Structural and functional analysis of engineered antibodies for cancer immunotherapy: insights into protein compactness and solvent accessibility

References

• Adams, E. M., Pezzotti, S., Ahlers, J., Rüttermann, M., Levin, M., Goldenzweig, A., Peleg, Y., Fleishman, S. J., Sagi, I., & Havenith, M. (2021). Local mutations can serve as a game changer for global protein solvent interaction. JACS Au, 1(7), 1076–1085. https://doi.org/10.1021/jacsau.1c00155
   PubMedGoogle Scholar
• Ahmad, Z. A., Yeap, S. K., Ali, A. M., Ho, W. Y., Alitheen, N. B. M., & Hamid, M. (2012). ScFv antibody: Principles and clinical application. Clinical & Developmental Immunology, 2012, 980250–980215. https://doi.org/10.1155/2012/980250
   PubMed Web of Science ®Google Scholar
• Aier, I., Varadwaj, P. K., & Raj, U. (2016). Structural insights into conformational stability of both wild-type and mutant EZH2 receptor. Scientific Reports, 6, 34984. https://doi.org/10.1038/srep34984
   PubMed Web of Science ®Google Scholar
• Allen, C., Her, S., & Jaffray, D. A. (2017). Radiotherapy for cancer: Present and future. Advanced Drug Delivery Reviews, 109, 1–2. https://doi.org/10.1016/j.addr.2017.01.004
   PubMed Web of Science ®Google Scholar
• Amir, M., Mohammad, T., Kumar, V., Alajmi, M. F., Rehman, M. T., Hussain, A., Alam, P., Dohare, R., Islam, A., Ahmad, F., & Hassan, M. I. (2019). Structural analysis and conformational dynamics of STN1 gene mutations involved in coat plus syndrome. Frontiers in Molecular Biosciences, 6, 41. https://doi.org/10.3389/fmolb.2019.00041
   PubMed Web of Science ®Google Scholar
• Bacac, M., Colombetti, S., Herter, S., Sam, J., Perro, M., Chen, S., Bianchi, R., Richard, M., Schoenle, A., Nicolini, V., Diggelmann, S., Limani, F., Schlenker, R., Hüsser, T., Richter, W., Bray-French, K., Hinton, H., Giusti, A. M., Freimoser-Grundschober, A., … Umaña, P. (2018). CD20-TCB with obinutuzumab pretreatment as next-generation treatment of hematologic malignancies. Clinical Cancer Research, 24(19), 4785–4797. https://doi.org/10.1158/1078-0432.CCR-18-0455
   PubMed Web of Science ®Google Scholar
• Boateng, H. A. (2020). Periodic Coulomb tree method: An alternative to parallel particle mesh Ewald. Journal of Chemical Theory and Computation, 16(1), 7–17. https://doi.org/10.1021/acs.jctc.9b00648
   PubMed Web of Science ®Google Scholar
• Brinkmann, U., & Kontermann, R. E. (2017). The making of bispecific antibodies. MAbs, 9(2), 182–212. https://doi.org/10.1080/19420862.2016.1268307
   PubMed Web of Science ®Google Scholar
• Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). CHARMM: The biomolecular simulation program. Journal of Computational Chemistry, 30(10), 1545–1614. https://doi.org/10.1002/jcc.21287
   PubMed Web of Science ®Google Scholar
• Brown, D., & Clarke, J. H. R. (1984). A comparison of constant energy, constant temperature and constant pressure ensembles in molecular dynamics simulations of atomic liquids. Molecular Physics, 51(5), 1243–1252. https://doi.org/10.1080/00268978400100801
   Web of Science ®Google Scholar
• Carter, P., Andersen, C. A. F., & Rost, B. (2003). DSSPcont: Continuous secondary structure assignments for proteins. Nucleic Acids Research, 31(13), 3293–3295. https://doi.org/10.1093/nar/gkg626
   PubMed Web of Science ®Google Scholar
• Carter, P. J., & Lazar, G. A. (2018). Next generation antibody drugs: Pursuit of the ‘high-hanging fruit’. Nature Reviews. Drug Discovery, 17(3), 197–223. https://doi.org/10.1038/nrd.2017.227
   PubMed Web of Science ®Google Scholar
