Development of a human IgG4 bispecific antibody for dual targeting of interleukin-4 (IL-4) and interleukin-13 (IL-13) cytokines

Journal of Biological Chemistry

Volumn 288, Issue 37, 2013, Pages 26583-26593

  Spiess, Christoph ^a   Bevers, Jack ^a   Jackman, Janet ^b   Chiang, Nancy ^a   Nakamura, Gerald ^a   Dillon, Michael ^a   Liu, Hongbin ^c   Molina, Patricia ^c   Elliott, J Michael ^d   Shatz, Whitney ^d   Scheer, Justin M ^d   Giese, Glen ^e   Persson, Josefine ^e   Zhang, Yin ^a   Dennis, Mark S ^a   Giulianotti, James ^f   Gupta, Prateek ^f   Reilly, Dorothea ^f   Palma, Enzo ^f   Wang, Jianyong ^f   Stefanich, Eric ^f   Scheerens, Heleen ^a   Fuh, Germaine ^a   Wu, Lawren C ^c   more..

^a GENENTECH INC   (United States)

^b Departments of Immunology   (United States)

^c Departments of Protein Analytical Chemistry   (United States)

^d Departments of Protein Chemistry   (United States)

^e Departments of Development   (United States)

^f Early Stage Cell Culture ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINES; IN-VITRO; IN-VIVO; INTERLEUKIN-13; INTERLEUKIN-4;

BIOCHEMISTRY; BIOLOGY;

ANTIBODIES;

IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G4; IMMUNOGLOBULIN G4 ANTIBODY; INTERLEUKIN 13; INTERLEUKIN 13 ANTIBODY; INTERLEUKIN 4; INTERLEUKIN 4 ANTIBODY; LEBRIKIZUMAB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTICLE; BINDING AFFINITY; CELL PROLIFERATION; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG CLEARANCE; DRUG HALF LIFE; DRUG PURIFICATION; DRUG TISSUE LEVEL; FEMALE; GEL PERMEATION CHROMATOGRAPHY; HAPLORHINI; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TARGETING; SEQUENCE HOMOLOGY; SINGLE DRUG DOSE; SURFACE PLASMON RESONANCE;

ANTIBODY ENGINEERING; ASTHMA; CYTOKINE; IMMUNOGLOBULIN; KNOBS-INTO-HOLES; LEBRIKIZUMAB; LUNG; PROTEIN ASSEMBLY;

ANIMALS; ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULIN G; INTERLEUKIN-13; INTERLEUKIN-4; LUNG; MACACA FASCICULARIS; MALE; MICE; MICE, INBRED BALB C; PLASMIDS; PROTEIN ENGINEERING; SURFACE PLASMON RESONANCE;

EID: 84884194586     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.480483     Document Type: Article

References (42)

