The Structural Role of Antibody N-Glycosylation in Receptor Interactions

Structure

Volumn 23, Issue 9, 2015, Pages 1573-1583

  Subedi, Ganesh P ^a   Barb, Adam W ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; GLYCAN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN E; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G4; IMMUNOGLOBULIN M; RECEPTOR ANTIBODY; ASPARAGINE; IMMUNOGLOBULIN G; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CONFORMATION; GLYCOSYLATION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN QUATERNARY STRUCTURE; RECEPTOR BINDING; CHEMISTRY; METABOLISM; MOLECULAR MODEL; X RAY CRYSTALLOGRAPHY;

ASPARAGINE; CRYSTALLOGRAPHY, X-RAY; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY;

EID: 84947032537     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.06.015     Document Type: Article

References (83)

1. G.P. Adams, and L.M. Weiner Monoclonal antibody therapy of cancer Nat. Biotechnol. 23 2005 1147 1157
2. A.A. Ahmed, J. Giddens, A. Pincetic, J.V. Lomino, J.V. Ravetch, L.X. Wang, and P.J. Bjorkman Structural characterization of anti-inflammatory immunoglobulin G Fc proteins J. Mol. Biol. 426 2014 3166 3179
3. J.N. Arnold, M.R. Wormald, R.B. Sim, P.M. Rudd, and R.A. Dwek The impact of glycosylation on the biological function and structure of human immunoglobulins Annu. Rev. Immunol. 25 2007 21 50
4. A.W. Barb Intramolecular N-glycan/polypeptide interactions observed at multiple N-glycan remodeling steps through [(13)C,(15)N]-N-acetylglucosamine labeling of immunoglobulin G1 Biochemistry 54 2015 313 322
5. A.W. Barb, and J.H. Prestegard NMR analysis demonstrates immunoglobulin G N-glycans are accessible and dynamic Nat. Chem. Biol. 7 2011 147 153
6. A.W. Barb, E.K. Brady, and J.H. Prestegard Branch-specific sialylation of IgG-Fc glycans by ST6Gal-I Biochemistry 48 2009 9705 9707
7. A.W. Barb, L. Meng, Z. Gao, R.W. Johnson, K.W. Moremen, and J.H. Prestegard NMR characterization of immunoglobulin G Fc glycan motion on enzymatic sialylation Biochemistry 51 2012 4618 4626
8. K. Baruah, T.A. Bowden, B.A. Krishna, R.A. Dwek, M. Crispin, and C.N. Scanlan Selective deactivation of serum IgG: a general strategy for the enhancement of monoclonal antibody receptor interactions J. Mol. Biol. 420 2012 1 7
9. L. Baudino, Y. Shinohara, F. Nimmerjahn, J. Furukawa, M. Nakata, E. Martinez-Soria, F. Petry, J.V. Ravetch, S. Nishimura, and S. Izui Crucial role of aspartic acid at position 265 in the CH2 domain for murine IgG2a and IgG2b Fc-associated effector functions J. Immunol. 181 2008 6664 6669
10. H.M. Berman, T. Battistuz, T.N. Bhat, W.F. Bluhm, P.E. Bourne, K. Burkhardt, Z. Feng, G.L. Gilliland, L. Iype, S. Jain, and et al. The Protein Data Bank Acta Crystallogr. D Biol. Crystallogr. 58 2002 899 907
11. M.J. Borrok, S.T. Jung, T.H. Kang, A.F. Monzingo, and G. Georgiou Revisiting the role of glycosylation in the structure of human IgG Fc ACS Chem. Biol. 7 2012 1596 1602
12. S. Bournazos, F. Klein, J. Pietzsch, M.S. Seaman, M.C. Nussenzweig, and J.V. Ravetch Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity Cell 158 2014 1243 1253
13. P. Bruhns, B. Iannascoli, P. England, D.A. Mancardi, N. Fernandez, S. Jorieux, and M. Daeron Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses Blood 113 2009 3716 3725
14. J. Cavanagh, W.J. Fairbrother, A.G. Palmer, M. Rance, and N.J. Skelton Protein NMR Spectroscopy: Principles and Practice Second Edition 2007 Academic Press
15. H.E. Chadd, and S.M. Chamow Therapeutic antibody expression technology Curr. Opin. Biotechnol. 12 2001 188 194
16. A.C. Chan, and P.J. Carter Therapeutic antibodies for autoimmunity and inflammation Nat. Rev. Immunol. 10 2010 301 316
