References
- Slaga D, Ellerman D, Lombana TN, Vij R, Li J, Hristopoulos M, Clark R, Johnston J, Shelton A, Mai E, et al. Avidity-based binding to Her2 results in selective killing of HER2-overexpressing cells by anti-HER2/CD3. Sci Transl Med. 2018;10:eaat5775. doi:https://doi.org/10.1126/scitranslmed.aat5775.
- Rudnick SI, Lou J, Shaller CC, Tang Y, Klein-Szanto AJ, 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;71:2250–15. doi:https://doi.org/10.1158/0008-5472.CAN-10-2277.
- Harms BD, Kearns JD, Su SV, Kohli N, Nielsen UB, Schoeberl B. Optimizing properties of antireceptor antibodies using kinetic computational models and experiments. Methods Enzymol. 2012;502:67–87.
- Zhou Y, Goenaga AL, Harms BD, Zou H, Lou J, Conrad F, Adams GP, Schoeberl B, Nielsen UB, Marks JD. Impact of intrinsic affinity on functional binding and biological activity of EGFR antibodies. Mol Cancer Ther. 2012;11:1467–76. doi:https://doi.org/10.1158/1535-7163.MCT-11-1038.
- Tannock IF, Rotin D. Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res. 1989;49:4373–84.
- Stubbs M, McSheehy PM, Griffiths JR, Bashford CL. Causes and consequences of tumour acidity and implications for treatment. Mol Med Today. 2000;6:15–19. doi:https://doi.org/10.1016/S1357-4310(99)01615-9.
- Kato Y, Ozawa S, Miyamoto C, Maehata Y, Suzuki A, Maeda T, Baba Y. Acidic extracellular microenvironment and cancer. Cancer Cell Int. 2013;13:89. doi:https://doi.org/10.1186/1475-2867-13-89.
- Zhang X, Lin Y, Gillies RJ. Tumor pH and its measurement. J Nucl Med. 2010;51:1167–70. doi:https://doi.org/10.2967/jnumed.109.068981.
- Damaghi M, Wojtkowiak JW, Gillies RJ. pH sensing and regulation in cancer. Front Physiol. 2013;4:370. doi:https://doi.org/10.3389/fphys.2013.00370.
- Hashim AI, Zhang X, Wojtkowiak JW, Martinez GV, Gillies RJ. Imaging pH and metastasis. NMR Biomed. 2011;24:582–91. doi:https://doi.org/10.1002/nbm.1644.
- Gillies RJ, Raghunand N, Karczmar GS, Bhujwalla ZM. MRI of the tumor microenvironment. J Magn Reson Imaging. 2002;16:430–50. doi:https://doi.org/10.1002/(ISSN)1522-2586.
- Estrella V, Chen T, Lloyd M, Wojtkowiak J, Cornnell HH, Ibrahim-Hashim A, Bailey K, Balagurunathan Y, Rothberg JM, Sloane BF, et al. Acidity generated by the tumor microenvironment drives local invasion. Cancer Res. 2013;73:1524–35. doi:https://doi.org/10.1158/0008-5472.CAN-12-2796.
- Gerweck LE, Seetharaman K. Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer. Cancer Res. 1996;56:1194–98.
- Corbet C, Feron O. Tumour acidosis: from the passenger to the driver’s seat. Nat Rev Cancer. 2017;17:577–93. doi:https://doi.org/10.1038/nrc.2017.77.
- Harguindey S, Reshkin SJ. The new pH-centric anticancer paradigm in oncology and medicine. Semin Cancer Biol. 2017;43:1–4. doi:https://doi.org/10.1016/j.semcancer.2017.02.008.
- Damaghi M, Tafreshi NK, Lloyd MC, Sprung R, Estrella V, Wojtkowiak JW, Morse DL, Koomen JM, Bui MM, Gatenby RA, et al. Chronic acidosis in the tumour microenvironment selects for overexpression of LAMP2 in the plasma membrane. Nat Commun. 2015;6:8752. doi:https://doi.org/10.1038/ncomms9752.
