Revisiting the role of glycosylation in the structure of human IgG Fc

ACS Chemical Biology

Volumn 7, Issue 9, 2012, Pages 1596-1602

  Borrok, M Jack ^a   Jung, Sang Taek ^a   Kang, Tae Hyun ^a   Monzingo, Arthur F ^b   Georgiou, George ^a,b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; IMMUNOGLOBULIN FC FRAGMENT;

ARTICLE; ESCHERICHIA COLI; GLYCOSYLATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

CRYSTALLOGRAPHY, X-RAY; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SCATTERING, SMALL ANGLE;

EID: 84867836578     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300130k     Document Type: Article

References (49)

1. Nimmerjahn, F., and Ravetch, J. (2007) Antibodies, Fc receptors and cancer. Curr. Opin. Immunol. 19, 239-245. (Pubitemid 46356962)
2. Nimmerjahn, F., and Ravetch, J. (2008) Fc receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47.
3. Jefferis, R., Lund, J., and Pound, J. D. (1998) IgG-Fc-mediated effector functions: molecular definition of interaction sites for effector ligands and the role of glycosylation. Immunol. Rev. 163, 59-76. (Pubitemid 28327862)
4. Jefferis, R. (2009) Glycoforms of human IgG in health and disease. Trends Glycosci. Glycotechnol. 21, 105-117.
5. Nesspor, T. C., Raju, T. S., Chin, C.-N., Vafa, O., and Brezski, R. J. (2012) Avidity confers FcgR binding and immune effector function to aglycosylated immunoglobulin G1. J. Mol. Recognit. 25, 147-154.
6. Tao, M. H., and Morrison, S. L. (1989) Studies of aglycosylated chimeric mouse-human IgG - Role of carbohydrate in the structure and effector functions mediated by the human IgG constant region. J. Immunol. 143, 2595-2601. (Pubitemid 19260070)
7. Walker, M. R., Lund, J., Thompson, K. M., and Jefferis, R. (1989) Aglycosylation of human IgG1 and IgG3 monoclonal antibodies can eliminate recognition by human cells expressing FcgammaRI and or FcgammaRII receptors. Biochem. J. 259, 347-353. (Pubitemid 19111668)
8. Beck, A., Cochet, O., and Wurch, T. (2010) GlycoFi's technology to control the glycosylation of recombinant therapeutic proteins. Expert Opin. Drug Discovery 5, 95-111.
9. Jefferis, R. (2009) Glycosylation as a strategy to improve antibody-based therapeutics. Nat. Rev. Drug Discovery 8, 226-234.
10. Niwa, R., Sakurada, M., Kobayashi, Y., Uehara, A., Matsushima, K., Ueda, R., Nakamura, K., and Shitara, K. (2005) Enhanced natural killer cell binding and activation by low-fucose IgG1 antibody results in potent antibody-dependent cellular cytotoxicity induction at lower antigen density. Clin. Cancer Res. 11, 2327-2336. (Pubitemid 40490194)
11. Okazaki, A., Shoji-Hosaka, E., Nakamura, K., Wakitani, M., Uchida, K., Kakita, S., Tsumoto, K., Kumagai, I., and Shitara, K. (2004) Fucose depletion from human IgG1 oligosaccharide enhances binding enthalpy and association rate between IgG1 and Fc gamma RIIIa. J. Mol. Biol. 336, 1239-1249. (Pubitemid 38229710)
12. Shields, R. L., Lai, J., Keck, R., O'Connell, L. Y., Hong, K., Meng, Y. G., Weikert, S. H. A., and Presta, L. G. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fc gamma RIII and antibody-dependent cellular toxicity. J. Biol. Chem. 277, 26733-26740. (Pubitemid 34951677)
13. Shinkawa, T., Nakamura, K., Yamane, N., Shoji-Hosaka, E., Kanda, Y., Sakurada, M., Uchida, K., Anazawa, H., Satoh, M., Yamasaki, M., Hanai, N., and Shitara, K. (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, 3466-3473. (Pubitemid 36801263)
