Biopharmaceutical Industry Practices for Sequence Variant Analyses of Recombinant Protein Therapeutics

References

1. 1.↵
   U.S. Food and Drug Administration. Guidance for Industry Q6B Specifications: Test Procedures and Acceptance Criteria for Biotechnological/Biological Products. U.S. Department of Health and Human Services Food and Drug Administration. Center for Drug Evaluation and Research (CDER), Center for Biologics Evaluation and Research (CBER), 1999: https://www.fda.gov/media/71510/download.

   Google Scholar
2. 2.↵
   1. Lian Z.,
   2. Wu Q.,
   3. Wang T.

   Identification and Characterization of a-1 Reading Frameshift in the Heavy Chain Constant Region of an IgG1 Recombinant Monoclonal Antibody Produced in CHO Cells. mAbs 2016, 8 (2), 358–370.

   OpenUrlGoogle Scholar
3. 3.↵
   1. Wan M.,
   2. Shiau F. Y.,
   3. Gordon W.,
   4. Wang G. Y.

   Variant Antibody Identification by Peptide Mapping. Biotechnol. Bioeng. 1999, 62 (4), 485–488.

   OpenUrlPubMedGoogle Scholar
4. 4.↵
   1. Zhang Z.,
   2. Shah B.,
   3. Bondarenko P. V.

   G/U and Certain Wobble Position Mismatches as Possible Main Causes of Amino Acid Misincorporations. Biochemistry 2013, 52 (45), 8165–8176.

   OpenUrlCrossRefPubMedWeb of ScienceGoogle Scholar
5. 5.↵
   1. Feeney L.,
   2. Carvalhal V.,
   3. Yu X. C.,
   4. Chan B.,
   5. Michels D. A.,
   6. Wang Y. J.,
   7. Shen A.,
   8. Ressl J.,
   9. Dusel B.,
   10. Laird M. W.

   Eliminating Tyrosine Sequence Variants in CHO Cell Lines Producing Recombinant Monoclonal Antibodies. Biotechnol. Bioeng. 2013, 110 (4), 1087–1097.

   OpenUrlCrossRefGoogle Scholar
6. 6.↵
   1. Fu J.,
   2. Bongers J.,
   3. Tao L.,
   4. Huang D.,
   5. Ludwig R.,
   6. Huang Y.,
   7. Qian Y.,
   8. Basch J.,
   9. Goldstein J.,
   10. Krishnan R.,
   11. You L.,
   12. Li Z. J.,
   13. Russell R. J.

   Characterization and Identification of Alanine to Serine Sequence Variants in an IgG4 Monoclonal Antibody Produced in Mammalian Cell Lines. J. Chromatogr. B 2012, 908, 1–8.

   OpenUrlGoogle Scholar
7. 7.↵
   1. Zeck A.,
   2. Regula J. T.,
   3. Larraillet V.,
   4. Mautz B.,
   5. Popp O.,
   6. Gopfert U.,
   7. Wiegeshoff F.,
   8. Vollertsen U. E.,
   9. Gorr I. H.,
   10. Koll H.,
   11. Papadimitriou A.

   Low Level Sequence Variant Analysis of Recombinant Proteins: An Optimized Approach. PloS One 2012, 7 (7), e40328.

   OpenUrlPubMedGoogle Scholar
8. 8.↵
   1. Zhang S.,
   2. Bartkowiak L.,
   3. Nabiswa B.,
   4. Mishra P.,
   5. Fann J.,
   6. Ouellette D.,
   7. Correia I.,
   8. Regier D.,
   9. Liu J.

   Identifying Low-Level Sequence Variants via Next Generation Sequencing to Aid Stable CHO Cell Line Screening. Biotechnol. Prog. 2015, 31 (4), 1077–1085.

   OpenUrlGoogle Scholar
9. 9.↵
   1. Wright C.,
   2. Groot J.,
   3. Swahn S.,
   4. McLaughlin H.,
   5. Liu M.,
   6. Xu C.,
   7. Sun C.,
   8. Zheng E.,
   9. Estes S.

   Genetic Mutation Analysis at Early Stages of Cell Line Development Using Next Generation Sequencing. Biotechnol. Prog. 2016, 32 (3), 813–817.

   OpenUrlGoogle Scholar
10. 10.↵
    1. Yu X. C.,
    2. Borisov O. V.,
    3. Alvarez M.,
    4. Michels D. A.,
    5. Wang Y. J.,
    6. Ling V.

