Bivalent binding on cells varies between anti-CD20 antibodies and is dose-dependent

References

• Pierpont TM, Limper CB, Richards KL. Past, present, and future of rituximab-the world’s first oncology monoclonal antibody therapy. Front Oncol. 2018;8:163. doi:https://doi.org/10.3389/fonc.2018.00163.
   PubMed Web of Science ®Google Scholar
• Salles G, Barrett M, Foà R, Maurer J, O’Brien S, Valente N, Wenger M, Maloney DG. Rituximab in B-cell hematologic malignancies: a review of 20 years of clinical experience. Adv. Ther. 2017;34:2232–13. doi:https://doi.org/10.1007/s12325-017-0612-x.
   PubMed Web of Science ®Google Scholar
• Chan HTC, Hughes D, French RR, Tutt AL, Walshe CA, Teeling JL, Glennie MJ, Cragg MS. CD20-induced lymphoma cell death is independent of both caspases and its redistribution into Triton X-100 insoluble membrane rafts. Cancer Res. 2003;63:5480–89.
   PubMed Web of Science ®Google Scholar
• Ivanov A, Beers SA, Walshe CA, Honeychurch J, Alduaij W, Cox KL, Potter KN, Murray S, Chan CHT, Klymenko T, et al. Monoclonal antibodies directed to CD20 and HLA-DR can elicit homotypic adhesion followed by lysosome-mediated cell death in human lymphoma and leukemia cells. J Clin Invest. 2009;119:2143–59. doi:https://doi.org/10.1172/JCI37884.
   PubMed Web of Science ®Google Scholar
• Wang W, Erbe AK, Hank JA, Morris ZS, Sondel PM. NK cell-mediated antibody-dependent cellular cytotoxicity in cancer immunotherapy. Front Immunol. 2015;6:368. doi:https://doi.org/10.3389/fimmu.2015.00368.
   PubMed Web of Science ®Google Scholar
• Meyer S, Leusen JHW, Boross P. Regulation of complement and modulation of its activity in monoclonal antibody therapy of cancer. mAbs. 2014;6:1133–44. doi:https://doi.org/10.4161/mabs.29670.
   PubMed Web of Science ®Google Scholar
• Weiskopf K, Weissman IL. Macrophages are critical effectors of antibody therapies for cancer. mAbs. 2015;7:303–10. doi:https://doi.org/10.1080/19420862.2015.1011450.
   PubMed Web of Science ®Google Scholar
• Herter S, Herting F, Mundigl O, Waldhauer I, Weinzierl T, Fauti T, Muth G, Ziegler-Landesberger D, Puijenbroek EV, Lang S, Duong MN, et al. Preclinical activity of the Type II CD20 antibody GA101 (Obinutuzumab) compared with rituximab and ofatumumab in vitro and in xenograft models. Mol Cancer Ther. 2013;12:2031–42. doi:https://doi.org/10.1158/1535-7163.MCT-12-1182.
   PubMed Web of Science ®Google Scholar
• Cragg MS, Morgan SM, Chan HTC, Morgan BP, Filatov AV, Johnson PWM, French RR, Glennie MJ. Complement-mediated lysis by anti-CD20 mAb correlates with segregation into lipid rafts. Blood. 2003;101:1045–52. doi:https://doi.org/10.1182/blood-2002-06-1761.
   PubMed Web of Science ®Google Scholar
• Diebolder CA, Beurskens FJ, de Jong RN, Koning RI, Strumane K, Lindorfer MA, Voorhorst M, Ugurlar D, Rosati S, Heck AJR, et al. Complement is activated by IgG hexamers assembled at the cell surface. Science. 2014;343:1260–63. doi:https://doi.org/10.1126/science.1248943.
   PubMed Web of Science ®Google Scholar
• Meyer S, Evers M, Jansen JHM, Buijs J, Broek B, Reitsma SE, Moerer P, Amini M, Kretschmer A, ten Broeke T, et al. New insights in Type I and II CD20 antibody mechanisms-of-action with a panel of novel CD20 antibodies. Br J Haematol. 2018;180:808–20. doi:https://doi.org/10.1111/bjh.15132.
