and functional characterization of disulfide isoforms of the human IgG2 subclass. J Biol Chem. 2008;283:16206–15. doi:10.1074/jbc.M709988200. PMID: 18339626.
  • Zhang A, Fang J, Chou RYT, Bondarenko PV, Zhang Z. Conformational difference in human IgG2 disulfide isoforms revealed by hydrogen/deuterium exchange mass spectrometry. Biochemistry. 2015;54:1956–62. doi:10.1021/bi5015216. PMID: 25730439.
  • Saphire EO, Parren PW, Pantophlet R, Zwick MB, Morris GM, Rudd PM, Dwek RA, Stanfield RL, Burton DR, Wilson IA. Crystal structure of a neutralizing human IgG against HIV-1: a template for vaccine design. Science. 2001;293:1155. doi:10.1126/science.1061692. PMID: 11498595.
  • Michaelsen TE, Brekke OH, Aase A, Sandin RH, Bremnes B, Sandlie I. One disulfide bond in front of the second heavy chain constant region is necessary and sufficient for effector functions of human IgG3 without a genetic hinge. Proc Nat Acad Sci. 1994;91:9243. doi:10.1073/pnas.91.20.9243. PMID: 7937748.
  • Shi RL, Xiao G, Dillon TM, McAuley A, Ricci MS, Bondarenko PV. Identification of critical chemical modifications by size exclusion chromatography of stressed antibody-target complexes with competitive binding. mAbs. 2021;13:1887612. doi:10.1080/19420862.2021.1887612. PMID: 33616001.
  • Hayes JM, Frostell A, Karlsson R, Müller S, Martín SM, Pauers M, Reuss F, Cosgrave EF, Anneren C, Davey GP, et al. Identification of Fc gamma receptor glycoforms that produce differential binding kinetics for rituximab. Mol Cell Proteomics. 2017;16:1770–88. doi:10.1074/mcp.M117.066944. PMID: 28576848.
  • Barb AW. Fc γ receptor compositional heterogeneity: considerations for immunotherapy development. J Biol Chem. 2021;296:100057. doi:10.1074/jbc.REV120.013168. PMID: 33172893.
  • Patel KR, Roberts JT, Subedi GP, Barb AW. Restricted processing of CD16a/Fc γ receptor IIIa N-glycans from primary human NK cells impacts structure and function. J Biol Chem. 2018;293:3477–89. doi:10.1074/jbc.RA117.001207. PMID: 29330305.
  • Washburn N, Meccariello R, Duffner J, Getchell K, Holte K, Prod’homme T, Srinivasan K, Prenovitz R, Lansing J, Capila I, et al. Characterization of endogenous human FcγRIII by mass spectrometry reveals site, allele and sequence specific glycosylation. Mol Cell Proteomics. 2019;18:534–45. doi:10.1074/mcp.RA118.001142. PMID: 30559323.
  • Hayes JM, Frostell A, Cosgrave EF, Struwe WB, Potter O, Davey GP, Karlsson R, Anneren C, Rudd PM. Fc gamma receptor glycosylation modulates the binding of IgG glycoforms: a requirement for stable antibody interactions. J Proteome Res. 2014;13:5471–85. doi:10.1021/pr500414q. PMID: 25345863.
  • Wojcik I, Sénard T, de Graaf EL, Janssen GMC, de Ru AH, Mohammed Y, van Veelen PA, Vidarsson G, Wuhrer M, Falck D. Site-Specific Glycosylation Mapping of Fc gamma receptor IIIb from neutrophils of individual healthy donors. Anal Chem. 2020 Oct 6;92(19):13172–81. doi:10.1021/acs.analchem.0c02342. PMID: 32886488.
  • Yamaguchi Y, Barb AW. A synopsis of recent developments defining how N-glycosylation impacts immunoglobulin G structure and function. Glycobiology. 2020 Mar 20;30(4):214–25. doi:10.1093/glycob/cwz068. PMID: 31822882.
  • Cambay F, Forest-Nault C, Dumoulin L, Seguin A, Henry O, Durocher Y, De Crescenzo G. Glycosylation of Fcγ receptors influences their interaction with various IgG1 glycoforms. Mol Immunol. 2020;121:144–58. doi:10.1016/j.molimm.2020.03.010. 2020/05/01/.
  • Ren D, Pipes GD, Liu D, Shih LY, Nichols AC, Treuheit MJ, Brems DN, Bondarenko PV. An improved trypsin digestion method minimizes digestion-induced modifications on proteins. Anal Biochem. 2009;392:12–21. doi:10.1016/j.ab.2009.05.018. PMID: 19457431.
  • Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6:359–62. doi:10.1038/nmeth.1322. PMID: 19377485.
  • Zhang Z. Large-scale identification and quantification of covalent modifications in therapeutic proteins. Anal Chem. 2009;81:8354–64. doi:10.1021/ac901193n.
  • Zhang Z. Prediction of low-energy collision-induced dissociation spectra of peptides. Anal Chem. 2004;76:3908–22. doi:10.1021/ac049951b. PMID: 15253624.
  • Retention Time ZZ. Alignment of LC/MS data by a divide-and-conquer algorithm. J Am Soc Mass Spectrom. 2012;23:764–72. doi:10.1007/s13361-011-0334-2. PMID: 22298290.
  • Seo N, Polozova A, Zhang M, Yates Z, Cao S, Li H, Kuhns S, Maher G, McBride HJ, Liu J. Analytical and functional similarity of Amgen biosimilar ABP 215 to bevacizumab. mAbs. 2018;10:678–91. doi:10.1080/19420862.2018.1452580. PMID: 29553864.