Post-translational modifications differentially affect IgG1 conformation and receptor binding

Molecular and Cellular Proteomics

Volumn 9, Issue 8, 2010, Pages 1716-1728

  Houde, Damian ^a,b   Peng, Yucai ^a   Berkowitz, Steven A ^a   Engen, John R ^b  

^a BIOGEN   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUTERIUM; FC GAMMA RECEPTOR IIIA; FC RECEPTOR; FUCOSE; GALACTOSE; HYDROGEN; IMMUNOGLOBULIN G1 ANTIBODY; METHIONINE; UNCLASSIFIED DRUG; IMMUNOGLOBULIN G; MUTANT PROTEIN; PROTON;

ANIMAL CELL; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FEMALE; FUCOSYLATION; GALACTOSYLATION; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RECEPTOR BINDING; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHO CELL LINE; CRICETULUS; GLYCOSYLATION; HAMSTER; HUMAN; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DEUTERIUM; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN G; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTONS; RECEPTORS, FC;

EID: 77955412238     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M900540-MCP200     Document Type: Article

References (51)

1. Walsh, C. T. (2006) Posttranslational Modification of Proteins: Expanding Nature's Inventory, 1st Ed., Roberts and Co. Publishers, Greenwood Village, CO
2. Johnson, L. N., and Barford, D. (1993) The effects of phosphorylation on the structure and function of proteins. Annu. Rev. Biophys. Biomol. Struct. 22, 199-232
3. Carter, P. J. (2006) Potent antibody therapeutics by design. Nat. Rev. Immunol. 6, 343-357
4. Saphire, E. O., Parren, P. W., 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
5. Garber, E., and Demarest, S. J. (2007) A broad range of Fab stabilities within a host of therapeutic IgGs. Biochem. Biophys. Res. Commun. 355, 751-757
6. Jefferis, R. (2009) Glycosylation as a strategy to improve antibody-based therapeutics. Nat. Rev. Drug Discov. 8, 226-234
7. Walsh, G., and Jefferis, R. (2006) Post-translational modifications in the context of therapeutic proteins. Nat. Biotechnol. 24, 1241-1252
8. Walsh, C. T., Garneau-Tsodikova, S., and Gatto, G. J., Jr. (2005) Protein posttranslational modifications: the chemistry of proteome diversifications. Angew. Chem. Int. Ed. Engl. 44, 7342-7372
9. Aebersold, R., and Mann, M. (2003) Mass spectrometry-based proteomics. Nature 422, 198-207
10. Bertolotti-Ciarlet, A., Wang, W., Lownes, R., Pristatsky, P., Fang, Y., McKelvey, T., Li, Y., Li, Y., Drummond, J., Prueksaritanont, T., and Vlasak, J. (2009) Impact of methionine oxidation on the binding of human IgG1 to Fc Rn and Fc gamma receptors. Mol. Immunol. 46, 1878-1882
11. Robison, A. J., Winder, D. G., Colbran, R. J., and Bartlett, R. K. (2007) Oxidation of calmodulin alters activation and regulation of CaMKII. Biochem. Biophys. Res. Commun. 356, 97-101
12. Silva, M. M., Lamarre, B., Cerasoli, E., Rakowska, P., Hills, A., Bailey, M. J., Wheeler, J. X., Burns, C. J., Gaines-Das, R. E., Jones, C., and Robinson, C. J. (2008) Physicochemical and biological assays for quality control of biopharmaceuticals: interferon alpha-2 case study. Biologicals 36, 383-392
13. Waak, J., Weber, S. S., Görner, K., Schall, C., Ichijo, H., Stehle, T., and Kahle, P. J. (2009) Oxidizable residues mediating protein stability and cytoprotective interaction of DJ-1 with apoptosis signal-regulating kinase 1. J. Biol. Chem. 284, 14245-14257
14. 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
15. Arnold, J. N., Wormald, M. R., Sim, R. B., Rudd, P. M., and Dwek, R. A. (2007) The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 25, 21-50
16. 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
17. Yamaguchi, Y., Nishimura, M., Nagano, M., Yagi, H., Sasakawa, H., Uchida, K., Shitara, K., and Kato, K. (2006) Glycoform-dependent conformational alteration of the Fc region of human immunoglobulin G1 as revealed by NMR spectroscopy. Biochim. Biophys. Acta 1760, 693-700
18. Nölting, B. (2006) Methods in Modern Biophysics, 2nd Ed., Springer, New York
19. Chruszcz, M., Wlodawer, A., and Minor, W. (2008) Determination of protein structures - a series of fortunate events. Biophys. J. 95, 1-9
20. Foster, M. P., McElroy, C. A., and Amero, C. D. (2007) Solution NMR of large molecules and assemblies. Biochemistry 46, 331-340
21. Sprangers, R., Velyvis, A., and Kay, L. E. (2007) Solution NMR of supramolecular complexes: providing new insights into function. Nat. Methods 4, 697-703
22. Houde, D., Arndt, J., Domeier, W., Berkowitz, S., and Engen, J. R. (2009) Characterization of IgG1 conformation and conformational dynamics by hydrogen/deuterium exchange mass spectrometry. Anal. Chem. 81, 2644-2651
