Enhanced sialylation of a human chimeric IgG1 variant produced in human and rodent cell lines

Journal of Immunological Methods

Volumn 428, Issue , 2016, Pages 30-36

  Mimura, Yusuke ^a,b   Kelly, Ronan M ^b,c   Unwin, Louise ^b   Albrecht, Simone ^b   Jefferis, Roy ^d   Goodall, Margaret ^d   Mizukami, Yoichi ^e   Mimura Kimura, Yuka ^a,b   Matsumoto, Tsuneo ^a   Ueoka, Hiroshi ^a   Rudd, Pauline M ^b  

^a NATIONAL SANYO HOSPITAL   (Japan)

^b NATIONAL INSTITUTE FOR BIOPROCESSING RESEARCH AND TRAINING   (Ireland)

^c ELI LILLY AND COMPANY   (United States)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^e YAMAGUCHI UNIVERSITY   (Japan)

Author keywords

Glycosylation; IgG; Intravenous immunoglobulin; Sialic acid; Therapeutic antibody

Indexed keywords

GALACTOSE; GLYCAN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G1; SIALIC ACID; IMMUNOGLOBULIN G; N ACETYLNEURAMINIC ACID;

ANIMAL CELL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CHO CELL LINE; CONTROLLED STUDY; FUCOSYLATION; GLYCOSYLATION; HEK293 CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SIALYLATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CHEMISTRY; CRICETULUS; GENETICS; METABOLISM; MOUSE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CHO CELLS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRICETULUS; GLYCOSYLATION; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; N-ACETYLNEURAMINIC ACID;

EID: 84954373522     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2015.11.009     Document Type: Article

References (41)

