279
Views
4
CrossRef citations to date
0
Altmetric
Review

Need for a risk-based control strategy for managing glycosylation profile for biosimilar products

ORCID Icon &
Pages 123-131 | Received 11 May 2021, Accepted 24 Aug 2021, Published online: 01 Sep 2021

References

  • Grilo AL, Mantalaris A. The increasingly human and profitable monoclonal antibody market. Trends Biotechnol [Internet]. 2019;37:9–16.
  • Jefferis R. Posttranslational modifications and the immunogenicity of biotherapeutics. J Immunol Res. 2016;2016.
  • Li W, Kerwin JL, Schiel J, et al. Structural elucidation of post-translational modifications in monoclonal antibodies. In: State-of-the-art Emerg Technol Ther Monoclon Antib Charact Vol 2 Biopharm Charact NISTmAb case study. ACS Publications; 2015. p. 119–183.
  • Majewska NI, Tejada ML, Betenbaugh MJ, et al. N-Glycosylation of IgG and IgG-like recombinant therapeutic Proteins: why is it important and how can we control it?. Annu Rev Chem Biomol Eng. 2020;11:311–338.
  • Kaur H. Characterization of glycosylation in monoclonal antibodies and its importance in therapeutic antibody development. Crit Rev Biotechnol. 2021;41:1–23.
  • Alt N, Zhang TY, Motchnik P, et al. Determination of critical quality attributes for monoclonal antibodies using quality by design principles. Biologicals. 2016;44(5):291–305.
  • As R, Is K, Joshi S, et al. Analytical characterization of biotherapeutic products, part I: quality attributes. LC-GC North Am. 2018;36:376–384.
  • Mastrangeli R, Audino MC, Palinsky W, et al. The formidable challenge of controlling high Mannose-Type N-Glycans in therapeutic mAbs. Trends Biotechnol. 2020. DOI:10.1016/j.tibtech.2020.05.009.
  • Zhang P, Woen S, Wang T, et al. Challenges of glycosylation analysis and control: an integrated approach to producing optimal and consistent therapeutic drugs. Drug Discov Today. 2016;21:740–765.
  • Chiu ML, Goulet DR, Teplyakov A, et al. Antibody structure and function: the basis for engineering therapeutics. Antibodies. 2019;8(4):55.
  • Administration USF and D. Development of therapeutic protein biosimilars: comparative analytical assessment and other quality-related considerations. In: Guidance for industry. 2019; p. 2019.
  • Use C for MP for H. European Medicines Agency (EMA). Guideline on development, production, characterization and specifications for monoclonal antibodies and related products 2009. EMEA/CHMP/BWP/157653. 2007.
  • Rudge SR, Nims RW. ICH Q6B specifications: test procedures and acceptance criteria for biotechnological/biological products. In: ICH Qual Guidel An Implement Guid. John Wiley & Sons; 2017: 467.
  • Thaysen-Andersen M, Packer NH. Site-specific glycoproteomics confirms that protein structure dictates formation of N-glycan type, core fucosylation and branching. Glycobiology. 2012;22(11):1440–1452.
  • Jennewein MF, Alter G. The immunoregulatory roles of antibody glycosylation. Trends Immunol. 2017;38(5):358–372.
  • Chung C-Y, Majewska NI, Wang Q, et al. SnapShot: n-glycosylation processing pathways across kingdoms. Cell. 2017;171(1):258.
  • Ivarsson M, TK V, Morbidelli M, et al. Evaluating the impact of cell culture process parameters on monoclonal antibody N-glycosylation. J Biotechnol. 2014;188:88–96.
  • Goh JB, Ng SK. Impact of host cell line choice on glycan profile. Crit Rev Biotechnol. 2018;38(6):851–867.
  • Blondeel EJM, Aucoin MG. Supplementing glycosylation: a review of applying nucleotide-sugar precursors to growth medium to affect therapeutic recombinant protein glycoform distributions. Biotechnol Adv. 2018;36:1505–1523.
  • Ghaderi D, Zhang M, Hurtado-Ziola N, et al. Production platforms for biotherapeutic glycoproteins. Occurrence, impact, and challenges of non-human sialylation. Biotechnol Genet Eng Rev. 2012;28(1):147–176.
