Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity

References

• Maggon K. Monoclonal antibody “gold rush”. Curr Med Chem. 2007;14:1978–11. doi:10.2174/092986707781368504.
   PubMed Web of Science ®Google Scholar
• Projan SJ, Gill D, Lu Z, Herrmann SH. Small molecules for small minds? The case for biologic pharmaceuticals. Expert Opin Biol Ther. 2004;4(8):1345–50. doi:10.1517/14712598.4.8.1345. PMID: 15268667.
   PubMed Web of Science ®Google Scholar
• Carter PJ, Lazar GA. Next generation antibody drugs: pursuit of the ‘high-hanging fruit’. Nat Rev Drug Discov. 2017;17:197–223. doi:10.1038/nrd.2017.227.
   PubMed Web of Science ®Google Scholar
• Hermeling S, Crommelin DJA, Schellekens H, Jiskoot W. Structure-immunogenicity relationships of therapeutic proteins. Pharm Res. 2004;21(6):897–903. doi:10.1023/B:PHAM.0000029275.41323.a6.
   PubMed Web of Science ®Google Scholar
• Maas C, Hermeling S, Bouma B, Jiskoot W, Gebbink MFBG. A role for protein misfolding in immunogenicity of biopharmaceuticals. J Biol Chem. 2007;282(4):2229–36. doi:10.1074/jbc.M605984200.
   PubMed Web of Science ®Google Scholar
• Vlasak J, Ionescu R. Fragmentation of monoclonal antibodies. MAbs. 2011;3(3):253–63. doi:10.4161/mabs.3.3.15608. PMID: 21487244.
   PubMed Web of Science ®Google Scholar
• Wang W, Singh S, Zeng DL, King K, Nema S. Antibody structure, instability, and formulation. J Pharm Sci. 2007;96(1):1–26. doi:10.1002/jps.20727. PMID: 16998873.
   PubMed Web of Science ®Google Scholar
• Gupta S, Jiskoot W, Schöneich C, Rathore AS. Oxidation and deamidation of monoclonal antibody products: potential impact on stability, biological activity, and efficacy. J Pharm Sci. 2022;111(4):903–18. doi:10.1016/j.xphs.2021.11.024. PMID: 34890632.
   PubMed Web of Science ®Google Scholar
• Liu H, Nowak C, Andrien B, Shao M, Ponniah G, Neill A. Impact of IgG Fc-oligosaccharides on recombinant monoclonal antibody structure, stability, safety, and efficacy. Biotechnol Prog. 2017;33(5):1173–81. doi:10.1002/btpr.2498. PMID: 28547754.
   PubMed Web of Science ®Google Scholar
• Gadgil HS, Bondarenko PV, Pipes GD, Dillon TM, Banks D, Abel J, Kleemann GR, Treuheit MJ. Identification of cysteinylation of a free cysteine in the fab region of a recombinant monoclonal IgG1 antibody using lys-C limited proteolysis coupled with LC/MS analysis. Anal Biochem. 2006;355(2):165–74. doi:10.1016/j.ab.2006.05.037. PMID: 16828048.
   PubMed Web of Science ®Google Scholar
• McSherry T, McSherry J, Ozaeta P, Longenecker K, Ramsay C, Fishpaugh J, Allen S. Cysteinylation of a monoclonal antibody leads to its inactivation. MAbs. 2016;8(4):718–25. doi:10.1080/19420862.2016.1160179. PMID: 27050640.
   PubMed Web of Science ®Google Scholar
• Seibert C, Sakmar TP. Toward a framework for sulfoproteomics: synthesis and characterization of sulfotyrosine-containing peptides. Peptide Science. 2008;90(3):459–77. doi:10.1002/bip.20821.
   Google Scholar
• Monigatti F, Hekking B, Steen H. Protein sulfation analysis—a primer. Biochimica Et Biophysica Acta (BBA) - Prot Proteom. 2006;1764(12):1904–13. doi:10.1016/j.bbapap.2006.07.002.
   PubMed Web of Science ®Google Scholar
• Stone MJ, Chuang S, Hou X, Shoham M, Zhu JZ. Tyrosine sulfation: an increasingly recognised post-translational modification of secreted proteins. N Biotechnol. 2009;25(5):299–317. doi:10.1016/j.nbt.2009.03.011.
   PubMed Web of Science ®Google Scholar
• Beisswanger R, Corbeil D, Vannier C, Thiele C, Dohrmann U, Kellner R, Ashman K, Niehrs C, Huttner WB. Existence of distinct tyrosylprotein sulfotransferase genes: molecular characterization of tyrosylprotein sulfotransferase-2. Proc Natl Acad Sci USA. 1998;95(19):11134–39. doi:10.1073/pnas.95.19.11134.
