4,664
Views
0
CrossRef citations to date
0
Altmetric
Report

Engineering hydrophobicity and manufacturability for optimized biparatopic antibody–drug conjugates targeting c-MET

, , , , , , , , , & ORCID Icon show all
Article: 2302386 | Received 05 Sep 2023, Accepted 03 Jan 2024, Published online: 12 Jan 2024

References

  • Markham A. Tepotinib: First Approval. Drugs. 2020;80:829–13. doi:10.1007/s40265-020-01317-9.
  • Awad MM, Liu S, II R, KC A, Dilly J, VW Z, ML J, RS H, Patil T, GJ R. et al. Acquired resistance to KRASG12C inhibition in cancer. N Engl J Med. 2021;384(25):2382–93. doi:10.1056/NEJMoa2105281.
  • Camidge DR, Davies KD. MET copy number as a secondary driver of epidermal growth factor receptor tyrosine kinase inhibitor resistance in EGFR -mutant non–small-Cell lung cancer. JCO. 2019;37(11):855–57. doi:10.1200/JCO.19.00033.
  • Chmielecki J, Gray JE, Cheng Y, Ohe Y, Imamura F, Cho BC, Lin M-C, Majem M, Shah R, Rukazenkov Y. et al. Candidate mechanisms of acquired resistance to first-line osimertinib in EGFR-mutated advanced non-small cell lung cancer. Nat Commun. 2023;14(1):1070. doi:10.1038/s41467-023-35961-y.
  • Yang J, Zhou P, Yu M. Zhang YCase report: high-level MET amplification as a resistance mechanism of ROS1-tyrosine kinase inhibitors in ROS1-rearranged non-smallcell lung cancer.Frontiers In Oncology [Internet]. 2021; 2023 Jul 5] 11: doi:10.3389/fonc.2021.645224.
  • Rong S, Segal S, Anver M, Resau JH, Vande Woude GF. Invasiveness and metastasis of NIH 3T3 cells induced by met-hepatocyte growth factor/scatter factor autocrine stimulation. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4731–35. doi:10.1073/pnas.91.11.4731.
  • Lai AZ, Cory S, Zhao H, Gigoux M, Monast A, Guiot M-C, Huang S, Tofigh A, Thompson C, Naujokas M. et al. Dynamic reprogramming of signaling upon met inhibition reveals a mechanism of drug resistance in gastric cancer. Sci Signal. 2014;7(322):ra38. doi:10.1126/scisignal.2004839.
  • Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat Rev Cancer. 2012;12(2):89–103. doi:10.1038/nrc3205.
  • KK-W T, Leung K-S, Cho W-S. MET-Targeting anticancer drugs—De novo design and identification by drug repurposing. DDC. 2023;2(3):591–623. doi:10.3390/ddc2030031.
  • De Mello RA, Neves NM, Amaral GA, Lippo EG, Castelo-Branco P, Pozza DH, Tajima CC, Antoniou G. The role of MET inhibitor therapies in the treatment of advanced non-small cell lung cancer. J Clin Med. 2020;9(6):1918. doi:10.3390/jcm9061918.
  • Garon EB, Brodrick P. Targeted therapy approaches for MET abnormalities in non-small cell lung cancer. Drugs. 2021;81(5):547–54. doi:10.1007/s40265-021-01477-2.
  • Huo X, Shen G, Liu Z, Liang Y, Li J, Zhao F, Ren D, Zhao J. Addition of immunotherapy to chemotherapy for metastatic triple-negative breast cancer: a systematic review and meta-analysis of randomized clinical trials. Crit Rev Oncol Hematol. 2021;168:103530. doi:10.1016/j.critrevonc.2021.103530.
  • Shah V, McNatty A, Simpson L, Ofori H, Raheem F. Amivantamab-vmjw: a novel treatment for patients with NSCLC harboring EGFR Exon 20 insertion mutation after progression on platinum-based chemotherapy. Biomedicines. 2023;11:950. doi:10.3390/biomedicines11030950.
  • Casaletto JB, Geddie ML, Abu-Yousif AO, Masson K, Fulgham A, Boudot A, Maiwald T, Kearns JD, Kohli N, Su S. et al. MM-131, a bispecific anti-Met/EpCAM mAb, inhibits HGF-dependent and HGF-independent met signaling through concurrent binding to EpCAM. Proc Natl Acad Sci U S A. 2019;116(15):7533–42. doi:10.1073/pnas.1819085116.