• Coloma, M. J., & Morrison, S. L. (1997). Design and production of novel tetravalent bispecific antibodies. Nature Biotechnology, 15(2), 159–163. https://doi.org/10.1038/nbt0297-159
   PubMed Web of Science ®Google Scholar
• Culka, M., & Rulíšek, L. (2019). Factors stabilising β-sheets in protein structures from a quantum-chemical perspective. The Journal of Physical Chemistry B, 123(30), 6453–6461. https://doi.org/10.1021/acs.jpcb.9b04866
   PubMed Web of Science ®Google Scholar
• Dey, J., Mahapatra, S. R., Lata, S., Patro, S., Misra, N., & Suar, M. (2022). Exploring Klebsiella pneumoniae capsule polysaccharide proteins to design multiepitope subunit vaccine to fight against pneumonia. Expert Review of Vaccines, 21(4), 569–587. https://doi.org/10.1080/14760584.2022.2021882
   PubMed Web of Science ®Google Scholar
• DiGiandomenico, A., Keller, A. E., Gao, C., Rainey, G. J., Warrener, P., Camara, M. M., Bonnell, J., Fleming, R., Bezabeh, B., Dimasi, N., Sellman, B. R., Hilliard, J., Guenther, C. M., Datta, V., Zhao, W., Gao, C., Yu, X.-Q., Suzich, J. A., & Stover, C. K. (2014). A multifunctional bispecific antibody protects against Pseudomonas aeruginosa. Science Translational Medicine, 6(262), 262ra155. https://doi.org/10.1126/scitranslmed.3009655
   PubMed Web of Science ®Google Scholar
• Fanger, M. W., & Guyre, P. M. (1991). Bispecific antibodies for targeted cellular cytotoxicity. Trends in Biotechnology, 9(11), 375–380. https://doi.org/10.1016/0167-7799(91)90129-6
   PubMed Web of Science ®Google Scholar
• Fanger, M. W., Morganelli, P. M., & Guyre, P. M. (1992). Bispecific antibodies. Critical Reviews in Immunology, 12(3–4), 101–124.
   PubMed Web of Science ®Google Scholar
• Gohlke, H., & Case, D. A. (2004). Converging free energy estimates: MM-PB(GB)SA studies on the protein–protein complex Ras–Raf. Journal of Computational Chemistry, 25(2), 238–250. https://doi.org/10.1002/jcc.10379
   PubMed Web of Science ®Google Scholar
• Guex, N., & Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-PDBViewer: An environment for comparative protein modeling. Electrophoresis, 18(15), 2714–2723. https://doi.org/10.1002/elps.1150181505
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L
   Web of Science ®Google Scholar
• Hu, J., & Wang, C. (2010). Molecular dynamics simulation of HIV-1 integrase dimer complexed with viral DNA. Chinese Journal of Chemistry, 28(1), 33–40. https://doi.org/10.1002/cjoc.201090032
   Web of Science ®Google Scholar
• Khan, M. T., Ali, S., Zeb, M. T., Kaushik, A. C., Malik, S. I., & Wei, D.-Q. (2020). Gibbs free energy calculation of mutation in PncA and RpsA associated with pyrazinamide resistance. Frontiers in Molecular Biosciences, 7, 52. https://doi.org/10.3389/fmolb.2020.00052
   PubMed Web of Science ®Google Scholar
• Khongorzul, P., Ling, C. J., Khan, F. U., Ihsan, A. U., & Zhang, J. (2020). Antibody–drug conjugates: A comprehensive review. Molecular Cancer Research, 18(1), 3–19. https://doi.org/10.1158/1541-7786.MCR-19-0582
   PubMed Web of Science ®Google Scholar
• Krawczyk, K., Liu, X., Baker, T., Shi, J., & Deane, C. M. (2014). Improving B-cell epitope prediction and its application to global antibody-antigen docking. Bioinformatics (Oxford, England), 30(16), 2288–2294. https://doi.org/10.1093/bioinformatics/btu190
   PubMed Web of Science ®Google Scholar
• Le Basle, Y., Chennell, P., Tokhadze, N., Astier, A., & Sautou, V. (2020). Physicochemical stability of monoclonal antibodies: A review. Journal of Pharmaceutical Sciences, 109(1), 169–190. https://doi.org/10.1016/j.xphs.2019.08.009
   PubMed Web of Science ®Google Scholar
