Site-specific glycosylation of an aglycosylated human IgG1-Fc antibody protein generates neoglycoproteins with enhanced function

Chemistry and Biology

Volumn 10, Issue 9, 2003, Pages 807-814

  Watt, Gregory M ^a   Lund, John ^b   Levens, Michaela ^b   Kolli, V S Kumar ^a   Jefferis, Royston ^b   Boons, Geert Jan ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0141565183     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2003.08.006     Document Type: Article

References (42)

1. Varki A. Biological roles of oligosaccharides. all of the theories are correct Glycobiology. 3:1993;97-130.
2. Sears P., Wong C.H. Enzyme action in glycoprotein synthesis. Cell. Mol. Life Sci. 54:1998;223-252.
3. Dwek R. Glycobiology. toward understanding the function of sugars Chem. Rev. 96:1996;683-720.
4. Imperiali B., O'Connor S.E. Effect of N-linked glycosylation on glycopeptide and glycoprotein structure. Curr. Opin. Chem. Biol. 3:1999;643-649.
5. Bertozzi C.R., Kiessling L.L. Chemical glycobiology. Science. 291:2001;2357-2364.
6. Helenius A., Aebi M. Intracellular functions of N-linked glycans. Science. 291:2001;2364-2369.
7. Knight P. The carbohydrate frontier. Biotechnology. 7:1989;35-40.
8. Jenkins N., Curling E.M.A. Glycosylation of recombinant proteins. problems and prospects Enzyme Microb. Technol. 16:1994;354-364.
9. Wright A., Morrison S.L. Effect of glycosylation on antibody function. implications for genetic engineering Trends Biotechnol. 15:1997;26-32.
10. Lund J., Takahashi N., Pound J.D., Goodall M., Nakagawa H., Jefferis R. Oligosaccharide-protein interactions in IgG can modulate recognition by Fcχ receptors. FASEB J. 9:1995;115-119.
11. 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. 37:2000;697-706.
12. 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. 276:2001;45539-45547.
13. Deisenhofer J. Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein-A from Staphylococcus-Aureus at 2.9-Å and 2.8-Å resolution. Biochemistry. 20:1981;2361-2370.
14. Sondermann P., Huber R., Oosthuizen V., Uwe J. The 3.2-Å crystal structure of the Human IgG1 Fc fragment-FcyRIII complex. Nature. 406:2000;267-273.
15. Parekh R.B., Dwek R.A., Sutton B.J., Fernandes D.L., Leung A., Stanworth D., Rademacher T.W., Mizuochi T., Taniguchi T., Matsuta K.et al. Association of rheumatoid-arthritis and primary osteo-arthritis with changes in the glycosylation pattern of total serum IgG. Nature. 316:1985;452-457.
16. Rudd P.M., Elliott T., Cresswell P., Wilson I.A., Dwek R.A. Glycosylation and the immune system. Science. 291:2001;2370-2376.
17. Jefferis R. Glycosylation of human IgG antibodies. relevance to therapeutic applications BioPharm. 14:2001;19-24.
18. Savage C.O.S., Harper L., Holland M. New findings in pathogenesis of antineutrophil cytoplasm antibody-associated vasculitis. Curr. Opin. Rheumatol. 14:2002;15-22.
19. Davis B.G. Synthesis of glycoproteins. Chem. Rev. 102:2002;579-601.
20. Kochendoerfer G.G., Kent S.B.H. Chemical protein synthesis. Curr. Opin. Chem. Biol. 3:1999;665-671.
21. Witte K., Sears P., Martin R., Wong C.-H. Enzymatic glycoprotein synthesis. preparation of ribonuclease glycoforms via enzymatic glycopeptide condensation and glycosylation J. Am. Chem. Soc. 119:1997;2114-2118.
22. Tolbert T.J., Wong C.H. Intein-mediated synthesis of proteins containing carbohydrates and other molecular probes. J. Am. Chem. Soc. 122:2000;5421-5428.
23. Shin Y., Winans K.A., Backes B.J., Kent S.B.H., Ellman J.A., Bertozzi C.R. Fmoc-based synthesis of peptide-thioesters. application to the total chemical synthesis of a glycoprotein by native chemical ligation J. Am. Chem. Soc. 121:1999;11684-11689.