14. Krapp, S., Mimura, Y., Jefferis, R., Huber, R., and Sondermann, P. (2003) Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J. Mol. Biol. 325, 979-989. (Pubitemid 36263407)
15. Feige, M. J., Nath, S., Catharino, S. R., Weinfurtner, D., Steinbacher, S., and Buchner, J. (2009) Structure of the murine unglycosylated IgG1 Fc fragment. J. Mol. Biol. 391, 599-608.
16. Jefferis, R. (2009) Aglycosylated antibodies and the methods of making and using them: WO2008030564. Expert Opin. Ther. Pat. 19, 101-105.
17. Mazor, Y., Van Blarcom, T., Mabry, R., Iverson, B., and Georgiou, G. (2007) Isolation of engineered, full-length antibodies from libraries expressed in Escherichia coli. Nat. Biotechnol. 25, 563-565. (Pubitemid 46834839)
18. Simmons, L., Reilly, D., Klimowski, L., Shantha Raju, T., Meng, G., Sims, P., Hong, K., Shields, R., Damico, L., and Rancatore, P. (2002) Expression of full-length immunoglobulins in Escherichia coli: rapid and efficient production of aglycosylated antibodies. J. Immunol. Methods 263, 133-147. (Pubitemid 34493816)
19. Jung, S. T., Kang, T. H., Kelton, W., and Georgiou, G. (2011) Bypassing glycosylation: engineering aglycosylated full-length IgG antibodies for human therapy. Curr. Opin. Biotechnol. 22, 858-67.
20. Jung, S. T., Reddy, S. T., Kang, T. H., Borrok, M. J., Sandlie, I., Tucker, P. W., and Georgiou, G. (2010) Aglycosylated IgG variants expressed in bacteria that selectively bind Fc gamma RI potentiate tumor cell killing by monocyte-dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 107, 604-609.
21. Sazinsky, S. L., Ott, R. G., Silver, N. W., Tidor, B., Ravetch, J. V., and Wittrup, K. D. (2008) Aglycosylated immunoglobulin G1 variants productively engage activating Fc receptors. Proc. Natl. Acad. Sci. U.S.A. 105, 20167-20172.
22. Lu, J. H., Ellsworth, J. L., Hamacher, N., Oak, S. W., and Sun, P. D. (2011) Crystal Structure of Fc gamma Receptor I and Its Implication in High Affinity gamma-Immunoglobulin Binding. J. Biol. Chem. 286, 40608-40613.
23. Shields, R. L., Namenuk, A. K., Hong, K., Meng, Y. G., Rae, J., Briggs, J., Xie, D., Lai, J., Stadlen, A., Li, B., Fox, J. A., and Presta, L. G. (2001) High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J. Biol. Chem. 276, 6591-6604.
24. Radaev, S., and Sun, P. (2002) Recognition of immunoglobulins by Fc gamma receptors. Mol. Immunol. 38, 1073-1083.
25. Matsumiya, S., Yamaguchi, Y., Saito, J., Nagano, M., Sasakawa, H., Otaki, S., Satoh, M., Shitara, K., and Kato, K. (2007) Structural comparison of fucosylated and nonfucosylated Fc fragments of human immunoglobulin G1. J. Mol. Biol. 368, 767-779. (Pubitemid 46527615)
26. Mimura, Y., Church, S., Ghirlando, R., Ashton, P. R., Dong, S., Goodall, M., Lund, J., and Jefferis, R. (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, 697-706. (Pubitemid 32244118)
27. Mimura, Y., Sondermann, P., Ghirlando, R., Lund, J., Young, S. P., Goodall, M., and Jefferis, R. (2001) Role of oligosaccharide residues of IgG1-Fc in Fc gamma RIIb binding. J. Biol. Chem. 276, 45539-45547.
28. Matsumiya, S., Yamaguchi, Y., Saito, J., Nagano, M., Sasakawa, H., Otaki, S., Satoh, M., Shitara, K., and Kato, K. (2011) Corrigendum to ?Structural Comparison of Fucosylated and Nonfucosylated Fc Fragments of Human Immunoglobulin G1? (vol 386, pg 767, 2007). J. Mol. Biol. 408, 1001-1001.
29. Prabakaran, P., Vu, B. K., Gan, J. H., Feng, Y., Dimitrov, D. S., and Ji, X. H. (2008) Structure of an isolated unglycosylated antibody C(H)2 domain. Acta Crystallogr. D 64, 1062-1067.
