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Application of quantitative protein mass spectrometric data in the early predictive analysis of membrane-bound target engagement by monoclonal antibodies

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Article: 2324485 | Received 18 Dec 2023, Accepted 23 Feb 2024, Published online: 04 Mar 2024

References

  • Crescioli , S, Kaplon H, Chenoweth, A, Wang, L, Visweswaraiah, J, Reichert JM. Antibodies to watch in 2024. MAbs. 2024;16(1):2297450. doi:10.1080/19420862.2023.2297450.
  • Dowden H, Munro J. Trends in clinical success rates and therapeutic focus. Nat Rev Drug Discov. 2019;18(7):495–12. doi:10.1038/d41573-019-00074-z.
  • Tarantino P, Tolaney SM. The dawn of the antibody–drug conjugates era: how T-DM1 reinvented the future of chemotherapy for solid tumors. Cancer Res. 2022;82(20):3659–3661. doi:10.1158/0008-5472.CAN-22-2324.
  • Martineau P, Watier H, Pèlegrin A, Turtoi A. Targets for MAbs: innovative approaches for their discovery & validation, LabEx MAbImprove 6th antibody industrial symposium, June 25-26, 2018, Montpellier, France. MAbs. 2019;11(5):812–25. doi:10.1080/19420862.2019.1612691.
  • An G. Concept of Pharmacologic Target-Mediated Drug Disposition in Large-Molecule and Small-Molecule Compounds. J Clin Pharmacol. 2020;60(2):149–163. doi:10.1002/jcph.1545.
  • Morgan P, Van Der Graaf PH, Arrowsmith J, Feltner DE, Drummond KS, Wegner CD, Street SDA. Can the flow of medicines be improved? Fundamental pharmacokinetic and pharmacological principles toward improving phase II survival. Drug Discovery Today. 2012;17(9–10):419–24. doi:10.1016/j.drudis.2011.12.020.
  • Huang Q, Szklarczyk D, Wang M, Simonovic M, von Mering C. PaxDb 5.0: Curated Protein Quantification Data Suggests Adaptive Proteome Changes in Yeasts. Mol Cell Proteomics. 2023;22(10):100640. doi:10.1016/j.mcpro.2023.100640.
  • Wang M, Weiss M, Simonovic M, Haertinger G, Schrimpf SP, Hengartner MO, von Mering C. PaxDb, a Database of Protein Abundance Averages Across All Three Domains of Life. Molecular & Cellular Proteomics: MCP. 2012;11(8):492–500. doi:10.1074/mcp.O111.014704.
  • Sepp A, Bergström M, Davies M. Cross-species/cross-modality physiologically based pharmacokinetics for biologics: 89Zr-labelled albumin-binding domain antibody GSK3128349 in humans. MAbs. 2020;12(1):e1832861. doi:10.1080/19420862.2020.1832861.
  • Sepp A, Meno-Tetang G, Weber A, Sanderson A, Schon O, Berges A. Computer-assembled cross-species/cross-modalities two-pore physiologically based pharmacokinetic model for biologics in mice and rats. J Pharmacokinet Pharmacodyn. 2019;46(4):339–359. doi:10.1007/s10928-019-09640-9.
  • Hsu JL, Hung M-C. The role of HER2, EGFR, and other receptor tyrosine kinases in breast cancer. Cancer Metastasis Rev. 2016;35(4):575–588. doi:10.1007/s10555-016-9649-6.
  • Bertelsen V, Stang E. The mysterious ways of ErbB2/HER2 trafficking. Membranes (Basel). 2014;4(3):424–46. doi:10.3390/membranes4030424.
  • Wegler C, Wiśniewski JR, Robertsen I, Christensen H, Kristoffer Hertel J, Hjelmesæth J, Jansson-Löfmark R, Åsberg A, Andersson TB, Artursson P. Drug disposition protein quantification in matched human jejunum and liver from donors with obesity. Clin Pharma And Therapeutics. 2022;111(5):1142–54. doi:10.1002/cpt.2558.
  • Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson Å, Kampf C, Sjöstedt E, Asplund A. et al. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419. doi:10.1126/science.1260419.