• Lee, J., Cheng, X., Swails, J. M., Yeom, M. S., Eastman, P. K., Lemkul, J. A., Wei, S., Buckner, J., Jeong, J. C., Qi, Y., Jo, S., Pande, V. S., Case, D. A., Brooks, C. L., MacKerell, A. D., Klauda, J. B., & Im, W. (2016). CHARMM-GUI input generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM simulations using the CHARMM36 additive force field. Journal of Chemical Theory and Computation, 12(1), 405–413. https://doi.org/10.1021/acs.jctc.5b00935
   PubMed Web of Science ®Google Scholar
• Liberis, E., Velickovic, P., Sormanni, P., Vendruscolo, M., & Liò, P. (2018). Parapred: Antibody paratope prediction using convolutional and recurrent neural networks. Bioinformatics (Oxford, England), 34(17), 2944–2950. https://doi.org/10.1093/bioinformatics/bty305
   PubMed Web of Science ®Google Scholar
• Lobanov, M. Y., Bogatyreva, N. S., & Galzitskaya, O. V. (2008). Radius of gyration as an indicator of protein structure compactness. Molecular Biology, 42(4), 623–628. https://doi.org/10.1134/S0026893308040195
   Web of Science ®Google Scholar
• Lu, R.-M., Hwang, Y.-C., Liu, I.-J., Lee, C.-C., Tsai, H.-Z., Li, H.-J., & Wu, H.-C. (2020). Development of therapeutic antibodies for the treatment of diseases. Journal of Biomedical Science, 27(1), 1. https://doi.org/10.1186/s12929-019-0592-z
   PubMed Web of Science ®Google Scholar
• Ma, H., Ó'Fágáin, C., & O'Kennedy, R. (2020). Antibody stability: A key to performance - Analysis, influences and improvement. Biochimie, 177, 213–225. https://doi.org/10.1016/j.biochi.2020.08.019
   PubMed Web of Science ®Google Scholar
• Ma, J., Mo, Y., Tang, M., Shen, J., Qi, Y., Zhao, W., Huang, Y., Xu, Y., & Qian, C. (2021). Bispecific antibodies: From research to clinical application. Frontiers in Immunology, 12, 626616. https://doi.org/10.3389/fimmu.2021.626616
   PubMed Web of Science ®Google Scholar
• Marcelino, A. M. C., & Gierasch, L. M. (2008). Roles of β-turns in protein folding: From peptide models to protein engineering. Biopolymers, 89(5), 380–391. https://doi.org/10.1002/bip.20960
   PubMed Web of Science ®Google Scholar
• Martis, E. A. F., & Coutinho, E. C. (2019). Free energy-based methods to understand drug resistance mutations. Challenges and Advances in Computational Chemistry and Physics, 27, 1–24.
   Google Scholar
• Moores, S. L., Chiu, M. L., Bushey, B. S., Chevalier, K., Luistro, L., Dorn, K., Brezski, R. J., Haytko, P., Kelly, T., Wu, S.-J., Martin, P. L., Neijssen, J., Parren, P. W. H. I., Schuurman, J., Attar, R. M., Laquerre, S., Lorenzi, M. V., & Anderson, G. M. (2016). A novel bispecific antibody targeting EGFR and cMet is effective against EGFR inhibitor-resistant lung tumors. Cancer Research, 76(13), 3942–3953. https://doi.org/10.1158/0008-5472.CAN-15-2833
   PubMed Web of Science ®Google Scholar
• Nagai, H., & Kim, Y. H. (2017). Cancer prevention from the perspective of global cancer burden patterns. Journal of Thoracic Disease, 9(3), 448–451. https://doi.org/10.21037/jtd.2017.02.75
   PubMed Web of Science ®Google Scholar
• Nolting, B. (2013). Linker technologies for antibody-drug conjugates. Methods in Molecular Biology (Clifton, NJ), 1045, 71–100. https://doi.org/10.1007/978-1-62703-541-5_5
   PubMedGoogle Scholar
• Nurgali, K., Jagoe, R. T., & Abalo, R. (2018). Editorial: Adverse effects of cancer chemotherapy: Anything new to improve tolerance and reduce sequelae? Frontiers in Pharmacology, 9, 245. https://doi.org/10.3389/fphar.2018.00245
   PubMed Web of Science ®Google Scholar
• Pekar, L. (2020). Biophysical and biochemical characterisation of a VHH-based IgG-like bi- and trispecific antibody platform. MAbs, 12.
