A general evidence-based sequence variant control limit for recombinant therapeutic protein development

References

• Ecker DM, Jones SD, Levine HL. The therapeutic monoclonal antibody market. MAbs. 2015;7:9–10. doi:https://doi.org/10.4161/19420862.2015.989042.
   PubMed Web of Science ®Google Scholar
• Weiner GJ. Building better monoclonal antibody-based therapeutics. Nat Rev Cancer. 2015;15:361–70. doi:https://doi.org/10.1038/nrc3930.
   PubMed Web of Science ®Google Scholar
• The Antibody Society. Antibody therapeutics approved or in regulatory review in the EU or US. [accessed 2020 June 7]. https://www.antibodysociety.org/resources/approved-antibodies/
   Google Scholar
• Valliere-Douglass J, Marzilli L, Deora A, Du Z, He L, Kumar S, Liu YH, Martin-Mueller H, Nwosu C, Stults J, et al. Biopharmaceutical industry practices for sequence variant analyses of recombinant protein therapeutics. PDA J Pharm Sci Technol. 2019. doi:https://doi.org/10.5731/pdajpst.2019.010009.
   Google Scholar
• Borisov OV, Alvarez M, Carroll JA, Brown PW. Sequence variants and sequence variant analysis in biotherapeutic proteins. State-of-the-art and emerging technologies for therapeutic monoclonal antibody characterization Volume 2. Biopharmaceutical characterization: the NISTmAb case study. ACS Publications; 2015. p. 63–117.
   Google Scholar
• Lin TJ, Beal KM, Brown PW, DeGruttola HS, Ly M, Wang W, Chu CH, Dufield RL, Casperson GF, Carroll JA, et al. Evolution of a comprehensive, orthogonal approach to sequence variant analysis for biotherapeutics. MAbs. 2019;11:1–12. doi:https://doi.org/10.1080/19420862.2018.1531965.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Shah B, Bondarenko PV. G/U and certain wobble position mismatches as possible main causes of amino acid misincorporations. Biochemistry. 2013;52:8165–76. doi:https://doi.org/10.1021/bi401002c.
   PubMed Web of Science ®Google Scholar
• Wong HE, Huang CJ, Zhang Z. Amino acid misincorporation in recombinant proteins. Biotechnol Adv. 2018;36:168–81. doi:https://doi.org/10.1016/j.biotechadv.2017.10.006.
   PubMed Web of Science ®Google Scholar
• Zeck A, Regula JT, Larraillet V, Mautz B, Popp O, Gopfert U, Wiegeshoff F, Vollertsen UEE, Gorr IH, Koll H, et al. Low level sequence variant analysis of recombinant proteins: an optimized approach. PLoS One. 2012;7:e40328. doi:https://doi.org/10.1371/journal.pone.0040328.
   PubMed Web of Science ®Google Scholar
• Khetan A, Huang YM, Dolnikova J, Pederson NE, Wen D, Yusuf-Makagiansar H, Chen P, Ryll T. Control of misincorporation of serine for asparagine during antibody production using CHO cells. Biotechnol Bioeng. 2010;107:116–23. doi:https://doi.org/10.1002/bit.22771.
   PubMed Web of Science ®Google Scholar
• Harris RP, Mattocks J, Green PS, Moffatt F, Kilby PM. Determination and control of low-level amino acid misincorporation in human thioredoxin protein produced in a recombinant Escherichia coli production system. Biotechnol Bioeng. 2012;109:1987–95. doi:https://doi.org/10.1002/bit.24462.
   PubMed Web of Science ®Google Scholar
• Harris RJ, Murnane AA, Utter SL, Wagner KL, Cox ET, Polastri GD, Helder JC, Sliwkowski MB. Assessing genetic heterogeneity in production cell lines: detection by peptide mapping of a low level Tyr to Gln sequence variant in a recombinant antibody. Biotechnology (N Y). 1993;11:1293–97. doi:https://doi.org/10.1038/nbt1193-1293.
   PubMedGoogle Scholar
• Zhang S, Bartkowiak L, Nabiswa B, Mishra P, Fann J, Ouellette D, Correia I, Regier D, Liu J. Identifying low-level sequence variants via next generation sequencing to aid stable CHO cell line screening. Biotechnol Prog. 2015;31:1077–85. doi:https://doi.org/10.1002/btpr.2119.
   PubMed Web of Science ®Google Scholar
• Kunkel TA. DNA replication fidelity. J Biol Chem. 2004;279:16895–98. doi:https://doi.org/10.1074/jbc.R400006200.
   PubMed Web of Science ®Google Scholar
• Imashimizu M, Oshima T, Lubkowska L, Kashlev M. Direct assessment of transcription fidelity by high-resolution RNA sequencing. Nucleic Acids Res. 2013;41:9090–104. doi:https://doi.org/10.1093/nar/gkt698.
   PubMed Web of Science ®Google Scholar
• Gout J-F, Thomas WK, Smith Z, Okamoto K, Lynch M. Large-scale detection of in vivo transcription errors. Proc Natl Acad Sci US A. 2013;110:18584–89. doi:https://doi.org/10.1073/pnas.1309843110.
