Engineering a monomeric Fc domain modality by N-glycosylation for the half-life extension of biotherapeutics

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16529-16537

  Ishino, Tetsuya ^a   Wang, Mengmeng ^a   Mosyak, Lidia ^a   Tam, Amy ^a   Duan, Weili ^a   Svenson, Kristine ^a   Joyce, Alison ^a   O'Hara, Denise M ^a   Lin, Laura ^a   Somers, William S ^a   Kriz, Ronald ^a  

^a PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITIES; BIOTHERAPEUTICS; DIMER INTERFACE; FC FUSION PROTEINS; N-GLYCOSYLATION; NEONATAL FC RECEPTORS; PROTEIN SURFACE; THERAPEUTIC PROTEIN;

BINDING ENERGY; MOLECULAR RECOGNITION; PROTEINS;

DIMERS;

FC RECEPTOR; MONOMER;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; GLYCOSYLATION; HALF LIFE TIME; HYDROPHOBICITY; IN VIVO STUDY; MALE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN STABILITY; TANDEM REPEAT;

ANTIBODY ENGINEERING; CRYSTAL STRUCTURE; GLYCOSYLATION; HALF-LIFE EXTENSION; N-GLYCOSYLATION; PHARMACOKINETICS; PROTEIN ENGINEERING;

ANIMALS; CELL LINE; GLYCOSYLATION; HALF-LIFE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; MALE; MICE; MICE, INBRED BALB C; PROTEIN BINDING; PROTEIN ENGINEERING; RECEPTORS, FC;

EID: 84878758122     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.457689     Document Type: Article

References (31)

