1,318
Views
0
CrossRef citations to date
0
Altmetric
Report

Bivalent non-human gal-α1-3-gal glycan epitopes in the Fc region of a monoclonal antibody model can be recognized by anti-Gal-α1-3-Gal IgE antibodies

, , , , & ORCID Icon
Article: 2239405 | Received 19 May 2023, Accepted 18 Jul 2023, Published online: 27 Jul 2023

References

  • Lu RM, Hwang YC, Liu IJ, Lee CC, Tsai HZ, Li HJ, Wu HC. Development of therapeutic antibodies for the treatment of diseases. J Biomed Sci. 2020;27(1):1. doi:10.1186/s12929-019-0592-z. PMID: 31894001.
  • Reusch D, Tejada ML. Fc glycans of therapeutic antibodies as critical quality attributes. Glycobiology. 2015;25(12):1325–15. doi:10.1093/glycob/cwv065. PMID: 26263923.
  • Kunert R, Reinhart D. Advances in recombinant antibody manufacturing. Appl Microbiol Biotechnol. 2016;100(8):3451–61. doi:10.1007/s00253-016-7388-9. PMID: 26936774.
  • Durocher Y, Butler M. Expression systems for therapeutic glycoprotein production. Curr Opin Biotechnol. 2009;20:700–07. doi:10.1016/j.copbio.2009.10.008. PMID: 19889531.
  • Stadlmann J, Pabst M, Kolarich D, Kunert R, Altmann F. Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics. 2008;8(14):2858–71. doi:10.1002/pmic.200700968. PMID: 18655055.
  • Bosques CJ, Collins BE, Meador JW 3rd, Sarvaiya H, Murphy JL, Dellorusso G, Bulik DA, Hsu IH, Washburn N, Sipsey SF, et al. Chinese hamster ovary cells can produce galactose-α-1,3-galactose antigens on proteins. Nat Biotechnol. 2010;28(11):1153–56. doi:10.1038/nbt1110-1153. PMID: 21057479.
  • Hinterholzer A, Moises J, Regl C, Schwap S, Rapp E, Huber CG, Schubert M. Unambiguous identification of α-Gal epitopes in intact monoclonal antibodies by NMR spectroscopy. MAbs. 2022;14(1):2132977. doi:10.1080/19420862.2022.2132977. PMID: 36239533.
  • She YM, Dai S, Tam RY. Highly sensitive characterization of non-human glycan structures of monoclonal antibody drugs utilizing tandem mass spectrometry. Sci Rep. 2022;12(1):15109. doi:10.1038/s41598-022-19488-8. PMID: 36068283.
  • Maeda E, Kita S, Kinoshita M, Urakami K, Hayakawa T, Kakehi K. Analysis of nonhuman N-glycans as the minor constituents in recombinant monoclonal antibody pharmaceuticals. Anal Chem. 2012;84(5):2373–79. doi:10.1021/ac300234a. PMID: 22394092.
  • Galili U. The α-gal epitope (Galα1-3Galβ1-4GlcNAc-R) in xenotransplantation. Biochimie. 2001;83(7):557–63. doi:10.1016/s0300-9084(01)01294-9. PMID: 11522383.
  • Jefferis R. Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discov. 2009;8(3):226–34. doi:10.1038/nrd2804. PMID: 19247305.
  • Sandrin MS, Vaughan HA, Dabkowski PL, McKenzie IF. Anti-pig IgM antibodies in human serum react predominantly with Gal(alpha 1-3)Gal epitopes. Proc Natl Acad Sci U S A. 1993;90:11391–95. doi:10.1073/pnas.90.23.11391. PMID: 7504304.
  • Eisenson DL, Hisadome Y, Yamada K. Progress in xenotransplantation: immunologic barriers, advances in gene editing, and successful ^Tolerance induction strategies in pig-to-primate transplantation. Front Immunol. 2022;13:899657. doi:10.3389/fimmu.2022.899657. PMID: 35663933.
  • Commins SP, James HR, Kelly LA, Pochan SL, Workman LJ, Perzanowski MS, Kocan KM, Fahy JV, Nganga LW, Ronmark E, et al. The relevance of tick bites to the production of IgE antibodies to the mammalian oligosaccharide galactose-α-1,3-galactose. J Allergy Clin Immunol. 2011;127(5):1286–93.e6. doi:10.1016/j.jaci.2011.02.019. PMID: 21453959.
  • Chung CH, Mirakhur B, Chan E, Le QT, 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(11):1109–17. doi:10.1056/NEJMoa074943. PMID: 18337601.