    Identification of Codon-Specific Serine to Asparagine Mistranslation in Recombinant Monoclonal Antibodies by High-Resolution Mass Spectrometry. Anal. Chem. 2009, 81 (22), 9282–9290.

    OpenUrlCrossRefPubMedGoogle Scholar
11. 11.↵
    1. Yates J. R.,
    2. Speicher S.,
    3. Griffin P. R.,
    4. Hunkapiller T.

    Peptide Mass Maps: A Highly Informative Approach to Protein Identification. Anal. Biochem. 1993, 214 (2), 397–408.

    OpenUrlCrossRefPubMedWeb of ScienceGoogle Scholar
12. 12.↵
    1. Pappin D. J.,
    2. Hojrup P.,
    3. Bleasby A. J.

    Rapid Identification of Proteins by Peptide-Mass Fingerprinting. Cur.r Biol. 1993, 3 (6), 327–332.

    OpenUrlCrossRefPubMedWeb of ScienceGoogle Scholar
13. 13.↵
    1. Henzel W. J.,
    2. Billeci T. M.,
    3. Stults J. T.,
    4. Wong S. C.,
    5. Grimley C.,
    6. Watanabe C.

    Identifying Proteins from Two-Dimensional Gels by Molecular Mass Searching of Peptide Fragments in Protein Sequence Databases. Proc. Natl. Acad. Sci. U.S.A. 1993, 90 (11), 5011–5015.

    OpenUrlAbstract/FREE Full TextGoogle Scholar
14. 14.↵
    1. Eng J. K.,
    2. McCormack A. L.,
    3. Yates J. R.

    An Approach to Correlate Tandem Mass Spectral Data of Peptides with Amino Acid Sequences in a Protein Database. J. Am. Soc. Mass Spectrom. 1994, 5 (11), 976–989.

    OpenUrlCrossRefPubMedWeb of ScienceGoogle Scholar
15. 15.↵
    1. Schiel J. E.,
    2. Davis D. L.,
    3. Borisov O. V.

    1. Borisov O. V.,
    2. Alvarez M.,
    3. Carroll J. A.,
    4. Brown P. W.

    Sequence Variants and Sequence Variant Analysis in Biotherapeutic Proteins. In State-of-the-Art and Emerging Technologies for Therapeutic Monoclonal Antibody Characterization Volume 2. Biopharmaceutical Characterization: The NISTmAb Case Study; Schiel J. E., Davis D. L., Borisov O. V., Eds.; ACS Symposium Series 1201; American Chemical Society, 2015; pp 63–117, Chapter 2.

    Google Scholar
16. 16.↵
    1. Yang Y.,
    2. Strahan A.,
    3. Li C.,
    4. Shen A.,
    5. Liu H.,
    6. Ouyang J.,
    7. Katta V.,
    8. Francissen K.,
    9. Zhang B.

    Detecting Low Level Sequence Variants in Recombinant Monoclonal Antibodies. mAbs 2010, 2 (3), 285–298.

    OpenUrlPubMedGoogle Scholar
17. 17.↵
    1. Harris R. J.,
    2. Murnane A. A.,
    3. Utter S. L.,
    4. Wagner K. L.,
    5. Cox E. T.,
    6. Polastri G. D.,
    7. Helder J. C.,
    8. Sliwkowski M. B.

    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.

    OpenUrlGoogle Scholar
18. 18.↵
    1. Li W.,
    2. Wypych J.,
    3. Duff R. J.

    Improved Sequence Variant Analysis Strategy by Automated False Positive Removal. mAbs 2017, 9 (6), 978–984.

    OpenUrlGoogle Scholar
19. 19.↵
    1. Wen D.,
    2. Vecchi M. M.,
    3. Gu S.,
    4. Su L.,
    5. Dolnikova J.,
    6. Huang Y. M.,
    7. Foley S. F.,
    8. Garber E.,
    9. Pederson N.,
    10. 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 (47), 32686–32694.

    OpenUrlAbstract/FREE Full TextGoogle Scholar
20. 20.↵
    1. Ren D.,
    2. Zhang J.,
    3. Pritchett R.,
    4. Liu H.,
    5. Kyauk J.,
    6. Luo J.,
    7. Amanullah A.

    Detection and Identification of a Serine to Arginine Sequence Variant in a Therapeutic Monoclonal Antibody. J. Chromatogr. B 2011, 879 (27), 2877–2884.

    OpenUrlGoogle Scholar
21. 21.↵
    1. Zhang J.,
    2. Chiodini R.,
    3. Badr A.,
    4. Zhang G.

