Evolution of a comprehensive, orthogonal approach to sequence variant analysis for biotherapeutics

References

• Reichert JM. Marketed therapeutic antibodies compendium. mAbs. 2012;4:413–415. doi:10.4161/mabs.19931.
   PubMed Web of Science ®Google Scholar
• Kaplon H, Reichert JM. Antibodies to watch in 2018. mAbs. 2018;10:183–203. doi:10.1080/19420862.2018.1415671.
   PubMed Web of Science ®Google Scholar
• Cafuir LA, Kempton CL. Current and emerging factor VIII replacement products for hemophilia A. Ther Adv Hematol. 2017;8:303–313. doi:10.1177/2040620717721458.
   PubMed Web of Science ®Google Scholar
• Lalonde ME, Durocher Y. Therapeutic glycoprotein production in mammalian cells. J Biotechnol. 2017;251:128–140. doi:10.1016/j.jbiotec.2017.04.028.
   PubMed Web of Science ®Google Scholar
• Wurm FM. Production of recombinant protein therapeutics in cultivated mammalian cells. Nat Biotechnol. 2004;22:1393–1398. doi:10.1038/nbt1026.
   PubMed Web of Science ®Google Scholar
• Borisov OV, Field M, Ling VT, Harris RJ. Characterization of oligosaccharides in recombinant tissue plasminogen activator produced in Chinese hamster ovary cells: two decades of analytical technology development. Anal Chem. 2009;81:9744–9754. doi:10.1021/ac901498k.
   PubMed Web of Science ®Google Scholar
• Mann M, Kelleher NL. Precision proteomics: the case for high resolution and high mass accuracy. Proc Natl Acad Sci U S A. 2008;105:18132–18138. doi:10.1073/pnas.0800788105.
   PubMed Web of Science ®Google Scholar
• Sidoli S, Kulej K, Garcia BA. Why proteomics is not the new genomics and the future of mass spectrometry in cell biology. J Cell Biol. 2017;216:21–24. doi:10.1083/jcb.201612010.
   PubMed Web of Science ®Google Scholar
• Borisov OV, Alvarez M, Carroll JA, Brown PW. Sequence Variants and Sequence Variant Analysis in Biotherapeutic Proteins. In: Schiel JE, Davis DL, Borisov OV, editors. State-of-the-Art and Emerging Technologies for Therapeutic Monoclonal Antibody Characterization Volume 2 Biopharmaceutical Characterization: the NISTmAb Case Study: American Chemical Society; ACS Symposium Series. Washington (DC): American Chemical Society; 2015. p. 63–117.
   Google Scholar
• Yang Y, Strahan A, Li C, Shen A, Liu H, Ouyang J, Katta V, Francissen K, Zhang B. Detecting low level sequence variants in recombinant monoclonal antibodies. mAbs. 2010;2:285–298.
   PubMed Web of Science ®Google Scholar
• Frye C, Deshpande R, Estes S, Francissen K, Joly J, Lubiniecki A, Munro T, Russell R, Wang T, Anderson K. Industry view on the relative importance of “clonality” of biopharmaceutical-producing cell lines. Biologicals: J Int Assoc Biol Standardization. 2016;44:117–122. doi:10.1016/j.biologicals.2016.01.001.
   Google Scholar
• Calos MP, Lebkowski JS, Botchan MR. High mutation frequency in DNA transfected into mammalian cells. Proc Natl Acad Sci U S A. 1983;80:3015–3019.
   PubMed Web of Science ®Google Scholar
• Razzaque A, Mizusawa H, Seidman MM. Rearrangement and mutagenesis of a shuttle vector plasmid after passage in mammalian cells. Proc Natl Acad Sci U S A. 1983;80:3010–3014.
   PubMed Web of Science ®Google Scholar
• Dorai H, Sauerwald T, Campbell A, Kyung YS, Goldstein J, Magill A, Lewis MJ, Tang QM, Jan D, Ganguly S, et al. Investigation of product microheterogeneity – A case study in rapid detection of mutation in mammalian production cell lines. BioProcess Intl. 2007;66–72.
