Progress in overcoming the chain association issue in bispecific heterodimeric IgG antibodies

References

• Beck A, Wurch T, Bailly C, Corvaia N. Strategies and challenges for the next generation of therapeutic antibodies. Nat Rev Immunol 2010; 10:345 - 52; http://dx.doi.org/10.1038/nri2747; PMID: 20414207
   PubMed Web of Science ®Google Scholar
• Carter PJ. Introduction to current and future protein therapeutics: a protein engineering perspective. Exp Cell Res 2011; 317:1261 - 9; http://dx.doi.org/10.1016/j.yexcr.2011.02.013; PMID: 21371474
   PubMed Web of Science ®Google Scholar
• Chan AC, Carter PJ. Therapeutic antibodies for autoimmunity and inflammation. Nat Rev Immunol 2010; 10:301 - 16; http://dx.doi.org/10.1038/nri2761; PMID: 20414204
   PubMed Web of Science ®Google Scholar
• Fischer N, Léger O. Bispecific antibodies: molecules that enable novel therapeutic strategies. Pathobiology 2007; 74:3 - 14; http://dx.doi.org/10.1159/000101046; PMID: 17496428
   PubMed Web of Science ®Google Scholar
• Mouquet H, Warncke M, Scheid JF, Seaman MS, Nussenzweig MC. Enhanced HIV-1 neutralization by antibody heteroligation. Proc Natl Acad Sci U S A 2012; 109:875 - 80; http://dx.doi.org/10.1073/pnas.1120059109; PMID: 22219363
   PubMed Web of Science ®Google Scholar
• Atwal JK, Chen Y, Chiu C, Mortensen DL, Meilandt WJ, Liu Y, et al. A therapeutic antibody targeting BACE1 inhibits amyloid-β production in vivo. Sci Transl Med 2011; 3:84ra43; http://dx.doi.org/10.1126/scitranslmed.3002254; PMID: 21613622
   PubMed Web of Science ®Google Scholar
• Topp MS, Kufer P, Gökbuget N, Goebeler M, Klinger M, Neumann S, et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J Clin Oncol 2011; 29:2493 - 8; http://dx.doi.org/10.1200/JCO.2010.32.7270; PMID: 21576633
   PubMed Web of Science ®Google Scholar
• Linke R, Klein A, Seimetz D. Catumaxomab: clinical development and future directions. MAbs 2010; 2:129 - 36; http://dx.doi.org/10.4161/mabs.2.2.11221; PMID: 20190561
   PubMed Web of Science ®Google Scholar
• Holmes D. Buy buy bispecific antibodies. Nat Rev Drug Discov 2011; 10:798 - 800; http://dx.doi.org/10.1038/nrd3581; PMID: 22037028
   PubMed Web of Science ®Google Scholar
• McDonagh CF, Huhalov A, Harms BD, Adams S, Paragas V, Oyama S, et al. Antitumor activity of a novel bispecific antibody that targets the ErbB2/ErbB3 oncogenic unit and inhibits heregulin-induced activation of ErbB3. Mol Cancer Ther 2012; 11:582 - 93; http://dx.doi.org/10.1158/1535-7163.MCT-11-0820; PMID: 22248472
   PubMed Web of Science ®Google Scholar
• Doppalapudi VR, Huang J, Liu D, Jin P, Liu B, Li L, et al. Chemical generation of bispecific antibodies. Proc Natl Acad Sci U S A 2010; 107:22611 - 6; http://dx.doi.org/10.1073/pnas.1016478108; PMID: 21149738
   PubMed Web of Science ®Google Scholar
• Miller BR, Demarest SJ, Lugovskoy A, Huang F, Wu X, Snyder WB, et al. Stability engineering of scFvs for the development of bispecific and multivalent antibodies. Protein Eng Des Sel 2010; 23:549 - 57; http://dx.doi.org/10.1093/protein/gzq028; PMID: 20457695
   PubMed Web of Science ®Google Scholar
• Demarest SJ, Glaser SM. Antibody therapeutics, antibody engineering, and the merits of protein stability. Curr Opin Drug Discov Devel 2008; 11:675 - 87; PMID: 18729019
   PubMed Web of Science ®Google Scholar
• Fitzgerald J, Lugovskoy A. Rational engineering of antibody therapeutics targeting multiple oncogene pathways. MAbs 2011; 3:299 - 309; http://dx.doi.org/10.4161/mabs.3.3.15299; PMID: 21393992
   PubMed Web of Science ®Google Scholar
• Metz S, Haas AK, Daub K, Croasdale R, Stracke J, Lau W, et al. Bispecific digoxigenin-binding antibodies for targeted payload delivery. Proc Natl Acad Sci U S A 2011; 108:8194 - 9; http://dx.doi.org/10.1073/pnas.1018565108; PMID: 21536919