   PubMed Web of Science ®Google Scholar
• Li B, Zhao L, Guo H, Wang C, Zhang X, Wu L, Chen L, Tong Q, Qian W, Wang H, et al. Characterization of a rituximab variant with potent antitumor activity against rituximab-resistant B-cell lymphoma. Blood. 2009;114:5007–15. doi:https://doi.org/10.1182/blood-2009-06-225474.
   PubMed Web of Science ®Google Scholar
• Nishida M, Uematsu N, Kobayashi H, Matsunaga Y, Ishida S, Takata M, Niwa O, Padlan EA, Newman R. BM-ca is a newly defined type I/II anti-CD20 monoclonal antibody with unique biological properties. Int J Oncol. 2011;38:335–44. doi:https://doi.org/10.3892/ijo.2010.864.
   PubMed Web of Science ®Google Scholar
• Bornstein GG, Quéva C, Tabrizi M, van Abbema A, Chavez C, Wang P, Foord O, Ahluwalia K, Laing N, Raja S, et al. Development of a new fully human anti-CD20 monoclonal antibody for the treatment of B-cell malignancies. Invest New Drugs. 2010;28:561–74. doi:https://doi.org/10.1007/s10637-009-9291-z.
   PubMed Web of Science ®Google Scholar
• Teeling JL, Mackus WJM, Wiegman LJJM, van den Brakel JHN, Beers SA, French RR, van Meerten T, Ebeling S, Vink T, Slootstra JW, et al. The biological activity of human CD20 monoclonal antibodies is linked to unique epitopes on CD20. J Immunol. 2006;177:362–71. doi:https://doi.org/10.4049/jimmunol.177.1.362.
   PubMed Web of Science ®Google Scholar
• Niederfellner G, Lammens A, Mundigl O, Georges GJ, Schaefer W, Schwaiger M, Franke A, Wiechmann K, Jenewein S, Slootstra JW, et al. Epitope characterization and crystal structure of GA101 provide insights into the molecular basis for type I/II distinction of CD20 antibodies. Blood. 2011;118:358–67. doi:https://doi.org/10.1182/blood-2010-09-305847.
   PubMed Web of Science ®Google Scholar
• Teeling JL, French RR, Cragg MS, van den Brakel J, Pluyter M, Huang H, Chan C, Parren PWHI, Hack CE, Dechant M, et al. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas. Blood. 2004;104:1793–800. doi:https://doi.org/10.1182/blood-2004-01-0039.
   PubMed Web of Science ®Google Scholar
• Mössner E, Brünker P, Moser S, Püntener U, Schmidt C, Herter S, Grau R, Gerdes C, Nopora A, van Puijenbroek E, et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell–mediated B-cell cytotoxicity. Blood. 2010;115:4393–402. doi:https://doi.org/10.1182/blood-2009-06-225979.
   PubMed Web of Science ®Google Scholar
• Ferrara C, Stuart F, Sondermann P, Brünker P, Umaña P. The carbohydrate at FcgammaRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem. 2006;281:5032–36. doi:https://doi.org/10.1074/jbc.M510171200.
   PubMed Web of Science ®Google Scholar
• Bondza S, Foy E, Brooks J, Andersson K, Robinson J, Richalet P, Buijs J. Real-time characterization of antibody binding to receptors on living immune cells. Front. Immunol. 2017;8. doi:https://doi.org/10.3389/fimmu.2017.00455.