   PubMed Web of Science ®Google Scholar
• Ellis N, Gallant J. An estimate of the global error frequency in translation. Mol Gen Genet. 1982;188:169–72. doi:https://doi.org/10.1007/BF00332670.
   PubMedGoogle Scholar
• Edelmann P, Gallant J. Mistranslation in E. coli. Cell. 1977;10:131–37. doi:https://doi.org/10.1016/0092-8674(77)90147-7.
   PubMed Web of Science ®Google Scholar
• Fu J, Bongers J, Tao L, Huang D, Ludwig R, Huang Y, Qian Y, Basch J, Goldstein J, Krishnan R, et al. Characterization and identification of alanine to serine sequence variants in an IgG4 monoclonal antibody produced in mammalian cell lines. J Chromatogr B Analyt Technol Biomed Life Sci. 2012;908:1–8. doi:https://doi.org/10.1016/j.jchromb.2012.09.023.
   PubMed Web of Science ®Google Scholar
• DeGruttola HS, Marzilli L, Beal KM, Anderson K, Rouse JC. Sequence variant analysis of antibody biotherapeutics with ultrahigh-resolution mass spectrometry. Biotherapeutics analytical summit. Baltimore (MD); 2015.
   Google Scholar
• Huang Y, O’Mara B, Conover M, Ludwig R, Fu J, Tao L, Li ZJ, Rieble S, Grace MJ, Russell RJ. Glycine to glutamic acid misincorporation observed in a recombinant protein expressed by Escherichia coli cells. Protein Sci. 2012;21:625–32. doi:https://doi.org/10.1002/pro.2046.
   PubMed Web of Science ®Google Scholar
• Hutterer KM, Zhang Z, Michaels ML, Belouski E, Hong RW, Shah B, Berge M, Barkhordarian H, Le E, Smith S, et al. Targeted codon optimization improves translational fidelity for an Fc fusion protein. Biotechnol Bioeng. 2012;109:2770–77. doi:https://doi.org/10.1002/bit.24555.
   PubMed Web of Science ®Google Scholar
• Wen D, Vecchi MM, Gu S, Su L, Dolnikova J, Huang Y-M, Foley SF, Garber E, Pederson N, Meier W, et al. Discovery and investigation of misincorporation of serine at asparagine positions in recombinant proteins expressed in Chinese hamster ovary cells. J Biol Chem. 2009;284(47):32686–94. doi:https://doi.org/10.1074/jbc.M109.059360.
   PubMed Web of Science ®Google Scholar
• Feeney L, Carvalhal V, Yu XC, Chan B, Michels DA, Wang YJ, Shen A, Ressl J, Dusel B, Laird MW, et al. Eliminating tyrosine sequence variants in CHO cell lines producing recombinant monoclonal antibodies. Biotechnol Bioeng. 2013;110(4):1087–97. doi:https://doi.org/10.1002/bit.24759.
   PubMed Web of Science ®Google Scholar
• Raina M, Moghal A, Kano A, Jerums M, Schnier PD, Luo S, Deshpande R, Bondarenko PV, Lin H, Ibba M. Reduced amino acid specificity of mammalian tyrosyl-tRNA synthetase is associated with elevated mistranslation of Tyr codons. J Biol Chem. 2014;289:17780–90. doi:https://doi.org/10.1074/jbc.M114.564609.
   PubMed Web of Science ®Google Scholar
• Ni J, Gao M, James A, Yao J, Yuan T, Carpick B, D’Amore T, Farrell P. Investigation into the misincorporation of norleucine into a recombinant protein vaccine candidate. J Ind Microbiol Biotechnol. 2015;42:971–75. doi:https://doi.org/10.1007/s10295-015-1613-x.
   PubMed Web of Science ®Google Scholar
• Rogstad S, Faustino A, Ruth A, Keire D, Boyne M, Park J. A retrospective evaluation of the use of mass spectrometry in FDA biologics license applications. J Am Soc Mass Spectrom. 2017;28:786–94. doi:https://doi.org/10.1007/s13361-016-1531-9.
   PubMed Web of Science ®Google Scholar
• Kumar SR, Prabakaran M, Ashok Raj KV, He F, Kwang J. Amino acid substitutions improve the immunogenicity of H7N7HA protein and protect mice against lethal H7N7 viral challenge. PLoS One. 2015;10:e0128940. doi:https://doi.org/10.1371/journal.pone.0128940.
   PubMed Web of Science ®Google Scholar
• Joubert MK, Deshpande M, Yang J, Reynolds H, Bryson C, Fogg M, Baker MP, Herskovitz J, Goletz TJ, Zhou L,et al. Use of in vitro assays to assess immunogenicity risk of antibody-based biotherapeutics. PLoS One. 2016;11:e0159328. doi:https://doi.org/10.1371/journal.pone.0159328.
   PubMed Web of Science ®Google Scholar