  • Lee B-S, Kang S, Kim K-A, Song Y-J, Cheong KH, Cha H-Y, Kim C-H. Met degradation by SAIT301, a met monoclonal antibody, reduces the invasion and migration of nasopharyngeal cancer cells via inhibition of EGR-1 expression. Cell Death Disease. 2014;5(4):e1159. doi:10.1038/cddis.2014.119.
  • Liu L, Zeng W, Wortinger MA, Yan SB, Cornwell P, Peek VL, Stephens JR, Tetreault JW, Xia J, Manro JR. et al. LY2875358, a neutralizing and internalizing anti-MET bivalent antibody, inhibits HGF-dependent and HGF-independent MET activation and tumor growth. Clin Cancer Res. 2014;20(23):6059–70. doi:10.1158/1078-0432.CCR-14-0543.
  • Su Z, Han Y, Sun Q, Wang X, Xu T, Xie W, Huang X. Anti-MET VHH pool overcomes MET-Targeted cancer therapeutic resistance. Mol Cancer Ther. 2019;18(1):100–11. doi:10.1158/1535-7163.MCT-18-0351.
  • Benedetti F, Stadlbauer K, Stadlmayr G, Rüker F, Wozniak-Knopp G. A tetravalent biparatopic antibody causes strong HER2 internalization and inhibits cellular proliferation. Life (Basel). 2021;11(11):1157. doi:10.3390/life11111157.
  • DaSilva JO, Yang K, Perez Bay AE, Andreev J, Ngoi P, Pyles E, Franklin MC, Dudgeon D, Rafique A, Dore A. et al. A biparatopic antibody that modulates MET trafficking exhibits enhanced efficacy compared with parental antibodies in MET-Driven tumor models. Clin Cancer Res. 2020;26(6):1408–19. doi:10.1158/1078-0432.CCR-19-2428.
  • Paul D, Stern O, Vallis Y, Dhillon J, Buchanan A, McMahon H. Cell surface protein aggregation triggers endocytosis to maintain plasma membrane proteostasis. Nat Commun. 2023;14(1):947. doi:10.1038/s41467-023-36496-y.
  • DaSilva JO, Yang K, Surriga O, Nittoli T, Kunz A, Franklin MC, Delfino FJ, Mao S, Zhao F, Giurleo JT. et al. A biparatopic antibody–drug conjugate to treat MET-Expressing cancers, including those that are unresponsive to MET pathway blockade. Mol Cancer Ther. 2021;20(10):1966–76. doi:10.1158/1535-7163.MCT-21-0009.
  • Li JY, Perry SR, Muniz-Medina V, Wang X, Wetzel LK, Rebelatto MC, Hinrichs MJM, Bezabeh BZ, Fleming RL, Dimasi N. et al. A biparatopic HER2-targeting antibody-drug conjugate induces tumor regression in primary models refractory to or ineligible for HER2-targeted therapy. Cancer Cell. 2016;29(1):117–29. doi:10.1016/j.ccell.2015.12.008.
  • Oh SY, Lee YW, Lee EJ, Kim JH, Park Y, Heo SG, Yu MR, Hong MH, DaSilva J, Daly C. et al. Preclinical Study of a Biparatopic METxMET Antibody–Drug Conjugate, REGN5093-M114, Overcomes MET-driven Acquired Resistance to EGFR TKIs in EGFR-mutant NSCLC. Clin Cancer Res. 2023;29(1):221–32. doi:10.1158/1078-0432.CCR-22-2180.
  • Sellmann C, Doerner A, Knuehl C, Rasche N, Sood V, Krah S, Rhiel L, Messemer A, Wesolowski J, Schuette M. et al. Balancing selectivity and efficacy of bispecific Epidermal Growth Factor Receptor (EGFR) × c-MET antibodies and antibody-drug conjugates. J Biol Chem. 2016;291(48):25106–19. doi:10.1074/jbc.M116.753491.
  • Leung D, Wurst J, Liu T, Martinez R, Datta-Mannan A, Feng Y. Antibody conjugates-recent advances and future innovations. Antibodies. 2020;9(1):2. doi:10.3390/antib9010002.
  • Mckertish CM, Kayser V. Advances and limitations of antibody drug conjugates for cancer. Biomedicines. 2021;9(8):872. doi:10.3390/biomedicines9080872.
  • Tsuchikama K, An Z. Antibody-drug conjugates: recent advances in conjugation and linker chemistries. Protein Cell. 2018;9(1):33–46. doi:10.1007/s13238-016-0323-0.