23. Warnock, D., Bai, X., Autote, K., Gonzales, J., Kinealy, K., Yan, B., Qian, J., Stevenson, T., Zopf, D., and Bayer, R. J. (2005) In vitro galactosylation of human IgG at 1 kg scale using recombinant galactosyltransferase. Biotechnol. Bioeng. 92, 831-842
24. Houde, D., Kauppinen, P., Mhatre, R., and Lyubarskaya, Y. (2006) Determination of protein oxidation by mass spectrometry and method transfer to quality control. J. Chromatogr. A 1123, 189-198
25. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423
26. Glickman, J. F., Wu, X., Mercuri, R., Illy, C., Bowen, B. R., He, Y., and Sills, M. (2002) A comparison of ALPHAScreen, TR-FRET, and TRF as assay methods for FXR nuclear receptors. J. Biomol. Screen. 7, 3-10
27. Wales, T. E., Fadgen, K. E., Gerhardt, G. C., and Engen, J. R. (2008) High-speed and high-resolution UPLC separation at zero degrees Celsius. Anal. Chem. 80, 6815-6820
28. Silva, J. C., Gorenstein, M. V., Li, G. Z., Vissers, J. P., and Geromanos, S. J. (2006) Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol. Cell. Proteomics 5, 144-156
29. Weis, D. D., Engen, J. R., and Kass, I. J. (2006) Semi-automated data processing of hydrogen exchange mass spectra using HX-Express. J. Am. Soc. Mass Spectrom. 17, 1700-1703
30. Wales, T. E., and Engen, J. R. (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom. Rev. 25, 158-170
31. Burkitt, W., and O'Connor, G. (2008) Assessment of the repeatability and reproducibility of hydrogen/deuterium exchange mass spectrometry measurements. Rapid Commun. Mass Spectrom. 22, 3893-3901
32. Sondermann, P., Huber, R., Oosthuizen, V., and Jacob, U. (2000) The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex. Nature 406, 267-273
33. Boyd, P. N., Lines, A. C., and Patel, A. K. (1995) The effect of the removal of sialic acid, galactose and total carbohydrate on the functional activity of Campath-1H. Mol. Immunol. 32, 1311-1318
34. Radaev, S., and Sun, P. (2002) Recognition of immunoglobulins by Fc-gamma receptors. Mol. Immunol. 38, 1073-1083
35. 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
36. 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 FcgammaRIIIa. J. Mol. Biol. 336, 1239-1249
37. Satoh, M., Iida, S., and Shitara, K. (2006) Non-fucosylated therapeutic antibodies as next-generation therapeutic antibodies. Expert Opin. Biol. Ther. 6, 1161-1173
38. 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
39. Ionescu, R. M., Vlasak, J., Price, C., and Kirchmeier, M. (2008) Contribution of variable domains to the stability of humanized IgG1 monoclonal antibodies. J. Pharm. Sci. 97, 1414-1426
40. Liu, D., Ren, D., Huang, H., Dankberg, J., Rosenfeld, R., Cocco, M. J., Li, L., Brems, D. N., and Remmele, R. L., Jr. (2008) Structure and stability changes of human IgG1 Fc as a consequence of methionine oxidation. Biochemistry 47, 5088-5100
41. Smith, D. L., Deng, Y., and Zhang, Z. (1997) Probing the non-covalent structure of proteins by amide hydrogen exchange and mass spectrometry. J. Mass Spectrom. 32, 135-146
42. Engen, J. R. (2003) Analysis of protein complexes with hydrogen exchange and mass spectrometry. Analyst 128, 623-628
43. Radaev, S., Motyka, S., Fridman, W. H., Sautes-Fridman, C., and Sun, P. D. (2001) The structure of a human type III Fcgamma receptor in complex with Fc. J. Biol. Chem. 276, 16469-16477
44. 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- and 2.8-A resolution. Biochemistry 20, 2361-2370
45. Wormald, M. R., Rudd, P. M., Harvey, D. J., Chang, S. C., Scragg, I. G., and Dwek, R. A. (1997) Variations in oligosaccharide-protein interactions in immunoglobulin G determine the site-specific glycosylation profiles and modulate the dynamic motion of the Fc oligosaccharides. Biochemistry 36, 1370-1380
46. 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
47. Shoemaker, B. A., Portman, J. J., and Wolynes, P. G. (2000) Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. U.S.A. 97, 8868-8873
48. Dharmasiri, K., and Smith, D. L. (1996) Mass spectrometric determination of isotopic exchange rates of amide hydrogens located on the surfaces of proteins. Anal. Chem. 68, 2340-2344
49. Mandell, J. G., Falick, A. M., and Komives, E. A. (1998) Identification of protein-protein interfaces by decreased amide proton solvent accessibility. Proc. Natl. Acad. Sci. U.S.A. 95, 14705-14710
50. Engen, J. R. (2009) Analysis of protein conformation and dynamics by hydrogen/deuterium exchange MS. Anal. Chem. 81, 7870-7875
51. Krieger, E., Koraimann, G., and Vriend, G. (2002) Increasing the precision of comparative models with YASARA NOVA - a self-parameterizing force field. Proteins 47, 393-402