    The Impact of Next-Generation Sequencing on Genomics. J. Genet. Genomics 2011, 38 (3), 95–109.

    OpenUrlCrossRefPubMedWeb of ScienceGoogle Scholar
22. 22.↵
    U.S. Food and Drug Administration. Guidance for Stakeholders and Food and Drug Administration Staff: Use of Public Human Genetic Variant Databases to Support Clinical Validity for Genetic and Genomic-Based in Vitro Diagnostics. U.S. Department of Health and Human Services Food and Drug Administration. Center for Devices and Radiological Health, 2018; https://www.fda.gov/media/99200/download.

    Google Scholar
23. 23.↵
    U.S. Food and Drug Administration. Guidance for Stakeholders and Food and Drug Administration Staff: Considerations for Design, Development, and Analytical Validation of Next Generation Sequencing (NGS) – Based In Vitro Diagnostics (IVDs) Intended to Aid in the Diagnosis of Suspected Germline Diseases. U.S. Department of Health and Human Services Food and Drug Administration. Center for Devices and Radiological Health, 2018; https://www.fda.gov/media/99208/download.

    Google Scholar
24. 24.↵
    1. Voelkerding K. V.,
    2. Dames S. A.,
    3. Durtschi J. D.

    Next-Generation Sequencing: From Basic Research to Diagnostics. Clin. Chem. 2009, 55 (4), 641–658.

    OpenUrlAbstract/FREE Full TextGoogle Scholar
25. 25.↵
    1. Lin T. J.,
    2. Beal K. M.,
    3. Brown P. W.,
    4. DeGruttola H. S.,
    5. Ly M.,
    6. Wang W.,
    7. Chu C. H.,
    8. Dufield R. L.,
    9. Casperson G. F.,
    10. Carroll J. A.,
    11. Friese O. V.,
    12. Figueroa B. Jr..,
    13. Marzilli L. A.,
    14. Anderson K.,
    15. Rouse J. C.

    Evolution of a Comprehensive, Orthogonal Approach to Sequence Variant Analysis for Biotherapeutics. mAbs 2019, 11 (1), 1–12.

    OpenUrlGoogle Scholar
26. 26.↵
    1. Lin T. J.,
    2. Beal K. M.,
    3. DeGruttola H. S.,
    4. Brennan S.,
    5. Marzilli L. A.,
    6. Anderson K.

    Utilization of Sequence Variants as Biomarkers to Analyze Population Dynamics in Cloned Cell Lines. Biotechnol. Bioeng. 2017, 114 (8), 1744–1752.

    OpenUrlGoogle Scholar
27. 27.↵
    1. Guo D.,
    2. Gao A.,
    3. Michels D. A.,
    4. Feeney L.,
    5. Eng M.,
    6. Chan B.,
    7. Laird M. W.,
    8. Zhang B.,
    9. Yu X. C.,
    10. Joly J.,
    11. Snedecor B.,
    12. Shen A.

    Mechanisms of Unintended Amino Acid Sequence Changes in Recombinant Monoclonal Antibodies Expressed in Chinese Hamster Ovary (CHO) Cells. Biotechnol. Bioeng. 2010, 107 (1), 163–171.

    OpenUrlCrossRefPubMedGoogle Scholar
28. 28.↵
    1. Wong H. E.,
    2. Huang C. J.,
    3. Zhang Z.

    Amino Acid Misincorporation in Recombinant Proteins. Biotechnol Adv. 2018, 36 (1), 168–181.

    OpenUrlGoogle Scholar
29. 29.↵
    1. Khetan A.,
    2. Huang Y. M.,
    3. Dolnikova J.,
    4. Pederson N. E.,
    5. Wen D.,
    6. Yusuf-Makagiansar H.,
    7. Chen P.,
    8. Ryll T.

    Control of Misincorporation of Serine for Asparagine during Antibody Production Using CHO Cells. Biotechnol. Bioeng. 2010, 107 (1), 116–123.

    OpenUrlPubMedGoogle Scholar
30. 30.↵
    1. Ni J.,
    2. Gao M.,
    3. James A.,
    4. Yao J.,
    5. Yuan T.,
    6. Carpick B.,
    7. D'Amore T.,
    8. Farrell P.

    Investigation into the Misincorporation of Norleucine into a Recombinant Protein Vaccine Candidate. J. Ind. Microbiol. Biotechnol. 2015, 42 (6), 971–975.

    OpenUrlGoogle Scholar