  • Buecheler JW, Winzer M, Weber C, Gieseler H. Alteration of physicochemical properties for antibody-drug conjugates and their impact on stability. J Pharm Sci. 2020;109(1):161–68. doi:10.1016/j.xphs.2019.08.006.
  • Lyon RP, Bovee TD, Doronina SO, Burke PJ, Hunter JH, Neff-LaFord HD, Jonas M, Anderson ME, Setter JR, Senter PD. Reducing hydrophobicity of homogeneous antibody-drug conjugates improves pharmacokinetics and therapeutic index. Nat Biotechnol. 2015;33(7):733–35. doi:10.1038/nbt.3212.
  • Wagh A, Song H, Zeng M, Tao L, Das TK. Challenges and new frontiers in analytical characterization of antibody-drug conjugates. MAbs. 2018;10(2):222–43. doi:10.1080/19420862.2017.1412025.
  • Davis JH, Aperlo C, Li Y, Kurosawa E, Lan Y, Lo K-M, Huston JS. Seedbodies: fusion proteins based on strand-exchange engineered domain (SEED) CH3 heterodimers in an fc analogue platform for asymmetric binders or immunofusions and bispecific antibodies†. Protein Engineering, Design And Selection. 2010;23(4):195–202. doi:10.1093/protein/gzp094.
  • Labrijn AF, Meesters JI, De Goeij BECG, Van Den Bremer ETJ, Neijssen J, Van Kampen MD, Strumane K, Verploegen S, Kundu A, Gramer MJ. et al. Efficient generation of stable bispecific IgG1 by controlled Fab-arm exchange. Proc Natl Acad Sci U S A. 2013;110(13):5145–50. doi:10.1073/pnas.1220145110.
  • Evers A, Malhotra S, Bolick W-G, Najafian A, Borisovska M, Warszawski S, Fomekong Nanfack Y, Kuhn D, Rippmann F, Crespo A. et al. SUMO. Silico Sequence Assessment Using Multiple Optimization Parameters Methods Mol Biol. 2023;2681:383–98.
  • Schaefer W, Regula JT, Bähner M, Schanzer J, Croasdale R, Dürr H, Gassner C, Georges G, Kettenberger H, Imhof-Jung S. et al. Immunoglobulin domain crossover as a generic approach for the production of bispecific IgG antibodies. Proceedings of the National Academy of Sciences 2011; 108:11187–92.
  • Liu Y, Caffry I, Wu J, Geng SB, Jain T, Sun T, Reid F, Cao Y, Estep P, Yu Y. et al. High-throughput screening for developability during early-stage antibody discovery using self-interaction nanoparticle spectroscopy. MAbs. 2014;6(2):483–92. doi:10.4161/mabs.27431.
  • Jain T, Sun T, Durand S, Hall A, Houston NR, Nett JH, Sharkey B, Bobrowicz B, Caffry I, Yu Y. et al. Biophysical properties of the clinical-stage antibody landscape. Proc Natl Acad Sci U S A. 2017;114(5):944–49. doi:10.1073/pnas.1616408114.
  • Xu Y, Roach W, Sun T, Jain T, Prinz B, Yu T-Y, Torrey J, Thomas J, Bobrowicz P, Vásquez M. et al. Addressing polyspecificity of antibodies selected from an in vitro yeast presentation system: a FACS-based, high-throughput selection and analytical tool. Protein Eng Des Sel. 2013;26(10):663–70. doi:10.1093/protein/gzt047.
  • WO2023170240A1.
  • YY S. Amivantamab: First Approval. Drugs. 2021;81(11):1349–53. doi:10.1007/s40265-021-01561-7.
  • Cotton AD, Nguyen DP, Gramespacher JA, Seiple IB, Wells JA. Development of antibody-based PROTACs for the Degradation of the Cell-Surface Immune Checkpoint Protein PD-L1. J Am Chem Soc. 2021;143(2):593–98. doi:10.1021/jacs.0c10008.
  • Zhang H, Han Y, Yang Y, Lin F, Li K, Kong L, Liu H, Dang Y, Lin J, Chen PR. Covalently engineered nanobody chimeras for targeted membrane protein degradation. J Am Chem Soc. 2021;143(40):16377–82. doi:10.1021/jacs.1c08521.
  • Ahn G, Banik SM, Bertozzi CR. Degradation from the outside in: targeting extracellular and membrane proteins for degradation through the endolysosomal pathway. Cell Chem Biol. 2021;28(7):1072–80. doi:10.1016/j.chembiol.2021.02.024.