  • Graf JF, Scholz BJ, Zavodszky MI. BioDMET: a physiologically based pharmacokinetic simulation tool for assessing proposed solutions to complex biological problems. J Pharmacokinet Pharmacodyn. 2012;39(1):37–54. doi:10.1007/s10928-011-9229-x.
  • Brown GC. Total cell protein concentration as an evolutionary constraint on the metabolic control distribution in cells. J Theor Biol. 1991;153(2):195–203. doi:10.1016/S0022-5193(05)80422-9.
  • Wisniewski JR, Hein MY, Cox J, Mann M. A “proteomic ruler” for protein copy number and concentration estimation without spike-in standards. Molecular & Cellular Proteomics: MCP. 2014;13(12):3497–3506. doi:10.1074/mcp.M113.037309.
  • Leeman M, Choi J, Hansson S, Storm MU, Nilsson L. Proteins and antibodies in serum, plasma, and whole blood—size characterization using asymmetrical flow field-flow fractionation (AF4). Anal Bioanal Chem. 2018;410(20):4867–4873. doi:10.1007/s00216-018-1127-2.
  • Wiig H, Swartz MA. Interstitial fluid and lymph formation and transport: physiological regulation and roles in inflammation and cancer. Physiol Rev. 2012;92(3):1005–1060. doi:10.1152/physrev.00037.2011.
  • Muliaditan M, Sepp A. Application of quantitative protein mass spectrometric data in the early predictive analysis of target engagement by monoclonal antibodies. Clin Transl Sci. 2022;15(7):1634–1643. doi:10.1111/cts.13278.
  • Tokuda Y, Watanabe T, Omuro Y, Ando M, Katsumata N, Okumura A, Ohta M, Fujii H, Sasaki Y, Niwa T. et al. Dose escalation and pharmacokinetic study of a humanized anti-HER2 monoclonal antibody in patients with HER2/neu-overexpressing metastatic breast cancer. Br J Cancer. 1999;81(8):1419–1425. doi:10.1038/sj.bjc.6690343.
  • Fracasso PM, Burris H III, Arquette MA, Govindan R, Gao F, Wright LP, Goodner SA, Greco FA, Jones SF, Willcut N. et al. A phase 1 escalating single-dose and weekly fixed-dose study of Cetuximab: pharmacokinetic and pharmacodynamic rationale for dosing. Clin Cancer Res. 2007;13(3):986–993. doi:10.1158/1078-0432.CCR-06-1542.
  • Rohatgi A. WebPlotDigitizer. https://automeris.io/WebPlotDigitizer.
  • Wang W, Yin L, Gonzalez-Malerva L, Wang S, Yu X, Eaton S, Zhang S, Chen H-Y, LaBaer J, Tao N. In situ drug-receptor binding kinetics in single cells: a quantitative label-free study of anti-tumor drug resistance. Sci Rep. 2014;4(1):6609. doi:10.1038/srep06609.
  • Patel D, LahuiI A, Patel SP, Franklin M, Jiminez X, Hicklin DJ, Kang X. Monoclonal antibody cetuximab binds to and down-regulates constitutively activated epidermal growth factor receptor vIII on the cell surface. Anticancer Res. 2007;27:3355–66.
  • Leyton JV. Improving receptor-mediated intracellular access and accumulation of antibody therapeutics—the tale of HER2. Antibodies. 2020;9(3):32. doi:10.3390/antib9030032.
  • Sakai A, Tagami M, Kakehashi A, Katsuyama-Yoshikawa A, Misawa N, Wanibuchi H, Azumi A, Honda S. Expression, intracellular localization, and mutation of EGFR in conjunctival squamous cell carcinoma and the association with prognosis and treatment. PloS One. 2020;15(8):e0238120. doi:10.1371/journal.pone.0238120.
  • Stüber JC, Kast F, Plückthun A. High-throughput quantification of surface protein internalization and degradation. ACS Chem Biol. 2019;14(6):1154–1163. doi:10.1021/acschembio.9b00016.
  • Narod SA. Narod SA: disappearing breast cancers. Curr Oncol. 2012;19(2):59–60. doi:10.3747/co.19.1037.