   PubMed Web of Science ®Google Scholar
• Schanzer J, Jekle A, Nezu J, Lochner A, Croasdale R, Dioszegi M, et al. Development of tetravalent, bispecific CCR5 antibodies with antiviral activity against CCR5 monoclonal antibody-resistant HIV-1 strains. Antimicrob Agents Chemother 2011; 55:2369 - 78; http://dx.doi.org/10.1128/AAC.00215-10; PMID: 21300827
   PubMed Web of Science ®Google Scholar
• Digiammarino EL, Harlan JE, Walter KA, Ladror US, Edalji RP, Hutchins CW, et al. Ligand association rates to the inner-variable-domain of a dual-variable-domain immunoglobulin are significantly impacted by linker design. MAbs 2011; 3:487 - 94; http://dx.doi.org/10.4161/mabs.3.5.16326; PMID: 21814039
   PubMed Web of Science ®Google Scholar
• Wu C, Ying H, Grinnell C, Bryant S, Miller R, Clabbers A, et al. Simultaneous targeting of multiple disease mediators by a dual-variable-domain immunoglobulin. Nat Biotechnol 2007; 25:1290 - 7; http://dx.doi.org/10.1038/nbt1345; PMID: 17934452
   PubMed Web of Science ®Google Scholar
• Herrmann T, Grosse-Hovest L, Otz T, Krammer PH, Rammensee HG, Jung G. Construction of optimized bispecific antibodies for selective activation of the death receptor CD95. Cancer Res 2008; 68:1221 - 7; http://dx.doi.org/10.1158/0008-5472.CAN-07-6175; PMID: 18281499
   PubMed Web of Science ®Google Scholar
• Carlring J, De Leenheer E, Heath AW. A novel redox method for rapid production of functional bi-specific antibodies for use in early pilot studies. PLoS One 2011; 6:e22533; http://dx.doi.org/10.1371/journal.pone.0022533; PMID: 21811628
   PubMed Web of Science ®Google Scholar
• De Lau WB, Heije K, Neefjes JJ, Oosterwegel M, Rozemuller E, Bast BJ. Absence of preferential homologous H/L chain association in hybrid hybridomas. J Immunol 1991; 146:906 - 14; PMID: 1899099
   PubMed Web of Science ®Google Scholar
• Ménard S, Canevari S, Colnaghi MI. Hybrid antibodies in cancer diagnosis and therapy. Int J Biol Markers 1989; 4:131 - 4; PMID: 2693537
   PubMedGoogle Scholar
• Renner C, Jung W, Sahin U, Denfeld R, Pohl C, Trümper L, et al. Cure of xenografted human tumors by bispecific monoclonal antibodies and human T cells. Science 1994; 264:833 - 5; http://dx.doi.org/10.1126/science.8171337; PMID: 8171337
   PubMed Web of Science ®Google Scholar
• Lindhofer H, Mocikat R, Steipe B, Thierfelder S. Preferential species-restricted heavy/light chain pairing in rat/mouse quadromas. Implications for a single-step purification of bispecific antibodies. J Immunol 1995; 155:219 - 25; PMID: 7602098
   PubMed Web of Science ®Google Scholar
• Zeidler R, Reisbach G, Wollenberg B, Lang S, Chaubal S, Schmitt B, et al. Simultaneous activation of T cells and accessory cells by a new class of intact bispecific antibody results in efficient tumor cell killing. J Immunol 1999; 163:1246 - 52; PMID: 10415020
   PubMed Web of Science ®Google Scholar
• Chelius D, Ruf P, Gruber P, Plöscher M, Liedtke R, Gansberger E, et al. Structural and functional characterization of the trifunctional antibody catumaxomab. MAbs 2010; 2:309 - 19; http://dx.doi.org/10.4161/mabs.2.3.11791; PMID: 20418662
   PubMed Web of Science ®Google Scholar
• Carter P. Bispecific human IgG by design. J Immunol Methods 2001; 248:7 - 15; http://dx.doi.org/10.1016/S0022-1759(00)00339-2; PMID: 11223065
   PubMed Web of Science ®Google Scholar
• Merchant AM, Zhu Z, Yuan JQ, Goddard A, Adams CW, Presta LG, et al. An efficient route to human bispecific IgG. Nat Biotechnol 1998; 16:677 - 81; http://dx.doi.org/10.1038/nbt0798-677; PMID: 9661204
   PubMed Web of Science ®Google Scholar
