Modulating IgG effector function by Fc glycan engineering

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 13, 2017, Pages 3485-3490

  Li, Tiezheng ^a   DiLillo, David J ^b   Bournazos, Stylianos ^b   Giddens, John P ^a   Ravetch, Jeffrey V ^b   Wang, Lai Xi ^a  

^a University of Maryland   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Fc receptor; Glycosylation; IgG

Indexed keywords

FC RECEPTOR; GLYCAN; IMMUNOGLOBULIN G; RITUXIMAB; IMMUNOGLOBULIN FC FRAGMENT; POLYSACCHARIDE;

ADVERSE OUTCOME; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BINDING AFFINITY; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; EFFECTOR CELL; FUCOSYLATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN ENGINEERING; PROTEIN STRUCTURE; SIALYLATION; ANIMAL; C57BL MOUSE; GENETICS; GLYCOSYLATION; HUMAN; IMMUNOLOGY; METABOLISM;

ANIMALS; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; POLYSACCHARIDES; PROTEIN ENGINEERING; RECEPTORS, FC;

EID: 85016419499     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1702173114     Document Type: Article

References (30)

1. Pincetic A, et al. (2014) Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol 15(8):707-716.
2. Anthony RM, Ravetch JV (2010) A novel role for the IgG Fc glycan: The antiinflammatory activity of sialylated IgG Fcs. J Clin Immunol 30(Suppl 1):S9-S14.
3. Nimmerjahn F, Ravetch JV (2008) Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8(1):34-47.
4. Takahashi N, Nakagawa H, Fujikawa K, Kawamura Y, Tomiya N (1995) Threedimensional elution mapping of pyridylaminated N-linked neutral and sialyl oligosaccharides. Anal Biochem 226(1):139-146.
5. Wormald MR, et al. (1997) Variations in oligosaccharide-protein interactions in immunoglobulin G determine the site-specific glycosylation profiles and modulate the dynamic motion of the Fc oligosaccharides. Biochemistry 36(6):1370-1380.
6. Jefferis R (2005) Glycosylation of recombinant antibody therapeutics. Biotechnol Prog 21(1):11-16.
7. Umaña P, Jean-Mairet J, Moudry R, Amstutz H, Bailey JE (1999) Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotechnol 17(2):176-180.
8. Ferrara C, et al. (2011) Unique carbohydrate-carbohydrate interactions are required for high-affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci USA 108(31):12669-12674.
9. Kaneko Y, Nimmerjahn F, Ravetch JV (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313(5787):670-673.
10. Anthony RM, et al. (2008) Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 320(5874):373-376.
11. Anthony RM, Wermeling F, Karlsson MC, Ravetch JV (2008) Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA 105(50):19571-19578.
12. Sondermann P, Pincetic A, Maamary J, Lammens K, Ravetch JV (2013) General mechanism for modulating immunoglobulin effector function. Proc Natl Acad Sci USA 110(24):9868-9872.
13. Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS (2007) Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol 44(7):1524-1534.
14. Lin CW, et al. (2015) A common glycan structure on immunoglobulin G for enhancement of effector functions. Proc Natl Acad Sci USA 112(34):10611-10616.
15. Baković MP, et al. (2013) High-throughput IgG Fc N-glycosylation profiling by mass spectrometry of glycopeptides. J Proteome Res 12(2):821-831.
16. Huang W, Giddens J, Fan SQ, Toonstra C, Wang LX (2012) Chemoenzymatic glycoengineering of intact IgG antibodies for gain of functions. J Am Chem Soc 134(29): 12308-12318.
17. Li T, Tong X, Yang Q, Giddens JP, Wang LX (2016) Glycosynthase mutants of endoglycosidase S2 show potent transglycosylation activity and remarkably relaxed substrate specificity for antibody glycosylation remodeling. J Biol Chem 291(32):16508-16518.
18. DiLillo DJ, Ravetch JV (2015) Differential Fc-receptor engagement drives an antitumor vaccinal effect. Cell 161(5):1035-1045.
19. Alter G, Malenfant JM, Altfeld M (2004) CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 294(1-2):15-22.
20. DiLillo DJ, Tan GS, Palese P, Ravetch JV (2014) Broadly neutralizing hemagglutinin stalk-specific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat Med 20(2):143-151.
21. Smith P, DiLillo DJ, Bournazos S, Li F, Ravetch JV (2012) Mouse model recapitulating human Fcγ receptor structural and functional diversity. Proc Natl Acad Sci USA 109(16):6181-6186.
22. Yu X, et al. (2013) Engineering hydrophobic protein-carbohydrate interactions to fine-tune monoclonal antibodies. J Am Chem Soc 135(26):9723-9732.
23. Subedi GP, Barb AW (2016) The immunoglobulin G1 N-glycan composition affects binding to each low-affinity Fcγ receptor. MAbs 8(8):1512-1524.
24. Thomann M, Reckermann K, Reusch D, Prasser J, Tejada ML (2016) Fc-galactosylation modulates antibody-dependent cellular cytotoxicity of therapeutic antibodies. Mol Immunol 73:69-75.
25. Shields RL, et al. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 277(30):26733-26740.
26. Shinkawa T, et al. (2003) 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 278(5):3466-3473.
27. Kurogochi M, et al. (2015) Glycoengineered monoclonal antibodies with homogeneous glycan (M3, G0, G2, and A2) using a chemoenzymatic approach have different affinities for FcγRIIIa and variable antibody-dependent cellular cytotoxicity activities. PLoS One 10(7):e0132848.
28. Thomann M, et al. (2015) In vitro glycoengineering of IgG1 and its effect on Fc receptor binding and ADCC activity. PLoS One 10(8):e0134949.
29. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV (2005) FcgammaRIV: A novel FcR with distinct IgG subclass specificity. Immunity 23(1):41-51.
30. DiLillo DJ, Palese P, Wilson PC, Ravetch JV (2016) Broadly neutralizing anti-influenza antibodies require Fc receptor engagement for in vivo protection. J Clin Invest 126(2): 605-610