The development of bispecific hexavalent antibodies as a novel class of DOCK-AND-LOCK™ (DNL™) complexes

Antibodies

Volumn 2, Issue 2, 2013, Pages 353-370

  Chang, Chien Hsing ^a,b   Rossi, Edmund A ^a,b   Wang, Yang ^a   Cardillo, Thomas M ^a   Goldenberg, David M ^a,b,c  

^a IMMUNOMEDICS INC   (United States)

^b IBC Pharmaceuticals Inc   (United States)

^c GARDEN STATE CANCER CENTER   (United States)

Author keywords

Antibodies; Bispecific; Cancer; Conjugation; DNL ; Hexavalent; Site specific

Indexed keywords

BISPECIFIC ANTIBODY; BISPECIFIC HEXAVALENT ANTIBODY; CD20 ANTIBODY; CD20 ANTIGEN; CD74 ANTIBODY; CD74 ANTIGEN; EPRATUZUMAB; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN KAPPA CHAIN; LABETUZUMAB; MILATUZUMAB; RITUXIMAB; UNCLASSIFIED DRUG; VELTUZUMAB;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY PRODUCTION; ANTINEOPLASTIC ACTIVITY; BINDING AFFINITY; COMPLEMENT DEPENDENT CYTOTOXICITY; COMPUTER PROGRAM; DOCK AND LOCK METHOD; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; GEL PERMEATION CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SURFACE PLASMON RESONANCE;

EID: 84894609882     PISSN: 20734468     EISSN: None     Source Type: Journal    
DOI: 10.3390/antib2020353     Document Type: Review

References (66)

