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Simultaneous affinity maturation and developability enhancement using natural liability-free CDRs

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Article: 2115200 | Received 03 Mar 2022, Accepted 16 Aug 2022, Published online: 06 Sep 2022

References

  • Gram H, Marconi LA, Barbas CFs3rd, Collet TA, Lerner RA, Kang AS. In vitro selection and affinity maturation of antibodies from a naive combinatorial immunoglobulin library. Proc Natl Acad Sci U S A. 1992;89(8):1–14. doi:10.1073/pnas.89.8.3576.
  • Daugherty PS, Chen G, Iverson BL, Georgiou G. Quantitative analysis of the effect of the mutation frequency on the affinity maturation of single chain Fv antibodies. Proc Natl Acad Sci U S A. 2000;97:2029–34. doi:10.1073/pnas.030527597.
  • Lou J, Geren I, Garcia-Rodriguez C, Forsyth CM, Wen W, Knopp K, Brown J, Smith T, Smith LA, Marks JD, et al. Affinity maturation of human botulinum neurotoxin antibodies by light chain shuffling via yeast mating. Protein Eng Des Sel. 2010;23:311–19. doi:10.1093/protein/gzq001.
  • Park SG, Lee JS, Je EY, Kim IJ, Chung JH, Choi IH. Affinity maturation of natural antibody using a chain shuffling technique and the expression of recombinant antibodies in Escherichia coli. Biochem Biophys Res Commun. 2000;275:553–57. doi:10.1006/bbrc.2000.3336.
  • Marks JD, Griffiths AD, Malmqvist M, Clackson TP, Bye JM, Winter G. By-passing immunization: building high affinity human antibodies by chain shuffling. Biotechnology (N Y). 1992;10:779–83. doi:10.1038/nbt0792-779.
  • Tiller KE, Chowdhury R, Li T, Ludwig SD, Sen S, Maranas CD, Tessier PM. Facile affinity maturation of antibody variable domains using natural diversity mutagenesis. Front Immunol. 2017;8:986. doi:10.3389/fimmu.2017.00986.
  • Barderas R, Desmet J, Timmerman P, Meloen R, Casal JI. Affinity maturation of antibodies assisted by in silico modeling. Proc Natl Acad Sci U S A. 2008;105:9029–34. doi:10.1073/pnas.0801221105.
  • Rajpal A, Beyaz N, Haber L, Cappuccilli G, Yee H, Bhatt RR, et al. A general method for greatly improving the affinity of antibodies by using combinatorial libraries. Proc Natl Acad Sci U S A. 2005;102:8466–71. doi:10.1073/pnas.0503543102.
  • Schier R, Bye J, Apell G, McCall A, Adams GP, Malmqvist M, Weiner LM, Marks JD. Isolation of high-affinity monomeric human anti-c-erbB-2 single chain Fv using affinity-driven selection. J Mol Biol. 1996;255:28–43. doi:10.1006/jmbi.1996.0004.
  • Schier R, Marks JD. Efficient in vitro affinity maturation of phage antibodies using BIAcore guided selections. Hum Antibodies Hybridomas. 1996;7:97–105. doi:10.3233/HAB-1996-7302.
  • Yang WP, Green K, Pinz-Sweeney S, Briones AT, Burton DR, Barbas CF. 3rd. CDR walking mutagenesis for the affinity maturation of a potent human anti-HIV-1 antibody into the picomolar range. J Mol Biol. 1995;254:392–403. doi:10.1006/jmbi.1995.0626.
  • Boder ET, Midelfort KS, Wittrup KD. Directed evolution of antibody fragments with monovalent femtomolar antigen-binding affinity. Proc Natl Acad Sci USA. 2000;97:10701–05. doi:10.1073/pnas.170297297.
  • Low NM, Holliger PH, Winter G. Mimicking somatic hypermutation: affinity maturation of antibodies displayed on bacteriophage using a bacterial mutator strain. J Mol Biol. 1996;260:359–68. doi:10.1006/jmbi.1996.0406.
  • Lamdan H, Gavilondo JV, Munoz Y, Pupo A, Huerta V, Musacchio A, Pérez L, Ayala M, Rojas G, Balint RF, et al. Affinity maturation and fine functional mapping of an antibody fragment against a novel neutralizing epitope on human vascular endothelial growth factor. Mol Biosyst. 2013;9:2097–106. doi:10.1039/c3mb70136k.
  • Schier R, McCall A, Adams GP, Marshall KW, Merritt H, Yim M, Crawford RS, Weiner LM, Marks C, Marks JD, et al. Isolation of picomolar affinity anti-c-erbB-2 single-chain Fv by molecular evolution of the complementarity determining regions in the center of the antibody binding site. J Mol Biol. 1996;263:551–67. doi:10.1006/jmbi.1996.0598.