- Rohani N, Hao L, Alexis MS, Joughin BA, Krismer K, Moufarrej MN, Soltis AR, Lauffenburger DA, Yaffe MB, Burge CB, et al. Acidification of tumor at stromal boundaries drives transcriptome alterations associated with aggressive phenotypes. Cancer Res. 2019;79:1952–66. doi:https://doi.org/10.1158/0008-5472.CAN-18-1604.
- Tanokura M. 1H-NMR study on the tautomerism of the imidazole ring of histidine residues. I. Microscopic pK values and molar ratios of tautomers in histidine-containing peptides. Biochim Biophys Acta. 1983;742:576–85. doi:https://doi.org/10.1016/0167-4838(83)90276-5.
- Igawa T, Mimoto F, Hattori K. pH-dependent antigen-binding antibodies as a novel therapeutic modality. Biochim Biophys Acta. 2014;1844:1943–50. doi:https://doi.org/10.1016/j.bbapap.2014.08.003.
- Schroter C, Gunther R, Rhiel L, Becker S, Toleikis L, Doerner A, Becker J, Schonemann A, Nasu D, Neuteboom B, et al. A generic approach to engineer antibody pH-switches using combinatorial histidine scanning libraries and yeast display. MAbs. 2015;7:138–51. doi:https://doi.org/10.4161/19420862.2014.985993.
- Konning D, Zielonka S, Sellmann C, Schroter C, Grzeschik J, Becker S, Kolmar H. Isolation of a pH-sensitive IgNAR variable domain from a yeast-displayed, histidine-doped master library. Mar Biotechnol (NY). 2016;18:161–67. doi:https://doi.org/10.1007/s10126-016-9690-z.
- Tillotson BJ, Goulatis LI, Parenti I, Duxbury E, Shusta EV. Engineering an anti-transferrin receptor scFv for pH-sensitive binding leads to increased intracellular accumulation. PLoS One. 2015;10:e0145820. doi:https://doi.org/10.1371/journal.pone.0145820.
- Igawa T, Ishii S, Tachibana T, Maeda A, Higuchi Y, Shimaoka S, Moriyama C, Watanabe T, Takubo R, Doi Y, et al. Antibody recycling by engineered pH-dependent antigen binding improves the duration of antigen neutralization. Nat Biotechnol. 2010;28:1203–07. doi:https://doi.org/10.1038/nbt.1691.
- Murtaugh ML, Fanning SW, Sharma TM, Terry AM, Horn JR. A combinatorial histidine scanning library approach to engineer highly pH-dependent protein switches. Protein Sci. 2011;20:1619–31. doi:https://doi.org/10.1002/pro.696.
- Chaparro-Riggers J, Liang H, DeVay RM, Bai L, Sutton JE, Chen W, Geng T, Lindquist K, Casas MG, Boustany LM, et al. Increasing serum half-life and extending cholesterol lowering in vivo by engineering antibody with pH-sensitive binding to PCSK9. J Biol Chem. 2012;287:11090–97. doi:https://doi.org/10.1074/jbc.M111.319764.
- Devanaboyina SC, Lynch SM, Ober RJ, Ram S, Kim D, Puig-Canto A, Breen S, Kasturirangan S, Fowler S, Peng L, et al. The effect of pH dependence of antibody-antigen interactions on subcellular trafficking dynamics. MAbs. 2013;5:851–59. doi:https://doi.org/10.4161/mabs.26389.
- Bonvin P, Venet S, Fontaine G, Ravn U, Gueneau F, Kosco-Vilbois M, Proudfoot AE, Fischer N. De novo isolation of antibodies with pH-dependent binding properties. MAbs. 2015;7:294–302. doi:https://doi.org/10.1080/19420862.2015.1006993.
- Sarkar CA, Lowenhaupt K, Horan T, Boone TC, Tidor B, Lauffenburger DA. Rational cytokine design for increased lifetime and enhanced potency using pH-activated “histidine switching”. Nat Biotechnol. 2002;20:908–13. doi:https://doi.org/10.1038/nbt725.
- Heinzelman P, Krais J, Ruben E, Pantazes R. Engineering pH responsive fibronectin domains for biomedical applications. J Biol Eng. 2015;9:6. doi:https://doi.org/10.1186/s13036-015-0004-1.