  • Beck A, Reichert JM. Marketing approval of mogamulizumab: a triumph for glyco-engineering. MAbs. Taylor & Francis; 2012. p. 419–425.
  • Cameron F, McCormack PL. Obinutuzumab: first global approval. Drugs. 2014;74(1):147–154.
  • Markham A. Benralizumab: first global approval. Drugs. 2018;78(4):505–511.
  • Higel F, Seidl A, Sörgel F, et al. N-glycosylation heterogeneity and the influence on structure, function and pharmacokinetics of monoclonal antibodies and Fc fusion proteins. Eur J Pharm Biopharm [Internet]. 2016;100:94–100. Available from:.
  • Shields RL, Lai J, Keck R, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J Biol Chem. 2002;277(30):26733–26740.
  • Mizushima T, Yagi H, Takemoto E, et al. Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans. Genes Cells. 2011;16(11):1071–1080.
  • Pereira NA, Chan KF, Lin PC, et al. The “less-is-more” in therapeutic antibodies: afucosylated anti-cancer antibodies with enhanced antibody-dependent cellular cytotoxicity. MAbs. Taylor & Francis; 2018. p. 693–711.
  • Alessandri L, Ouellette D, Acquah A, et al. Increased serum clearance of oligomannose species present on a human IgG1 molecule. MAbs. Taylor & Francis; 2012. p. 509–520.
  • Tang F, Yang Y, Tang Y, et al. One-pot N-glycosylation remodeling of IgG with non-natural sialylglycopeptides enables glycosite-specific and dual-payload antibody–drug conjugates. Org Biomol Chem. 2016;14(40):9501–9518.
  • Arnold JN, Dwek RA, Rudd PM, et al. Mannan binding lectin and its interaction with immunoglobulins in health and in disease. Immunol Lett. 2006;106(2):103–110.
  • Shinkawa T, Nakamura K, Yamane N, 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. 2003;278(5):3466–3473.
  • Ferrara C, Brünker P, Suter T, et al. Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co‐expression of heterologous β1, 4‐N‐acetylglucosaminyltransferase III and Golgi α‐mannosidase II. Biotechnol Bioeng. 2006;93:851–861.
  • Peschke B, Keller CW, Weber P, et al. Fc-galactosylation of human immunoglobulin gamma isotypes improves C1q binding and enhances complement-dependent cytotoxicity. Front Immunol. 2017;8:646.
  • Zhang Q, Joubert MK, Polozova A, et al. Glycan engineering reveals interrelated effects of terminal galactose and core fucose on antibody‐dependent cell‐mediated cytotoxicity. Biotechnol Prog. 2020;36:e3045.
  • Bas M, Terrier A, Jacque E, et al. Fc sialylation prolongs serum half-life of therapeutic antibodies. J Immunol. 2019;202(5):1582–1594.
  • Thomann M, Malik S, Kuhne F, et al. Effects of sialic acid linkage on antibody-fragment crystallizable receptor binding and antibody dependent cytotoxicity depend on levels of fucosylation/bisecting. Bioanalysis. 2019;11(15):1437–1449.
  • Barbosa MDFS. Immunogenicity of biotherapeutics in the context of developing biosimilars and biobetters. Drug Discov Today. 2011;16:345–353.
  • Qian J, Liu T, Yang L, et al. Structural characterization of N-linked oligosaccharides on monoclonal antibody cetuximab by the combination of orthogonal matrix-assisted laser desorption/ionization hybrid quadrupole–quadrupole time-of-flight tandem mass spectrometry and sequential enzy. Anal Biochem. 2007;364:8–18.
  • Hajba L, Á S, Borza B, et al. On the glycosylation aspects of biosimilarity. Drug Discov Today [Internet]. 2018;23:616–625. Available from:.
  • Li M, Zhao R, Chen J, et al. Next generation of anti-PD-L1 Atezolizumab with enhanced anti-tumor efficacy in vivo. Sci Rep. 2021;11:1–11.
  • Costa AR, Rodrigues ME, Henriques M, et al. Glycosylation: impact, control and improvement during therapeutic protein production. Crit Rev Biotechnol. 2014;34(4):281–299.
  • Vandekerckhove K, Seidl A, Gutka H, et al. Rational selection, criticality assessment, and tiering of quality attributes and test methods for analytical similarity evaluation of biosimilars. AAPS J. 2018;20(4):68.
