Influence of the bispecific antibody IgG subclass on T cell redirection

References

• Thakur A, Lum LG. “NextGen” biologics: bispecific antibodies and emerging clinical results. Expert Opin Biol Ther. 2016;16:675–88. doi:10.1517/14712598.2016.1150996.
   PubMed Web of Science ®Google Scholar
• Kontermann RE, Brinkmann U. Bispecific antibodies. Drug Discov Today. 2015;20:838–47. doi:10.1016/j.drudis.2015.02.008.
   PubMed Web of Science ®Google Scholar
• Seimetz D, Lindhofer H, Bokemeyer C. Development and approval of the trifunctional antibody catumaxomab (anti-EpCAM x anti-CD3) as a targeted cancer immunotherapy. Cancer Treat Rev. 2010;36:458–67. doi:10.1016/j.ctrv.2010.03.001.
   PubMed Web of Science ®Google Scholar
• Przepiorka D, Ko CW, Deisseroth A, Yancey CL, Candau-Chacon R, Chiu HJ, Gehrke BJ, Gomez-Broughton C, Kane RC, Kirshner S, et al. FDA approval: blinatumomab. Clin Cancer Res. 2015;21:4035–39. doi:10.1158/1078-0432.CCR-15-0612.
   PubMed Web of Science ®Google Scholar
• Batlevi CL, Matsuki E, Brentjens RJ, Younes A. Novel immunotherapies in lymphoid malignancies. Nat Rev Clin Oncol. 2016;13:25–40. doi:10.1038/nrclinonc.2015.187.
   PubMed Web of Science ®Google Scholar
• Smith EJ, Olson K, Haber LJ, Varghese B, Duramad P, Tustian AD, Oyejide A, Kirshner JR, Canova L, Menon J, et al. A novel, native-format bispecific antibody triggering T-cell killing of B-cells is robustly active in mouse tumor models and cynomolgus monkeys. Sci Rep. 2015;5:17943. doi:10.1038/srep17943.
   PubMed Web of Science ®Google Scholar
• Spiess C, Zhai Q, Carter PJ. Alternative molecular formats and therapeutic applications for bispecific antibodies. Mol Immunol. 2015;67:95–106. doi:10.1016/j.molimm.2015.01.003.
   PubMed Web of Science ®Google Scholar
• Schaefer W, Regula JT, Bahner M, Schanzer J, Croasdale R, Durr H, Gassner C, Georges G, Kettenberger H, Imhof-Jung S, et al. Immunoglobulin domain crossover as a generic approach for the production of bispecific IgG antibodies. Proc Natl Acad Sci U S A. 2011;108:11187–92. doi:10.1073/pnas.1019002108.
   PubMed Web of Science ®Google Scholar
• Davis DM, Dustin ML. What is the importance of the immunological synapse? Trends Immunol. 2004;25:323–27. doi:10.1016/j.it.2004.03.007.
   PubMed Web of Science ®Google Scholar
• Dustin ML, Depoil D. New insights into the T cell synapse from single molecule techniques. Nat Rev Immunol. 2011;11:672–84. doi:10.1038/nri3066.
   PubMed Web of Science ®Google Scholar
• James JR, Vale RD. Biophysical mechanism of T-cell receptor triggering in a reconstituted system. Nature. 2012;487:64–69. doi:10.1038/nature11220.
   PubMed Web of Science ®Google Scholar
• van der Merwe PA, Dushek O. Mechanisms for T cell receptor triggering. Nat Rev Immunol. 2011;11:47–55. doi:10.1038/nri2887.
   PubMed Web of Science ®Google Scholar
• Alakoskela JM, Koner AL, Rudnicka D, Kohler K, Howarth M, Davis DM. Mechanisms for size-dependent protein segregation at immune synapses assessed with molecular rulers. Biophys J. 2011;100:2865–74. doi:10.1016/j.bpj.2011.05.013.