  • van Bueren JJL, Rispens T, Verploegen S, van der Palen-Merkus T, Stapel S, Workman LJ, James H, van Berkel PH, van de Winkel JG, Platts-Mills TA, et al. Anti-galactose-α-1,3-galactose IgE from allergic patients does not bind α-galactosylated glycans on intact therapeutic antibody Fc domains. Nat Biotechnol. 2011;29(7):574–76. doi:10.1038/nbt.1912. PMID: 21747378.
  • Qian J, Liu T, Yang L, Daus A, Crowley R, Zhou Q. Structural characterization of N-linked oligosaccharides on monoclonal antibody cetuximab by the combination of orthogonal matrix-assisted laser desorption/ionization hybrid quadrupole-quadrupole time-of-flight tandem mass spectrometry and sequential enzymatic digestion. Anal Biochem. 2007;364:8–18. doi:10.1016/j.ab.2007.01.023. PMID: 17362871.
  • Ayoub D, Jabs W, Resemann A, Evers W, Evans C, Main L, Baessmann C, Wagner-Rousset E, Suckau D, Beck A. Correct primary structure assessment and extensive glyco-profiling of cetuximab by a combination of intact, middle-up, middle-down and bottom-up ESI and MALDI mass spectrometry techniques. MAbs. 2013;5:699–710. doi:10.4161/mabs.25423. PMID: 23924801.
  • Smith DF, Larsen RD, Mattox S, Lowe JB, Cummings RD. Transfer and expression of a murine UDP-Gal: beta-D-Gal-alpha 1,3-galactosyltransferase gene in transfected Chinese hamster ovary cells. Competition reactions between the alpha 1,3-galactosyltransferase and the endogenous alpha 2,3-sialyltransferase. J Biol Chem. 1990;265:6225–34. doi:10.1016/S0021-9258(19)39314-7. PMID: 2108155.
  • Cummings RD, Mattox SA. Retinoic acid-induced differentiation of the mouse teratocarcinoma cell line F9 is accompanied by an increase in the activity of UDP-galactose: beta-D-galactosyl-alpha 1,3-galactosyltransferase. J Biol Chem. 1988;263:511–19. doi:10.1016/S0021-9258(19)57422-1. PMID: 3121614.
  • Zhang P, Woen S, Wang T, Liau B, Zhao S, Chen C, Yang Y, Song Z, Wormald MR, Yu C, et al. Challenges of glycosylation analysis and control: an integrated approach to producing optimal and consistent therapeutic drugs. Drug Discov Today. 2016;21:740–65. doi:10.1016/j.drudis.2016.01.006. PMID: 26821133.
  • Garcia JJ, Raez LE, Rosas D. A narrative review of biosimilars: a continued journey from the scientific evidence to practice implementation. Transl Lung Cancer Res. 2020;9:2113–19. doi:10.21037/tlcr-20-601. PMID: 33209630.
  • Goel N, Chance K. Biosimilars in rheumatology: understanding the rigor of their development. Rheumatol (Oxford). 2017;56:187–97. doi:10.1093/rheumatology/kew206. PMID: 27241704.
  • Schiestl M, Stangler T, Torella C, Cepeljnik T, Toll H, Grau R. Acceptable changes in quality attributes of glycosylated biopharmaceuticals. Nat Biotechnol. 2011;29:310–12. doi:10.1038/nbt.1839. PMID: 21478841.
  • Wang LX, Tong X, Li C, Giddens JP, Li T. Glycoengineering of antibodies for modulating functions. Annu Rev Biochem. 2019;88:433–59. doi:10.1146/annurev-biochem-062917-012911. PMID: 30917003.
  • Parsons TB, Struwe WB, Gault J, Yamamoto K, Taylor TA, Raj R, Wals K, Mohammed S, Robinson CV, Benesch JL, et al. Optimal synthetic glycosylation of a therapeutic antibody. Angew Chem Weinheim Bergstr Ger. 2016;128:2407–13. doi:10.1002/ange.201508723. PMID: 27546920.
  • Hatfield G, Tepliakova L, Gingras G, Stalker A, Li X, Aubin Y, Tam RY. Specific location of galactosylation in an afucosylated antiviral monoclonal antibody affects its FcgammaRIIIA binding affinity. Front Immunol. 2022;13:972168. doi:10.3389/fimmu.2022.972168. PMID: 36304448.
  • Aoyama M, Hashii N, Tsukimura W, Osumi K, Harazono A, Tada M, Kiyoshi M, Matsuda A, Ishii-Watabe A. Effects of terminal galactose residues in mannose α1-6 arm of Fc-glycan on the effector functions of therapeutic monoclonal antibodies. MAbs. 2019;11(5):826–36. doi:10.1080/19420862.2019.1608143. PMID: 30990348.
