In vitro glycoengineering of IgG1 and its effect on Fc receptor binding and ADCC activity

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Thomann, Marco ^a   Schlothauer, Tilman ^a   Dashivets, Tetyana ^a,c   Malik, Sebastian ^a   Avenal, Cecile ^b   Bulau, Patrick ^a   Rüger, Petra ^a   Reusch, Dietmar ^a  

^a ROCHE DIAGNOSTICS GMBH   (Germany)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c Munich Center for Integrated Protein Science   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; FC RECEPTOR IIA; GLYCAN; GLYCOSYLTRANSFERASE; IMMUNOGLOBULIN G1; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; FCGR1A PROTEIN, HUMAN; FCGR3A PROTEIN, HUMAN; GALACTOSE; IMMUNOGLOBULIN G; PROTEIN BINDING; RECOMBINANT PROTEIN; SIALIC ACID DERIVATIVE; SIALYLTRANSFERASE;

AFFINITY CHROMATOGRAPHY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BINDING AFFINITY; CYTOTOXICITY TEST; DEGLYCOSYLATION; FUCOSYLATION; GLYCOSYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PH; PROTEIN BINDING; PROTEIN INTERACTION; RECEPTOR BINDING; SIALYLATION; SURFACE PLASMON RESONANCE; BINDING SITE; CHEMISTRY; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; METABOLISM; PROTEIN ENGINEERING;

ANTIBODY-DEPENDENT CELL CYTOTOXICITY; BINDING SITES; GALACTOSE; GENE EXPRESSION; GLYCOSYLATION; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN G; PROTEIN BINDING; PROTEIN ENGINEERING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, IGG; RECOMBINANT PROTEINS; SIALIC ACIDS; SIALYLTRANSFERASES;

EID: 84942919876     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134949     Document Type: Article

References (36)