   PubMed Web of Science ®Google Scholar
• Klein JS, Gnanapragasam PN, Galimidi RP, Foglesong CP, West AP Jr., Bjorkman PJ. Examination of the contributions of size and avidity to the neutralization mechanisms of the anti-HIV antibodies b12 and 4E10. Proc Natl Acad Sci U S A. 2009;106:7385–90. doi:10.1073/pnas.0811427106.
   PubMed Web of Science ®Google Scholar
• Leong SR, Sukumaran S, Hristopoulos M, Totpal K, Stainton S, Lu E, Wong A, Tam L, Newman R, Vuillemenot BR, et al. An anti-CD3/anti-CLL-1 bispecific antibody for the treatment of acute myeloid leukemia. Blood. 2017;129:609–18. doi:10.1182/blood-2016-08-735365.
   PubMed Web of Science ®Google Scholar
• Bluemel C, Hausmann S, Fluhr P, Sriskandarajah M, Stallcup WB, Baeuerle PA, Kufer P. Epitope distance to the target cell membrane and antigen size determine the potency of T cell-mediated lysis by BiTE antibodies specific for a large melanoma surface antigen. Cancer Immunol Immunother. 2010;59:1197–209. doi:10.1007/s00262-010-0844-y.
   PubMed Web of Science ®Google Scholar
• Li J, Stagg NJ, Johnston J, Harris MJ, Menzies SA, DiCara D, Clark V, Hristopoulos M, Cook R, Slaga D, et al. Membrane-proximal epitope facilitates efficient T cell synapse formation by anti-FcRH5/CD3 and is a requirement for myeloma cell killing. Cancer Cell. 2017. doi:10.1016/j.ccell.2017.02.001.
   Web of Science ®Google Scholar
• Guest RD, Hawkins RE, Kirillova N, Cheadle EJ, Arnold J, O’Neill A, Irlam J, Chester KA, Kemshead JT, Shaw DM, et al. The role of extracellular spacer regions in the optimal design of chimeric immune receptors: evaluation of four different scFvs and antigens. J Immunother. 2005;28:203–11.
   PubMed Web of Science ®Google Scholar
• Roux KH, Strelets L, Michaelsen TE. Flexibility of human IgG subclasses. J Immunol. 1997;159:3372–82.
   PubMed Web of Science ®Google Scholar
• Liu H, May K. Disulfide bond structures of IgG molecules: structural variations, chemical modifications and possible impacts to stability and biological function. MAbs. 2012;4:17–23. doi:10.4161/mabs.4.1.18347.
   PubMed Web of Science ®Google Scholar
• Tian X, Vestergaard B, Thorolfsson M, Yang Z, Rasmussen HB, Langkilde AE. In-depth analysis of subclass-specific conformational preferences of IgG antibodies. IUCrJ. 2015;2:9–18. doi:10.1107/S205225251402209X.
   PubMed Web of Science ®Google Scholar
• Brinkmann U, Kontermann RE. The making of bispecific antibodies. MAbs. 2017;9:182–212. doi:10.1080/19420862.2016.1268307.
   PubMed Web of Science ®Google Scholar
• Carter PJ. Potent antibody therapeutics by design. Nat Rev Immunol. 2006;6:343–57. doi:10.1038/nri1837.
   PubMed Web of Science ®Google Scholar
• Kretschmer A, Schwanbeck R, Valerius T, Rosner T. Antibody isotypes for tumor immunotherapy. Transfus Med Hemother. 2017;44:320–26. doi:10.1159/000479240.
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Buijsse AO, van Den Bremer ET, Verwilligen AY, Bleeker WK, Thorpe SJ, Killestein J, Polman CH, Aalberse RC, Schuurman J, et al. Therapeutic IgG4 antibodies engage in Fab-arm exchange with endogenous human IgG4 in vivo. Nat Biotechnol. 2009;27:767–71. doi:10.1038/nbt.1553.
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Meesters JI, Priem P, de Jong RN, van Den Bremer ET, van Kampen MD, Gerritsen AF, Schuurman J, Parren PW. Controlled Fab-arm exchange for the generation of stable bispecific IgG1. Nat Protoc. 2014;9:2450–63. doi:10.1038/nprot.2014.169.