   PubMed Web of Science ®Google Scholar
• Pekar, L., Busch, M., Valldorf, B., Hinz, S. C., Toleikis, L., Krah, S., & Zielonka, S. (2020). Biophysical and biochemical characterization of a VHH-based IgG-like bi-and trispecific antibody platform. MAbs, 12(1), 1812210. https://doi.org/10.1080/19420862.2020.1812210
   Google Scholar
• Perez, P., Hoffman, R. W., Shaw, S., Bluestone, J. A., & Segal, D. M. (1985). Specific targeting of cytotoxic T cells by anti-T3 linked to anti-target cell antibody. Nature, 316(6026), 354–356. https://doi.org/10.1038/316354a0
   PubMed Web of Science ®Google Scholar
• Ramsey, D. C., Scherrer, M. P., Zhou, T., & Wilke, C. O. (2011). The relationship between relative solvent accessibility and evolutionary rate in protein evolution. Genetics, 188(2), 479–488. https://doi.org/10.1534/genetics.111.128025
   PubMed Web of Science ®Google Scholar
• Reichert, J. M., & Dhimolea, E. (2012). The future of antibodies as cancer drugs. Drug Discovery Today, 17(17–18), 954–963. https://doi.org/10.1016/j.drudis.2012.04.006
   PubMed Web of Science ®Google Scholar
• Saini, S. (2023). Exploring the role of framework mutations in enabling breadth of a cross-reactive antibody (CR3022) against the SARS-CoV-2 RBD and its variants of concern. Journal of Biomolecular Structure and Dynamics, 41.
   Web of Science ®Google Scholar
• Saini, S., & Kumar, Y. (2021). Chapter 9 - Bispecific antibodies: A promising entrant in cancer immunotherapy. In Yasha Hasija (Ed.), Translational Biotechnology. Academic Press, 233-266. ISBN 9780128219720. https://doi.org/10.1016/B978-0-12-821972-0.00014-9. (https://www.sciencedirect.com/science/article/pii/B9780128219720000149)
   Google Scholar
• Saini, S., Pareekh, S., & Kumar, Y. (2023). Investigating the structural impact of Omicron RBD mutation on antibody escape and receptor management. Journal of Biomolecular Structure and Dynamics, 1-11. https://doi.org/10.1080/07391102.2023.2222174.
   Google Scholar
• Schirrmacher, V. (2019). From chemotherapy to biological therapy: A review of novel concepts to reduce the side effects of systemic cancer treatment (Review). International Journal of Oncology, 54(2), 407–419. https://doi.org/10.3892/ijo.2018.4661
   PubMed Web of Science ®Google Scholar
• Schmidtke, P., Le Guilloux, V., Maupetit, J., & Tufféry, P. (2010). fpocket: Online tools for protein ensemble pocket detection and tracking. Nucleic Acids Research, 38(Web Server issue), W582–W589. https://doi.org/10.1093/nar/gkq383
   PubMed Web of Science ®Google Scholar
• Schritt, D., Li, S., Rozewicki, J., Katoh, K., Yamashita, K., Volkmuth, W., Cavet, G., & Standley, D. M. (2019). Repertoire builder: High-throughput structural modeling of B and T cell receptors. Molecular Systems Design & Engineering, 4(4), 761–768. https://doi.org/10.1039/C9ME00020H
   Web of Science ®Google Scholar
• Segal, D. M., Weiner, G. J., & Weiner, L. M. (1999). Bispecific antibodies in cancer therapy. Current Opinion in Immunology, 11(5), 558–562. https://doi.org/10.1016/S0952-7915(99)00015-1
   PubMed Web of Science ®Google Scholar
• Sheyi, R., de la Torre, B. G., & Albericio, F. (2022). Linkers: An assurance for controlled delivery of antibody-drug conjugate. Pharmaceutics, 14(2), 396. https://doi.org/10.3390/pharmaceutics14020396
   PubMed Web of Science ®Google Scholar
• Staerz, U. D., Kanagawa, O., & Bevan, M. J. (1985). Hybrid antibodies can target sites for attack by T cells. Nature, 314(6012), 628–631. https://doi.org/10.1038/314628a0
   PubMed Web of Science ®Google Scholar