1. Reichert, J. M. What are the antibodies to watch in 2013? mAbs 2013, 5, 1-4.
2. Leonard, J. P.; Coleman, M.; Ketas, J.; Ashe, M.; Fiore, J. M.; Furman, R. R.; Niesvizky, R.; Shore, T.; Chadburn, A.; Horne, H.; et al. Combination antibody therapy with epratuzumab and rituximab in relapsed or refractory non-Hodgkin's lymphoma. J. Clin. Oncol. 2005, 23, 5044-5051.
3. Strauss, S. J.; Morschhauser, F.; Rech, J.; Repp, R.; Solal-Celigny, P.; Zinzani, P. L.; Engert, A.; Coiffier, B.; Hoelzer, D. F.; Wegener, W. A.; et al. Multicenter phase II trial of immunotherapy with the humanized anti-CD22 antibody, epratuzumab, in combination with rituximab, in refractory or recurrent non-Hodgkin's lymphoma. J. Clin. Oncol. 2006, 24, 3880-3886.
4. Leonard, J. P.; Schuster, S. J.; Emmanouilides, C.; Couture, F.; Teoh, N.; Wegener, W. A.; Coleman, M.; Goldenberg, D. M. Durable complete responses from therapy with combined epratuzumab and rituximab: Final results from an international multicenter, phase 2 study in recurrent, indolent, non-Hodgkin lymphoma. Cancer 2008, 113, 2714-2723.
5. Tonra, J. R.; Corcoran, E.; Deevi, D. S.; Steiner, P.; Kearney, J.; Li, H.; Ludwig, D. L.; Zhu, Z.; Witte, L.; Surguladze, D.; et al. Prioritization of EGFR/IGF-IR/VEGFR2 combination targeted therapies utilizing cancer models. Anticancer Res. 2009, 29, 1999-2008.
6. Alinari, L.; Yu, B.; Christian, B. A.; Yan, F.; Shin, J.; Lapalombella, R.; Hertlein, E.; Lustberg, M. E.; Quinion, C.; Zhang, X.; et al. Combination anti-CD74 (milatuzumab) and anti-CD20 (rituximab) monoclonal antibody therapy has in vitro and in vivo activity in mantle cell lymphoma. Blood 2011, 117, 4530-4541.
7. Loisel, S.; Andre, P. A.; Golay, J.; Buchegger, F.; Kadouche, J.; Cerutti, M.; Bologna, L.; Kosinski, M.; Viertl, D.; Delaloye, A. B.; et al. Antitumour effects of single or combined monoclonal antibodies directed against membrane antigens expressed by human B cells leukaemia. Mol. Cancer 2011, 10, 42.
8. Skartved, N. J.; Jacobsen, H. J.; Pedersen, M. W.; Jensen, P. F.; Sen, J. W.; Jorgensen, T. K.; Hey, A.; Kragh, M. Preclinical pharmacokinetics and safety of Sym004: A synergistic antibody mixture directed against epidermal growth factor receptor. Clin. Cancer Res. 2011, 17, 5962-5972.
9. Fuentes, G.; Scaltriti, M.; Baselga, J.; Verma, C. S. Synergy between trastuzumab and pertuzumab for human epidermal growth factor 2 (Her2) from colocalization: An in silico based mechanism. Breast Cancer Res. 2011, 13, R54.
10. Dong, J.; Demarest, S. J.; Sereno, A.; Tamraz, S.; Langley, E.; Doern, A.; Snipas, T.; Perron, K.; Joseph, I.; Glaser, S. M.; et al. Combination of two insulin-like growth factor-I receptor inhibitory antibodies targeting distinct epitopes leads to an enhanced antitumor response. Mol. Cancer Ther. 2010, 9, 2593-2604.
11. Kontermann, R. B. Dual targeting strategies with bispecific antibodies. mAbs 2012, 4, 182-197.
12. Schubert, I.; Stein, C.; Fey, G. H. Dual-targeting for the elimination of cancer cells with increased selectivity. Antibodies 2012, 1, 1-18.
13. van der Neut Kolfschoten, M.; Schuurman, J.; Losen, M.; Bleeker, W. K.; Martinez-Martinex, P.; Vermeulen, E.; den Bleker, T. H.; Wiegman, L.; Vink, T.; Aarden, L. A.; et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science 2007, 317, 1554-1557.
14. Burton, D. R.; Wilson, I. A. Immunology. Square-dancing antibodies. Science 2007, 317, 1507-1508.
15. Labrijn, A. F.; Buijsse, A. O.; van den Bremer, E. T. J.; Verwilligen, A. Y. W.; Bleeker, W. K.; Thorpe, S. J.; Killestein, J.; Polman, C. H.; Aalberse, R. C.; Schuurman, J.; et al. Therapeutic IgG4 antibodies engage in Fab-arm exchange with endogenous human IgG4 in vivo. Nat. Biotechnol. 2009, 27, 767-771.