   Google Scholar
• Guo D, Gao A, Michels DA, Feeney L, Eng M, Chan B, Laird MW, Zhang B, Yu XC, Joly J, et al. Mechanisms of unintended amino acid sequence changes in recombinant monoclonal antibodies expressed in Chinese Hamster Ovary (CHO) cells. Biotechnol Bioeng. 2010;107:163–171. doi:10.1002/bit.22780.
   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:10.1371/journal.pone.0040328.
   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:10.1016/j.jchromb.2012.09.023.
   PubMed Web of Science ®Google Scholar
• Lin TJ, Beal KM, DeGruttola HS, Brennan S, Marzilli LA, Anderson K. Utilization of sequence variants as biomarkers to analyze population dynamics in cloned cell lines. Biotechnol Bioeng. 2017;114:1744–1752. doi:10.1002/bit.26298.
   PubMed Web of Science ®Google Scholar
• Wong HE, Huang CJ, Zhang Z. Amino acid misincorporation in recombinant proteins. Biotechnol Adv. 2018;36:168–181. doi:10.1016/j.biotechadv.2017.10.006.
   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;52:8165–8176. doi:10.1021/bi401002c.
   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;107:116–123. doi:10.1002/bit.22771.
   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. Eliminating tyrosine sequence variants in CHO cell lines producing recombinant monoclonal antibodies. Biotechnol Bioeng. 2013;110:1087–1097. doi:10.1002/bit.24759.
   PubMed Web of Science ®Google Scholar
• Bostrom J, Haber L, Koenig P, Kelley RF, Fuh G. High affinity antigen recognition of the dual specific variants of herceptin is entropy-driven in spite of structural plasticity. PloS ONE. 2011;6:e17887. doi:10.1371/journal.pone.0017887.
   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.Nat Biotechnol. 1993;11:1293–1297.
   Google Scholar
• Gu S, Wen D, Weinreb PH, Sun Y, Zhang L, Foley SF, Kshirsagar R, Evans D, Mi S, Meier W, et al. Characterization of trisulfide modification in antibodies. Anal Biochem. 2010;400:89–98. doi:10.1016/j.ab.2010.01.019.
   PubMed Web of Science ®Google Scholar
• Rogers RS, Abernathy M, Richardson DD, Rouse JC, Sperry JB, Swann P, Wypych J, Yu C, Zang L, Deshpande R. A view on the importance of “Multi-Attribute Method” for measuring purity of biopharmaceuticals and improving overall control strategy. AAPS J. 2017;20:7. doi:10.1208/s12248-017-0168-3.
   Google 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;31:1077–1085. doi:10.1002/btpr.2119.
   PubMed Web of Science ®Google Scholar
• Chevreux G, Tilly N, Bihoreau N. Fast analysis of recombinant monoclonal antibodies using IdeS proteolytic digestion and electrospray mass spectrometry. Anal Biochem. 2011;415:212–214. doi:10.1016/j.ab.2011.04.030.
   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;42:971–975. doi:10.1007/s10295-015-1613-x.
   PubMed Web of Science ®Google Scholar
• Wen D, Vecchi MM, Gu S, Su L, Dolnikova J, Huang YM, Foley SF, Garber E, Pederson N, Meier W. Discovery and investigation of misincorporation of serine at asparagine positions in recombinant proteins expressed in Chinese hamster ovary cells. J Biol Chem. 2009;284:32686–32694. doi:10.1074/jbc.M109.059360.
   PubMed Web of Science ®Google Scholar
• Yu XC, Borisov OV, Alvarez M, Michels DA, Wang YJ, Ling V. Identification of codon-specific serine to asparagine mistranslation in recombinant monoclonal antibodies by high-resolution mass spectrometry. Anal Chem. 2009;81:9282–9290. doi:10.1021/ac901541h.
   PubMed Web of Science ®Google Scholar