Correlating the Impact of Well-Defined Oligosaccharide Structures on Physical Stability Profiles of IgG1-Fc Glycoforms

Journal of Pharmaceutical Sciences

Volumn 105, Issue 2, 2016, Pages 588-601

  More, Apurva S ^a   Toprani, Vishal M ^a   Okbazghi, Solomon Z ^a   Kim, Jae H ^a   Joshi, Sangeeta B ^a   Middaugh, C Russell ^a   Tolbert, Thomas J ^a   Volkin, David B ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

conformation; Fc; formulation; glycosylation; IgG; monoclonal antibody; spectroscopy; stability

Indexed keywords

ACTIVIN RECEPTOR 2B IMMUNOGLOBULIN G1 FC FRAGMENT FUSION PROTEIN; BIOSIMILAR AGENT; MACROGOL; MANNOSE; OLIGOSACCHARIDE; SODIUM CHLORIDE; SUCROSE; GLYCOPROTEIN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; MACROGOL DERIVATIVE;

ARTICLE; CHEMICAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; DRUG CONFORMATION; DRUG FORMULATION; DRUG SOLUBILITY; DRUG STABILITY; MATHEMATICAL MODEL; PARTICLE SIZE; PH; PRECIPITATION; TEMPERATURE DEPENDENCE; THERMODYNAMICS; CHEMISTRY; GLYCOSYLATION; PROTEIN CONFORMATION;

DRUG STABILITY; GLYCOPROTEINS; GLYCOSYLATION; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; OLIGOSACCHARIDES; POLYETHYLENE GLYCOLS; PROTEIN CONFORMATION;

EID: 84964553219     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1016/j.xphs.2015.10.014     Document Type: Article

References (63)