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Meesters JI, de Goeij BE, van Den Bremer ET, Neijssen J, van Kampen MD, Strumane K, Verploegen S, Kundu A, Gramer MJ, et al. Efficient generation of stable bispecific IgG1 by controlled Fab-arm exchange. Proc Natl Acad Sci U S A. 2013;110:5145–50. doi:10.1073/pnas.1220145110.
   PubMed Web of Science ®Google Scholar
• Loffler A, Kufer P, Lutterbuse R, Zettl F, Daniel PT, Schwenkenbecher JM, Riethmuller G, Dorken B, Bargou RC. A recombinant bispecific single-chain antibody, CD19 x CD3, induces rapid and high lymphoma-directed cytotoxicity by unstimulated T lymphocytes. Blood. 2000;95:2098–103.
   PubMed Web of Science ®Google Scholar
• Kung P, Goldstein G, Reinherz EL, Schlossman SF. Monoclonal antibodies defining distinctive human T cell surface antigens. Science. 1979;206:347–49.
   Google Scholar
• Hezareh M, Hessell AJ, Jensen RC, van de Winkel JG, Parren PW. Effector function activities of a panel of mutants of a broadly neutralizing antibody against human immunodeficiency virus type 1. J Virol. 2001;75:12161–68. doi:10.1128/JVI.75.24.12161-12168.2001.
   PubMed Web of Science ®Google Scholar
• Oganesyan V, Gao C, Shirinian L, Wu H, Dall’Acqua WF. Structural characterization of a human Fc fragment engineered for lack of effector functions. Acta Crystallogr D Biol Crystallogr. 2008;64:700–04. doi:10.1107/S0907444908007877.
   PubMed Web of Science ®Google Scholar
• Vafa O, Gilliland GL, Brezski RJ, Strake B, Wilkinson T, Lacy ER, Scallon B, Teplyakov A, Malia TJ, Strohl WR. An engineered Fc variant of an IgG eliminates all immune effector functions via structural perturbations. Methods. 2014;65:114–26. doi:10.1016/j.ymeth.2013.06.035.
   PubMed Web of Science ®Google Scholar
• Lobanov M, Bogatyreva NS, Galzitskaia OV. [Radius of gyration is indicator of compactness of protein structure]. Mol Biol (Mosk). 2008;42:701–06.
   PubMed Web of Science ®Google Scholar
• Anderson DR, Grillo-Lopez A, Varns C, Chambers KS, Hanna N. Targeted anti-cancer therapy using rituximab, a chimaeric anti-CD20 antibody (IDEC-C2B8) in the treatment of non-hodgkin’s B-cell lymphoma. Biochem Soc Trans. 1997;25:705–08.
   PubMed Web of Science ®Google Scholar
• Strop P, Ho WH, Boustany LM, Abdiche YN, Lindquist KC, Farias SE, Rickert M, Appah CT, Pascua E, Radcliffe T, et al. Generating bispecific human IgG1 and IgG2 antibodies from any antibody pair. J Mol Biol. 2012;420:204–19. doi:10.1016/j.jmb.2012.04.020.
   PubMed Web of Science ®Google Scholar
• Dillon M, Yin Y, Zhou J, McCarty L, Ellerman D, Slaga D, Junttila TT, Han G, Sandoval W, Ovacik MA, et al. Efficient production of bispecific IgG of different isotypes and species of origin in single mammalian cells. MAbs. 2017;9:213–30. doi:10.1080/19420862.2016.1267089.
   PubMed Web of Science ®Google Scholar
• Dall’Acqua WF, Kiener PA, Wu H. Properties of human IgG1s engineered for enhanced binding to the neonatal Fc receptor (FcRn). J Biol Chem. 2006;281:23514–24. doi:10.1074/jbc.M604292200.
   PubMed Web of Science ®Google Scholar
• Dall’Acqua WF, Woods RM, Ward ES, Palaszynski SR, Patel NK, Brewah YA, Wu H, Kiener PA, Langermann S. Increasing the affinity of a human IgG1 for the neonatal Fc receptor: biological consequences. J Immunol. 2002;169:5171–80. doi:10.4049/jimmunol.169.9.5171.