16. Milstein, C.; Cuello, A. C. Hybrid hybridomas and their use in immunochemistry. Nature 1983, 305, 537-540.
17. Staerz, U. D.; Bevan, M. J. Hybrid hybridoma producing a bispecific monoclonal antibody that can focus effector T-cell activity. Proc. Nat. Acad. Sci. USA 1986, 83, 1453-1457.
18. Perez, P.; Hoffman, R. W.; Shaw, S.; Bluestone, J. A.; Segal, D. M. Specific targeting of cytotoxic T cells by anti-T3 linked to anti-target cell antibody. Nature 1985, 316, 354-356.
19. Brennan, M.; Davison, P. F.; Paulus, H. Preparation of bispecific antibodies by chemical recombination of monoclonal immunoglobulin G1 fragments. Science 1985, 229, 81-83.
20. Glennie, M. J.; McBride, H. M.; Worth, A. T.; Stevenson, G. T. Preparation and performance of bispecific F(ab' gamma)2 antibody containing thioether-linked Fab' gamma fragments. J. Immunol. 1987, 139, 2367-2375.
21. Kriangkum, J.; Xu, B.; Nagata, L. P.; Fulton, R. E.; Suresh, M. R. Bispecific and bifunctional single chain recombinant antibodies. Biomol. Eng. 2001, 18, 31-40.
22. Muller, D.; Kontermann, R. E. Recombinant bispecific antibodies for cellular cancer immunotherapy. Curr. Opin. Mol. Ther. 2007, 9, 319-326.
23. Hollander, N. Bispecific antibodies for cancer therapy. Immunotherapy 2009, 1, 211-222.
24. Marvin, J. S.; Zhu, Z. Recombinant approaches to IgG-like bispecific antibodies. Acta Pharmacol. Sin. 2005, 26, 649-658.
25. Coloma, M. J.; Morrison, S. L. Design and production of novel tetravalent bispecific antibodies. Nat. Biotechnol. 1997, 15, 159-163.
26. Lu, D.; Zhang, H.; Ludwig, D.; Persaud, A.; Jimenez, X.; Burtrum, D.; Balderes, P.; Liu, M.; Bohlen, P.; Witte, L.; et al. Simultaneous blockade of both the epidermal growth factor receptor and the insulin-like growth factor receptor signaling pathways in cancer cells with a fully human recombinant bispecific antibody. J. Biol. Chem. 2004, 279, 2856-2865.
27. Lu, D.; Zhang, H.; Koo, H.; Tonra, J.; Balderes, P.; Prewett, M.; Corcoran, E.; Mangalampalli, V.; Bassi, R.; Anselma, D.; et al. A fully human recombinant IgG-like bispecific antibody to both the epidermal growth factor receptor and the insulin-like growth factor receptor for enhanced antitumor activity. J. Biol. Chem. 2005, 280, 19665-19672.
28. Shen, J.; Vil, M. D.; Jimenez, X.; Iacolina, M.; Zhang, H.; Zhu, Z. Single variable domain-IgG fusion. A novel recombinant approach to Fc domain-containing bispecific antibodies. J. Biol. Chem. 2006, 281, 10706-10714.
29. Shen, J.; Vil, M. D.; Jimenez, X.; Zhang, H.; Lacolina, M.; Mangalampalli, V.; Balderes, P.; Ludwig, D. L.; Zhu, Z. Single variable domain antibody as a versatile building block for the construction of IgG-like bispecific antibodies. J. Immunol. Methods 2007, 318, 65-74.
30. Asano, R.; Watanabe, Y.; Kawaguchi, H.; Fukuzawa, H.; Nakanishi, T.; Umetzu, M.; Hayashi, H.; Katayose, Y.; Unno, M.; Kudo, T.; et al. Highly effective recombinant format of a humanized IgG-like bispecific antibody for cancer immunotherapy with retargeting of lymphocytes to tumor cells. J. Biol. Chem. 2007, 282, 27659-27665.
31. Wu, C.; Ying, H.; Grinnell, C.; Bryant, S.; Miller, R.; Clabbers, A.; Bose, S.; McCarthy, D.; Zhu, R. R.; Santora, L.; et al. Simultaneous targeting of multiple disease mediators by a dual-variable-domain immunoglobulin. Nat. Biotechnol. 2007, 25, 1290-1297.
32. Rossi, E. A.; Goldenberg, D. M.; Cardillo, T. M.; McBride, W. J.; Sharkey, R. M.; Chang, C. H. Stably tethered multifunctional structures of defined composition made by the dock and lock method for use in cancer targeting. Proc. Natl. Acad. Sci. USA 2006, 103, 6841-6846.
33. Chang, C. H.; Rossi, E. A.; Goldenberg, D. M. The dock and lock method: A novel platform technology for building multivalent, multifunctional structures of defined composition with retained bioactivity. Clin. Cancer Res. 2007, 13, 5586s-5591s.