   PubMed Web of Science ®Google Scholar
• Huttner WB. Tyrosine sulfation and the secretory pathway. Annu Rev Physiol. 1988;50(1):363–76. doi:10.1146/annurev.ph.50.030188.002051. PMID: 3288098.
   PubMedGoogle Scholar
• Baeuerle PA, Huttner WB. Tyrosine sulfation of yolk proteins 1, 2, and 3 in drosophila melanogaster. J Biol Chem. 1985;260(10):6434–39. doi:10.1016/S0021-9258(18)88991-8. PMID: 3922974.
   PubMed Web of Science ®Google Scholar
• Zhao J, Saunders J, Schussler SD, Rios S, Insaidoo FK, Fridman AL, Li H, Liu YH. Characterization of a novel modification of a CHO-produced mAb: evidence for the presence of tyrosine sulfation. MAbs. 2017;9(6):985–95. doi:10.1080/19420862.2017.1332552. PMID: 28590151.
   PubMed Web of Science ®Google Scholar
• Tyshchuk O, Gstöttner C, Funk D, Nicolardi S, Frost S, Klostermann S, Becker T, Jolkver E, Schumacher F, Koller CF, et al. Characterization and prediction of positional 4-hydroxyproline and sulfotyrosine, two post-translational modifications that can occur at substantial levels in CHO cells-expressed biotherapeutics. MAbs. 2019;11(7):1219–32. doi:10.1080/19420862.2019.1635865.
   PubMed Web of Science ®Google Scholar
• Klein C, Schaefer W, Regula JT, Dumontet C, Brinkmann U, Bacac M, Umaña P. Engineering therapeutic bispecific antibodies using CrossMab technology. Methods. 2019;154:21–31. doi:10.1016/j.ymeth.2018.11.008. PMID: 30453028.
   PubMed Web of Science ®Google Scholar
• Surowka M, Schaefer W, Klein C. Ten years in the making: application of CrossMab technology for the development of therapeutic bispecific antibodies and antibody fusion proteins. MAbs. 2021;13(1):1967714. doi:10.1080/19420862.2021.1967714. PMID: 34491877.
   PubMed Web of Science ®Google Scholar
• Klein C, Schaefer W, Regula JT. The use of CrossMAb technology for the generation of bi- and multispecific antibodies. MAbs. 2016;8(6):1010–20. doi:10.1080/19420862.2016.1197457. PMID: 27285945.
   PubMed Web of Science ®Google Scholar
• Bacac M, Klein C, Umana P. CEA TCB: a novel head-to-tail 2: 1 T cell bispecific antibody for treatment of CEA-positive solid tumors. Oncoimmunol. 2016;5(8):e1203498. doi:10.1080/2162402x.2016.1203498. PMID: 27622073.
   PubMed Web of Science ®Google Scholar
• Chen G, Zhang Y, Trinidad JC, Dann C. Distinguishing sulfotyrosine containing peptides from their phosphotyrosine counterparts using mass spectrometry. J Am Soc Mass Spectrom. 2018;29(3):455–62. doi:10.1007/s13361-017-1854-1.
   PubMed Web of Science ®Google Scholar
• Valente JJ, Payne RW, Manning MC, Wilson WW, Henry CS. Colloidal behavior of proteins: effects of the second virial coefficient on solubility, crystallization and aggregation of proteins in aqueous solution. Curr Pharm Biotechnol. 2005;6(6):427–36. doi:10.2174/138920105775159313. PMID: 16375727.
   PubMed Web of Science ®Google Scholar
• Yagami T, Kitagawa K, Aida C, Fujiwara H, Futaki S. Stabilization of a tyrosine O-sulfate residue by a cationic functional group: formation of a conjugate acid-base pair. J Pept Res. 2000;56(4):239–49. doi:10.1034/j.1399-3011.2000.00746.x. PMID: 11083063.
   PubMedGoogle Scholar
• Oshannessy DJ, Brighamburke M, Soneson KK, Hensley P, Brooks I. Determination of rate and equilibrium binding constants for macromolecular interactions using surface plasmon resonance: use of nonlinear least squares analysis methods. Anal Biochem. 1993;212(2):457–68. doi:10.1006/abio.1993.1355.
   PubMed Web of Science ®Google Scholar
• O’Shannessy DJ, Brigham-Burke M, Karl Soneson K, Hensley P, Brooks I. Determination of rate and equilibrium binding constants for macromolecular interactions by surface plasmon resonance. In: Part B: numerical computer methods. Vol. 240. Elsevier; 1994. pp. 323–49. doi:10.1016/S0076-6879(94)40054-7.
