A common glycan structure on immunoglobulin G for enhancement of effector functions

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

Volumn 112, Issue 34, 2015, Pages 10611-10616

  Lin, Chin Wei ^a,b,c   Tsai, Ming Hung ^d   Li, Shiou Ting ^a   Tsai, Tsung I ^a   Chu, Kuo Ching ^d   Liu, Ying Chih ^d   Lai, Meng Yu ^a,d   Wu, Chia Yu ^a   Tseng, Yung Chieh ^a,e   Shivatare, Sachin S ^d   Wang, Chia Hung ^d   Chao, Ping ^d   Wang, Shi Yun ^d   Shih, Hao Wei ^d   Zeng, Yi Fang ^d   You, Tsai Hong ^d   Liao, Jung Yu ^d   Tu, Yu Chen ^d   Lin, Yih Shyan ^d   Chuang, Hong Yang ^d   Chen, Chia Lin ^a,b,c   Tsai, Charng Sheng ^d   Huang, Chiu Chen ^d   Lin, Nan Horng ^d   Ma, Che ^a   Wu, Chung Yi ^a,b   Wong, Chi Huey ^a,b,c   more..

^a GENOMICS RESEARCH CENTER   (Taiwan)

^b ACADEMIA SINICA   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d CHO PHARMA INC   (Taiwan)

^e NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

Endoglycosidase; Fc glycosylation; Glycoengineered antibodies; Homogeneous antibodies; Sugar oxazoline

Indexed keywords

ALPHA LEVO FUCOSIDASE; GLYCAN; IMMUNOGLOBULIN G; RITUXIMAB; SIALIC ACID DERIVATIVE; BACTERIAL PROTEIN; ENDO-N-ACETYLNEURAMINIDASE; FC RECEPTOR; FCGR3A PROTEIN, HUMAN; IMMUNOGLOBULIN FC FRAGMENT; N ACETYLGLUCOSAMINE; POLYSACCHARIDE; SIALIDASE; TRASTUZUMAB; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTEROIDES FRAGILIS; BINDING AFFINITY; CARBOHYDRATE ANALYSIS; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS PYOGENES; ANIMAL; B CELL LYMPHOMA; BAGG ALBINO MOUSE; CHEMISTRY; ENZYMOLOGY; FEMALE; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; ORTHOMYXOVIRIDAE INFECTIONS; PATHOLOGY; PROTEIN ENGINEERING; STRUCTURE ACTIVITY RELATION; TUMOR CELL LINE;

ACETYLGLUCOSAMINE; ALPHA-L-FUCOSIDASE; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; BACTERIAL PROTEINS; BACTEROIDES FRAGILIS; CELL LINE, TUMOR; FEMALE; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; LYMPHOMA, B-CELL; MICE; MICE, INBRED BALB C; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; POLYSACCHARIDES; PROTEIN ENGINEERING; RECEPTORS, IGG; RITUXIMAB; SIALIC ACIDS; STREPTOCOCCUS PYOGENES; STRUCTURE-ACTIVITY RELATIONSHIP; TRASTUZUMAB;

EID: 84940551820     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513456112     Document Type: Article

References (41)