• Stansfeld, P. J., & Sansom, M. S. P. (2011). Molecular simulation approaches to membrane proteins. Structure (London, England: 1993), 19(11), 1562–1572. https://doi.org/10.1016/j.str.2011.10.002
   PubMed Web of Science ®Google Scholar
• Sudeshna Panda, S., Dey, J., Mahapatra, S. R., Kushwaha, G. S., Misra, N., Suar, M., & Ghosh, M. (2022). Investigation on structural prediction of pectate lyase enzymes from different microbes and comparative docking studies with pectin: The economical waste from food industry. Geomicrobiology Journal, 39(3–5), 294–305. https://doi.org/10.1080/01490451.2021.1992042
   Web of Science ®Google Scholar
• Sumbalova, L., Stourac, J., Martinek, T., Bednar, D., & Damborsky, J. (2018). HotSpot Wizard 3.0: Web server for automated design of mutations and smart libraries based on sequence input information. Nucleic Acids Research, 46(W1), W356–W362. https://doi.org/10.1093/nar/gky417
   PubMed Web of Science ®Google Scholar
• Sun, H., Li, Y., Shen, M., Tian, S., Xu, L., Pan, P., Guan, Y., & Hou, T. (2014). Assessing the performance of MM/PBSA and MM/GBSA methods. 5. Improved docking performance using high solute dielectric constant MM/GBSA and MM/PBSA rescoring. Physical Chemistry Chemical Physics, 16(40), 22035–22045. https://doi.org/10.1039/c4cp03179b
   PubMed Web of Science ®Google Scholar
• Sun, H., Li, Y., Tian, S., Xu, L., & Hou, T. (2014). Assessing the performance of MM/PBSA and MM/GBSA methods. 4. Accuracies of MM/PBSA and MM/GBSA methodologies evaluated by various simulation protocols using PDBbind data set. Physical Chemistry Chemical Physics, 16(31), 16719–16729. https://doi.org/10.1039/c4cp01388c
   PubMed Web of Science ®Google Scholar
• Thakur, A., Huang, M., & Lum, L. G. (2018). Bispecific antibody based therapeutics: Strengths and challenges. Blood Reviews, 32(4), 339–347. https://doi.org/10.1016/j.blre.2018.02.004
   PubMed Web of Science ®Google Scholar
• Tohme, S., Simmons, R. L., & Tsung, A. (2017). Surgery for cancer: A trigger for metastases. Cancer Research, 77(7), 1548–1552. https://doi.org/10.1158/0008-5472.CAN-16-1536
   PubMed Web of Science ®Google Scholar
• Weng, G., Wang, E., Wang, Z., Liu, H., Zhu, F., Li, D., & Hou, T. (2019). HawkDock: A web server to predict and analyse the protein–protein complex based on computational docking and MM/GBSA. Nucleic Acids Research, 47(W1), W322–W330. https://doi.org/10.1093/nar/gkz397
   PubMed Web of Science ®Google Scholar
• Wolf, E., Hofmeister, R., Kufer, P., Schlereth, B., & Baeuerle, P. A. (2005). BiTEs: Bispecific antibody constructs with unique anti-tumor activity. Drug Discovery Today, 10(18), 1237–1244. https://doi.org/10.1016/S1359-6446(05)03554-3
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Wang, N., Raab, R. W., McKown, R. L., Irwin, J. A., Kwon, I., van Kuppevelt, T. H., & Laurie, G. W. (2013). Targeting of heparanase-modified syndecan-1 by prosecretory mitogen lacritin requires conserved core GAGAL plus heparan and chondroitin sulfate as a novel hybrid binding site that enhances selectivity. The Journal of Biological Chemistry, 288(17), 12090–12101. https://doi.org/10.1074/jbc.M112.422717
   PubMed Web of Science ®Google Scholar
• Zhao, R. Y., Wilhelm, S. D., Audette, C., Jones, G., Leece, B. A., Lazar, A. C., Goldmacher, V. S., Singh, R., Kovtun, Y., Widdison, W. C., Lambert, J. M., & Chari, R. V. J. (2011). Synthesis and evaluation of hydrophilic linkers for antibody–maytansinoid conjugates. Journal of Medicinal Chemistry, 54(10), 3606–3623. https://doi.org/10.1021/jm2002958
   PubMed Web of Science ®Google Scholar