Determination of critical quality attributes for monoclonal antibodies using quality by design principles

Biologicals

Volumn 44, Issue 5, 2016, Pages 291-305

  Alt, Nadja ^a   Zhang, Taylor Y ^c   Motchnik, Paul ^c   Taticek, Ron ^c   Quarmby, Valerie ^c   Schlothauer, Tilman ^a   Beck, Hermann ^b   Emrich, Thomas ^a   Harris, Reed J ^c  

^a ROCHE DIAGNOSTICS GMBH   (Germany)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c GENENTECH INC   (United States)

Author keywords

Critical quality attribute; Quality by design; Risk ranking and filtering

Indexed keywords

MONOCLONAL ANTIBODY; RECOMBINANT PROTEIN;

ANIMAL; CHEMISTRY; GENETICS; HUMAN; IMMUNOLOGY; QUALITY CONTROL;

ANIMALS; ANTIBODIES, MONOCLONAL; HUMANS; QUALITY CONTROL; RECOMBINANT PROTEINS;

EID: 84995790815     PISSN: 10451056     EISSN: 10958320     Source Type: Journal    
DOI: 10.1016/j.biologicals.2016.06.005     Document Type: Article

References (56)

1. [1] CMC Biotech Working Group, A-MAb: a case study in bioprocess development. 2009, CASSS, Emeryville, CA.
2. [2] International Conference on Harmonization of Technical Requirements for Registration of Pharmaceuticals for Human Use, ICH harmonized tripartite guideline, pharmaceutical development. Q8 R2, August 2009.
3. [3] Lynne Krummen, Christof Finkler, Introduction to the Application of QbD principles for the Development of Monoclonal Antibodies, Biologicals Vol X.
4. [4] Ferrara, C., Brünker, P., Suter, T., Moser, S., Püntener, U., Umana, P., Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous beta1, 4-N-acetylglucosaminyltransferase III and Golgi alphamannosidase II. Biotechnol Bioeng 93:5 (2006), 851–861.
5. [5] Haberger, M., Bomans, K., Diepold, K., Hook, M., Gassner, J., Schlothauer, T., et al. Assessment of chemical modifications of sites in the CDRs of recombinant antibodies: susceptibility vs. functionality of critical quality attributes. MAbs 6 (2014), 327–339.
6. [6] Raju, T.S., Briggs, J.B., Chamow, S.M., Winkler, M.E., Jones, A.J.S., Glycoengineering of therapeutic glycoproteins: in vitro galactosylation and sialylation of glycoproteins with terminal N-acetylglucosamine and galactose residues. Biochemistry 40 (2001), 8868–8876.
7. [7] Thomann, M., Schlothauer, T., Dashivets, T., Malik, S., Avenal, C., Bulau, P., et al. In vitro glycoengineering of IgG1 and its effect on Fc receptor binding and ADCC activity. PLoS One, 10, 2015, e0134949.
8. [8] Stracke, J.O., Emrich, T., Rüger, P., Schlothauer, T., Kling, L., Knaupp, A., et al. A novel approach to investigate the impact of methionine oxidation on pharmacokinetic properties of therapeutic antibodies. MAbs 6:5 (2014), 1229–1242, 10.4161/mabs.29601.
9. [9] Haberger, M., Heidenreich, A.K., Schlothauer, T., Hook, M., Gassner, J., Bomans, K., et al. Functional assessment of antibody oxidation by native mass spectrometry. MAbs 7 (2015), 891–900.
10. [10] Harris, R.J., Kabakoff, B., Macchi, F.D., Shen, F.J., Kwong, M., Andya, J., et al. Identification of multiple sources of charge heterogeneity in a recombinant antibody. J Chromatogr B 752 (2001), 233–245.
11. [11] Ferrara, C., Stuart, F., Sondermann, P., Brünker, P., Umana, P., The carbohydrate at FcγRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem 281 (2006), 5032–5036.
12. [12] Ha, S., Ou, Y., Vlasak, J., Li, Y., Wang, S., Vo, K., et al. Isolation and characterization of IgG1 with asymmetrical Fc glycosylation. Glycobiology 21:8 (2011), 1087–1096.
13. [13] Yang, Y., Stella, C., Wang, W., Schoneich, C., Gennaro, L., Characterization of oxidative carbonylation on recombinant monoclonal antibodies. Anal Chem 86:10 (2014), 4799–4806.
14. [14] Butko, M., Pallat, H., Cordoba, A., Yu, X.C., Recombinant antibody color resulting from advanced glycation end product modifications. Anal Chem 86:19 (2014), 9816–9823.
15. [15] Bozhinov, A., Handzhiyski, Y., Genov, K., Daskalovska, V., Niwa, T., Ivanov, I., et al. Advanced glycation end products contribute to the immunogenicity of IFN-β pharmaceuticals. J Allergy Clin Immunol 129:3 (2012), 855–858.