1. Ahmed A.A., Giddens J., Pincetic A., Lomino J.V., Ravetch J.V., Wang L.X., Bjorkman P.J. Structural characterization of anti-inflammatory immunoglobulin G Fc proteins. J. Mol. Biol. 2014, 426:3166-3179.
2. Anthony R.M., Ravetch J.V. A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs. J. Clin. Immunol. 2010, 30(Suppl. 1):S9-14.
3. Anthony R.M., Kobayashi T., Wermeling F., Ravetch J.V. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature 2011, 475:110-113.
4. Anthony R.M., Nimmerjahn F., Ashline D.J., Reinhold V.N., Paulson J.C., Ravetch J.V. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 2008, 320:373-376.
5. Bruggemann M., Williams G.T., Bindon C.I., Clark M.R., Walker M.R., Jefferis R., Waldmann H., Neuberger M.S. Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J. Exp. Med. 1987, 166:1351-1361.
6. Campbell I.K., Miescher S., Branch D.R., Mott P.J., Lazarus A.H., Han D., Maraskovsky E., Zuercher A.W., Neschadim A., Leontyev D., McKenzie B.S., Kasermann F. Therapeutic effect of IVIG on inflammatory arthritis in mice is dependent on the Fc portion and independent of sialylation or basophils. J. Immunol. 2014, 192:5031-5038.
7. Campbell M.P., Royle L., Radcliffe C.M., Dwek R.A., Rudd P.M. GlycoBase and autoGU: tools for HPLC-based glycan analysis. Bioinformatics 2008, 24:1214-1216.
8. Chung C.H., Mirakhur B., Chan E., Le Q.T., Berlin J., Morse M., Murphy B.A., Satinover S.M., Hosen J., Mauro D., Slebos R.J., Zhou Q., Gold D., Hatley T., Hicklin D.J., Platts-Mills T.A. Cetuximab-induced anaphylaxis and IgE specific for galactose-alpha-1,3-galactose. N. Engl. J. Med. 2008, 358:1109-1117.
9. Crispin M., Yu X., Bowden T.A. Crystal structure of sialylated IgG Fc: implications for the mechanism of intravenous immunoglobulin therapy. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E3544-E3546.
10. Ferrara C., Brunker P., Suter T., Moser S., Puntener U., Umana P. Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous beta1, 4-N-acetylglucosaminyltransferase III and Golgi alpha-mannosidase II. Biotechnol. Bioeng. 2006, 93:851-861.
11. Fiebiger B.M., Maamary J., Pincetic A., Ravetch J.V. Protection in antibody- and T cell-mediated autoimmune diseases by antiinflammatory IgG Fcs requires type II FcRs. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E2385-E2394.
12. Galili U., Anaraki F., Thall A., Hill-Black C., Radic M. One percent of human circulating B lymphocytes are capable of producing the natural anti-Gal antibody. Blood 1993, 82:2485-2493.
13. Guhr T., Bloem J., Derksen N.I., Wuhrer M., Koenderman A.H., Aalberse R.C., Rispens T. Enrichment of sialylated IgG by lectin fractionation does not enhance the efficacy of immunoglobulin G in a murine model of immune thrombocytopenia. PLoS One 2011, 6:e21246.
14. Jassal R., Jenkins N., Charlwood J., Camilleri P., Jefferis R., Lund J. Sialylation of human IgG-Fc carbohydrate by transfected rat alpha2,6-sialyltransferase. Biochem. Biophys. Res. Commun. 2001, 286:243-249.
15. Jefferis R. Antibody therapeutics: isotype and glycoform selection. Expert. Opin. Biol. Ther. 2007, 7:1401-1413.
16. Jefferis R. Glycosylation as a strategy to improve antibody-based therapeutics. Nat. Rev. Drug Discov. 2009, 8:226-234.
17. Kaneko Y., Nimmerjahn F., Ravetch J.V. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006, 313:670-673.
18. Kasermann F., Boerema D.J., Ruegsegger M., Hofmann A., Wymann S., Zuercher A.W., Miescher S. Analysis and functional consequences of increased Fab-sialylation of intravenous immunoglobulin (IVIG) after lectin fractionation. PLoS One 2012, 7:e37243.
19. Leontyev D., Katsman Y., Ma X.Z., Miescher S., Kasermann F., Branch D.R. Sialylation-independent mechanism involved in the amelioration of murine immune thrombocytopenia using intravenous gammaglobulin. Transfusion 2012, 52:1799-1805.
20. Longmore G.D., Schachter H. Product-identification and substrate-specificity studies of the GDP-l-fucose:2-acetamido-2-deoxy-beta-d-glucoside (FUC goes to Asn-linked GlcNAc) 6-alpha-l-fucosyltransferase in a Golgi-rich fraction from porcine liver. Carbohydr. Res. 1982, 100:365-392.
21. Lund J., Takahashi N., Pound J.D., Goodall M., Jefferis R. Multiple interactions of IgG with its core oligosaccharide can modulate recognition by complement and human Fc gamma receptor I and influence the synthesis of its oligosaccharide chains. J. Immunol. 1996, 157:4963-4969.