  • EMA. Reflection paper on statistical methodology for the comparative assessment of quality attributes in drug development. EMA Guidel. 2018;44:1–24.
  • Yu B, Zeng L, Yang H, et al. A risk-based approach to setting acceptance criteria for pharmaceutical process comparability. J Pharm Innov. 2017;12(4):357–366.
  • Tsong Y, Dong X, Shen M, et al. Development of statistical methods for analytical similarity assessment. J Biopharm Stat. 2017;27:197–205.
  • Seely RJ, Haury J. Applications of failure modes and effects analysis to biotechnology manufacturing processes. Taylor & Francis Boca Raton; 2005.
  • Sangode PB, Metre SG. Power distribution operational risk model driven by FMEA and ISM approach. Int J Qual Reliab Manag. 2020.
  • Rathore AS, Chirmule N, Malani H, et al. Reimagining affordable biosimilars. BioPharm Int. 2020;33(10);16-22,58.
  • Rathore AS, Stevenson JG, Chhabra H, et al. The global landscape on interchangeability of biosimilars. Expert Opin Biol Ther. 2021. DOI:10.1080/14712598.2021.1889511.
  • Planinc A, Dejaegher B, Vander Heyden Y, et al. Batch-to-batch N-glycosylation study of infliximab, trastuzumab and bevacizumab, and stability study of bevacizumab. Eur J Hosp Pharm. 2017;24(5):286–292.
  • De Wachter C., Van Landuyt L., Callewaert N. (2018) Engineering of Yeast Glycoprotein Expression. In: Rapp E., Reichl U. (eds) Advances in Glycobiotechnology. Advances in Biochemical Engineering/Biotechnology, vol 175. Springer, Cham. https://doi.org/10.1007/10_2018_69
  • Palomares L.A., Srivastava I.K., Ramírez O.T., Cox M.M.J. (2018) Glycobiotechnology of the Insect Cell-Baculovirus Expression System Technology. In: Rapp E., Reichl U. (eds) Advances in Glycobiotechnology. Advances in Biochemical Engineering/Biotechnology, vol 175. Springer, Cham. https://doi.org/10.1007/10_2018_61.
  • Montero-Morales L, Steinkellner H. Advanced plant-based glycan engineering. Front Bioeng Biotechnol. 2018;6:81.
  • Donini R, Haslam SM, Kontoravdi C, et al. Glycoengineering Chinese hamster ovary cells: a short history. Biochem Soc Trans. 2021;49(2):915–931.
  • Narimatsu Y, Büll C, Chen Y-H, et al. Genetic glycoengineering in mammalian cells. J Biol Chem. 2021;296.
  • Batra J, Rathore AS. Glycosylation of monoclonal antibody products: current status and future prospects. Biotechnol Prog. 2016;32(5):1091–1102.
  • Velayudhan J, feng CY, Rohrbach A, et al. Demonstration of functional similarity of proposed biosimilar ABP 501 to adalimumab. BioDrugs. 2016;30:339–351.
  • Liu J, Eris T, Li C, et al. Assessing analytical similarity of proposed amgen biosimilar ABP 501 to adalimumab. BioDrugs. 2016;30(4):321–338.
  • Kang J, Kim SY, Vallejo D, et al. Multifaceted assessment of rituximab biosimilarity: the impact of glycan microheterogeneity on Fc function. Eur J Pharm Biopharm [Internet]. 2020;146:111–124.
  • Pisupati K, Tian Y, Okbazghi S, et al. A multidimensional analytical comparison of remicade and the biosimilar remsima. Anal Chem. 2017;89(9):4838–4846.
  • Upton R, Bell L, Guy C, et al. Orthogonal assessment of biotherapeutic glycosylation: a case study correlating N-Glycan core fucosylation of herceptin with mechanism of action. Anal Chem. 2016;88(20):10259–10265.
  • Cerutti ML, Pesce A, Bès C, et al. Physicochemical and biological characterization of RTXM83, a new rituximab biosimilar. BioDrugs. 2019;33(3):307–319.
  • Lee C, Jeong M, Lee JAJ, et al. Glycosylation profile and biological activity of remicade® compared with flixabi® and remsima®. MAbs [Internet]. 2017;9:968–977.