• Zhu Z, Presta LG, Zapata G, Carter P. Remodeling domain interfaces to enhance heterodimer formation. Protein Sci 1997; 6:781 - 8; http://dx.doi.org/10.1002/pro.5560060404; PMID: 9098887
   PubMed Web of Science ®Google Scholar
• Ridgway JB, Presta LG, Carter P. ‘Knobs-into-holes’ engineering of antibody CH3 domains for heavy chain heterodimerization. Protein Eng 1996; 9:617 - 21; http://dx.doi.org/10.1093/protein/9.7.617; PMID: 8844834
   PubMedGoogle Scholar
• Atwell S, Ridgway JB, Wells JA, Carter P. Stable heterodimers from remodeling the domain interface of a homodimer using a phage display library. J Mol Biol 1997; 270:26 - 35; http://dx.doi.org/10.1006/jmbi.1997.1116; PMID: 9231898
   PubMed Web of Science ®Google Scholar
• Jin H, Yang R, Zheng Z, Romero M, Ross J, Bou-Reslan H, et al. MetMAb, the one-armed 5D5 anti-c-Met antibody, inhibits orthotopic pancreatic tumor growth and improves survival. Cancer Res 2008; 68:4360 - 8; http://dx.doi.org/10.1158/0008-5472.CAN-07-5960; PMID: 18519697
   PubMed Web of Science ®Google Scholar
• Martens T, Schmidt NO, Eckerich C, Fillbrandt R, Merchant M, Schwall R, et al. A novel one-armed anti-c-Met antibody inhibits glioblastoma growth in vivo. Clin Cancer Res 2006; 12:6144 - 52; http://dx.doi.org/10.1158/1078-0432.CCR-05-1418; PMID: 17062691
   PubMed Web of Science ®Google Scholar
• Surati M, Patel P, Peterson A, Salgia R. Role of MetMAb (OA-5D5) in c-MET active lung malignancies. Expert Opin Biol Ther 2011; 11:1655 - 62; http://dx.doi.org/10.1517/14712598.2011.626762; PMID: 22047509
   PubMed Web of Science ®Google Scholar
• Igawa T, Tsunoda H. Methods for producing polypeptides by regulating polypeptide association. WO2006106905. 2006.
   Google Scholar
• Gunasekaran K, Pentony M, Shen M, Garrett L, Forte C, Woodward A, et al. Enhancing antibody Fc heterodimer formation through electrostatic steering effects: applications to bispecific molecules and monovalent IgG. J Biol Chem 2010; 285:19637 - 46; http://dx.doi.org/10.1074/jbc.M110.117382; PMID: 20400508
   PubMed Web of Science ®Google Scholar
• Moore GL, Bautista C, Pong E, Nguyen DH, Jacinto J, Eivazi A, et al. A novel bispecific antibody format enables simultaneous bivalent and monovalent co-engagement of distinct target antigens. MAbs 2011; 3:546 - 57; http://dx.doi.org/10.4161/mabs.3.6.18123; PMID: 22123055
   PubMed Web of Science ®Google Scholar
• Davis JH, Aperlo C, Li Y, Kurosawa E, Lan Y, Lo KM, et al. SEEDbodies: fusion proteins based on strand-exchange engineered domain (SEED) CH3 heterodimers in an Fc analogue platform for asymmetric binders or immunofusions and bispecific antibodies. Protein Eng Des Sel 2010; 23:195 - 202; http://dx.doi.org/10.1093/protein/gzp094; PMID: 20299542
   PubMed Web of Science ®Google Scholar
• Muda M, Gross AW, Dawson JP, He C, Kurosawa E, Schweickhardt R, et al. Therapeutic assessment of SEED: a new engineered antibody platform designed to generate mono- and bispecific antibodies. Protein Eng Des Sel 2011; 24:447 - 54; http://dx.doi.org/10.1093/protein/gzq123; PMID: 21498564
   PubMed Web of Science ®Google Scholar
• Pack P, Kujau M, Schroeckh V, Knüpfer U, Wenderoth R, Riesenberg D, et al. Improved bivalent miniantibodies, with identical avidity as whole antibodies, produced by high cell density fermentation of Escherichia coli. Biotechnology (N Y) 1993; 11:1271 - 7; PMID: 7764189
   PubMedGoogle Scholar
• Kostelny SA, Cole MS, Tso JY. Formation of a bispecific antibody by the use of leucine zippers. J Immunol 1992; 148:1547 - 53; PMID: 1531669
   PubMed Web of Science ®Google Scholar
• Christensen EH, Eaton DL, Vendel AC, Wranik B. Coiled coil and/or tether containing protein complexes and uses thereof. WO2011034605. 2011.