  • Majumder S, Islam MT, Righetti R. Non-invasive imaging of interstitial fluid transport parameters in solid tumors in vivo. Sci Rep. 2023;13(1):7132. doi:10.1038/s41598-023-33651-9.
  • Gullick WJ, Marsden JJ, Whittle N, Ward B, Bobrow L, Waterfield MD. Expression of epidermal growth factor receptors on human Cervical, Ovarian, and Vulval Carcinomas. Cancer Res. 1986;46:285–92.
  • Onsum MD, Geretti E, Paragas V, Kudla AJ, Moulis SP, Luus L, Wickham TJ, McDonagh CF, MacBeath G, Hendriks BS. Single-cell quantitative HER2 measurement identifies heterogeneity and distinct subgroups within traditionally defined HER2-positive patients. The American Journal Of Pathology. 2013;183(5):1446–60. doi:10.1016/j.ajpath.2013.07.015.
  • Akaike H. An information criterion (AIC). Math Sci. 1976;14:5–9.
  • Dunlap T, Cao Y. Physiological considerations for modeling in vivo antibody-target interactions. Front Pharmacol. 2022;13:13. doi:10.3389/fphar.2022.856961.
  • Li X, Jusko W, Cao Y. Role of interstitial fluid turnover on target suppression by therapeutic biologics using a minimal physiologically-based pharmacokinetic (mPBPK) model. J Pharmacol Exp Ther. 2018;367(1):1–8. doi:10.1124/jpet.118.250134.
  • Plum PS, Gebauer F, Krämer M, Alakus H, Berlth F, Chon S-H, Schiffmann L, Zander T, Büttner R, Hölscher AH. et al. HER2/neu (ERBB2) expression and gene amplification correlates with better survival in esophageal adenocarcinoma. BMC Cancer. 2019;19(1):38. doi:10.1186/s12885-018-5242-4.
  • Bianconi E, Piovesan A, Facchin F, Beraudi A, Casadei R, Frabetti F, Vitale L, Pelleri MC, Tassani S, Piva F. et al. An estimation of the number of cells in the human body. Ann Hum Biol. 2013;40(6):463–471. doi:10.3109/03014460.2013.807878.
  • Wee P, Wang Z. Epidermal growth factor receptor cell proliferation signaling pathways. Cancers. 2017;9(5):52. doi:10.3390/cancers9050052.
  • Sorkin A, Duex JE. Quantitative analysis of endocytosis and turnover of epidermal growth factor (EGF) and EGF receptor. Curr Protoc Cell Biol. 2010;46(1):15–4. Chapter 15:Unit 15 14. doi:10.1002/0471143030.cb1514s46.
  • Larson JS, Goodman LJ, Tan Y, Defazio-Eli L, Paquet AC, Cook JW, Rivera A, Frankson K, Bose J, Chen L. et al. Analytical validation of a highly quantitative, sensitive, accurate, and reproducible assay (HERmark®) for the measurement of HER2 total protein and HER2 homodimers in FFPE breast cancer tumor specimens. Patholog Res Int. 2010;2010:1–14. doi:10.4061/2010/814176.
  • Gutierrez C, Schiff R. HER2: biology, detection, and clinical implications. Arch Pathol Lab Med. 2011;135(1):55–62. doi:10.5858/2010-0454-RAR.1.
  • Mager DE, Jusko WJ. General pharmacokinetic model for drugs exhibiting target-mediated drug disposition. J Pharmacokinet Pharmacodyn. 2001;28(6):507–532. doi:10.1023/A:1014414520282.
  • van Waterschoot RAB, Parrott NJ, Olivares-Morales A, Lavé T, Rowland M, Smith DA. Impact of target interactions on small-molecule drug disposition: an overlooked area. Nat Rev Drug Discov. 2018;17(4):299–299. doi:10.1038/nrd.2018.26.
  • Hendriks BS, Opresko LK, Wiley HS, Lauffenburger D. Coregulation of Epidermal Growth Factor Receptor/Human Epidermal Growth Factor Receptor 2 (HER2) Levels and Locations. Quant Anal HER2 Overexpression Eff. 2003;63:1130–37.