   PubMed Web of Science ®Google Scholar
• Tam S, McCarthy S, Armstrong A, Somani S, Wu S-J, Liu X, Gervais A, Ernst R, Saro D, Decker R, et al. Functional, biophysical, and structural characterization of human IgG1 and IgG4 Fc variants with ablated immune functionality. Antibodies. 2017;6:12. doi:10.3390/antib6030012.
   Web of Science ®Google Scholar
• Chauhan AK, Chen C, Moore TL, DiPaolo RJ. Induced expression of fcgammariiia (CD16a) on CD4+ T cells triggers generation of IFN-gammahigh subset. J Biol Chem. 2015;290:5127–40. doi:10.1074/jbc.M114.599266.
   PubMed Web of Science ®Google Scholar
• Kjer-Nielsen L, Dunstone MA, Kostenko L, Ely LK, Beddoe T, Mifsud NA, Purcell AW, Brooks AG, McCluskey J, Rossjohn J. Crystal structure of the human T cell receptor CD3 epsilon gamma heterodimer complexed to the therapeutic mAb OKT3. Proc Natl Acad Sci U S A. 2004;101:7675–80. doi:10.1073/pnas.0402295101.
   PubMed Web of Science ®Google Scholar
• Cheng M, Ahmed M, Xu H, Cheung NK. Structural design of disialoganglioside GD2 and CD3-bispecific antibodies to redirect T cells for tumor therapy. Int J Cancer. 2015;136:476–86. doi:10.1002/ijc.29007.
   PubMed Web of Science ®Google Scholar
• Rankin CT, Veri MC, Gorlatov S, Tuaillon N, Burke S, Huang L, Inzunza HD, Li H, Thomas S, Johnson S, et al. CD32B, the human inhibitory Fc-gamma receptor IIB, as a target for monoclonal antibody therapy of B-cell lymphoma. Blood. 2006;108:2384–91. doi:10.1182/blood-2006-05-020602.
   PubMed Web of Science ®Google Scholar
• Psathas JN, Doonan PJ, Raman P, Freedman BD, Minn AJ, Thomas-Tikhonenko A. The Myc-miR-17-92 axis amplifies B-cell receptor signaling via inhibition of ITIM proteins: a novel lymphomagenic feed-forward loop. Blood. 2013;122:4220–29. doi:10.1182/blood-2012-12-473090.
   PubMed Web of Science ®Google Scholar
• Hubbard MA, Thorkildson P, Kozel TR, AuCoin DP. Constant domains influence binding of mouse-human chimeric antibodies to the capsular polypeptide of bacillus anthracis. Virulence. 2013;4:483–88. doi:10.4161/viru.25711.
   PubMed Web of Science ®Google Scholar
• McCloskey N, Turner MW, Steffner P, Owens R, Goldblatt D. Human constant regions influence the antibody binding characteristics of mouse-human chimeric IgG subclasses. Immunology. 1996;88:169–73. doi:10.1111/j.1365-2567.1996.tb00001.x.
   PubMed Web of Science ®Google Scholar
• Morelock MM, Rothlein R, Bright SM, Robinson MK, Graham ET, Sabo JP, Owens R, King DJ, Norris SH, Scher DS, et al. Isotype choice for chimeric antibodies affects binding properties. J Biol Chem. 1994;269:13048–55.
   PubMed Web of Science ®Google Scholar
• Kai M, Motoki K, Yoshida H, Emuta C, Chisaka Y, Tsuruhata K, Endo C, Muto M, Shimabe M, Nishiyama U, et al. Switching constant domains enhances agonist activities of antibodies to a thrombopoietin receptor. Nat Biotechnol. 2008;26:209–11. doi:10.1038/nbt1376.
   PubMed Web of Science ®Google Scholar
• Sampei Z, Igawa T, Soeda T, Funaki M, Yoshihashi K, Kitazawa T, Muto A, Kojima T, Nakamura S, Hattori K. Non-antigen-contacting region of an asymmetric bispecific antibody to factors IXa/X significantly affects factor VIII-mimetic activity. MAbs. 2015;7:120–28. doi:10.4161/19420862.2015.989028.