  • Lin J, Jin J, Shen Y, Zhang L, Gong G, Bian H, Chen H, Nagle DG, Wu Y, Zhang W. et al. Emerging protein degradation strategies: expanding the scope to extracellular and membrane proteins. Theranostics. 2021;11(17):8337–49. doi:10.7150/thno.62686.
  • Kelton C, Wesolowski JS, Soloviev M, Schweickhardt R, Fischer D, Kurosawa E, McKenna SD, Gross AW. Anti-EGFR biparatopic-SEED antibody has enhanced combination-activity in a single molecule. Arch Biochem Biophys. 2012;526(2):219–25. doi:10.1016/j.abb.2012.03.005.
  • Lewis SM, Wu X, Pustilnik A, Sereno A, Huang F, Rick HL, Guntas G, Leaver-Fay A, Smith EM, Ho C. et al. Generation of bispecific IgG antibodies by structure-based design of an orthogonal fab interface. Nat Biotechnol. 2014;32(2):191–98. doi:10.1038/nbt.2797.
  • Reilly RM, Ji C, Matuszak RP, Anderson MG, Tucker L, Klunder N, Lazo AL, Boghaert ER, Pysz MA, D’Souza A. et al. Abstract 6311: ABBV-400: An ADC delivering a novel topoisomerase 1 inhibitor to c-Met-positive solid tumors. Cancer Res. 2023;83(7_Supplement):6311. doi:10.1158/1538-7445.AM2023-6311.
  • Bhatta P, Whale KD, Sawtell AK, Thompson CL, Rapecki SE, Cook DA, Twomey BM, Mennecozzi M, Starkie LE, Barry EMC. et al. Bispecific antibody target pair discovery by high-throughput phenotypic screening using in vitro combinatorial fab libraries. MAbs. 2021;13(1):1859049. doi:10.1080/19420862.2020.1859049.
  • Dengl S, Mayer K, Bormann F, Duerr H, Hoffmann E, Nussbaum B, Tischler M, Wagner M, Kuglstatter A, Leibrock L. et al. Format chain exchange (FORCE) for high-throughput generation of bispecific antibodies in combinatorial binder-format matrices. Nat Commun. 2020;11(1):4974. doi:10.1038/s41467-020-18477-7.
  • Apaja PM, Lukacs GL. Protein homeostasis at the plasma membrane. Physiology. 2014;29(4):265–77. doi:10.1152/physiol.00058.2013.
  • Dyson MR, Masters E, Pazeraitis D, Perera RL, Syrjanen JL, Surade S, Thorsteinson N, Parthiban K, Jones PC, Sattar M. et al. Beyond affinity: selection of antibody variants with optimal biophysical properties and reduced immunogenicity from mammalian display libraries. MAbs. 2020;12(1):1829335. doi:10.1080/19420862.2020.1829335.
  • Huhtinen O, Salbo R, Lamminmäki U, Prince S. Selection of biophysically favorable antibody variants using a modified flp-in CHO mammalian display platform. Front Bioeng Biotechnol. 2023;11:1170081. doi:10.3389/fbioe.2023.1170081.
  • Makowski EK, Chen H, Lambert M, Bennett EM, Eschmann NS, Zhang Y, Zupancic JM, Desai AA, Smith MD, Lou W. et al. Reduction of therapeutic antibody self-association using yeast-display selections and machine learning. MAbs. 2022;14(1):2146629. doi:10.1080/19420862.2022.2146629.
  • Gérard A, Woolfe A, Mottet G, Reichen M, Castrillon C, Menrath V, Ellouze S, Poitou A, Doineau R, Briseno-Roa L. et al. High-throughput single-cell activity-based screening and sequencing of antibodies using droplet microfluidics. Nat Biotechnol. 2020;38(6):715–21. doi:10.1038/s41587-020-0466-7.
  • Mason DM, Friedensohn S, Weber CR, Jordi C, Wagner B, Meng SM, Ehling RA, Bonati L, Dahinden J, Gainza P. et al. Optimization of therapeutic antibodies by predicting antigen specificity from antibody sequence via deep learning. Nat Biomed Eng. 2021;5(6):600–12. doi:10.1038/s41551-021-00699-9.