1. Köhler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256(5517):495-497.
2. Kang AS, Barbas CF, Janda KD, Benkovic SJ, Lerner RA (1991) Linkage of recognition and replication functions by assembling combinatorial antibody Fab libraries along phage surfaces. Proc Natl Acad Sci USA 88(10):4363-4366.
3. McCafferty J, Griffiths AD, Winter G, Chiswell DJ (1990) Phage antibodies: Filamentous phage displaying antibody variable domains. Nature 348(6301):552-554.
4. Tiller T, et al. (2008) Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329(1-2):112-124.
5. Shields RL, et al. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fc?RIII and antibody-dependent cellular toxicity. J Biol Chem 277(30):26733-26740.
6. 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 Chem278(5):3466-3473.
7. Okazaki A, et al. (2004) Fucose depletion from human IgG1 oligosaccharide enhances binding enthalpy and association rate between IgG1 and Fc?RIIIa. J Mol Biol 336(5):1239-1249.
8. Ferrara C, et al. (2011) Unique carbohydrate?carbohydrate interactions are required for high affinity binding between Fc?RIII and antibodies lacking core fucose. Proc Natl Acad Sci USA 108(31):12669-12674.
9. Cooper DL, et al.; YEAR Consortium (2012) Fc?RIIIa expression on monocytes in rheumatoid arthritis: Role in immune-complex stimulated TNF production and nonresponse to methotrexate therapy. PLoS One 7(1):e28918.
10. Gornik I, Maravi -c G, Dumi -c J, Flögel M, Lauc G (1999) Fucosylation of IgG heavy chains is increased in rheumatoid arthritis. Clin Biochem 32(8):605-608.
11. Anthony RM, et al. (2008) Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 320(5874):373-376.
12. Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS (2007) Higher levels of sialylated Fc glycans in immunoglobulin Gmolecules can adversely impact functionality. Mol Immunol 44(7):1524-1534.
13. Kaneko Y, Nimmerjahn F, Ravetch JV (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313(5787):670-673.
14. Van De Geijn FE, et al. (2009) Immunoglobulin G galactosylation and sialylation are associated with pregnancy-induced improvement of rheumatoid arthritis and the postpartum flare: Results from a large prospective cohort study. Arthritis Res Ther 11(6):R193.
15. Dawson PE, Kent SBH (2000) Synthesis of native proteins by chemical ligation. Annu Rev Biochem 69(1):923-960.
16. Dawson PE, Muir TW, Clark-Lewis I, Kent SB (1994) Synthesis of proteins by native chemical ligation. Science 266(5186):776-779.
17. Muir TW (2003) Semisynthesis of proteins by expressed protein ligation. Annu Rev Biochem 72(1):249-289.
18. Saxon E, Bertozzi CR (2000) Cell surface engineering by a modified Staudinger reaction. Science 287(5460):2007-2010.
19. Nilsson BL, Kiessling LL, Raines RT (2001) High-yielding Staudinger ligation of a phosphinothioester and azide to form a peptide. Org Lett 3(1):9-12.
20. Liu L, Hong Z-Y, Wong C-H (2006) Convergent glycopeptide synthesis by traceless Staudinger ligation and enzymatic coupling. ChemBioChem 7(3):429-432.
21. Brik A, Yang Y-Y, Ficht S, Wong C-H (2006) Sugar-assisted glycopeptide ligation. J Am Chem Soc 128(17):5626-5627.
22. Witte K, Sears P, Martin R, Wong C-H (1997) Enzymatic glycoprotein synthesis: Preparation of ribonuclease glycoforms via enzymatic glycopeptide condensation and glycosylation. J Am Chem Soc 119(9):2114-2118.
23. Yamane-Ohnuki N, et al. (2004) 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 87(5):614-622.
24. Davies J, et al. (2001) Expression of GnTIII in a recombinant anti-CD20 CHO production cell line: Expression of antibodies with altered glycoforms leads to an increase in ADCC through higher affinity for FC ? RIII. Biotechnol Bioeng 74(4):288-294.
25. Zou G, et al. (2011) Chemoenzymatic synthesis and Fc? receptor binding of homogeneous glycoforms of antibody Fc domain. Presence of a bisecting sugar moiety enhances the affinity of Fc to Fc?IIIa receptor. J Am Chem Soc 133(46):18975-18991.
26. Huang W, Giddens J, Fan S-Q, Toonstra C, Wang L-X (2012) Chemoenzymatic glycoengineering of intact IgG antibodies for gain of functions. J Am Chem Soc 134(29): 12308-12318.
27. Goodfellow JJ, et al. (2012) An endoglycosidase with alternative glycan specificity allows broadened glycoprotein remodelling. J Am Chem Soc 134(19):8030-8033.
28. Kobayashi S, Kiyosada T, Shoda S-i (1996) Synthesis of artificial chitin: Irreversible catalytic behavior of a glycosyl hydrolase through a transition state analogue substrate. J Am Chem Soc 118(51):13113-13114.
29. Shoda S-i, et al. (2002) Efficientmethod for the elongation of the N-acetylglucosamine unit by combined use of chitinase and ?-galactosidase. Helv Chim Acta 85(11):3919-3936.
30. Huang W, Li J, Wang L-X (2011) Unusual transglycosylation activity of Flavobacterium meningosepticum endoglycosidases enables convergent chemoenzymatic synthesis of core fucosylated complex N-glycopeptides. ChemBioChem 12(6):932-941.
31. Umekawa M, et al. (2010) Efficient transfer of sialo-oligosaccharide onto proteins by combined use of a glycosynthase-like mutant of Mucor hiemalis endoglycosidase and synthetic sialo-complex-type sugar oxazoline. Biochim Biophys Acta 1800(11):1203-1209.
32. Collin M, Olsén A (2001) EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J 20(12):3046-3055.
33. Mimura Y, et al. (2000) 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 37(12-13):697-706.
34. DiLillo DJ, Ravetch JV (2015) Differential Fc-receptor engagement drives an anti-tumor vaccinal effect. Cell 161(5):1035-1045.
35. Niwa R, et al. (2004) Enhancement of the antibody-dependent cellular cytotoxicity of low-fucose IgG1 Is independent of Fc?RIIIa functional polymorphism. Clin Cancer Res 10(18 Pt 1):6248-6255.
36. Raju TS, Lang SE (2014) Diversity in structure and functions of antibody sialylation in the Fc. Curr Opin Biotechnol 30(0):147-152.
37. Rezvani AR, Maloney DG (2011) Rituximab resistance. Best Pract Res Clin Haematol 24(2):203-216.
38. Barok M, et al. (2007) Trastuzumab causes antibody-dependent cellular cytotoxicitymediated growth inhibition of submacroscopic JIMT-1 breast cancer xenografts despite intrinsic drug resistance. Mol Cancer Ther 6(7):2065-2072.
39. 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.
40. DiLillo DJ, Tan GS, Palese P, Ravetch JV (2014) Broadly neutralizing hemagglutinin stalk-specific antibodies require Fc?R interactions for protection against influenza virus in vivo. Nat Med 20(2):143-151.
41. Corti D, et al. (2011) A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333(6044):850-856.