1. Kontermann, R. (2012) Dual targeting strategies with bispecific antibodies. MAbs 4, 182-197
2. Dhimolea, E., and Reichert, J. M. (2012) World Bispecific Antibody Summit, September 27-28, 2011, Boston, MA. MAbs 4, 4-13
3. Chelius, D., Ruf, P., Gruber, P., Plöscher, M., Liedtke, R., Gansberger, E., Hess, J., Wasiliu, M., and Lindhofer, H. (2010) Structural and functional characterization of the trifunctional antibody catumaxomab. MAbs 2, 309-319
4. Dennis, M. S. (2002) Albumin binding as a general strategy for improving the pharmacokinetics of proteins. J. Biol. Chem. 277, 35035-35043
5. Atwell, S., Ridgway, J. B., Wells, J. A., and Carter, P. (1997) Stable heterodimers from remodeling the domain interface of a homodimer using a phage display library. J. Mol. Biol. 270, 26-35
6. Ridgway, J. B., Presta, L. G., and Carter, P. (1996) "Knobs-into- holes" engineering of antibody CH3 domains for heavy chain heterodimerization. Protein Eng. 9, 617-621
7. Davis, J. H., Aperlo, C., Li, Y., Kurosawa, E., Lan, Y., Lo, K.-M., and Huston, J. S. (2010) 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. 23, 195-202
8. Gunasekaran, K., Pentony, M., Shen, M., Garrett, L., Forte, C., Woodward, A., Ng, S. B., Born, T., Retter, M., Manchulenko, K., Sweet, H., Foltz, I. N., Wittekind, M., and Yan, W. (2010) Enhancing antibody Fc heterodimer formation through electrostatic steering effects. Applications to bispecific molecules and monovalent IgG. J. Biol. Chem. 285, 19637-19646
9. Strop, P., Ho, W.-H., Boustany, L. M., Abdiche, Y. N., Lindquist, K. C., Farias, S. E., Rickert, M., Appah, C. T., Pascua, E., Radcliffe, T., Sutton, J., Chaparro-Riggers, J., Chen, W., Casas, M. G., Chin, S. M., Wong, O. K., Liu, S.-H., Vergara, G., Shelton, D., Rajpal, A., and Pons, J. (2012) Generating bispecific human IgG1 and IgG2 antibodies from any antibody pair. J. Mol. Biol. 420, 204-219
10. Labrijn, A. F., Meesters, J. I., de Goeij, B. E., van den Bremer, E. T., Neijssen, J., van Kampen, M. D., Strumane, K., Verploegen, S., Kundu, A., Gramer, M. J., van Berkel, P. H., van de Winkel, J. G., Schuurman, J., and Parren, P. W. (2013) Efficient generation of stable bispecific IgG1 by controlled Fab-arm exchange. Proc. Natl. Acad. Sci. U.S.A. 110, 5145-5150
11. Merchant, A. M., Zhu, Z., Yuan, J. Q., Goddard, A., Adams, C. W., Presta, L. G., and Carter, P. (1998) An efficient route to human bispecific IgG. Nat. Biotechnol. 16, 677-681
12. Jackman, J., Chen, Y., Huang, A., Moffat, B., Scheer, J. M., Leong, S. R., Lee, W. P., Zhang, J., Sharma, N., Lu, Y., Iyer, S., Shields, R. L., Chiang, N., Bauer, M. C., Wadley, D., Roose-Girma, M., Vandlen, R., Yansura, D. G., Wu, Y., and Wu, L. C. (2010) Development of a two-part strategy to identify a therapeutic human bispecific antibody that inhibits IgE receptor signaling. J. Biol. Chem. 285, 20850-20859
13. Wranik, B. J., Christensen, E. L., Schaefer, G., Jackman, J. K., Vendel, A. C., and Eaton, D. (2012) LUZ-Y, a novel platform for the mammalian cell production of full-length IgG-bispecific antibodies. J. Biol. Chem. 287, 43331-43339
14. Schaefer, W., Regula, J. T., Bähner, M., Schanzer, J., Croasdale, R., Dürr, H., Gassner, C., Georges, G., Kettenberger, H., Imhof-Jung, S., Schwaiger, M., Stubenrauch, K. G., Sustmann, C., Thomas, M., Scheuer, W., and Klein, C. (2011) Immunoglobulin domain crossover as a generic approach for the production of bispecific IgG antibodies. Proc. Natl. Acad. Sci. U.S.A. 108, 11187-11192
15. Spiess, C., Merchant, M., Huang, A., Zheng, Z., Yang, N.-Y., Peng, J., Ellerman, D., Shatz, W., Reilly, D., Yansura, D. G., and Scheer, J. M. (2013) Bispecific antibodies with natural architecture produced by co-culture of bacteria expressing two distinct half-antibodies. Nat. Biotechnol. 31, 753-758
16. Yu, Y. J., Zhang, Y., Kenrick, M., Hoyte, K., Luk, W., Lu, Y., Atwal, J., Elliott, J. M., Prabhu, S., Watts, R. J., and Dennis, M. S. (2011) Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target. Sci. Transl. Med. 3, 84ra44
17. Hershey, G. K. (2003) IL-13 receptors and signaling pathways. An evolving web. J. Allergy Clin. Immunol. 111, 677-690 ; quiz 691
18. Wynn, T. A. (2003) IL-13 effector functions. Annu. Rev. Immunol. 21, 425-456
19. LaPorte, S. L., Juo, Z. S., Vaclavikova, J., Colf, L. A., Qi, X., Heller, N. M., Keegan, A. D., and Garcia, K. C. (2008) Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132, 259-272