34. Rossi, E. A.; Goldenberg, D. M.; Chang, C. H. Complex and defined biostructures with the dock-and-lock method. Trends Pharmacol. Sci. 2012, 33, 474-481.
35. Rossi, E. A.; Goldenberg, D. M.; Chang, C. H. The Dock-and-Lock method combines recombinant engineering with site-specific covalent conjugation to generate multifunctional structures. Bioconjug. Chem. 2012, 23, 309-323.
36. Rossi, E. A.; Goldenberg, D. M.; Cardillo, T. M.; Stein, R.; Chang, C. H. Hexavalent bispecific antibodies represent a new class of anticancer therapeutics: 1. Properties of anti-CD20/CD22 antibodies in lymphoma. Blood 2009, 113, 6161-6171.
37. Gupta, P.; Goldenberg, D. M.; Rossi, E. A.; Chang, C. H. Multiple signaling pathways induced by hexavalent, monospecific, anti-CD20 and hexavalent, bispeciifc, anti-CD20/CD22 humanized antibodies correlate with enhanced cytotoxicity to B-cell lymphomas and leukemia. Blood 2010, 116, 3258-3267.
38. Gupta, P.; Goldenberg, D. M.; Rossi, E. A.; Cardillo, T. M.; Byrd, J. C.; Muthusamy, N.; Furman, R. R.; Chang, C. H. Dual-targeting immunotherapy of lymphoma: Potent cytotoxicity of anti-CD20/CD74 bispecific antibodies in mantle cell and other lymphomas. Blood 2012, 119, 3767-3778.
39. Chang, C. H.; Rossi, E. A.; Sharkey, R. M.; Goldenberg, D. M. The Dock-and-Lock (DNL) approach to novel bispecific antibodies. In Bispecific Antibodies; Kontermann, R. E., Ed.; Springer-Verlag: Berlin/Heidelberg, Germany, 2011; Chapter 12, pp. 199-216.
40. Rossi, E. A.; Chang, C. H.; Cardillo, T. M.; Goldenberg, D. M. Optimization of multivalent bispecific antibodies and immunocytokines with improved in vivo properties. Bioconjug. Chem. 2013, 24, 63-71.
41. Baillie, G. S.; Scott, J. D.; Houslay, M. D. Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett. 2005, 579, 3264-3270.
42. Wong, W.; Scott, J. D. AKAP signaling complexes: Focal points in space and time. Nat. Rev. Mol. Cell Biol. 2004, 5, 959-970.
43. Newlon, M. G.; Roy, M.; Morikis, D.; Hausken, Z. E.; Coghlan, V.; Scott, J. D.; Jennings, P. A. The molecular basis for protein kinase A anchoring revealed by solution NMR. Nat. Struct. Biol. 1999, 6, 222-227.
44. Carr, D. W.; Stofko-Hahn, R. E.; Fraser, I. D.; Bishop, S. M.; Acott, T. S.; Brennan, R. G.; Scott, J. D. Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J. Biol. Chem. 1991, 266, 14188-14192.
45. Colledge, M.; Scott, J. D. AKAPs: From structure to function. Trends Cell Biol. 1999, 9, 216-222.
46. Newlon, M. G.; Roy, M.; Morikis, D.; Carr, D. W.; Westphal, R. R.; Scott, J. D.; Jennings, P. A. A novel mechanism of PKA anchoring revealed by solution structures of anchoring complexes. EMBO J. 2001, 20, 1651-1662.
47. Rossi, E. A.; Sharkey, R. M.; McBride, W.; Karacay, H.; Zeng, L.; Hansen, H. J.; Goldenberg, D. M.; Chang, C. H. Development of new multivalent-bispecific agents for pretargeting tumor localization and therapy. Clin. Cancer Res. 2003, 9, 3886s-3896s.
48. Rossi, E. A.; Chang, C. H.; Losman, M. J.; Sharkey, R. M.; Karacay, H.; McBride, W.; Cardillo, T. M.; Hansen, H. J; Qu, Z.; Horak, I. D.; et al. Pretargeting of carcinoembryonic antigen-expressing cancers with a trivalent bispecific fusion protein produced in myeloma cells. Clin. Cancer Res. 2005, 11, 7122s-7129s.
49. Sharkey, R. M.; Cardillo, T. M.; Rossi, E. A.; Chang, C. H.; Karacay, H.; McBride, W. J.; Hansen, H. J.; Horak, I. D.; Goldenberg, D. M. Signal amplification in molecular imaging by pretargeting a multivalent, bispecific antibody. Nat. Med. 2005, 11, 1250-1255.
50. Alto, N. M.; Soderling, S. H.; Hoshi, N.; Langeberg, L. K.; Fayos, R.; Jennings, P. A.; Scott, J. D. Bioinformatic design of A-kinase anchoring protein-in silico: A potent and selective peptide antagonist of type II protein kinase A anchoring. Proc. Natl. Acad. Sci. USA 2003, 100, 4445-4450.