17. R.A. Clynes, T.L. Towers, L.G. Presta, and J.V. Ravetch Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets Nat. Med. 6 2000 443 446
18. G. Cornilescu, J.L. Marquardt, M. Ottiger, and A. Bax Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase J. Am. Chem. Soc. 120 1998 6836 6837
19. M. Crispin, T.A. Bowden, C.H. Coles, K. Harlos, A.R. Aricescu, D.J. Harvey, D.I. Stuart, and E.Y. Jones Carbohydrate and domain architecture of an immature antibody glycoform exhibiting enhanced effector functions J. Mol. Biol. 387 2009 1061 1066
20. M. Crispin, X. Yu, and T.A. Bowden Crystal structure of sialylated IgG Fc: implications for the mechanism of intravenous immunoglobulin therapy Proc. Natl. Acad. Sci. USA 110 2013 E3544 E3546
21. J. Deisenhofer 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- and 2.8-A resolution Biochemistry 20 1981 2361 2370
22. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
23. W.L. DeLano, M.H. Ultsch, A.M. de Vos, and J.A. Wells Convergent solutions to binding at a protein-protein interface Science 287 2000 1279 1283
24. B.T. Farmer 2nd, K.L. Constantine, V. Goldfarb, M.S. Friedrichs, M. Wittekind, J. Yanchunas Jr., J.G. Robertson, and L. Mueller Localizing the NADP+ binding site on the MurB enzyme by NMR Nat. Struct. Biol. 3 1996 995 997
25. M.J. Feige, S. Nath, S.R. Catharino, D. Weinfurtner, S. Steinbacher, and J. Buchner Structure of the murine unglycosylated IgG1 Fc fragment J. Mol. Biol. 391 2009 599 608
26. C. Ferrara, S. Grau, C. Jager, P. Sondermann, P. Brunker, I. Waldhauer, M. Hennig, A. Ruf, A.C. Rufer, M. Stihle, and et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose Proc. Natl. Acad. Sci. USA 108 2011 12669 12674
27. M. Frank, R.C. Walker, W.N. Lanzilotta, J.H. Prestegard, and A.W. Barb Immunoglobulin G1 Fc domain motions: implications for Fc engineering J. Mol. Biol. 426 2014 1799 1811
28. E.C. Franklin Structure and function of immunoglobulins Acta Endocrinol. Suppl. (Copenh.) 194 1975 77 95
29. Y. Gavel, and G. von Heijne Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering Protein Eng. 3 1990 433 442
30. S.R. Hanson, E.K. Culyba, T.L. Hsu, C.H. Wong, J.W. Kelly, and E.T. Powers The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability Proc. Natl. Acad. Sci. USA 106 2009 3131 3136
31. R. Huber, J. Deisenhofer, P.M. Colman, M. Matsushima, and W. Palm Crystallographic structure studies of an IgG molecule and an Fc fragment Nature 264 1976 415 420
32. R. Ishima, and D.A. Torchia Protein dynamics from NMR Nat. Struct. Biol. 7 2000 740 743
33. S.R. Jaffe, B. Strutton, Z. Levarski, J. Pandhal, and P.C. Wright Escherichia coli as a glycoprotein production host: recent developments and challenges Curr. Opin. Biotechnol. 30 2014 205 210
34. C. Janeway, K.P. Murphy, P. Travers, and M. Walport Janeway's Immuno Biology Seventh Edition 2008 Garland Science
35. R. Jefferis Recombinant antibody therapeutics: the impact of glycosylation on mechanisms of action Trends Pharmacol. Sci. 30 2009 356 362
36. R. Jefferis, J. Lund, and J.D. Pound IgG-Fc-mediated effector functions: molecular definition of interaction sites for effector ligands and the role of glycosylation Immunol. Rev. 163 1998 59 76
37. X.R. Jiang, A. Song, S. Bergelson, T. Arroll, B. Parekh, K. May, S. Chung, R. Strouse, A. Mire-Sluis, and M. Schenerman Advances in the assessment and control of the effector functions of therapeutic antibodies Nat. Rev. Drug Discov. 10 2011 101 111
38. Y. Kaneko, F. Nimmerjahn, and J.V. Ravetch Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation Science 313 2006 670 673
39. K. Kato, Y. Yamaguchi, and Y. Arata Stable-isotope-assisted NMR approaches to glycoproteins using immunoglobulin G as a model system Prog. Nucl. Magn. Reson. Spectrosc. 56 2010 346 359