20. Mueller, T. D., Zhang, J.-L., Sebald, W., and Duschl, A. (2002) Structure, binding, and antagonists in the IL-4/IL-13 receptor system. Biochim. Biophys. Acta 1592, 237-250
21. Nelms, K., Keegan, A. D., Zamorano, J., Ryan, J. J., and Paul, W. E. (1999) The IL-4 receptor. Signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17, 701-738
22. Wills-Karp, M. (2004) Interleukin-13 in asthma pathogenesis. Immunol. Rev. 202, 175-190
23. Brightling, C. E., Saha, S., and Hollins, F. (2010) Interleukin-13. Prospects for new treatments. Clin. Exp. Allergy 40, 42-49
24. Finkelman, F. D., Hogan, S. P., Hershey, G. K., Rothenberg, M. E., and Wills-Karp, M. (2010) Importance of cytokines in murine allergic airway disease and human asthma. J. Immunol. 184, 1663-1674
25. Maes, T., Joos, G. F., and Brusselle, G. G. (2012) Targeting interleukin-4 in asthma. Lost in translation? Am. J. Respir. Cell Mol. Biol. 47, 261-270
26. Steinke, J. W., and Borish, L. (2001) Th2 cytokines and asthma. Interleukin-Its role in the pathogenesis of asthma, and targeting it for asthma treatment with interleukin-4 receptor antagonists. Respir. Res. 2, 66-70
27. Corren, J., Lemanske, R. F., Hanania, N. A., Korenblat, P. E., Parsey, M. V., Arron, J. R., Harris, J. M., Scheerens, H., Wu, L. C., Su, Z., Mosesova, S., Eisner, M. D., Bohen, S. P., and Matthews, J. G. (2011) Lebrikizumab treatment in adults with asthma. N. Engl. J. Med. 365, 1088-1098
28. Gauvreau, G. M., Boulet, L.-P., Cockcroft, D. W., Fitzgerald, J. M., Carlsten, C., Davis, B. E., Deschesnes, F., Duong, M., Durn, B. L., Howie, K. J., Hui, L., Kasaian, M. T., Killian, K. J., Strinich, T. X., Watson, R. M., Y, N., Zhou, S., Raible, D., and O'Byrne, P. M. (2011) Effects of interleukin-13 blockade on allergen-induced airway responses in mild atopic asthma. Am. J. Respir. Crit. Care Med. 183, 1007-1014
29. Piper, E., Brightling, C., Niven, R., Oh, C., Faggioni, R., Poon, K., She, D., Kell, C., May, R. D., Geba, G. P., and Molfino, N. A. (2013) A phase II placebo-controlled study of tralokinumab in moderate-to-severe asthma. Eur. Respir. J. 41, 330-338
30. Ingram, J. L., and Kraft, M. (2012) IL-13 in asthma and allergic disease. Asthma phenotypes and targeted therapies. J. Allergy Clin. Immunol. 130, 829-842; quiz 843-844
31. Webb, S. (2011) Attacks on asthma. Nat. Biotechnol. 29, 860-863
32. Baker, K. N., Rendall, M. H., Patel, A., Boyd, P., Hoare, M., Freedman, R. B., and James, D. C. (2002) Rapid monitoring of recombinant protein products. A comparison of current technologies. Trends Biotechnol. 20, 149-156
33. Simmons, L. C., Reilly, D., Klimowski, L., Raju, T. S., Meng, G., Sims, P., Hong, K., Shields, R. L., Damico, L. A., Rancatore, P., and Yansura, D. G. (2002) Expression of full-length immunoglobulins in Escherichia coli. Rapid and efficient production of aglycosylated antibodies. J. Immunol. Methods 263, 133-147
34. Reilly, D. E., and Yansura, D. G. (2010) Antibody Engineering (Kontermann, R., and Dübel, S., eds), pp. 331-344, Springer, Berlin
35. Ultsch, M., Bevers, J., Nakamura, G., Vandlen, R., Kelley, R. F., Wu, L. C., and Eigenbrot, C. (2013) Structural basis of signaling blockade by anti- IL-13 antibody lebrikizumab. J. Mol. Biol. 425, 1330-1339
36. Aalberse, R. C., and Schuurman, J. (2002) IgG4 breaking the rules. Immunology 105, 9-19
37. Berkmen, M. (2005) The nonconsecutive disulfide bond of Escherichia coli phytase (AppA) renders it dependent on the protein-disulfide isomerase, DsbC. J. Biol. Chem. 280, 11387-11394
38. Dall'Acqua, W., Simon, A. L., Mulkerrin, M. G., and Carter, P. (1998) Contribution of domain interface residues to the stability of antibody CH3 domain homodimers. Biochemistry 37, 9266-9273
39. Stubenrauch, K., Wessels, U., Regula, J. T., Kettenberger, H., Schleypen, J., and Kohnert, U. (2010) Impact of molecular processing in the hinge region of therapeutic IgG4 antibodies on disposition profiles in cynomolgus monkeys. Drug Metab. Dispos. 38, 84-91
40. Rennard, S. I., Basset, G., Lecossier, D., O'Donnell, K. M., Pinkston, P., Martin, P. G., and Crystal, R. G. (1986) Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution. J. Appl. Physiol. 60, 532-538
41. Nirula, A., Glaser, S. M., Kalled, S. L., and Taylor, F. R. (2011) What is IgG4? A review of the biology of a unique immunoglobulin subtype. Curr. Opin. Rheumatol. 23, 119-124
42. Jung, S. T., Kang, T. H., Kelton, W., and Georgiou, G. (2011) Bypassing glycosylation. Engineering aglycosylated full-length IgG antibodies for human therapy. Curr. Opin. Biotechnol. 22, 858-867