  • Lee JH, Paek K, Moon JH, et al. Biological characterization of SB3, a Trastuzumab biosimilar, and the influence of changes in reference product characteristics on the similarity assessment. BioDrugs. 2019;33:411–422.
  • Montacir O, Montacir H, Eravci M, et al. Comparability study of rituximab originator and follow-on biopharmaceutical. J Pharm Biomed Anal [Internet]. 2017;140:239–251.
  • Fang J, Doneanu C, Alley WR, et al. Advanced assessment of the physicochemical characteristics of remicade® and inflectra® by sensitive LC/MS techniques. MAbs. 2016;8(6):1021–1034.
  • Lee J, Kang HA, Bae JS, et al. Evaluation of analytical similarity between trastuzumab biosimilar CT-P6 and reference product using statistical analyses. MAbs. Taylor & Francis; 2018. p. 547–571.
  • Visser J, Feuerstein I, Stangler T, et al. Physicochemical and functional comparability between the proposed biosimilar rituximab GP2013 and originator rituximab. BioDrugs. 2013;27(5):495–507.
  • López-Morales CA, Miranda-Hernández MP, Juárez-Bayardo LC, et al. Physicochemical and biological characterization of a biosimilar trastuzumab. Biomed Res Int. 2015;2015.
  • Seo N, Huang Z, Kuhns S, et al. Analytical and functional similarity of biosimilar ABP 798 with rituximab reference product. Biologicals. 2020;68:79–91.
  • Xie L, Zhang E, Xu Y, et al. Demonstrating analytical similarity of Trastuzumab biosimilar HLX02 to herceptin® with a panel of sensitive and orthogonal methods including a novel FcγRIIIa affinity chromatography technology. BioDrugs [Internet]. 2020;34(3):363–379.
  • Declerck P, Tebbey PW. Importance of manufacturing consistency of the glycosylated monoclonal antibody adalimumab (humira®) and potential impact on the clinical use of biosimilars. GaBI J. 2016;5(2):70–73.
  • Hutterer KM, Polozova A, Kuhns S, et al. Assessing analytical and functional similarity of proposed amgen biosimilar ABP 980 to trastuzumab. BioDrugs. 2019;33(3):321–333.
  • Shang TQ, Saati A, Toler KN, et al. Development and application of a robust N-glycan profiling method for heightened characterization of monoclonal antibodies and related glycoproteins. J Pharm Sci. 2014;103(7):1967–1978.
  • Liu R, Giddens J, McClung CM, et al. Evaluation of a glycoengineered monoclonal antibody via LC-MS analysis in combination with multiple enzymatic digestion. MAbs [Internet]. 2016;8:340–346. Available from:.
  • Da Silva A, Kronthaler U, Koppenburg V, et al. Target-directed development and preclinical characterization of the proposed biosimilar rituximab GP2013. Leuk Lymphoma. 2014;55(7):1609–1617.
  • Zhang E, Xie L, Qin P, et al. Quality by design–based assessment for analytical similarity of adalimumab biosimilar HLX03 to humira®. AAPS J. 2020;22(3):1–14.
  • Schreiber S, Yamamoto K, Muniz R, et al. Physicochemical analysis and biological characterization of FKB327 as a biosimilar to adalimumab. Pharmacol Res Perspect. 2020;8(3):1–13.
  • Bandyopadhyay S, Mahajan M, Mehta T, et al. Physicochemical and functional characterization of a biosimilar adalimumab ZRC-3197. Biosimilars. 2014;1. DOI:10.2147/BS.S75573.
  • Kronthaler U, Fritsch C, Hainzl O, et al. Comparative functional and pharmacological characterization of sandoz proposed biosimilar adalimumab (GP2017): rationale for extrapolation across indications. Expert Opin Biol Ther [Internet]. 2018;18:921–930.
  • Beyer B, Walch N, Jungbauer A, et al. How similar is biosimilar? A comparison of infliximab therapeutics in regard to charge variant profile and antigen binding affinity. Biotechnol J. 2019;14(4):1–9.
  • Lee KH, Lee J, Bae JS, et al. Analytical similarity assessment of rituximab biosimilar CT-P10 to reference medicinal product. MAbs [Internet]. 2018;10:380–396.
  • Sanchez-De Melo I, Grassi P, Ochoa F, et al. N-glycosylation profile analysis of trastuzumab biosimilar candidates by normal phase liquid chromatography and MALDI-TOF MS approaches. J Proteomics [Internet]. 2015;127:225–233.