   Google Scholar
• Engelberts PJ, Voorhorst M, Schuurman J, van Meerten T, Bakker JM, Vink T, Mackus WJM, Breij ECW, Derer S, Valerius T, et al. Type I CD20 Antibodies Recruit the B Cell Receptor for Complement-Dependent Lysis of Malignant B Cells. J Immunol. 2016;197:4829–4837. doi:https://doi.org/10.4049/jimmunol.1600811 12
   PubMed Web of Science ®Google Scholar
• Natsume A, Shimizu‐Yokoyama Y, Satoh M, Shitara K, Niwa R. Engineered anti-CD20 antibodies with enhanced complement-activating capacity mediate potent anti-lymphoma activity. Cancer Sci. 2009;100:2411–18. doi:https://doi.org/10.1111/j.1349-7006.2009.01327.x.
   PubMed Web of Science ®Google Scholar
• Singh V, Gupta D, Arora R, Tripathi RP, Almasan A, Macklis RM. Surface levels of CD20 determine anti-CD20 antibodies mediated cell death in vitro. PLoS One. 2014;9. doi:https://doi.org/10.1371/journal.pone.0111113.
   Google Scholar
• Bondza S, Björkelund H, Nestor M, Andersson K, Buijs J. Novel real-time proximity assay for characterizing multiple receptor interactions on living cells. Anal Chem. 2017;89:13212–18. doi:https://doi.org/10.1021/acs.analchem.7b02983.
   PubMed Web of Science ®Google Scholar
• Rougé L, Chiang N, Steffek M, Kugel C, Croll TI, Tam C, Estevez A, Arthur CP, Koth CM, Ciferri C, et al. Structure of CD20 in complex with the therapeutic monoclonal antibody rituximab. Science. 2020;367:1224–30. doi:https://doi.org/10.1126/science.aaz9356.
   PubMed Web of Science ®Google Scholar
• Lindorfer MA, Cook EM, Tupitza JC, Zent CS, Burack R, de Jong RN, Beurskens FJ, Schuurman J, Parren PWHI, Taylor RP, et al. Real-time analysis of the detailed sequence of cellular events in mAb-mediated complement-dependent cytotoxicity of B-cell lines and of chronic lymphocytic leukemia B-cells. Mol Immunol. 2016;70:13–23. doi:https://doi.org/10.1016/j.molimm.2015.12.007.
   PubMed Web of Science ®Google Scholar
• Strasser J, de Jong RN, Beurskens FJ, Wang G, Heck AJR, Schuurman J, Parren PWHI, Hinterdorfer P, Preiner J, et al. Unraveling the macromolecular pathways of IgG oligomerization and complement activation on antigenic surfaces. Nano Lett. 2019;19:4787–96. doi:https://doi.org/10.1021/acs.nanolett.9b02220.
   PubMed Web of Science ®Google Scholar
• Klein C, Lammens A, Schäfer W, Georges G, Schwaiger M, Mössner E, Hopfner K-P, Umaña P, Niederfellner G. Epitope interactions of monoclonal antibodies targeting CD20 and their relationship to functional properties. mAbs. 2013;5:22–33. doi:https://doi.org/10.4161/mabs.22771.
   PubMed Web of Science ®Google Scholar
• Oldham RJ, Cleary KLS, Cragg MS. CD20 and its antibodies: past, present, and future. Forum Immunopathol Dis Ther. 2014;5:7–23.
   Google Scholar
• Wang B, Yang C, Jin X, Du Q, Wu H, Dall’Acqua W, Mazor Y. Regulation of antibody-mediated complement-dependent cytotoxicity by modulating the intrinsic affinity and binding valency of IgG for target antigen. mAbs. 2020;12:1690959. doi:https://doi.org/10.1080/19420862.2019.1690959.
   PubMed Web of Science ®Google Scholar
• Uchiyama S, Suzuki Y, Otake K, Yokoyama M, Ohta M, Aikawa S, Komatsu M, Sawada T, Kagami Y, Morishima Y, et al. Development of novel humanized anti-CD20 antibodies based on affinity constant and epitope. Cancer Sci. 2010;101:201–09. doi:https://doi.org/10.1111/j.1349-7006.2009.01392.x.
   PubMed Web of Science ®Google Scholar