16. [16] Rakwalska, M., Rospert, S., The ribosome-bound chaperones RAC and Ssb1/2p are required for accurate translation in Saccharomyces cerevisiae. Mol Cell Biol 24 (2004), 9186–9197.
17. [17] Salas-Marco, J., Bedwell, D.M., Discrimination between defection in elongation fidelity and termination efficiency provides mechanistic insights into translational readthrough. J Mol Biol 248 (2005), 801–815.
18. [18] Drummond, D.A., Wilke, C.O., Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134 (2008), 341–352.
19. [19] Plant, E.W., Nguyen, P., Russ, J.R., Pittman, Y.R., Nguyen, T., Quesinberry, J.T., et al. Differentiating between near- and non-cognate codons in saccharomyces cerevisiae. PLoS One, 2, 2007, e517.
20. [20] Antes, B., Amon, S., Rizzi, A., Wiederkum, S., Kainer, M., Szolar, O., et al. Analysis of lysine clipping of a humanized Lewis-Y specific IgG antibody and its relation to Fc mediated effector function. J Chromatogr B Anal Technol Biomed Life Sci 852 (2007), 250–256.
21. [21] US Department of Health and Human Services Food and Drug Administration, Guidance for industry: statistical approaches to establishing bioequivalence. 2001, FDA, Rockville, MD.
22. [22] Hochhaus, G., Brookman, L., Fox, H., Johnson, C., Matthews, J., Ren, S., et al. Pharmacodynamics of omalizumab: implications for optimised dosing strategies and clinical efficacy in the treatment of allergic asthma. Curr Med Res Opin 19:6 (2003), 491–498.
23. [23] Khawli, L.A., Goswami, S., Hutchinson, R., Kwong, Z.W., Yang, J., Wang, X., et al. Charge variants in IgG1: isolation, characterization, in vitro binding properties and pharmacokinetics in rats. mAbs 2 (2010), 613–624.
24. [24] Ferrant, J.L., Benjamin, C.D., Cutler, A.H., Kalled, S.L., Hsu, Y., Garber, E.A., et al. The contribution of Fc effector mechansims in the efficacy of anti-DC154 immunotherapy depends on the nature of the immune challenge. Int Immunol 16:11 (2004), 1583–1594.
25. [25] Schlothauer, T., Rueger, P., Stracke, J.O., Hertenberger, H., Fingas, F., Kling, L., et al. Analytical FcRn affinity chromatography for functional characterization of monoclonal antibodies. MAbs 5:4 (2013), 576–586.
26. [26] Bumbaca, D., Boswell, A.C., Fielder, P.J., Khawli, L.A., Physicochemical and biochemical factors influencing the pharmacokinetics of antibody therapeutics. AAPS 14 (2012), 554–558.
27. [27] Götze, A.M., Liu, Y.D., Zhang, Z., Shah, B., Lee, E., Bondarenko, P.V., et al. High-mannose glycans on the Fc region of therapeutic IgG antibodies increase serum clearance in humans. Glycobiology 21 (2011), 949–959.
28. [28] Bryson, C.J., Jones, T.D., Baker, M.P., Prediction of immunogenicity of therapeutic proteins. Biodrugs 24:1 (2010), 1–8.
29. [29] De Groot, A.S., Scott, D.W., Immunogenicity of protein therapeutics. Trends Immunol 28:11 (2007), 482–490.
30. [30] Koren, E., Smith, H.W., Shores, E., Shankar, G., Finco-Kent, D., Rup, B., et al. Recommendations on risk-based strategies for detection and characterization of antibodies against biotechnology products. J Immunol Methods 333 (2008), 1–9.
31. [31] Van Schie, K.A., Wolbink, G.-J., Rispens, T., Cross-reactive and pre-existing antibodies to therapeutic antibodies – effects on treatment and immunogenicity. mAbs, 2015, 10.1080/19420862.2015.1048411 accepted.
32. [32] Casadevall, N., Nataf, J., Viron, B., Kolta, A., Kiladjian, J.J., Martin-Dupont, P., et al. Pure red-cell aplasia after treatment with recombinant erythropoietin. N Engl J Med 346 (2002), 469–475.
33. [33] Chung, C.H., Mirakhur, B., Chan, E., Le, Q.T., Berlin, J., Morse, M., et al. Cetuximab-induced anaphylaxis and IgE specific for galactose-alpha-1-3-galactose. N. Engl J Med 358 (2008), 1109–1117.
34. [34] Higashi, H., Naiki, M., Antigen of “serum sickness” type of heterophile antibodies in human sera: identification as gangliosides with N-glycoylneuraminic acid. Biochem Biophys Res Commun 79 (1977), 388–395.
35. [35] Chen, X., Lin, D.Y., Flynn, G.C., The effect of Fc glycan forms on human IgG2 antibody clearance in humans. Glycobiology 19 (2009), 240–249.