  • Nupur N, Chhabra N, Dash R, et al. Assessment of structural and functional similarity of biosimilar products: rituximab as a case study. MAbs. Taylor & Francis; 2018. p. 143–158.
  • Giorgetti J, D’Atri V, Canonge J, et al. Monoclonal antibody N-glycosylation profiling using capillary electrophoresis – mass spectrometry: assessment and method validation. Talanta. 2018;178:530–537.
  • Flores-Ortiz LF, Campos-García VR, Perdomo-Abúndez FC, et al. Physicochemical properties of rituximab. J Liq Chromatogr Relat Technol. 2014;37(10):1438–1452.
  • Seo N, Polozova A, Zhang M, et al. Analytical and functional similarity of amgen biosimilar ABP 215 to bevacizumab. MAbs [Internet]. 2018;10(4):678–691.
  • Peraza MA, Rule KE, Shiue MHI, et al. Nonclinical assessments of the potential biosimilar PF-06439535 and bevacizumab. Regul Toxicol Pharmacol [Internet]. 2018;95:236–243.
  • Hurst S, Ryan AM, Ng CK, et al. Comparative nonclinical assessments of the proposed biosimilar PF-05280014 and trastuzumab (herceptin®). BioDrugs. 2014;28:451–459.
  • Miranda-Hernández MP, López-Morales CA, Piña-Lara N, et al. Pharmacokinetic comparability of a biosimilar trastuzumab anticipated from its physicochemical and biological characterization. Biomed Res Int. 2015;2015.
  • Derzi M, Shoieb AM, Ripp SL, et al. Comparative nonclinical assessments of the biosimilar PF-06410293 and originator adalimumab. Regul Toxicol Pharmacol [Internet]. 2020;112:104587.
  • Hong J, Lee Y, Lee C, et al. Physicochemical and biological characterization of SB2, a biosimilar of remicade® (infliximab). MAbs [Internet]. 2017;9:364–382.
  • Derzi M, Johnson TR, Shoieb AM, et al. Nonclinical evaluation of PF-06438179: a potential biosimilar to remicade® (infliximab). Adv Ther. 2016;33(11):1964–1982.
  • Jung SK, Lee KH, Jeon JW, et al. Physicochemical characterization of remsima®. MAbs. 2014;6(5):1163–1177.
  • Magnenat L, Palmese A, Fremaux C, et al. Demonstration of physicochemical and functional similarity between the proposed biosimilar adalimumab MSB11022 and humira®. MAbs [Internet]. 2017;9(1):127–139.
  • Lee N, Lee JAJ, Yang H, et al. Evaluation of similar quality attribute characteristics in SB5 and reference product of adalimumab. MAbs [Internet]. 2019;11:129–144.
  • Segu Z, Stone T, Berdugo C, et al. A rapid method for relative quantification of N-glycans from a therapeutic monoclonal antibody during trastuzumab biosimilar development. MAbs. Taylor & Francis; 2020. p. 1750794.
  • Carillo S, Pérez-Robles R, Jakes C, et al. Comparing different domains of analysis for the characterisation of N-glycans on monoclonal antibodies. J Pharm Anal. 2020;10(1):23–34.
  • Li C, Rossomando A, Wu SL, et al. Comparability analysis of anti-CD20 commercial (rituximab) and RNAi-mediated fucosylated antibodies by two LC-MS approaches. MAbs. 2013;5:565–575.
  • Kim S, Song J, Park S, et al. Drifts in ADCC-related quality attributes of herceptin®: impact on development of a trastuzumab biosimilar. MAbs. 2017;9(4):704–714.
  • Tebbey PW, Varga A, Naill M, et al. Consistency of quality attributes for the glycosylated monoclonal antibody humira® (adalimumab). MAbs. 2015;7(5):805–811.
  • Xu Y, Xie L, Zhang E, et al. Physicochemical and functional assessments demonstrating analytical similarity between rituximab biosimilar HLX01 and the mabThera®. MAbs. 2019;11(3):606–620.
  • Lee JAJ, Yang J, Lee C, et al. Demonstration of functional similarity of a biosimilar adalimumab SB5 to humira ®. Biologicals [Internet]. 2019;58:7–15.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.