- Traxlmayr MW, Lobner E, Hasenhindl C, Stadlmayr G, Oostenbrink C, Ruker F, Obinger C. Construction of pH-sensitive Her2-binding IgG1-Fc by directed evolution. Biotechnol J. 2014;9:1013–22. doi:https://doi.org/10.1002/biot.201300483.
- Bailey LJ, Sheehy KM, Hoey RJ, Schaefer ZP, Ura M, Kossiakoff AA. Applications for an engineered protein-G variant with a pH controllable affinity to antibody fragments. J Immunol Methods. 2014;415:24–30. doi:https://doi.org/10.1016/j.jim.2014.10.003.
- Gera N, Hill AB, White DP, Carbonell RG, Rao BM. Design of pH sensitive binding proteins from the hyperthermophilic Sso7d scaffold. PLoS One. 2012;7:e48928. doi:https://doi.org/10.1371/journal.pone.0048928.
- Strauch EM, Fleishman SJ, Baker D. Computational design of a pH-sensitive IgG binding protein. Proc Natl Acad Sci U S A. 2014;111:675–80. doi:https://doi.org/10.1073/pnas.1313605111.
- Tsukamoto M, Watanabe H, Ooishi A, Honda S. Engineered protein A ligands, derived from a histidine-scanning library, facilitate the affinity purification of IgG under mild acidic conditions. J Biol Eng. 2014;8:15. doi:https://doi.org/10.1186/1754-1611-8-15.
- Seijsing J, Lindborg M, Hoiden-Guthenberg I, Bonisch H, Guneriusson E, Frejd FY, Abrahmsen L, Ekblad C, Lofblom J, Uhlen M, et al. An engineered affibody molecule with pH-dependent binding to FcRn mediates extended circulatory half-life of a fusion protein. Proc Natl Acad Sci U S A. 2014;111:17110–15. doi:https://doi.org/10.1073/pnas.1417717111.
- Ghetie V, Popov S, Borvak J, Radu C, Matesoi D, Medesan C, Ober RJ, Ward ES. Increasing the serum persistence of an IgG fragment by random mutagenesis. Nat Biotechnol. 1997;15:637–40. doi:https://doi.org/10.1038/nbt0797-637.
- Lippow SM, Wittrup KD, Tidor B. Computational design of antibody-affinity improvement beyond in vivo maturation. Nat Biotechnol. 2007;25:1171–76. doi:https://doi.org/10.1038/nbt1336.
- Vivcharuk V, Baardsnes J, Deprez C, Sulea T, Jaramillo M, Corbeil CR, Mullick A, Magoon J, Marcil A, Durocher Y, et al. Assisted design of antibody and protein therapeutics (ADAPT). PLoS One. 2017;12:e0181490. doi:https://doi.org/10.1371/journal.pone.0181490.
- Spassov VZ, Yan L. pH-selective mutagenesis of protein-protein interfaces: in silico design of therapeutic antibodies with prolonged half-life. Proteins. 2013;81:704–14. doi:https://doi.org/10.1002/prot.v81.4.
- Bostrom J, Yu SF, Kan D, Appleton BA, Lee CV, Billeci K, Man W, Peale F, Ross S, Wiesmann C, et al. Variants of the antibody herceptin that interact with HER2 and VEGF at the antigen binding site. Science. 2009;323:1610–14. doi:https://doi.org/10.1126/science.1165480.
- Sulea T, Hussack G, Ryan S, Tanha J, Purisima EO. Application of assisted design of antibody and protein therapeutics (ADAPT) improves efficacy of a Clostridium difficile toxin A single-domain antibody. Sci Rep. 2018;8:2260. doi:https://doi.org/10.1038/s41598-018-20599-4.
- DeFazio-Eli L, Strommen K, Dao-Pick T, Parry G, Goodman L, Winslow J. Quantitative assays for the measurement of HER1-HER2 heterodimerization and phosphorylation in cell lines and breast tumors: applications for diagnostics and targeted drug mechanism of action. Breast Cancer Res. 2011;13:R44. doi:https://doi.org/10.1186/bcr2866.
- 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. Am J Pathol. 2013;183:1446–60. doi:https://doi.org/10.1016/j.ajpath.2013.07.015.
- Press MF, Cordon-Cardo C, Slamon DJ. Expression of the HER-2/neu proto-oncogene in normal human adult and fetal tissues. Oncogene. 1990;5:953–62.