   Google Scholar
• Karlsson R, Pol E, Frostell Å. Comparison of surface plasmon resonance binding curves for characterization of protein interactions and analysis of screening data. Anal Biochem. 2016;502:53–63. doi:10.1016/j.ab.2016.03.007. PMID: 27019155.
   PubMed Web of Science ®Google Scholar
• Dudgeon K, Rouet R, Kokmeijer I, Schofield P, Stolp J, Langley D, Stock D, Christ D. General strategy for the generation of human antibody variable domains with increased aggregation resistance. Proc Natl Acad Sci USA. 2012;109(27):10879–84. doi:10.1073/pnas.1202866109.
   PubMed Web of Science ®Google Scholar
• Banks DD, Gadgil HS, Pipes GD, Bondarenko PV, Hobbs V, Scavezze JL, Kim J, Jiang XR, Mukku V, Dillon TM. Removal of cysteinylation from an unpaired sulfhydryl in the variable region of a recombinant monoclonal IgG1 antibody improves homogeneity, stability, and biological activity. J Pharm Sci. 2008;97(2):775–90. doi:10.1002/jps.21014. PMID: 17786988.
   PubMed Web of Science ®Google Scholar
• Banks DD, Latypov RF, Ketchem RR, Woodard J, Scavezze JL, Siska CC, Razinkov VI. Native-state solubility and transfer free energy as predictive tools for selecting excipients to include in protein formulation development studies. J Pharm Sci. 2012;101(8):2720–32. doi:10.1002/jps.23219.
   PubMed Web of Science ®Google Scholar
• Banks DD, Cordia JF, Spasojevic V, Sun J, Franc S, Cho Y. Isotonic concentrations of excipients control the dimerization rate of a therapeutic immunoglobulin G1 antibody during refrigerated storage based on their rank order of native-state interaction. Protein Sci. 2018;27(12):2073–83. doi:10.1002/pro.3518.
   PubMed Web of Science ®Google Scholar
• Kingsbury JS, Saini A, Auclair SM, Fu L, Lantz MM, Halloran KT, Calero-Rubio C, Schwenger W, Airiau CY, Zhang J, et al. A single molecular descriptor to predict solution behavior of therapeutic antibodies. Sci Adv. 2020;6(32):eabb0372. doi:10.1126/sciadv.abb0372.
   PubMed Web of Science ®Google Scholar
• Quigley A, Williams DR. The second virial coefficient as a predictor of protein aggregation propensity: a self-interaction chromatography study. Eur J Pharm Biopharm. 2015;96:282–90. doi:10.1016/j.ejpb.2015.07.025. PMID: 26259782.
   PubMed Web of Science ®Google Scholar
• Minton AP. Influence of macromolecular crowding upon the stability and state of association of proteins: predictions and observations. J Pharm Sci. 2005;94(8):1668–75. doi:10.1002/jps.20417.
   PubMed Web of Science ®Google Scholar
• Wang Y, Latypov RF, Lomakin A, Meyer JA, Kerwin BA, Vunnum S, Benedek GB. Quantitative evaluation of colloidal stability of antibody solutions using PEG-induced liquid–liquid phase separation. Mol Pharmaceut. 2014;11(5):1391–402. doi:10.1021/mp400521b.
   PubMed Web of Science ®Google Scholar
• Cai CX, Doria-Rose NA, Schneck NA, Ivleva VB, Tippett B, Shadrick WR, O’Connell S, Coooper JW, Schneiderman Z, Zhang B, et al. Tyrosine O-sulfation proteoforms affect HIV-1 monoclonal antibody potency. Sci Rep. 2022;12(1):8433–44. doi:10.1038/s41598-022-12423-x.
   PubMed Web of Science ®Google Scholar
• Yang ZR. Predicting sulfotyrosine sites using the random forest algorithm with significantly improved prediction accuracy. BMC Bioinform. 2009;10(1):361. doi:10.1186/1471-2105-10-361. PMID: 19874585.
   PubMedGoogle Scholar
• Chang WC, Lee TY, Shien DM, Hsu JB, Horng JT, Hsu PC, Wang TY, Huang HD, Pan RL. Incorporating support vector machine for identifying protein tyrosine sulfation sites. J Comput Chem. 2009;30(15):2526–37. doi:10.1002/jcc.21258. PMID: 19373826.
   PubMed Web of Science ®Google Scholar
• Liu R, Zhang Y, Kumar A, Huhn S, Hullinger L, Du Z. Modulating tyrosine sulfation of recombinant antibodies in CHO cell culture by host selection and sodium chlorate supplementation. Biotechnol J. 2021;16(9):2100142. doi:10.1002/biot.202100142.
   Web of Science ®Google Scholar