Selective deactivation of serum IgG: A general strategy for the enhancement of monoclonal antibody receptor interactions

Journal of Molecular Biology

Volumn 420, Issue 1-2, 2012, Pages 1-7

  Baruah, Kavitha ^a   Bowden, Thomas A ^b   Krishna, Benjamin A ^a   Dwek, Raymond A ^a   Crispin, Max ^a   Scanlan, Christopher N ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

ADCC; antibody; endoglycosidase; Fc receptor; glycosylation

Indexed keywords

CD16 ANTIGEN; EPITOPE; FC GAMMA RECEPTOR IIIA; FC RECEPTOR; GLYCAN; IMMUNOGLOBULIN G; MANNOSE OLIGOSACCHARIDE; MONOCLONAL ANTIBODY; N ACETYL BETA GLUCOSAMINIDASE; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CANCER CELL; CELL SURFACE; DISSOCIATION; ENZYME ACTIVITY; HUMAN; HYDROLYSIS; IMMUNOGLOBULIN BLOOD LEVEL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RECEPTOR BINDING; ROOM TEMPERATURE;

EID: 84861804997     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.04.002     Document Type: Article

References (42)

1. Nimmerjahn F., and Ravetch J.V. Fcγ receptors as regulators of immune responses Nat. Rev., Immunol. 8 2008 34 47
2. Siberil S., Dutertre C.A., Fridman W.H., and Teillaud J.L. FcγR: the key to optimize therapeutic antibodies? Crit. Rev. Oncol./Hematol. 62 2007 26 33
3. Stavenhagen J.B., Gorlatov S., Tuaillon N., Rankin C.T., Li H., and Burke S. Fc optimization of therapeutic antibodies enhances their ability to kill tumor cells in vitro and controls tumor expansion in vivo via low-affinity activating Fcγ receptors Cancer Res. 67 2007 8882 8890
4. Bruhns P., Iannascoli B., England P., Mancardi D.A., Fernandez N., Jorieux S., and Daeron M. Specificity and affinity of human Fcγ receptors and their polymorphic variants for human IgG subclasses Blood 113 2009 3716 3725
5. Jefferis R. Antibody therapeutics: isotype and glycoform selection Expert Opin. Biol. Ther. 7 2007 1401 1413
6. Jefferis R. Glycosylation as a strategy to improve antibody-based therapeutics Nat. Rev., Drug Discov. 8 2009 226 234
7. Barb A.W., and Prestegard J.H. NMR analysis demonstrates immunoglobulin G N-glycans are accessible and dynamic Nat. Chem. Biol. 7 2011 147 153
8. Krapp S., Mimura Y., Jefferis R., Huber R., and Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity J. Mol. Biol. 325 2003 979 989
9. Edberg J.C., and Kimberly R.P. Cell type-specific glycoforms of FcγRIIIa (CD16): differential ligand binding J. Immunol. 159 1997 3849 3857
10. Mizushima T., Yagi H., Takemoto E., Shibata-Koyama M., Isoda Y., and Iida S. Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans Genes Cells 16 2011 1071 1080
11. Ferrara C., Grau S., Jager C., Sondermann P., Brunker P., and Waldhauer I. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcγRIII and antibodies lacking core fucose Proc. Natl Acad. Sci. USA 108 2011 12669 12674
12. Strohl W.R. Optimization of Fc-mediated effector functions of monoclonal antibodies Curr. Opin. Biotechnol. 20 2009 685 691
13. Preithner S., Elm S., Lippold S., Locher M., Wolf A., and da Silva A.J. High concentrations of therapeutic IgG1 antibodies are needed to compensate for inhibition of antibody-dependent cellular cytotoxicity by excess endogenous immunoglobulin G Mol. Immunol. 43 2006 1183 1193
14. Kanda Y., Yamada T., Mori K., Okazaki A., Inoue M., and Kitajima-Miyama K. Comparison of biological activity among nonfucosylated therapeutic IgG1 antibodies with three different N-linked Fc oligosaccharides: the high-mannose, hybrid, and complex types Glycobiology 17 2007 104 118
15. Iida S., Misaka H., Inoue M., Shibata M., Nakano R., and Yamane-Ohnuki N. Nonfucosylated therapeutic IgG1 antibody can evade the inhibitory effect of serum immunoglobulin G on antibody-dependent cellular cytotoxicity through its high binding to FcγRIIIa Clin. Cancer Res. 12 2006 2879 2887
16. Satoh M., Iida S., and Shitara K. Non-fucosylated therapeutic antibodies as next-generation therapeutic antibodies Expert Opin. Biol. Ther. 6 2006 1161 1173
17. Stuart D.I., Levine M., Muirhead H., and Stammers D.K. Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 Å J. Mol. Biol. 134 1979 109 142
18. Walter T.S., Diprose J.M., Mayo C.J., Siebold C., Pickford M.G., and Carter L. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 2005 651 657
19. Otwinowski A., and Minor W. Processing of X-ray diffraction data collected in oscillation mode C.W. Carter, R.M. Sweet, Methods in Enzymology 276 1997 Academic Press New York, NY 307 326