  • Fan JQ, Kondo A, Kato I, Lee YC. High-performance liquid chromatography of glycopeptides and oligosaccharides on graphitized carbon columns. Anal Biochem. 1994;219:224–29. doi:10.1006/abio.1994.1261. PMID: 8080079.
  • She YM, Tam RY, Li X, Rosu-Myles M, Sauve S. Resolving isomeric structures of native glycans by nanoflow porous graphitized carbon chromatography–mass spectrometry. Anal Chem. 2020;92(20):14038–46. doi:10.1021/acs.analchem.0c02951. PMID: 32960038.
  • Elices MJ, Goldstein IJ. Biosynthesis of Bi-, Tri-, and tetraantennary oligosaccharides containing α-D-Galactosyl residues at their nonreducing termini. J Biol Chem. 1989;264(3):1375–80. doi:10.1016/S0021-9258(18)94197-9. PMID: 2492275.
  • Johnson LS, Braden B, inventors; MedImmune Inc., Bowie State University, assignees. Crystals and Structure of Synagis FAB. United States patent US 6,955,717 B2 2005 Oct 18.
  • Li T, Tong X, Yang Q, Giddens JP, Wang LX. Glycosynthase mutants of endoglycosidase S2 show potent transglycosylation activity and remarkably relaxed substrate specificity for antibody glycosylation remodeling. J Biol Chem. 2016;291:16508–18. doi:10.1074/jbc.M116.738765. PMID: 27288408.
  • Mariotte D, Dupont B, Gervais R, Galais MP, Laroche D, Tranchant A, Comby E, Bouhier-Leporrier K, Reimund JM, Le Mauff B. Anti-cetuximab IgE ELISA for identification of patients at a high risk of cetuximab-induced anaphylaxis. MAbs. 2011;3:396–401. doi:10.4161/mabs.3.4.16293. PMID: 21654207.
  • Dupont B, Mariotte D, Dugue AE, Clarisse B, Grellard JM, Babin E, Chauffert B, Dakpe S, Moldovan C, Bouhier-Leporrier K, et al. Utility of serum anti-cetuximab immunoglobulin E levels to identify patients at a high risk of severe hypersensitivity reaction to cetuximab. Br J Clin Pharmacol. 2017;83:623–31. doi:10.1111/bcp.13140. PMID: 27662818.
  • Serrier J, Davy JB, Dupont B, Clarisse B, Parienti JJ, Petit G, Khoy K, Ollivier Y, Gervais R, Mariotte D, et al. Validation of an anti-α-Gal IgE fluoroenzyme-immunoassay for the screening of patients at risk of severe anaphylaxis to cetuximab. Bmc Cancer. 2023;23(1):32. doi:10.1186/s12885-023-10501-5. PMID: 36624467.
  • Fussl F, Trappe A, Carillo S, Jakes C, Bones J. Comparative elucidation of cetuximab heterogeneity on the intact protein level by cation exchange chromatography and capillary electrophoresis coupled to mass spectrometry. Anal Chem. 2020;92:5431–38. doi:10.1021/acs.analchem.0c00185. PMID: 32105056.
  • Lippold S, Nicolardi S, Wuhrer M, Falck D. Proteoform-resolved fcɤriiia binding assay for fab glycosylated monoclonal antibodies achieved by affinity chromatography mass spectrometry of Fc moieties. Front Chem. 2019;7:698. doi:10.3389/fchem.2019.00698. PMID: 31709228.
  • Ruhaak LR, Zauner G, Huhn C, Bruggink C, Deelder AM, Wuhrer M. Glycan labeling strategies and their use in identification and quantification. Anal Bioanal Chem. 2010;397:3457–81. doi:10.1007/s00216-010-3532-z. PMID: 20225063.
  • Smith SA, Chruszcz M, Chapman MD, Pomes A. Human monoclonal ige antibodies—a major milestone in allergy. Curr Allergy Asthma Rep. 2023;23(1):53–65. doi:10.1007/s11882-022-01055-w. PMID: 36459330.
  • Wurth MA, Hadadianpour A, Horvath DJ, Daniel J, Bogdan O, Goleniewska K, Pomes A, Hamilton RG, Peebles RS Jr., Smith SA. Human IgE mAbs define variability in commercial Aspergillus extract allergen composition. JCI Insight. 2018;3. doi:10.1172/jci.insight.123387. PMID: 30333320.