40. A. Kobata The N-linked sugar chains of human immunoglobulin G: their unique pattern, and their functional roles Biochim. Biophys. Acta 1780 2008 472 478
41. S. Krapp, Y. Mimura, R. Jefferis, R. Huber, and P. Sondermann Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity J. Mol. Biol. 325 2003 979 989
42. G.A. Lazar, A.J. Chirino, W. Dang, J.R. Desjarlais, S.K. Doberstein, R.J. Hayes, S.B. Karki, and O. Vafa Optimized Fc Variants and Methods for Their Generation 2009 US Patent US7662925 B2
43. K. Lindorff-Larsen, R.B. Best, M.A. Depristo, C.M. Dobson, and M. Vendruscolo Simultaneous determination of protein structure and dynamics Nature 433 2005 128 132
44. Y. Liu, and J.H. Prestegard Measurement of one and two bond N-C couplings in large proteins by TROSY-based J-modulation experiments J. Magn. Reson. 200 2009 109 118
45. J. Lund, N. Takahashi, J.D. Pound, M. Goodall, H. Nakagawa, and R. Jefferis Oligosaccharide-protein interactions in IgG can modulate recognition by Fc gamma receptors FASEB J. 9 1995 115 119
46. J. Lund, N. Takahashi, J.D. Pound, M. Goodall, and R. Jefferis 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. 157 1996 4963 4969
47. A. Lux, X. Yu, C.N. Scanlan, and F. Nimmerjahn Impact of immune complex size and glycosylation on IgG binding to human FcgammaRs J. Immunol. 190 2013 4315 4323
48. S. Matsumiya, Y. Yamaguchi, J. Saito, M. Nagano, H. Sasakawa, S. Otaki, M. Satoh, K. Shitara, and K. Kato Structural comparison of fucosylated and nonfucosylated Fc fragments of human immunoglobulin G1 J. Mol. Biol. 368 2007 767 779
49. H.D. Mertens, and D.I. Svergun Structural characterization of proteins and complexes using small-angle X-ray solution scattering J. Struct. Biol. 172 2010 128 141
50. Y. Mimura, P. Sondermann, R. Ghirlando, J. Lund, S.P. Young, M. Goodall, and R. Jefferis Role of oligosaccharide residues of IgG1-Fc in Fc gamma RIIb binding J. Biol. Chem. 276 2001 45539 45547
51. A. Mittermaier, and L.E. Kay New tools provide new insights in NMR studies of protein dynamics Science 312 2006 224 228
52. T. Mizuochi, T. Taniguchi, A. Shimizu, and A. Kobata Structural and numerical variations of the carbohydrate moiety of immunoglobulin G J. Immunol. 129 1982 2016 2020
53. T. Mizushima, H. Yagi, E. Takemoto, M. Shibata-Koyama, Y. Isoda, S. Iida, K. Masuda, M. Satoh, and K. Kato Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans Genes Cells 16 2011 1071 1080
54. F. Nimmerjahn, and J.V. Ravetch Fcgamma receptors as regulators of immune responses Nat. Rev. Immunol. 8 2008 34 47
55. A. Nisonoff, F.C. Wissler, L.N. Lipman, and D.L. Woernley Separation of univalent fragments from the bivalent rabbit antibody molecule by reduction of disulfide bonds Arch. Biochem. Biophys. 89 1960 230 244
56. M. Nose, and H. Wigzell Biological significance of carbohydrate chains on monoclonal antibodies Proc. Natl. Acad. Sci. USA 80 1983 6632 6636
57. R.R. Porter The hydrolysis of rabbit γ-globulin and antibodies with crystalline papain Biochem. J. 73 1959 119 126
58. J.H. Prestegard, D.A. Agard, K.W. Moremen, L.A. Lavery, L.C. Morris, and K. Pederson Sparse labeling of proteins: structural characterization from long range constraints J. Magn. Reson. 241 2014 32 40
59. T.S. Raju Terminal sugars of Fc glycans influence antibody effector functions of IgGs Curr. Opin. Immunol. 20 2008 471 478
60. T.L. Religa, R. Sprangers, and L.E. Kay Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR Science 328 2010 98 102
61. A.C. Roque, C.R. Lowe, and M.A. Taipa Antibodies and genetically engineered related molecules: production and purification Biotechnol. Prog. 20 2004 639 654
62. S.L. Sazinsky, R.G. Ott, N.W. Silver, B. Tidor, J.V. Ravetch, and K.D. Wittrup Aglycosylated immunoglobulin G1 variants productively engage activating Fc receptors Proc. Natl. Acad. Sci. USA 105 2008 20167 20172