36. [36] Rosenberg, A.S., Effects of protein aggregates: an immunologic perspective. AAPS J 8:3 (2006), E501–E507.
37. [37] Wang, W., Singh, S.K., Li, N., Toler, M.R., King, K.R., Neema, S., Immunogenicity of protein aggregates – concerns and realities. Int J Pharm 431 (2012), 1–11.
38. [38] Brian Kelley, Mary Cromwell, Joe Jerkins & others. Integration of QbD Risk Assessment Tools and Overall Risk Management, Biologicals Vol X.
39. [39] Reusch, D., Tejada, M.L., Fc glycans of therapeutic antibodies as critical quality attributes. Glycobiology 25:12 (2015), 1325–1334.
40. [40] Shields, R.L., Lai, J., Keck, R., O'Connell, L.Y., Hong, K., Meng, Y.G., et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 277:30 (2002), 26733–26740.
41. [41] Shinkawa, T., Nakamura, K., Yamane, N., Shoji-Hosaka, E., Kanda, Y., Sakurada, M., et al. 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 (2003), 3466–3473.
42. [42] Umana, P., Jean-Mairet, J., Moudry, R., Amstutz, H., Bailey, J.E., Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotechnol 17 (1999), 176–180.
43. [43] Kanda, Y., Yamada, T., Mori, K., Okazaki, A., Inoue, M., Kitajima-Miyama, K., et al. Comparison of biological activity among nonfucosylated therapeutic IgG1 antibodies with three different N-linked Fc oligosaccharides: the highmannose, hybrid, and complex types. Glycobiology 17 (2007), 104–118.
44. [44] Quan, C., Alcala, E., Petkovska, I., Matthews, D., Canova-Davis, E., Taticek, R., et al. A study in glycation of a therapeutic recombinant humanized monoclonal antibody: where it is, how it got there, and how it affects charge-based behavior. Anal Biochem 373 (2008), 179–191.
45. [45] Zhang, B., Yang, Y., Yuk, I., Pai, R., McKay, P., Eigenbrot, C., et al. Unveiling a glycation hot spot in a recombinant humanized monoclonal antibody. Anal Chem 80 (2008), 2379–2390.
46. [46] Lapolla, A., Fedele, D., Garbeglio, M., Martano, L., Tonani, R., Seraglia, R., et al. Matrix-assisted laser desorption/ionization mass spectrometry, enzymatic digestion, and molecular modeling in the study of nonenzymatic glycation of IgG. J Am Soc Mass Spectrom 11 (2000), 153–159.
47. [47] Jefferis, R., Antibody therapeutics: isotype and glycoform selection. Expert Opin Biol Ther 7 (2007), 1401–1413.
48. [48] Ellison, J.W., Berson, B.F., Hood, L.E., The nucleotide sequence of a human immunoglobulin Cγ1 gene. Nucleic Acids Res 10 (1982), 4071–4079.
49. [49] Harris, R.J., Processing of C-terminal lysine and arginine residues of proteins isolated from mammalian cell culture. J Chrom A 705 (1995), 129–134.
50. [50] Sondermann, P., Oosthuizen, V., Mediation and modulation of antibody function. Biochem Soc Trans 30 (2002), 481–486.
51. [51] Edelman, G.M., Cunningham, B.A., Gall, W.E., Gottlieb, P.D., Rutishauser, U., Waxdal, M.J., The covalent structure of an entire γG immunoglobulin molecule. PNAS 63 (1969), 78–85.
52. [52] Shyong, B., A study to link the abundance of C-terminal lysine in an antibody drug in blood to changes in bioavailability. Genentech Process Sciences Internal Report, July 29, 2005.
53. [53] Cai, B., Pan, H., Flynn, G.C., C-terminal lysine processing of human immunoglobulin G2 heavy chain in vivo. Biotechnol Bioeng 108 (2011), 404–412.
54. [54] Zhang, T., Zhang, J., Hewitt, D., Tran, B., Gao, X., Qiu, Z.J., et al. Identification and characterization of buried unpaired cysteines in a recombinant monoclonal IgG1 antibody. Anal Chem 84:16 (2012), 7112–7123, 10.1021/ac301426h.
55. [55] Götze, A.M., Liu, Y.D., Arroll, T., Chu, L., Flynn, G.C., Rates and impact of human antibody glycation in vivo. Glycobiology 22 (2012), 221–234.
56. [56] Flynn, G.C., Nyberg, G.B., Using quality by design principles in setting a control strategy for product quality attributes in: state-of-the-art and emerging technologies for therapeutic monoclonal antibody characterization volume 1. monoclonal antibody therapeutics: structure, function, and regulatory space. [Chapter 5] ACS Symp Ser 1176 (2014), 117–150.