1. Jefferis R. Recombinant antibody therapeutics: the impact of glycosylation on mechanisms of action. Trends in pharmacological sciences 2009;30(7):356-62. doi: 10.1016/j.tips.2009.04.007 PMID: 19552968
2. Pacis E, Yu M, Autsen J, Bayer R, Li F. Effects of cell culture conditions on antibody N-linked glycosylation-what affects high mannose 5 glycoform. Biotechnol Bioeng 2011.
3. Ahn WS, Jeon JJ, Jeong YR, Lee SJ, Yoon SK. Effect of culture temperature on erythropoietin production and glycosylation in a perfusion culture of recombinant CHO cells. Biotechnol Bioeng 2008;101(6):1234-44. doi: 10.1002/bit.22006 PMID: 18980186
4. Raju TS, Jordan RE. Galactosylation variations in marketed therapeutic antibodies. MAbs 2012;4(3):385-91. doi: 10.4161/mabs.19868 PMID: 22531450
5. Schiestl M, Stangler T, Torella C, Cepeljnik T, Toll H, Grau R. Acceptable changes in quality attributes of glycosylated biopharmaceuticals. Nat. Biotechnol. 2011;29(4):310-312. doi: 10.1038/nbt.1839 PMID: 21478841
6. Chung S, Quarmby V, Gao X, Ying Y, Lin L, Reed C, et al. Quantitative evaluation offucose reducing effects in a humanized antibody on Fcgamma receptor binding and antibody-dependent cell-mediated cytotoxicity activities. MAbs. 2012;4(3):326-340. doi: 10.4161/mabs.19941 PMID: 22531441
7. Niwa R, Sakurada M, Kobayashi Y, Uehara A, Matsushima K, Ueda R, et al. Enhanced natural killer cell binding and activation by low-fucose IgG1 antibody results in potent antibody-dependent cellular cytotoxicity induction at lower antigen density. Clin. Cancer Res. 2005;11(6):2327-2336. PMID: 15788684
8. Shields RL, Lai J, Keck R, O'Connell LY, Hong K, Meng YG, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcgammaRIII and antibody-dependent cellulartoxicity. J. Biol. Chem. 2002;277(30):26733-26740. PMID: 11986321
9. Yamane-Ohnuki N, Kinoshita S, Inoue-Urakubo M, Kusunoki M, Iida S, Nakano R, et al. Establishment of FUT8 knockout Chinese hamster ovary cells: an ideal host cell line for producing completely defucosylated antibodies with enhanced antibody-dependent cellular cytotoxicity. Biotechnol. Bioeng. 2004;87(5):614-622. PMID: 15352059
10. Boyd PN, Lines AC, Patel AK. The effect of the removal of sialic acid, galactose and total carbohydrate on the functional activity of Campath-1H. Mol. Immunol. 1995;32(17-18):1311-1318. PMID: 8643100
11. Hodoniczky J, Zheng YZ, James DC. Control of recombinant monoclonal antibody effector functions by Fc N-glycan remodeling in vitro. Biotechnol. Prog. 2005;21(6):1644-1652. PMID: 16321047
12. Shinkawa T, Nakamura K, Yamane N, Shoji-Hosaka E, Kanda Y, Sakurada M, et al. The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complextype oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem. 2003;278(5):3466-3473. PMID: 12427744
13. Houde D, Peng Y, Berkowitz SA, Engen JR. Post-translational modifications differentially affect IgG1 conformation and receptor binding. Mol. Cell Proteomics. 2010;9(8):1716-1728. doi: 10.1074/mcp. M900540-MCP200 PMID: 20103567
14. Kumpel BM, Wang Y, Griffiths HL, Hadley AG, Rook GA. The biological activity of human monoclonal IgG anti-D is reduced by beta-galactosidase treatment. Hum. Antibodies Hybridomas 1995;6(3):82-88. PMID: 8597627
15. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fcsialylation. Science 2006;313(5787):670-673. PMID: 16888140
16. Naso MF, Tam SH, Scallon BJ, Raju TS. Engineering host cell lines to reduce terminal sialylation of secreted antibodies. MAbs. 2010;2(5):519-527. doi: 10.4161/mabs.2.5.13078 PMID: 20716959
17. Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. Higher levels of sialylated Fcglycansin immunoglobulin G molecules can adversely impact functionality. Mol. Immunol. 2007;44(7):1524-1534. PMID: 17045339
18. Kapur R, Einarsdottir HK, Vidarsson G. IgG-effector functions: "the good, the bad and the ugly". Immunology letters 2014;160(2):139-44. doi: 10.1016/j.imlet.2014.01.015 PMID: 24495619
19. Stadlmann J, Pabst M, Altmann F. Analytical and Functional Aspects of Antibody Sialylation. Journal of clinical immunology 2010.
20. Huang W, Giddens J, Fan SQ, Toonstra C, Wang LX. Chemoenzymaticglycoengineeringof intact IgG antibodies for gain of functions. J. Am. Chem. Soc. 2012;134(29):12308-12318. doi: 10.1021/ja3051266 PMID: 22747414
21. Fujii S, Nishiura T, Nishikawa A, Miura R, Taniguchi N. Structural heterogeneity of sugar chains in immunoglobulin G. Conformation of immunoglobulin G molecule and substrate specificities of glycosyltransferases. The Journal of biological chemistry 1990;265(11):6009-18. PMID: 2138613
22. Raju TS, Briggs JB, Chamow SM, Winkler ME, Jones AJ. Glycoengineering of therapeutic glycoproteins: in vitro galactosylation and sialylation of glycoproteins with terminal N-acetylglucosamine and galactose residues. Biochemistry 2001;40(30):8868-76. PMID: 11467948
23. Warnock D, Bai X, Autote K, Gonzales J, Kinealy K, Yan B, et al. In vitro galactosylation of human IgG at 1 kg scale using recombinant galactosyltransferase. Biotechnology and bioengineering 2005;92(7):831-42. PMID: 16187338
24. Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. Journal of molecular biology 2003;325(5):979-89. PMID: 12527303
25. Mimura Y, Church S, Ghirlando R, Ashton PR, Dong S, Goodall M, et al. The influence of glycosylation on the thermal stability and effector function expression of human IgG1-Fc: properties of a series of truncated glycoforms. Molecular immunology 2000;37(12-13):697-706. PMID: 11275255
26. Diepold K, Bomans K, Wiedmann M, Zimmermann B, Petzold A, Schlothauer T, et al. Simultaneous assessment of Asp isomerization and Asn deamidation in recombinant antibodies by LC-MS following incubation at elevated temperatures. PloS one 2012;7(1):e30295. doi: 10.1371/journal.pone.0030295 PMID: 22272329
27. Schnueriger A, Grau R, Sondermann P, Schreitmueller T, Marti S, Zocher M. Development of a quantitative, cell-line based assay to measure ADCC activity mediated by therapeutic antibodies. Mol. Immunol. 2011;48(12-13):1512-1517. doi: 10.1016/j.molimm.2011.04.010 PMID: 21570725
28. Barb AW, Brady EK, Prestegard JH. Branch-specific sialylation of IgG-Fc glycans by ST6Gal-I. Biochemistry 2009;48(41):9705-9707. doi: 10.1021/bi901430h PMID: 19772356
29. Schlothauer T, Rueger P, Stracke JO, Hertenberger H, Fingas F, Kling L, et al. Analytical FcRn affinity chromatography for functional characterization of monoclonal antibodies. MAbs. 2013;5(4):576-586. doi: 10.4161/mabs.24981 PMID: 23765230
30. Ferrara C, Stuart F, Sondermann P, Brunker P, Umana P. The carbohydrate at FcgammaRIIIaAsn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. The Journal of biological chemistry 2006;281(8):5032-6. PMID: 16330541
31. Gottschalk PG, Dunn JR. Measuring parallelism, linearity, and relative potency in bioassay and immunoassay data. Journal of biopharmaceutical statistics 2005;15(3):437-63. PMID: 15920890
32. Sondermann P, Kaiser J, Jacob U. Molecular basis for immune complex recognition: a comparison of Fc-receptor structures. Journal of molecular biology 2001;309(3):737-49. PMID: 11397093
33. Smith KG, Clatworthy MR. FcgammaRIIB in autoimmunity and infection: evolutionary and therapeutic implications. Nat Rev Immunol 2010;10(5):328-43. doi: 10.1038/nri2762 PMID: 20414206
34. Nimmerjahn F, Ravetch JV. Fc-receptors as regulators of immunity. Advances in immunology 2007;96:179-204. PMID: 17981207
35. Bohm S, Schwab I, Lux A, Nimmerjahn F. The role of sialic acid as a modulator of the anti-inflammatory activity of IgG. Seminars in immunopathology 2012;34(3):443-53. doi: 10.1007/s00281-012-0308-x PMID: 22437760
36. Zeck A, Pohlentz G, Schlothauer T, Peter-Katalinic J, Regula JT. Cell type-specific and site directed N-glycosylation pattern of FcgammaRIIIa. Journal of proteome research 2011;10(7):3031-9. doi: 10. 1021/pr1012653 PMID: 21561106