- Rodriguez CE, Reidel SI, de Kier Joffe EDB, Jasnis MA, Fiszman GL. Autophagy protects from trastuzumab-induced cytotoxicity in HER2 overexpressing breast tumor spheroids. PLoS One. 2015;10:e0137920. doi:https://doi.org/10.1371/journal.pone.0137920.
- Gangadhara S, Smith C, Barrett-Lee P, Hiscox S. 3D culture of Her2+ breast cancer cells promotes AKT to MAPK switching and a loss of therapeutic response. BMC Cancer. 2016;16:345. doi:https://doi.org/10.1186/s12885-016-2377-z.
- Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol. 2007;7:715–25. doi:https://doi.org/10.1038/nri2155.
- Burmeister WP, Huber AH, Bjorkman PJ. Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature. 1994;372:379–83. doi:https://doi.org/10.1038/372379a0.
- Beck A, Goetsch L, Dumontet C, Corvaia N. Strategies and challenges for the next generation of antibody-drug conjugates. Nat Rev Drug Discov. 2017;16:315–37. doi:https://doi.org/10.1038/nrd.2016.268.
- Masters JC, Nickens DJ, Xuan D, Shazer RL, Amantea M. Clinical toxicity of antibody drug conjugates: A meta-analysis of payloads. Invest New Drugs. 2018;36:121–35. doi:https://doi.org/10.1007/s10637-017-0520-6.
- Bartholoma MD. Radioimmunotherapy of solid tumors: approaches on the verge of clinical application. J Labelled Comp Radiopharm. 2018;61:715–26. doi:https://doi.org/10.1002/jlcr.3619.
- Brinkmann U, KontermannRE. The making of bispecific antibodies. MAbs. 2017;9:182–212. doi:https://doi.org/10.1080/19420862.2016.1268307.
- Dotti G, Gottschalk S, Savoldo B, Brenner MK. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev. 2014;257:107–26. doi:https://doi.org/10.1111/imr.2013.257.issue-1.
- Krivov GG, Shapovalov MV, Dunbrack RL Jr. Improved prediction of protein side-chain conformations with SCWRL4. Proteins. 2009;77:778–95. doi:https://doi.org/10.1002/prot.v77:4.
- Naim M, Bhat S, Rankin KN, Dennis S, Chowdhury SF, Siddiqi I, Drabik P, Sulea T, Bayly CI, Jakalian A, et al. Solvated interaction energy (SIE) for scoring protein-ligand binding affinities. 1. Exploring the parameter space. J Chem Inf Model. 2007;47:122–33. doi:https://doi.org/10.1021/ci600406v.
- Sulea T, Purisima EO. The solvated interaction energy method for scoring binding affinities. Methods Mol Biol. 2012;819:295–303.
- Guerois R, Nielsen JE, Serrano L. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol. 2002;320:369–87. doi:https://doi.org/10.1016/S0022-2836(02)00442-4.
- Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, Serrano L. The FoldX web server: an online force field. Nucl Acids Res. 2005;33:W382–388. doi:https://doi.org/10.1093/nar/gki387.
- O’Conchuir S, Barlow KA, Pache RA, Ollikainen N, Kundert K, O’Meara MJ, Smith CA, Kortemme T. A web resource for standardized benchmark datasets, metrics, and Rosetta protocols for macromolecular modeling and design. PLoS One. 2015;10:e0130433. doi:https://doi.org/10.1371/journal.pone.0130433.
- Rohl CA, Strauss CE, Misura KM, Baker D. Protein structure prediction using Rosetta. Methods Enzymol. 2004;383:66–93.
- Sulea T, Vivcharuk V, Corbeil CR, Deprez C, Purisima EO. Assessment of solvated interaction energy function for ranking antibody-antigen binding affinities. J Chem Inf Model. 2016;56:1292–303. doi:https://doi.org/10.1021/acs.jcim.6b00043.
- Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J. 2000;78:1606–19. doi:https://doi.org/10.1016/S0006-3495(00)76713-0.
- Brautigam CA. Calculations and publication-quality illustrations for analytical ultracentrifugation data. Methods Enzymol. 2015;562:109–33.