20. McCoy A.J., Gross-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
21. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132
22. Winn M.D., Murshudov G.N., and Papiz M.Z. Macromolecular TLS refinement in REFMAC at moderate resolutions Methods Enzymol. 374 2003 300 321
23. Brezski R.J., and Jordan R.E. Cleavage of IgGs by proteases associated with invasive diseases: an evasion tactic against host immunity? MAbs 2 2010 212 220
24. Collin M., Svensson M.D., Sjoholm A.G., Jensenius J.C., Sjobring U., and Olsen A. EndoS and SpeB from Streptococcus pyogenes inhibit immunoglobulin- mediated opsonophagocytosis Infect. Immun. 70 2002 6646 6651
25. Fischman A.J., Fucello A.J., Pellegrino-Gensey J.L., Geltofsky J., Yarmush M.L., Rubin R.H., and Strauss H.W. Effect of carbohydrate modification on the localization of human polyclonal IgG at focal sites of bacterial infection J. Nucl. Med. 33 1992 1378 1382
26. Allhorn M., Briceno J.G., Baudino L., Lood C., Olsson M.L., Izui S., and Collin M. The IgG-specific endoglycosidase EndoS inhibits both cellular and complement-mediated autoimmune hemolysis Blood 115 2010 5080 5088
27. Allhorn M., Olin A.I., Nimmerjahn F., and Collin M. Human IgG/FcγR interactions are modulated by streptococcal IgG glycan hydrolysis PLoS One 3 2008 e1413
28. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., and Wang X. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 2007 W375 W383
29. Feige M.J., Nath S., Catharino S.R., Weinfurtner D., Steinbacher S., and Buchner J. Structure of the murine unglycosylated IgG1 Fc fragment J. Mol. Biol. 391 2009 599 608
30. Woof J.M., and Burton D.R. Human antibody-Fc receptor interactions illuminated by crystal structures Nat. Rev., Immunol. 4 2004 89 99
31. Yamaguchi Y., Nishimura M., Nagano M., Yagi H., Sasakawa H., and Uchida K. Glycoform-dependent conformational alteration of the Fc region of human immunoglobulin G1 as revealed by NMR spectroscopy Biochim. Biophys. Acta 1760 2006 693 700
32. Houde D., Arndt J., Domeier W., Berkowitz S., and Engen J.R. Characterization of IgG1 conformation and conformational dynamics by hydrogen/deuterium exchange mass spectrometry Anal. Chem. 81 2009 5966
33. Sazinsky S.L., Ott R.G., Silver N.W., Tidor B., Ravetch J.V., and Wittrup K.D. Aglycosylated immunoglobulin G1 variants productively engage activating Fc receptors Proc. Natl Acad. Sci. USA 105 2008 20167 20172
34. Albert H., Collin M., Dudziak D., Ravetch J.V., and Nimmerjahn F. In vivo enzymatic modulation of IgG glycosylation inhibits autoimmune disease in an IgG subclass-dependent manner Proc. Natl Acad. Sci. USA 105 2008 15005 15009
35. Goetze A.M., Zhang Z., Liu L., Jacobsen F.W., and Flynn G.C. Rapid LC-MS screening for IgG Fc modifications and allelic variants in blood Molecular Immunology 49 2011 338 352
36. Zhou Q., Shankara S., Roy A., Qiu H., Estes S., and McVie-Wylie A. Development of a simple and rapid method for producing non-fucosylated oligomannose containing antibodies with increased effector function Biotechnol. Bioeng. 99 2008 652 665
37. Crispin M., Bowden T.A., Coles C.H., Harlos K., Aricescu A.R., and Harvey D.J. Carbohydrate and domain architecture of an immature antibody glycoform exhibiting enhanced effector functions J. Mol. Biol. 387 2009 1061 1066
38. Goetze A.M., Liu Y.D., Zhang Z., Shah B., Lee E., Bondarenko P.V., and Flynn G.C. High-mannose glycans on the Fc region of therapeutic IgG antibodies increase serum clearance in humans Glycobiology 21 2011 949 959
39. Chang V.T., Crispin M., Aricescu A.R., Harvey D.J., Nettleship J.E., and Fennelly J.A. Glycoprotein structural genomics: solving the glycosylation problem Structure 15 2007 267 273
40. Scanlan C.N., Ritchie G.E., Baruah K., Crispin M., Harvey D.J., and Singer B.B. Inhibition of mammalian glycan biosynthesis produces non-self antigens for a broadly neutralising, HIV-1 specific antibody J. Mol. Biol. 372 2007 16 22
41. Crispin M., Harvey D.J., Chang V.T., Yu C., Aricescu A.R., and Jones E.Y. Inhibition of hybrid- and complex-type glycosylation reveals the presence of the GlcNAc transferase I-independent fucosylation pathway Glycobiology 16 2006 748 756
42. Harvey D.J., Merry A.H., Royle L., Campbell M.P., Dwek R.A., and Rudd P.M. Proposal for a standard system for drawing structural diagrams of N- and O-linked carbohydrates and related compounds Proteomics 9 2009 3796 3801