1. Brambell, F. W., Hemmings, W. A., and Morris, I. G. (1964) A theoretical model of γ-globulin catabolism. Nature 203, 1352-1354
2. Raghavan, M., Bonagura, V. R., Morrison, S. L., and Bjorkman, P. J. (1995) Analysis of the pH dependence of the neonatal Fc receptor/immunoglobulin G interaction using antibody and receptor variants. Biochemistry 34, 14649-14657
3. Morell, A., Terry, W. D., and Waldmann, T. A. (1970) Metabolic properties of IgG subclasses in man. J. Clin. Invest. 49, 673-680
4. Lobo, E. D., Hansen, R. J., and Balthasar, J. P. (2004) Antibody pharmacokinetics and pharmacodynamics. J. Pharm. Sci. 93, 2645-2668 (Pubitemid 39506617)
5. Marrack, J. (1955) The structure of antigen-antibody aggregates and complement fixation. Annu. Rev. Microbiol. 9, 369-386
6. Prat, M., Crepaldi, T., Pennacchietti, S., Bussolino, F., and Comoglio, P. M. (1998) Agonistic monoclonal antibodies against the Met receptor dissect the biological responses to HGF. J. Cell Sci. 111, 237-247 (Pubitemid 28064148)
7. Demignot, S., Pimm, M. V., and Baldwin, R. W. (1990) Comparison of biodistribution of 791T/36 monoclonal antibody and its Fab/c fragment in BALB/c mice and nude mice bearing human tumor xenografts. Cancer Res. 50, 2936-2942 (Pubitemid 20170741)
8. Dumont, J. A., Low, S. C., Peters, R. T., and Bitonti, A. J. (2006) Monomeric Fc fusions: impact on pharmacokinetic and biological activity of protein therapeutics. BioDrugs 20, 151-160 (Pubitemid 43845335)
9. Shakin-Eshleman, S. H., Spitalnik, S. L., and Kasturi, L. (1996) The amino acid at the X position of an Asn-X-Ser sequon is an important determinant of N-linked core-glycosylation efficiency. J. Biol. Chem. 271, 6363-6366 (Pubitemid 26095445)
10. Solá, R. J., and Griebenow, K. (2009) Effects of glycosylation on the stability of protein pharmaceuticals. J. Pharm. Sci. 98, 1223-1245
11. Elliott, S., Lorenzini, T., Asher, S., Aoki, K., Brankow, D., Buck, L., Busse, L., Chang, D., Fuller, J., Grant, J., Hernday, N., Hokum, M., Hu, S., Knudten, A., Levin, N., Komorowski, R., Martin, F., Navarro, R., Osslund, T., Rogers, G., Rogers, N., Trail, G., and Egrie, J. (2003) Enhancement of therapeutic protein in vivo activities through glycoengineering. Nat. Biotechnol. 21, 414-421 (Pubitemid 36397662)
12. Roitsch, T., and Lehle, L. (1989) Structural requirements for protein N-glycosylation. Influence of acceptor peptides on cotranslational glycosylation of yeast invertase and site-directed mutagenesis around a sequon sequence. Eur. J. Biochem. 181, 525-529
13. Bause, E., and Legler, G. (1981) The role of the hydroxy amino acid in the triplet sequence Asn-Xaa-Thr(Ser) for the N-glycosylation step during glycoprotein biosynthesis. Biochem. J. 195, 639-644
14. Edelman, G. M., Cunningham, B. A., Gall, W. E., Gottlieb, P. D., Rutishauser, U., and Waxdal, M. J. (1969) The covalent structure of an entire γG immunoglobulin molecule. Proc. Natl. Acad. Sci. U.S.A. 63, 78-85
15. Zalevsky, J., Chamberlain, A. K., Horton, H. M., Karki, S., Leung, I. W., Sproule, T. J., Lazar, G. A., Roopenian, D. C., and Desjarlais, J. R. (2010) Enhanced antibody half-life improves in vivo activity. Nat. Biotechnol. 28, 157-159
16. Yeung, Y. A., Leabman, M. K., Marvin, J. S., Qiu, J., Adams, C. W., Lien, S., Starovasnik, M. A., and Lowman, H. B. (2009) Engineering human IgG1 affinity to human neonatal Fc receptor: impact of affinity improvement on pharmacokinetics in primates. J. Immunol. 182, 7663-7671
17. Suzuki, T., Ishii-Watabe, A., Tada, M., Kobayashi, T., Kanayasu-Toyoda, T., Kawanishi, T., and Yamaguchi, T. (2010) Importance of neonatal FcR in regulating the serum half-life of therapeutic proteins containing the Fc domain of human IgG1: a comparative study of the affinity of monoclonal antibodies and Fc-fusion proteins to human neonatal FcR. J. Immunol. 184, 1968-1976
18. Wang, W., Lu, P., Fang, Y., Hamuro, L., Pittman, T., Carr, B., Hochman, J., and Prueksaritanont, T. (2011) Monoclonal antibodies with identical Fc sequences can bind to FcRn differentially with pharmacokinetic consequences. Drug Metab. Dispos. 39, 1469-1477
19. Oganesyan, V., Damschroder, M. M., Leach, W., Wu, H., and Dall'Acqua, W. F. (2008) Structural characterization of a mutated, ADCC-enhanced human Fc fragment. Mol. Immunol. 45, 1872-1882
20. Rose, R. J., van Berkel, P. H., van den Bremer, E. T., Labrijn, A. F., Vink, T., Schuurman, J., Heck, A. J., and Parren, P. W. (2013) Mutation of Y407 in the CH3 domain dramatically alters glycosylation and structure of human IgG. mAbs 5, 219-228
21. Ying, T., Chen, W., Gong, R., Feng, Y., and Dimitrov, D. S. (2012) Soluble monomeric IgG1 Fc. J. Biol. Chem. 287, 19399-19408
22. Gribben, J. G., Devereux, S., Thomas, N. S., Keim, M., Jones, H. M., Goldstone, A. H., and Linch, D. C. (1990) Development of antibodies to unprotected glycosylation sites on recombinant human GM-CSF. Lancet 335, 434-437 (Pubitemid 20054650)
23. Krapp, S., Mimura, Y., Jefferis, R., Huber, R., and Sondermann, P. (2003) Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J. Mol. Biol. 325, 979-989 (Pubitemid 36263407)
24. Ye, L., Zeng, R., Bai, Y., Roopenian, D. C., and Zhu, X. (2011) Efficient mucosal vaccination mediated by the neonatal Fc receptor. Nat. Biotechnol. 29, 158-163
25. Datta-Mannan, A., Witcher, D. R., Tang, Y., Watkins, J., Jiang, W., and Wroblewski, V. J. (2007) Humanized IgG1 variants with differential binding properties to the neonatal Fc receptor: relationship to pharmacokinetics in mice and primates. Drug Metab. Dispos. 35, 86-94 (Pubitemid 46036480)
26. Deng, R., Loyet, K. M., Lien, S., Iyer, S., DeForge, L. E., Theil, F. P., Lowman, H. B., Fielder, P. J., and Prabhu, S. (2010) Pharmacokinetics of humanized monoclonal anti-tumor necrosis factor-α antibody and its neonatal Fc receptor variants in mice and cynomolgus monkeys. Drug Metab. Dispos. 38, 600-605
27. Ober, R. J., Radu, C. G., Ghetie, V., and Ward, E. S. (2001) Differences in promiscuity for antibody-FcRn interactions across species: implications for therapeutic antibodies. Int. Immunol. 13, 1551-1559 (Pubitemid 33133882)
28. Vaccaro, C., Zhou, J., Ober, R. J., and Ward, E. S. (2005) Engineering the Fc region of immunoglobulin G to modulate in vivo antibody levels. Nat. Biotechnol. 23, 1283-1288 (Pubitemid 41486856)
29. Tesar, D. B., Tiangco, N. E., and Bjorkman, P. J. (2006) Ligand valency affects transcytosis, recycling and intracellular trafficking mediated by the neonatal Fc receptor. Traffic 7, 1127-1142 (Pubitemid 44203994)
30. Burmeister, W. P., Huber, A. H., and Bjorkman, P. J. (1994) Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature 372, 379-383 (Pubitemid 24363442)
31. Raghavan, M., and Bjorkman, P. J. (1996) Fc receptors and their interactions with immunoglobulins. Annu. Rev. Cell Dev. Biol. 12, 181-220 (Pubitemid 26422713)