   PubMed Web of Science ®Google Scholar
• Le Gall F, Reusch U, Little M, Kipriyanov SM. Effect of linker sequences between the antibody variable domains on the formation, stability and biological activity of a bispecific tandem diabody. Protein Eng Des Sel. 2004;17:357–66. doi:10.1093/protein/gzh039.
   PubMed Web of Science ®Google Scholar
• Stamova S, Feldmann A, Cartellieri M, Arndt C, Koristka S, Apel F, Wehner R, Schmitz M, Bornhauser M, von Bonin M, et al. Generation of single-chain bispecific green fluorescent protein fusion antibodies for imaging of antibody-induced T cell synapses. Anal Biochem. 2012;423:261–68. doi:10.1016/j.ab.2011.12.042.
   PubMed Web of Science ®Google Scholar
• Feldmann A, Stamova S, Bippes CC, Bartsch H, Wehner R, Schmitz M, Temme A, Cartellieri M, Bachmann M. Retargeting of T cells to prostate stem cell antigen expressing tumor cells: comparison of different antibody formats. Prostate. 2011;71:998–1011. doi:10.1002/pros.21315.
   PubMed Web of Science ®Google Scholar
• Wang X, Mathieu M, Brezski RJ. IgG Fc engineering to modulate antibody effector functions. Protein Cell. 2018;9:63–73. doi:10.1007/s13238-017-0473-8.
   PubMed Web of Science ®Google Scholar
• Vitale LA, Thomas LJ, He LZ, O’Neill T, Widger J, Crocker A, Sundarapandiyan K, Storey JR, Forsberg EM, Weidlick J, et al. Development of CDX-1140, an agonist CD40 antibody for cancer immunotherapy. Cancer Immunol Immunother. 2019;68:233–45. doi:10.1007/s00262-018-2267-0.
   PubMed Web of Science ®Google Scholar
• Rosner T, Kahle S, Montenegro F, Matlung HL, Jansen JHM, Evers M, Beurskens F, Leusen JHW, van Den Berg TK, Valerius T. Immune effector functions of human IgG2 antibodies against EGFR. Mol Cancer Ther. 2019;18:75–88. doi:10.1158/1535-7163.MCT-18-0341.
   PubMed Web of Science ®Google Scholar
• Kubota T, Niwa R, Satoh M, Akinaga S, Shitara K, Hanai N. Engineered therapeutic antibodies with improved effector functions. Cancer Sci. 2009;100:1566–72. doi:10.1111/j.1349-7006.2009.01222.x.
   PubMed Web of Science ®Google Scholar
• Borlak J, Langer F, Spanel R, Schondorfer G, Dittrich C. Immune-mediated liver injury of the cancer therapeutic antibody catumaxomab targeting EpCAM, CD3 and Fcgamma receptors. Oncotarget. 2016;7:28059–74. doi:10.18632/oncotarget.8574.
   PubMedGoogle Scholar
• Guinier A, Fournet G. Small-angle scatterring of X-rays. New York: Wiley; 1955.
   Google Scholar
• Gomez-Abad C, Pisonero H, Blanco-Aparicio C, Roncador G, Gonzalez-Menchen A, Martinez-Climent JA, Mata E, Rodriguez ME, Munoz-Gonzalez G, Sanchez-Beato M, et al. PIM2 inhibition as a rational therapeutic approach in B-cell lymphoma. Blood. 2011;118:5517–27. doi:10.1182/blood-2011-03-344374.
   PubMed Web of Science ®Google Scholar
• Jarantow SW, Bushey BS, Pardinas JR, Boakye K, Lacy ER, Sanders R, Sepulveda MA, Moores SL, Chiu ML. Impact of cell-surface antigen expression on target engagement and function of an epidermal growth factor receptor x c-MET bispecific antibody. J Biol Chem. 2015;290:24689–704. doi:10.1074/jbc.M115.651653.
   PubMed Web of Science ®Google Scholar