22. Mimura Y., Lund J., Church S., Dong S., Li J., Goodall M., Jefferis R. Butyrate increases production of human chimeric IgG in CHO-K1 cells whilst maintaining function and glycoform profile. J. Immunol. Methods 2001, 247:205-216.
23. Mimura Y., Sondermann P., Ghirlando R., Lund J., Young S.P., Goodall M., Jefferis R. Role of oligosaccharide residues of IgG1-Fc in Fc gamma RIIb binding. J. Biol. Chem. 2001, 276:45539-45547.
24. Mimura Y., Church S., Ghirlando R., Ashton P.R., Dong S., Goodall M., Lund J., Jefferis R. The influence of glycosylation on the thermal stability and effector function expression of human IgG1-Fc: properties of a series of truncated glycoforms. Mol. Immunol. 2000, 37:697-706.
25. Mimura Y., Ghirlando R., Sondermann P., Lund J., Jefferis R. The molecular specificity of IgG-Fc interactions with Fc gamma receptors. Adv. Exp. Med. Biol. 2001, 495:49-53.
26. Mimura Y., Jefferis R., Mimura-Kimura Y., Abrahams J., Rudd P.M. Glycosylation of therapeutic IgGs. Therapeutic Monoclonal Antibodies: From the Bench to the Clinic 2009, 67-89. Wiley & Sons, Hoboken. Z. An (Ed.).
27. Nimmerjahn F., Anthony R.M., Ravetch J.V. Agalactosylated IgG antibodies depend on cellular Fc receptors for in vivo activity. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8433-8437.
28. Othy S., Topcu S., Saha C., Kothapalli P., Lacroix-Desmazes S., Kasermann F., Miescher S., Bayry J., Kaveri S.V. Sialylation may be dispensable for reciprocal modulation of helper T cells by intravenous immunoglobulin. Eur. J. Immunol. 2014, 44:2059-2063.
29. Raymond C., Robotham A., Spearman M., Butler M., Kelly J., Durocher Y. Production of alpha2,6-sialylated IgG1 in CHO cells. MAbs 2015, 7:571-583.
30. Royle L., Radcliffe C.M., Dwek R.A., Rudd P.M. Detailed structural analysis of N-glycans released from glycoproteins in SDS-PAGE gel bands using HPLC combined with exoglycosidase array digestions. Methods Mol. Biol. 2006, 347:125-143.
31. Scallon B.J., Tam S.H., McCarthy S.G., Cai A.N., Raju T.S. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol. Immunol. 2007, 44:1524-1534.
32. Schwab I., Nimmerjahn F. Intravenous immunoglobulin therapy: how does IgG modulate the immune system?. Nature Reviews Immunology 2013, 13:176-189.
33. Schwab I., Mihai S., Seeling M., Kasperkiewicz M., Ludwig R.J., Nimmerjahn F. Broad requirement for terminal sialic acid residues and FcgammaRIIB for the preventive and therapeutic activity of intravenous immunoglobulins in vivo. Eur. J. Immunol. 2014, 44:1444-1453.
34. Shields R.L., Lai J., Keck R., O'Connell L.Y., Hong K., Meng Y.G., Weikert S.H., Presta L.G. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J. Biol. Chem. 2002, 277:26733-26740.
35. Shinkawa T., Nakamura K., Yamane N., Shoji-Hosaka E., Kanda Y., Sakurada M., Uchida K., Anazawa H., Satoh M., Yamasaki M., Hanai N., Shitara K. The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem. 2003, 278:3466-3473.
36. Subedi G.P., Hanson Q.M., Barb A.W. Restricted motion of the conserved immunoglobulin G1 N-glycan is essential for efficient FcgammaRIIIa binding. Structure 2014, 22:1478-1488.
37. Takeuchi M., Takasaki S., Miyazaki H., Kato T., Hoshi S., Kochibe N., Kobata A. Comparative study of the asparagine-linked sugar chains of human erythropoietins purified from urine and the culture medium of recombinant Chinese hamster ovary cells. J. Biol. Chem. 1988, 263:3657-3663.
38. Umana P., Jean-Mairet J., Moudry R., Amstutz H., Bailey J.E. Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat. Biotechnol. 1999, 17:176-180.
39. Washburn N., Schwab I., Ortiz D., Bhatnagar N., Lansing J.C., Medeiros A., Tyler S., Mekala D., Cochran E., Sarvaiya H., Garofalo K., Meccariello R., Meador J.W., Rutitzky L., Schultes B.C., Ling L., Avery W., Nimmerjahn F., Manning A.M., Kaundinya G.V., Bosques C.J. Controlled tetra-Fc sialylation of IVIg results in a drug candidate with consistent enhanced anti-inflammatory activity. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E1297-E1306.
40. Yu X., Baruah K., Harvey D.J., Vasiljevic S., Alonzi D.S., Song B.D., Higgins M.K., Bowden T.A., Scanlan C.N., Crispin M. Engineering hydrophobic protein-carbohydrate interactions to fine-tune monoclonal antibodies. J. Am. Chem. Soc. 2013, 135:9723-9732.
41. Yu X., Vasiljevic S., Mitchell D.A., Crispin M., Scanlan C.N. Dissecting the molecular mechanism of IVIg therapy: the interaction between serum IgG and DC-SIGN is independent of antibody glycoform or Fc domain. J. Mol. Biol. 2013, 425:1253-1258.