24. Marcaurelle L.A., Bertozzi C.R. New directions in the synthesis of glycopeptide mimetics. Chem. Eur. J. 5:1999;1384-1390.
25. Macmillan D., Bertozzi C.R. New directions in glycoprotein engineering. Tetrahedron. 56:2000;9515-9525.
26. Danishefsky S., Allen J. From the laboratory to the clinic. a retrospective on fully synthetic carbohydrate-based anticancer vaccines Angew. Chem. Int. Ed. Engl. 40:2000;836-863.
27. Dullenkopf W., Ritter S., Forunato S., Old L., Schmidt R. Synthesis of a structurally defined antigen-immunostimulant combination for use in cancer vaccines. Chem. Eur. J. 5:1999;2432-2438.
28. Reichel, F., Ashton, P.R., and Boons, G.J. (1997). Synthetic carbohydrate-based vaccines: synthesis of an L-glycero-D-manno-heptose antigen-T-epitope-lipopeptide conjugate. Chem. Commun., 2087-2088.
29. Macindoe, W.M., van Oijen, A., and Boons, G.J. (1998). A unique highly facile method for synthesising disulfide linked neoglycoconjugates: a new approach for remodelling of peptides and proteins. Chem. Commun., 847-848.
30. Macmillan D., Bill R.M., Sage K.A., Fern D., Flitsch S.L. Selective in vitro glycosylation of recombinant proteins. semi-synthesis of novel homogeneous glycoforms of Human erythropoietin Chem. Biol. 8:2001;133-145.
31. Lund J., Takahashi N., Pound J.D., Goodall M., Jefferis R. Multiple interactions of IgG1 with its core oligosaccharide can modulate recognition by complement and human Fcχ receptor 1 and influence the synthesis of oligosaccharide chains. J. Immunol. 157:1996;4963-4969.
32. Imberty A., Perez S. Stereochemistry of the N-glycosylation sites in glycoproteins. Protein Eng. 8:1995;699-709.
33. Grassetti D.R., Murray J.F. Jr. Determination of sulfhydrile groups with 2,2- or 4,4-dithiodipyridine. Arch. Biochem. Biophys. 119:1967;41-49.
34. Lund J., Takahashi N., Popplewell A., Goodall M., Pound J.D., Tyler R., King D.J., Jefferis R. Expression and characterization of truncated forms of humanized L243 IgG1. architectural features can influence synthesis of its oligosaccharide chains and affect superoxide production triggered through human Fcχ receptor 1 Eur. J. Biochem. 267:2000;1-12.
35. Bennett K.L., Smith S.V., Truscott R.J.W., Sheil M.M. Monitoring papain digestion of a monoclonal antibody by electrospray ionization mass spectrometry. Anal. Biochem. 245:1997;17-27.
36. Bill R.M., Flitsch S.L. Chemical and biological approaches to glycoprotein synthesis. Chem. Biol. 3:1996;145-149.
37. Wong S.Y., Guile G.R., Dwek R.A., Arsequell G. Synthetic glycosylation of proteins using N-(beta-saccharide) iodoacetamides. applications in site-specific glycosylation and solid-phase enzymic oligosaccharide synthesis Biochem. J. 300:1994;843-850.
38. Tsuchiya N., Endo T., Matsuta K., Yoshinoya S., Aikawa T., Kosuge E., Takeuchi F., Miyamoto T., Kobata A. Effects of galactose depletion from oligosaccharide chains on immunological activities of human-IgG. J. Rheumatol. 16:1989;285-290.
39. Jassal R., Jenkins N., Charlwood J., Camilleri P., Jefferis R., Lund J. Sialylation of human IgG-Fc carbohydrate by transfected rat a2,6-sialyltransferase. Biochem. Biophys. Res. Commun. 286:2001;243-249.
40. Umana P., Jean-Mairet J., Mouldy R., Amstutz H., Bailey J.E. Engineered glycoforms of IgG1 with optimised ADCC. Nat. Biotechnol. 17:1999;176-180.
41. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:1951;265-275.
42. Lund J., Winter G., Jones P.T., Pound J.D., Tanaka T., Walker M.R., Artymiuk P.J., Arata Y., Burton D.R., Jefferis R.et al. Human Fc-gamma-RI and Fc-gamma-RII interact with distinct but overlapping sites on Human-IgG. J. Immunol. 147:1991;2657-2662.