63. B.J. Scallon, S.H. Tam, S.G. McCarthy, A.N. Cai, and T.S. Raju Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality Mol. Immunol. 44 2007 1524 1534
64. A.M. Scott, J.D. Wolchok, and L.J. Old Antibody therapy of cancer Nat. Rev. Cancer 12 2012 278 287
65. N. Sethuraman, and T.A. Stadheim Challenges in therapeutic glycoprotein production Curr. Opin. Biotechnol. 17 2006 341 346
66. S. Siberil, C.A. Dutertre, W.H. Fridman, and J.L. Teillaud FcgammaR: The key to optimize therapeutic antibodies? Crit. Rev. Oncol. Hematol. 62 2007 26 33
67. N. Silva-Martin, S.G. Bartual, E. Ramirez-Aportela, P. Chacon, C.G. Park, and J.A. Hermoso Structural basis for selective recognition of endogenous and microbial polysaccharides by macrophage receptor SIGN-R1 Structure 22 2014 1595 1606
68. N. Singh, J. Pirsch, and M. Samaniego Antibody-mediated rejection: treatment alternatives and outcomes Transplant. Rev. (Orlando) 23 2009 34 46
69. M.X. Sliwkowski, and I. Mellman Antibody therapeutics in cancer Science 341 2013 1192 1198
70. P. Sondermann Crystal structures of human IgG-Fc fragments and their complexes with Fcγ receptors F. Nimmerjahn, Molecular and Cellular Mechanisms of Antibody Activity 2013 Springer Science+Business Media 61 83
71. P. Sondermann, R. Huber, V. Oosthuizen, and U. Jacob The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex Nature 406 2000 267 273
72. G.P. Subedi, Q.M. Hanson, and A.W. Barb Restricted motion of the conserved immunoglobulin G1 N-glycan is essential for efficient FcgammaRIIIa binding Structure 22 2014 1478 1488
73. B.J. Sutton, and D.C. Phillips The three-dimensional structure of the carbohydrate within the Fc fragment of immunoglobulin G Biochem. Soc. Trans. 11 1983 130 132
74. V. Tugarinov, P.M. Hwang, and L.E. Kay Nuclear magnetic resonance spectroscopy of high-molecular-weight proteins Annu. Rev. Biochem. 73 2004 107 146
75. V. Tugarinov, V. Kanelis, and L.E. Kay Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy Nat. Protoc. 1 2006 749 754
76. A.S. Vandersall-Nairn, R.K. Merkle, K. O'Brien, T.N. Oeltmann, and K.W. Moremen Cloning, expression, purification, and characterization of the acid α-mannosidase from Trypanosoma cruzi Glycobiology 8 1998 1183 1194
77. A. Varki Essentials of Glycobiology Second Edition 2009 Cold Spring Harbor Laboratory Press
78. J.M. Word, S.C. Lovell, J.S. Richardson, and D.C. Richardson Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation J. Mol. Biol. 285 1999 1735 1747
79. H. Yagi, Y. Zhang, M. Yagi-Utsumi, T. Yamaguchi, S. Iida, Y. Yamaguchi, and K. Kato Backbone 1H, 13C, and 15N resonance assignments of the Fc fragment of human immunoglobulin G glycoprotein Biomol. NMR Assign. 2014
80. Y. Yamaguchi, K. Kato, M. Shindo, S. Aoki, K. Furusho, K. Koga, N. Takahashi, Y. Arata, and I. Shimada Dynamics of the carbohydrate chains attached to the Fc portion of immunoglobulin G as studied by NMR spectroscopy assisted by selective C-13 labeling of the glycans J. Biomol. NMR 12 1998 385 394
81. Y. Yamaguchi, M. Nishimura, M. Nagano, H. Yagi, H. Sasakawa, K. Uchida, K. Shitara, and K. Kato Glycoform-dependent conformational alteration of the Fc region of human immunoglobulin G1 as revealed by NMR spectroscopy Biochim. Biophys. Acta 1760 2006 693 700
82. X. Yu, K. Baruah, D.J. Harvey, S. Vasiljevic, D.S. Alonzi, B.D. Song, M.K. Higgins, T.A. Bowden, C.N. Scanlan, and M. Crispin Engineering hydrophobic protein-carbohydrate interactions to fine-tune monoclonal antibodies J. Am. Chem. Soc. 135 2013 9723 9732
83. M. Zweckstetter, and A. Bax Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR J. Am. Chem. Soc. 122 2000 3791 3792