   Google Scholar
• Houtzager E, Pinto RD, Logtenberg T, Throsby M, Kramer RA, De Kruif CA. Antibody producing non-mammals. WO2009157771. 2009.
   Google Scholar
• McWhirter J, Macdonald L, Stevens S, Davis S, Buckler DR, Murphy AJ. Common light chain mouse. WO2011097603. 2011.
   Google Scholar
• Jackman J, Chen Y, Huang A, Moffat B, Scheer JM, Leong SR, et al. Development of a two-part strategy to identify a therapeutic human bispecific antibody that inhibits IgE receptor signaling. J Biol Chem 2010; 285:20850 - 9; http://dx.doi.org/10.1074/jbc.M110.113910; PMID: 20444694
   PubMed Web of Science ®Google Scholar
• Igawa T, Tsunoda H, Kikuchi Y, Yoshida M, Tanaka M, Koga A, et al. VH/VL interface engineering to promote selective expression and inhibit conformational isomerization of thrombopoietin receptor agonist single-chain diabody. Protein Eng Des Sel 2010; 23:667 - 77; http://dx.doi.org/10.1093/protein/gzq034; PMID: 20576629
   PubMed Web of Science ®Google Scholar
• Schaefer W, Regula JT, Bähner M, Schanzer J, Croasdale R, Dürr H, 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; http://dx.doi.org/10.1073/pnas.1019002108; PMID: 21690412
   PubMed Web of Science ®Google Scholar
• Cain C. Crossing over to bispecificity. SciBX 2011; 4:1 - 4
   Google Scholar
• Rennel ES, Regula JT, Harper SJ, Thomas M, Klein C, Bates DO. A human neutralizing antibody specific to Ang-2 inhibits ocular angiogenesis. Microcirculation 2011; 18:598 - 607; http://dx.doi.org/10.1111/j.1549-8719.2011.00120.x; PMID: 21851472
   PubMed Web of Science ®Google Scholar
• Davis S, Smith E, Macdonald D, Olson KL. Readily isolated bispecific antibodies with native immunoglobulin format. WO2010151792. 2011.
   Google Scholar
• Igawa T, Tsunoda H. Antibody Modification Method For Purifying Bispecific Antibody. WO2007114325. 2011.
   Google Scholar
• Yu YJ, Zhang Y, Kenrick M, Hoyte K, Luk W, Lu Y, et al. Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target. Sci Transl Med 2011; 3:84ra44; http://dx.doi.org/10.1126/scitranslmed.3002230; PMID: 21613623
   PubMed Web of Science ®Google Scholar
• Stubenrauch K, Wessels U, Regula JT, Kettenberger H, Schleypen J, Kohnert U. Impact of molecular processing in the hinge region of therapeutic IgG4 antibodies on disposition profiles in cynomolgus monkeys. Drug Metab Dispos 2010; 38:84 - 91; http://dx.doi.org/10.1124/dmd.109.029751; PMID: 19850673
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Buijsse AO, van den Bremer ET, Verwilligen AY, Bleeker WK, Thorpe SJ, et al. Therapeutic IgG4 antibodies engage in Fab-arm exchange with endogenous human IgG4 in vivo. Nat Biotechnol 2009; 27:767 - 71; http://dx.doi.org/10.1038/nbt.1553; PMID: 19620983
   PubMed Web of Science ®Google Scholar
• van der Neut Kolfschoten M, Schuurman J, Losen M, Bleeker WK, Martínez-Martínez P, Vermeulen E, et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science 2007; 317:1554 - 7; http://dx.doi.org/10.1126/science.1144603; PMID: 17872445
   PubMed Web of Science ®Google Scholar
• Schuurman J, Vink T, Van De Winkel J, Labrijn AF, Aalberse R, Van Der Neut Kolfschoten M et al. Heterodimeric Antibody Fc-Containing Proteins And Methods For Production Thereof. WO2011131746. 2011.