  • Durbin KR, Phipps C, Liao X. Mechanistic modeling of antibody–drug conjugate internalization at the cellular level reveals inefficient processing steps. Mol Cancer Ther. 2018;17(6):1341–1351. doi:10.1158/1535-7163.MCT-17-0672.
  • Lammerts van Bueren JJ, Bleeker WK, Bøgh HO, Houtkamp M, Schuurman J, van de Winkel JGJ, Parren PWHI. Effect of target dynamics on pharmacokinetics of a novel therapeutic antibody against the epidermal growth factor receptor: implications for the mechanisms of action. 2006;66(15):7630–38. doi:10.1158/0008-5472.CAN-05-4010.
  • Cheng J, Liang M, Carvalho MF, Tigue N, Faggioni R, Roskos LK, Vainshtein I. Molecular mechanism of HER2 rapid internalization and redirected trafficking induced by anti-HER2 biparatopic antibody. Antibodies (Basel). 2020;9(3):49. doi:10.3390/antib9030049.
  • Austin CD, De Mazière AM, Pisacane PI, van Dijk SM, Eigenbrot C, Sliwkowski MX, Klumperman J, Scheller RH. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and Geldanamycin. Mol Biol Cell. 2004;15(12):5268–82. doi:10.1091/mbc.e04-07-0591.
  • Fehling-Kaschek M, Peckys DB, Kaschek D, Timmer J, Jonge N. Mathematical modeling of drug-induced receptor internalization in the HER2-positive SKBR3 breast cancer cell-line. Sci Rep. 2019;9(1):12709. doi:10.1038/s41598-019-49019-x.
  • Maass KF, Kulkarni C, Betts AM, Wittrup KD. Determination of cellular processing rates for a Trastuzumab-Maytansinoid Antibody-Drug Conjugate (ADC) highlights key parameters for ADC design. AAPS J. 2016;18(3):635–646. doi:10.1208/s12248-016-9892-3.
  • Rudnick SI, Lou J, Shaller CC, Tang Y, Klein-Szanto AJP, Weiner LM, Marks JD, Adams GP. Influence of affinity and antigen internalization on the uptake and penetration of anti-HER2 antibodies in solid tumors. Cancer Res. 2011;71(6):2250–2259. doi:10.1158/0008-5472.CAN-10-2277.
  • Pereira PMR, Sharma SK, Carter LM, Edwards KJ, Pourat J, Ragupathi A, Janjigian YY, Durack JC, Lewis JS. Caveolin-1 mediates cellular distribution of HER2 and affects trastuzumab binding and therapeutic efficacy. Nat Commun. 2018;9(1):5137. doi:10.1038/s41467-018-07608-w.
  • Yano S, Kondo K, Yamaguchi M, Richmond G, Hutchison M, Wakeling A, Averbuch S, Wadsworth P. Distribution and function of EGFR in human tissue and the effect of EGFR tyrosine kinase inhibition. Anticancer Res. 2003;23:3639–50.
  • Epenetos AA, Snook D, Durbin H, Johnson PM, Taylor-Papadimitriou J. Limitations of radiolabeled monoclonal antibodies for localization of human neoplasms. Cancer Res. 1986;46:3183–91.
  • Mach J-P, Carrel S, Forni M, Ritschard J, Donath A, Alberto P. Tumor localization of radio-labeled antibodies against carcinoembryonic antigen in patients with carcinoma. N Engl J Med. 1980;303(1):5–10. doi:10.1056/NEJM198007033030102.
  • Enever C, Batuwangala T, Plummer C, Sepp A. Next generation immunotherapeutics-honing the magic bullet. Curr Opin Biotechnol. 2009;20(4):405–11. doi:10.1016/j.copbio.2009.07.002.
  • Reig-Lopez J, Tang W, Fernandez-Teruel C, Merino-Sanjuan M, Mangas-Sanjuan V, Boulton DW, Sharma P. Application of population physiologically based pharmacokinetic modelling to optimize target expression and clearance mechanisms of therapeutic monoclonal antibodies. Brit J Clinical Pharma. 2023;89(9):2691–702. doi:10.1111/bcp.15745.