1. 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
2. A. Beck, T. Wurch, C. Bailly, and N. Corvaia Strategies and challenges for the next generation of therapeutic antibodies Nat Rev Immunol 10 5 2010 345 352
3. M. Dalziel, M. Crispin, C.N. Scanlan, N. Zitzmann, and R.A. Dwek Emerging principles for the therapeutic exploitation of glycosylation Science 343 6166 2014 1235681
4. D.M. Ecker, S.D. Jones, and H.L. Levine The therapeutic monoclonal antibody market MAbs 7 1 2015 9 14
5. A. Beck, E. Wagner-Rousset, D. Ayoub, A. Van Dorsselaer, and S. Sanglier-Cianferani Characterization of therapeutic antibodies and related products Anal Chem 85 2 2013 715 736
6. R. Niwa, and M. Satoh The current status and prospects of antibody engineering for therapeutic use: focus on glycoengineering technology J Pharm Sci 104 3 2015 930 941
7. R. Jefferis Glycosylation as a strategy to improve antibody-based therapeutics Nat Rev Drug Discov 8 3 2009 226 234
8. Y. Mimura, P. Sondermann, R. Ghirlando, and et al. Role of oligosaccharide residues of IgG1-Fc in Fc gamma RIIb binding J Biol Chem 276 49 2001 45539 45547
9. 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 5 2003 979 989
10. D. Hristodorov, R. Fischer, and L. Linden With or without sugar? (A) glycosylation of therapeutic antibodies Mol Biotechnol 54 3 2013 1056 1068
11. X. Yu, K. Baruah, D.J. Harvey, and et al. Engineering hydrophobic protein-carbohydrate interactions to fine-tune monoclonal antibodies J Am Chem Soc 135 26 2013 9723 9732
12. C.W. Lin, M.H. Tsai, S.T. Li, and et al. A common glycan structure on immunoglobulin G for enhancement of effector functions Proc Natl Acad Sci U S A 112 34 2015 10611 10616
13. L. Liu Antibody glycosylation and its impact on the pharmacokinetics and pharmacodynamics of monoclonal antibodies and Fc-fusion proteins J Pharm Sci 104 6 2015 1866 1884
14. R.M. Anthony, F. Wermeling, and J.V. Ravetch Novel roles for the IgG Fc glycan Ann N Y Acad Sci 1253 2012 170 180
15. H. Li, and M. d'Anjou Pharmacological significance of glycosylation in therapeutic proteins Curr Opin Biotechnol 20 6 2009 678 684
16. M. Yu, D. Brown, C. Reed, and et al. Production, characterization, and pharmacokinetic properties of antibodies with N-linked mannose-5 glycans MAbs 4 4 2012 475 487
17. R.J. Sola, and K. Griebenow Effects of glycosylation on the stability of protein pharmaceuticals J Pharm Sci 98 4 2009 1223 1245
18. K. Zheng, M. Yarmarkovich, C. Bantog, R. Bayer, and T.W. Patapoff Influence of glycosylation pattern on the molecular properties of monoclonal antibodies MAbs 6 3 2014 649 658
19. C.H. Li, L.O. Narhi, J. Wen, and et al. Effect of pH, temperature, and salt on the stability of Escherichia coli- and Chinese hamster ovary cell-derived IgG1 Fc Biochemistry 51 50 2012 10056 10065
20. Y. Lu, K. Westland, Y.H. Ma, and H. Gadgil Evaluation of effects of Fc domain high-mannose glycan on antibody stability J Pharm Sci 101 11 2012 4107 4117
21. W. Wang, S. Singh, D.L. Zeng, K. King, and S. Nema Antibody structure, instability, and formulation J Pharm Sci 96 1 2007 1 26
22. R. Jefferis Isotype and glycoform selection for antibody therapeutics Arch Biochem Biophys 526 2 2012 159 166
23. 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 9 2012 1596 1602
24. P.M. Buck, S. Kumar, and S.K. Singh Consequences of glycan truncation on Fc structural integrity MAbs 5 6 2013 904 916
25. H. Liu, G.G. Bulseco, and J. Sun Effect of posttranslational modifications on the thermal stability of a recombinant monoclonal antibody Immunol Lett 106 2 2006 144 153
26. R.J. Sola, and K. Griebenow Glycosylation of therapeutic proteins: an effective strategy to optimize efficacy BioDrugs 24 1 2010 9 21
27. D. Houde, J. Arndt, W. Domeier, S. Berkowitz, and J.R. Engen Characterization of IgG1 conformation and conformational dynamics by hydrogen/deuterium exchange mass spectrometry Anal Chem 81 7 2009 2644 2651
28. D. Kameoka, E. Masuzaki, T. Ueda, and T. Imoto Effect of buffer species on the unfolding and the aggregation of humanized IgG J Biochem 142 3 2007 383 391
29. T. Wang, O.S. Kumru, L. Yi, and et al. Effect of ionic strength and pH on the physical and chemical stability of a monoclonal antibody antigen-binding fragment J Pharm Sci 102 8 2013 2520 2537
30. W. Cheng, S.B. Joshi, F. He, and et al. Comparison of high-throughput biophysical methods to identify stabilizing excipients for a model IgG2 monoclonal antibody: conformational stability and kinetic aggregation measurements J Pharm Sci 101 5 2012 1701 1720
31. V. Kayser, N. Chennamsetty, V. Voynov, K. Forrer, B. Helk, and B.L. Trout Glycosylation influences on the aggregation propensity of therapeutic monoclonal antibodies Biotechnol J 6 1 2011 38 44
32. TS Raju Impact of Fc Glycosylation on monoclonal antibody effector functions and degradation by proteases SJ Shire, W Gombotz, K Bechtold-Peters, J Andya, Current Trends in Monoclonal Antibody Development and Manufacturing 2010 Springer New York 249 269
33. D. Hristodorov, R. Fischer, H. Joerissen, B. Muller-Tiemann, H. Apeler, and L. Linden Generation and comparative characterization of glycosylated and aglycosylated human IgG1 antibodies Mol Biotechnol 53 3 2013 326 335
34. E. Sedlak, J.V. Schaefer, J. Marek, P. Gimeson, and A. Pluckthun Advanced analyses of kinetic stabilities of iggs modified by mutations and glycosylation Protein Sci 24 7 2015 1100 1113
35. Y. Yamaguchi, M. Nishimura, M. Nagano, and et al. Glycoform-dependent conformational alteration of the Fc region of human immunoglobulin G1 as revealed by NMR spectroscopy Biochim Biophys Acta 1760 4 2006 693 700