30. Kato, K., Sautes-Fridman, C., Yamada, W., Kobayashi, K., Uchiyama, S., Kim, H., Enokizono, J., Galinha, A., Kobayashi, Y., Fridman, W. H., Arata, Y., and Shimada, I. (2000) Structural basis of the interaction between IgG and Fc gamma receptors. J. Mol. Biol. 295, 213-224. (Pubitemid 30045355)
31. Oganesyan, V., Damschroder, M. M., Leach, W., Wu, H., and Dall'Acqua, W. F. (2008) Structural characterization of a mutated, ADCC-enhanced human Fc fragment. Mol. Immunol. 45, 1872-1882.
32. Borrok, M. J., Zhu, Y. M., Forest, K. T., and Kiessling, L. L. (2009) Structure-based design of a periplasmic binding protein antagonist that prevents domain closure. ACS Chem. Biol. 4, 447-456.
33. Komeiji, Y., Ueno, Y., and Uebayasi, M. (2002) Molecular dynamics simulations revealed Ca2+-dependent conformational change of calmodulin. FEBS Lett. 521, 133-139. (Pubitemid 34628473)
34. Shilton, B., Flocco, M., Nilsson, M., and Mowbray, S. (1996) Conformational changes of three periplasmic receptors for bacterial chemotaxis and transport: the maltose-, glucose/galactose-and ribosebinding proteins. J. Mol. Biol. 264, 350-363. (Pubitemid 26402702)
35. Guinier, A., and Fournet, G. (Eds.) (1955) Small-Angle Scattering of X-rays, John Wiley and Sons, New York.
36. Sondermann, P., Huber, R., Oosthuizen, V., and Jacob, U. (2000) The 3.2-angstrom crystal structure of the human IgG1 Fc fragment-Fc gamma RIII complex. Nature 406, 267-273. (Pubitemid 30604397)
37. Ferrara, C., Grau, S., Jager, C., Sondermann, P., Brunker, P., Waldhauer, I., Hennig, M., Ruf, A., Rufer, A. C., Stihle, M., Umana, P., and Benz, J. (2011) Unique carbohydrate-carbohydrate interactions are required for high affinity binding between Fc gamma RIII and antibodies lacking core fucose. Proc. Natl. Acad. Sci. U.S.A. 108, 12669-12674.
38. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
39. McCoy, A., Grosse-Kunstleve, R., Storoni, L., and Read, R. (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr. D 61, 458-464. (Pubitemid 43934606)
40. Storoni, L., McCoy, A., and Read, R. (2004) Likelihoodenhanced fast rotation functions. Acta Crystallogr. D 60, 432-438.
41. Winn, M., Murshudov, G., and Papiz, M. (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Method Enzymol. 374, 300-321. (Pubitemid 37531815)
42. Winn, M. (2002) An overview of the CCP4 project in protein crystallography: an example of a collaborative project. J. Synchrotron Radiat. 10, 23-25. (Pubitemid 36515712)
43. Kleywegt, G. (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D 52, 842-857. (Pubitemid 27064310)
44. DeLano, W. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, Palo Alto, CA, USA; http://www.pymol.org.
45. Konarev, P., Petoukhov, M., Volkov, V., and Svergun, D. (2006) ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39, 277-286.
46. Konarev, P., Volkov, V., Sokolova, A., Koch, M., and Svergun, D. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282.
47. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886. (Pubitemid 29269438)
48. Deisenhofer, J. (1981) 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. Biochem. 20, 2361-2370. (Pubitemid 11089772)
49. Saphire, E. O., Parren, P., Pantophlet, R., Zwick, M. B., Morris, G. M., Rudd, P. M., Dwek, R. A., Stanfield, R. L., Burton, D. R., and Wilson, I. A. (2001) Crystal structure of a neutralizing human IgG against HIV-1: A template for vaccine design. Science 293, 1155-1159. (Pubitemid 32758099)