   Google Scholar
• Strop P, Ho WH, Boustany LM, Abdiche YN, Lindquist KC, Farias SE, et al. Generating bispecific human IgG1 and IgG2 antibodies from any antibody pair. J Mol Biol 2012; 420:204 - 19; http://dx.doi.org/10.1016/j.jmb.2012.04.020; PMID: 22543237
   PubMed Web of Science ®Google Scholar
• Fagète S, Fischer N. Smarter drugs: a focus on pan-specific monoclonal antibodies. BioDrugs 2011; 25:357 - 64; http://dx.doi.org/10.2165/11594690-000000000-00000; PMID: 22050338
   PubMed Web of Science ®Google Scholar
• Buatois V, Fagète S, Magistrelli G, Chatel L, Fischer N, Kosco-Vilbois MH, et al. Pan-CC chemokine neutralization restricts splenocyte egress and reduces inflammation in a model of arthritis. J Immunol 2010; 185:2544 - 54; http://dx.doi.org/10.4049/jimmunol.1000182; PMID: 20644170
   PubMed Web of Science ®Google Scholar
• Alejo A, Ruiz-Argüello MB, Ho Y, Smith VP, Saraiva M, Alcami A. A chemokine-binding domain in the tumor necrosis factor receptor from variola (smallpox) virus. Proc Natl Acad Sci U S A 2006; 103:5995 - 6000; http://dx.doi.org/10.1073/pnas.0510462103; PMID: 16581912
   PubMed Web of Science ®Google Scholar
• Fagète S, Rousseau F, Magistrelli G, Gueneau F, Ravn U, Kosco-Vilbois MH, et al. Dual specificity of anti-CXCL10-CXCL9 antibodies is governed by structural mimicry. J Biol Chem 2012; 287:1458 - 67; http://dx.doi.org/10.1074/jbc.M111.253658; PMID: 22041899
   PubMed Web of Science ®Google Scholar
• Bostrom J, Haber L, Koenig P, Kelley RF, Fuh G. High affinity antigen recognition of the dual specific variants of herceptin is entropy-driven in spite of structural plasticity. PLoS One 2011; 6:e17887; http://dx.doi.org/10.1371/journal.pone.0017887; PMID: 21526167
   PubMed Web of Science ®Google Scholar
• Bostrom J, Yu SF, Kan D, Appleton BA, Lee CV, Billeci K, et al. Variants of the antibody herceptin that interact with HER2 and VEGF at the antigen binding site. Science 2009; 323:1610 - 4; http://dx.doi.org/10.1126/science.1165480; PMID: 19299620
   PubMed Web of Science ®Google Scholar
• Bostrom J, Lee CV, Haber L, Fuh G. Improving antibody binding affinity and specificity for therapeutic development. [xiii.] Methods Mol Biol 2009; 525:353 - 76, xiii; http://dx.doi.org/10.1007/978-1-59745-554-1_19; PMID: 19252851
   PubMedGoogle Scholar
• Schaefer G, Haber L, Crocker LM, Shia S, Shao L, Dowbenko D, et al. A two-in-one antibody against HER3 and EGFR has superior inhibitory activity compared with monospecific antibodies. Cancer Cell 2011; 20:472 - 86; http://dx.doi.org/10.1016/j.ccr.2011.09.003; PMID: 22014573
   PubMed Web of Science ®Google Scholar
• Wozniak-Knopp G, Bartl S, Bauer A, Mostageer M, Woisetschläger M, Antes B, et al. Introducing antigen-binding sites in structural loops of immunoglobulin constant domains: Fc fragments with engineered HER2/neu-binding sites and antibody properties. Protein Eng Des Sel 2010; 23:289 - 97; http://dx.doi.org/10.1093/protein/gzq005; PMID: 20150180
   PubMed Web of Science ®Google Scholar
• Huang H, Lai JY, Do J, Liu D, Li L, Del Rosario J, et al. Specifically targeting angiopoietin-2 inhibits angiogenesis, Tie2-expressing monocyte infiltration, and tumor growth. Clin Cancer Res 2011; 17:1001 - 11; http://dx.doi.org/10.1158/1078-0432.CCR-10-2317; PMID: 21233403
   PubMed Web of Science ®Google Scholar