  • Datta-Mannan A, Choi H, Jin Z, Lu J, Liu L, Stokell D, Murphy A, Dunn K, Martinez M, Feng Y. Reducing target binding affinity improves the Therapeutic Index of Anti-MET Antibody Drug Conjugate in tumor Bearing Animals [internet]. Preprints; 2023 [cited 2023 Jul 5]. Available from: https://www.authorea.com/users/623549/articles/646245-reducing-target-binding-affinity-improves-the-therapeutic-index-of-anti-met-antibody-drug-conjugate-in-tumor-bearing-animals?commit=63c8ca0e12d2bd20e890c99d3daac08bed23b502
  • Colombo R, Rich JR. The therapeutic window of antibody drug conjugates: a dogma in need of revision. Cancer Cell. 2022;40(11):1255–63. doi:10.1016/j.ccell.2022.09.016.
  • Chemical Computing Group (CCG). | research [Internet]. [cited 2022 Aug 25]; Available from: https://www.chemcomp.com/Research-Citing_MOE.htm
  • The PyMOL Molecular Graphics System, Version 2.3 Schrödinger, LLC. [Internet]. [cited 2022 Aug 25]; Available from: https://www.schrodinger.com/products/pymol
  • Kozakov D, Brenke R, Comeau SR, Vajda SP. PIPER: an FFT-based protein docking program with pairwise potentials. Proteins. 2006;65(2):392–406. doi:10.1002/prot.21117.
  • Schrödinger release 2021-3: BioLuminate Schrödinger LLC: New York, 2021 [Internet]. [cited 2022 Aug 25]; Available from: https://www.schrodinger.com/products/bioluminate
  • Sankar K, Krystek SR Jr, Carl SM, Day T, Maier JKX. AggScore: prediction of aggregation-prone regions in proteins based on the distribution of surface patches. Proteins Struct Funct Bioinf. 2018;86(11):1147–56. doi:10.1002/prot.25594.
  • Ahmed L, Gupta P, Martin KP, Scheer JM, Nixon AE, Kumar S. Intrinsic physicochemical profile of marketed antibody-based biotherapeutics. Proc Natl Acad Sci U S A. 2021;118(37):e2020577118. doi:10.1073/pnas.2020577118.
  • Benatuil L, Perez JM, Belk J, Hsieh C-M. An improved yeast transformation method for the generation of very large human antibody libraries. Protein Eng Des Sel. 2010;23(4):155–59. doi:10.1093/protein/gzq002.
  • Weaver-Feldhaus JM, Lou J, Coleman JR, Siegel RW, Marks JD, Feldhaus MJ. Yeast mating for combinatorial fab library generation and surface display. FEBS Lett. 2004;564(1–2):24–34. doi:10.1016/S0014-5793(04)00309-6.
  • Gaa R, Kumari K, Mayer HM, Yanakieva D, Tsai S-P, Joshi S, Guenther R, Doerner A. An integrated mammalian library approach for optimization and enhanced microfluidics-assisted antibody hit discovery. Artif Cells, Nanomed Biotechnol. 2023;51(1):74–82. doi:10.1080/21691401.2023.2173219.
  • Elter A, Bogen JP, Hinz SC, Fiebig D, Macarrón Palacios A, Grzeschik J, Hock B, Kolmar H. Humanization of Chicken‐Derived scFv using yeast surface display and NGS data mining. Biotechnol J. 2021;16(3):2000231. doi:10.1002/biot.202000231.
  • Schröter C, Krah S, Beck J, Könning D, Grzeschik J, Valldorf B, Zielonka S, Kolmar H. Isolation of pH-sensitive antibody fragments by fluorescence-activated cell sorting and yeast surface display. Methods Mol Biol. 2018;1685:311–31.
  • Becht E, McInnes L, Healy J, Dutertre C-A, Kwok IWH, Ng LG, Ginhoux F, Newell EW. Dimensionality reduction for visualizing single-cell data using UMAP. Nat Biotechnol. 2019;37(1):38–44. doi:10.1038/nbt.4314.
  • Yanakieva D, Pekar L, Evers A, Fleischer M, Keller S, Mueller-Pompalla D, Toleikis L, Kolmar H, Zielonka S, Krah S. Beyond bispecificity: controlled fab arm exchange for the generation of antibodies with multiple specificities. MAbs. 2022;14:2018960. doi:10.1080/19420862.2021.2018960.
  • Makowski EK, Wu L, Gupta P, Tessier PM. Discovery-stage identification of drug-like antibodies using emerging experimental and computational methods. MAbs. 2021;13(1):1895540. doi:10.1080/19420862.2021.1895540.