  • Khatri K, Richardson CM, Glesner J, Kapingidza AB, Mueller GA, Zhang J, Dolamore C, Vailes LD, Wunschmann S, Peebles RS Jr., et al. Human IgE monoclonal antibody recognition of mite allergen Der p 2 defines structural basis of an epitope for IgE cross-linking and anaphylaxis in vivo. PNAS Nexus. 2022;1(3):c054. doi:10.1093/pnasnexus/pgac054. PMID: 35799831.
  • Hadadianpour A, Daniel J, Zhang J, Spiller BW, Makaraviciute A, DeWitt AM, Walden HS, Hamilton RG, Peebles RS Jr., Nutman TB, et al. Human IgE mAbs identify major antigens of parasitic worm infection. J Allergy Clin Immunol. 2022;150(6):1525–33. doi:10.1016/j.jaci.2022.05.022. PMID: 35760390.
  • Savitz J, Geaney C, Banks TA. A case of anaphylaxis to palivizumab. Ann Allergy Asthma Immunol. 2014;113:236–37. doi:10.1016/j.anai.2014.06.006. PMID: 25065351.
  • Resch B. Product review on the monoclonal antibody palivizumab for prevention of respiratory syncytial virus infection. Hum Vaccin Immunother. 2017;13:2138–49. doi:10.1080/21645515.2017.1337614. PMID: 28605249.
  • Deisenhofer J. Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein a from Staphylococcus aureus at 2.9- and 2.8-A resolution. Biochemistry. 1981;20(9):2361–70. doi:10.1021/bi00512a001. PMID: 7236608.
  • Barb AW, Prestegard JH. NMR analysis demonstrates immunoglobulin G N-glycans are accessible and dynamic. Nat Chem Biol. 2011;7:147–53. doi:10.1038/nchembio.511. PMID: 21258329.
  • Yamaguchi Y, Kato K, Shindo M, Aoki S, Furusho K, Koga K, Takahashi N, Arata Y, Shimada I. Dynamics of the carbohydrate chains attached to the Fc portion of immunoglobulin G as studied by NMR spectroscopy assisted by selective 13C labeling of the glycans. J Biomol NMR. 1998;12:385–94. doi:10.1023/a:1008392229694. PMID: 9835046.
  • Barb AW, Brady EK, Prestegard JH. Branch-specific sialylation of IgG-Fc glycans by ST6Gal-I. Biochemistry. 2009;48:9705–07. doi:10.1021/bi901430h. PMID: 19772356.
  • Lungulescu CV, Ungureanu BS, Turcu-Stiolica A, Ghimpau V, Artene SA, Cazacu IM, Grecu AF, Dinescu VC, Croitoru A, Volovat SR. The role of IgE specific for galactose-α-1,3-galactose in predicting cetuximab induced hypersensitivity reaction: a systematic review and a diagnostic meta-analysis. Sci Rep. 2020;10(1):21355. doi:10.1038/s41598-020-78497-7. PMID: 33288791.
  • Subedi GP, Hanson QM, Barb AW. Restricted motion of the conserved immunoglobulin G1 N-Glycan is essential for efficient FcγRIIIa binding. Structure. 2014;22(10):1478–88. doi:10.1016/j.str.2014.08.002. PMID: 25199692.
  • Crispin M, Yu X, Bowden TA. Crystal structure of sialylated IgG Fc: implications for the mechanism of intravenous immunoglobulin therapy. Proc Natl Acad Sci U S A. 2013;110:E3544–3546. doi:10.1073/pnas.1310657110. PMID: 23929778.
  • Van Coillie J, Schulz MA, Bentlage AEH, de Haan N, Ye Z, Geerdes DM, van Esch WJE, Hafkenscheid L, Miller RL, Narimatsu Y, et al. Role of N-Glycosylation in FcgammaRIIIa interaction with IgG. Front Immunol. 2022;13:987151. doi:10.3389/fimmu.2022.987151. PMID: 36189205.
  • Li T, DiLillo DJ, Bournazos S, Giddens JP, Ravetch JV, Wang LX. Modulating IgG effector function by Fc glycan engineering. Proc Natl Acad Sci USA. 2017;114:3485–90. doi:10.1073/pnas.1702173114. PMID: 28289219.
  • Sjogren J, Struwe WB, Cosgrave EF, Rudd PM, Stervander M, Allhorn M, Hollands A, Nizet V, Collin M. EndoS2 is a unique and conserved enzyme of serotype M49 group a Streptococcus that hydrolyses N-linked glycans on IgG and α1-acid glycoprotein. Biochem J. 2013;455(1):107–18. doi:10.1042/BJ20130126. PMID: 23865566.