36. J.M. Hayes, E.F. Cosgrave, W.B. Struwe, and et al. Glycosylation and Fc receptors Curr Top Microbiol Immunol 382 2014 165 199
37. M. Schiestl, T. Stangler, C. Torella, T. Cepeljnik, H. Toll, and R. Grau Acceptable changes in quality attributes of glycosylated biopharmaceuticals Nat Biotechnol 29 4 2011 310 312
38. N. Sethuraman, and T.A. Stadheim Challenges in therapeutic glycoprotein production Curr Opin Biotechnol 17 4 2006 341 346
39. A. Beck, and J.M. Reichert Marketing approval of mogamulizumab: a triumph for glyco-engineering MAbs 4 4 2012 419 425
40. Y. Wei, C. Li, W. Huang, B. Li, S. Strome, and L.X. Wang Glycoengineering of human IgG1-Fc through combined yeast expression and in vitro chemoenzymatic glycosylation Biochemistry 47 39 2008 10294 10304
41. M. Federici, A. Lubiniecki, P. Manikwar, and D.B. Volkin Analytical lessons learned from selected therapeutic protein drug comparability studies Biologicals 41 3 2013 131 147
42. A. Lubiniecki, D.B. Volkin, M. Federici, and et al. Comparability assessments of process and product changes made during development of two different monoclonal antibodies Biologicals 39 1 2011 9 22
43. L.A. Bui, S. Hurst, G.L. Finch, and et al. Key considerations in the preclinical development of biosimilars Drug Discov Today 20 Suppl 1 2015 3 15
44. D.J. Crommelin, V.P. Shah, I. Klebovich, and et al. The similarity question for biologicals and non-biological complex drugs Eur J Pharm Sci 76 2015 10 17
45. M.A. Alsenaidy, J.H. Kim, R. Majumdar, and et al. High-throughput biophysical analysis and data visualization of conformational stability of an IgG1 monoclonal antibody after deglycosylation J Pharm Sci 102 11 2013 3942 3956
46. M.A. Alsenaidy, N.K. Jain, J.H. Kim, C.R. Middaugh, and D.B. Volkin Protein comparability assessments and potential applicability of high throughput biophysical methods and data visualization tools to compare physical stability profiles Front Pharmacol 5 2014 39
47. M.A. Alsenaidy, S.Z. Okbazghi, J.H. Kim, and et al. Physical stability comparisons of IgG1-Fc variants: effects of N-glycosylation site occupancy and Asp/Gln residues at site Asn 297 J Pharm Sci 103 6 2014 1613 1627
48. R. Chaudhuri, Y. Cheng, C.R. Middaugh, and D.B. Volkin High-throughput biophysical analysis of protein therapeutics to examine interrelationships between aggregate formation and conformational stability AAPS J 16 1 2014 48 64
49. S. Yageta, T.M. Lauer, B.L. Trout, and S. Honda Conformational and colloidal stabilities of isolated constant domains of human immunoglobulin G and their impact on antibody aggregation under acidic conditions Mol Pharm 12 5 2015 1443 1455
50. S.Z. Okbazghi, A.S. More, D. White, and et al. Production, characterization, and biological evaluation of well-defined IgG1 Fc glycoforms as a model system for biosimilarity analysis J Pharm Sci 105 2016 559 574
51. O. Mozziconacci, S. Okbazghi, A.S. More, D.B. Volkin, T. Tolbert, and C. Schöneich Comparative evaluation of the chemical stability of four well-defined IgG1 Fc glycoforms J Pharm Sci. 2016 105 2016 575 587
52. J.H. Kim, S.B. Joshi, T.J. Tolbert, C.R. Middaugh, D.B. Volkin, and A.S. Hall Biosimilarity assessments of model IgG1-Fc glycoforms using a machine learning approach J Pharm Sci. 105 2016 602 612
53. T.J. Gibson, K. McCarty, I.J. McFadyen, and et al. Application of a high-throughput screening procedure with PEG-induced precipitation to compare relative protein solubility during formulation development with IgG1 monoclonal antibodies J Pharm Sci 100 3 2011 1009 1021
54. C.R. Middaugh, W. T, R.N. Haire, and A. Rosenberg Determination of the apparent thermodynamic activities of saturated protein solutions J Biol Chem 254 2 1979 367 370
55. P. Manikwar, R. Majumdar, J.M. Hickey, and et al. Correlating excipient effects on conformational and storage stability of an IgG1 monoclonal antibody with local dynamics as measured by hydrogen/deuterium-exchange mass spectrometry J Pharm Sci 102 7 2013 2136 2151
56. N.R. Maddux, S.B. Joshi, D.B. Volkin, J.P. Ralston, and C.R. Middaugh Multidimensional methods for the formulation of biopharmaceuticals and vaccines J Pharm Sci 100 10 2011 4171 4197
57. J.H. Kim, V. Iyer, S.B. Joshi, D.B. Volkin, and C.R. Middaugh Improved data visualization techniques for analyzing macromolecule structural changes Protein Sci 21 10 2012 1540 1553
58. R. Ghirlando, J. Lund, M. Goodall, and R. Jefferis Glycosylation of human IgG-Fc: influences on structure revealed by differential scanning micro-calorimetry Immunol Lett 68 1 1999 47 55
59. S.J. Wu, J. Luo, K.T. O'Neil, and et al. Structure-based engineering of a monoclonal antibody for improved solubility Protein Eng Des Sel 23 8 2010 643 651
60. C.R. Middaugh, and G.W. Litman Atypical glycosylation of an IgG monoclonal cryoimmunoglobulin J Biol Chem 262 8 1987 3671 3673
61. K. Zheng, C. Bantog, and R. Bayer The impact of glycosylation on monoclonal antibody conformation and stability MAbs 3 6 2011 568 576
62. R.F. Latypov, S. Hogan, H. Lau, H. Gadgil, and D. Liu Elucidation of acid-induced unfolding and aggregation of human immunoglobulin IgG1 and IgG2 Fc J Biol Chem 287 2 2012 1381 1396
63. R. Majumdar, P. Manikwar, J.M. Hickey, and et al. Effects of salts from the Hofmeister series on the conformational stability, aggregation propensity, and local flexibility of an IgG1 monoclonal antibody Biochemistry 52 19 2013 3376 3389