51. Burns-Hamuro, L. L.; Ma, Y.; Kammerer, S.; Reineke, U.; Self, C.; Cook, C.; Olson, G. L.; Cantor, C. R.; Braun, A.; Taylor, S. S. Designing isoform-specific peptide disruptors of protein kinase A localization. Proc. Natl. Acad. Sci. USA 2003, 100, 4072-4077.
52. Rossi, E. A.; Goldenberg, D. M.; Cardillo, T. M.; Stein, R.; Chang, C. H. CD20-targeted tetrameric interferon-α, a novel and potent immunocytokine for the therapy of B-cell lymphomas. Blood 2009, 114, 3864-3871.
53. Binz, H. K.; Pluckthun, A. Engineered proteins as specific binding reagents. Curr. Opin. Biotechnol. 2005, 16, 459-469.
54. Binz, H. K.; Amstutz, P.; Pluckthun, A. Engineering novel binding proteins from nonimmunoglobulin domains. Nat. Biotechnol. 2005, 23, 1257-1268.
55. Hey, T.; Fiedler, E.; Rudolph, R.; Fiedler, M. Artificial, non-antibody binding proteins for pharmaceutical and industrial applications. Trends Biotechnol. 2005, 23, 514-522.
56. Hosse, R. J.; Rothe, A.; Power, B. E. A new generation of protein display scaffold for molecular recognition. Protein Sci. 2006, 15, 14-27.
57. Chang, C. H.; Rossi, E. A.; Cardillo, T. M.; Nordstrom, D. L.; McBride, W. J.; Goldenberg, D. M. A new method to produce monoPEGylated dimeric cytokines shown with human interferon-α2b. Bioconjug. Chem. 2009, 20, 1899-1907.
58. Rossi, E. A.; Goldenberg, D. M.; Cardillo, T. M.; Stein, R.; Wang, Y.; Chang, C. H. Novel designs of multivalent anti-CD20 humanized antibodies as improved lymphoma therapeutics. Cancer Res. 2008, 68, 8384-8392.
59. Chang, C. H.; Wang, Y.; Trisal, P.; Li, R.; Rossi, D. L.; Nair, A.; Gupta, P.; Losman, M.; Cardillo, T. M.; Rossi, E. A.; et al. Evaluation of a novel hexavalent humanized anti-IGF-1R antibody and its bivalent parental IgG in diverse cancer cell lines. PLoS One 2012, 7, e44235.
60. Stein, R.; Qu, Z.; Chen, S.; Rosario, A.; Shi, V.; Hayes, M.; Horak, I. D.; Hansen, H. J.; Goldenberg, D. M. Characterization of a new humanized anti-CD20 monoclonal antibody, IMMU-106, and Its use in combination with the humanized anti-CD22 antibody, epratuzumab, for the therapy of non-Hodgkin's lymphoma. Clin. Cancer Res. 2004, 10, 2868-2878.
61. Gold, D. V.; Goldenberg, D. M.; Karacay, H.; Rossi, E. A.; Chang, C. H.; Cardillo, T. M.; McBride, W. J.; Sharkey, R. M. A novel bispecific, trivalent antibody construct for targeting pancreatic carcinoma. Cancer Res. 2008, 68, 4819-4826.
62. Sharkey, R. M.; van Rij, C. M.; Karacay, H.; Rossi, E. A.; Frielink, C.; Regino, C.; Cardillo, T. M.; McBride, W. J.; Chang, C. H.; et al. A new tri-Fab bispecific antibody for pretargeting Trop-2-expressing epithelial cancers. J. Nucl. Med. 2012, 53, 1625-1632.
63. Rossi, E. A.; Rossi, D. L.; Cardillo, T. M.; Stein, R.; Goldenberg, D. M.; Chang, C. H. Preclinical studies on targeted delivery of multiple interferon-alpha-2b to HLA-DR in diverse hematological cancers. Blood 2011, 118, 1877-1884.
64. Rossi, E. A.; Rossi, D. L.; Stein, R.; Goldenberg, D. M.; Chang, C. H. A bispecific antibody-IFN2b immunocytokine targeting CD20 and HLA-DR is highly toxic to human lymphoma and multiple myeloma cells. Cancer Res. 2010, 70, 7600-7609.
65. Chang, C. H.; Hinkula, J.; Loo, M.; Falkeborn, T.; Li, R.; Cardillo, T. M.; Rossi, E. A.; Goldenberg, D. M.; Wahren, B. A novel class of anti-HIV agents with multiple copies of enfuvirtide enhances inhibition of viral replication and cellular transmission in vitro. PLoS One 2012, 7, e41235.
66. Blanco-Toribio, A.; Sainz-Pastor, N.; Álvarez-Cienfuegos, A.; Merino, N.; Cuesta, A. M.; Sánchez-Martín, D.; Bonet, J.; Santos-Valle, P.; Sanz, L.; Oliva, B.; et al. Generation and characterization of monospecific and bispecific hexavalanet trimerbodies. mAbs 2013, 5, 70-79.