  • Chan DTY, Jenkinson L, Haynes SW, Austin M, Diamandakis A, Burschowsky D, Seewooruthun C, Addyman A, Fiedler S, Ryman S, et al. Extensive sequence and structural evolution of Arginase 2 inhibitory antibodies enabled by an unbiased approach to affinity maturation. Proc Natl Acad Sci U S A. 2020;117:16949–60. doi:10.1073/pnas.1919565117.
  • Hanes J, Jermutus L, Weber-Bornhauser S, Bosshard HR, Pluckthun A. Ribosome display efficiently selects and evolves high-affinity antibodies in vitro from immune libraries. Proc Natl Acad Sci U S A. 1998;95:14130–35. doi:10.1073/pnas.95.24.14130.
  • Hanes J, Schaffitzel C, Knappik A, Pluckthun A. Picomolar affinity antibodies from a fully synthetic naive library selected and evolved by ribosome display. Nat Biotechnol. 2000;18:1287–92. doi:10.1038/82407.
  • Ohlin M, Owman H, Mach M, Borrebaeck CAK. Light chain shuffling of a high affinity antibody results in a drift in epitope recognition. Mol Immunol. 1996;33:47–56. doi:10.1016/0161-5890(95)00123-9.
  • Julian MC, Lee CC, Tiller KE, Rabia LA, Day EK, Schick AJ, et al. 3rd Co-evolution of affinity and stability of grafted amyloid-motif domain antibodies. Protein Eng Des Sel. 2015;28:339–50. doi:10.1093/protein/gzv050.
  • Chou K-C, Némethy G, Pottle M, Scheraga HA. Energy of stabilization of the right-handed βαβ crossover in proteins. J Mol Biol. 1989;205:241–49. doi:10.1016/0022-2836(89)90378-1.
  • Du Q, Wei D, Chou K-C. Correlations of amino acids in proteins. Peptides. 2003;24:1863–69. doi:10.1016/j.peptides.2003.10.012.
  • Teixeira AAR, Erasmus MF, D’Angelo S, Naranjo L, Ferrara F, Leal-Lopes C, Durrant O, Galmiche C, Morelli A, Scott-Tucker A, et al. Drug-like antibodies with high affinity, diversity and developability directly from next-generation antibody libraries. MAbs. 2021;13:1980942. doi:10.1080/19420862.2021.1980942.
  • Ferrara F, Erasmus MF, D’Angelo S, Leal-Lopes C, Teixeira AA, Choudhary A, et al. A pandemic-enabled comparison of discovery platforms demonstrates a naïve antibody library can match the best immune-sourced antibodies. Nat Commun. pp.13. 2022. doi:10.1038/s41467-021-27594-w
  • Erasmus MF, D’Angelo S, Ferrara F, Naranjo L, Teixeira AA, Buonpane R, et al. A single donor is sufficient to produce a highly functional in vitro antibody library. Commun Biol. pp.4. 2021. doi:10.1038/s42003-020-01536-6
  • Sydow JF, Lipsmeier F, Larraillet V, Hilger M, Mautz B, Molhoj M, et al. Structure-based prediction of asparagine and aspartate degradation sites in antibody variable regions. PLoS One. 2014;9:e100736. doi:10.1371/journal.pone.0100736.
  • Kelly RL, Le D, Zhao J, Wittrup KD. Reduction of nonspecificity motifs in synthetic antibody libraries. J Mol Biol. 2018;430:119–30. doi:10.1016/j.jmb.2017.11.008.
  • Kumar S, Singh SK. Developability of Biotherapeutics: computational approaches. Florida (US): CRC Press; 2016.
  • Gavel Y, von Heijne G. Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng. 1990;3:433–42. doi:10.1093/protein/3.5.433.
  • Bethea D, Wu SJ, Luo J, Hyun L, Lacy ER, Teplyakov A, Jacobs SA, O’Neil KT, Gilliland GL, Feng Y, et al. Mechanisms of self-association of a human monoclonal antibody CNTO607. Protein Eng Des Sel. 2012;25:531–37. doi:10.1093/protein/gzs047.
  • Wu SJ, Luo J, O’Neil KT, Kang J, Lacy ER, Canziani G, Baker A, Huang M, Tang QM, Raju TS, et al. Structure-based engineering of a monoclonal antibody for improved solubility. Protein Eng Des Sel. 2010;23:643–51. doi:10.1093/protein/gzq037.
  • Vlasak J, Ionescu R. Fragmentation of monoclonal antibodies. MAbs. 2011;3:253–63. doi:10.4161/mabs.3.3.15608.
  • Boder ET, Wittrup KD. Optimal screening of surface-displayed polypeptide libraries. Biotechnol Prog. 1998;14:55–62. doi:10.1021/bp970144q.
  • VanAntwerp JJ, Wittrup KD. Fine affinity discrimination by yeast surface display and flow cytometry. Biotechnol Prog. 2000;16:31–37. doi:10.1021/bp990133s.
  • Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14:1188–90. doi:10.1101/gr.849004.
  • Lundström I. Real-time biospecific interaction analysis. Biosens Bioelectron. 1994;9:725–36. doi:10.1016/0956-5663(94)80071-5.
  • Kang AS, Jones TM, Burton DR. Antibody redesign by chain shuffling from random combinatorial immunoglobulin libraries. Proc Natl Acad Sci U S A. 1991;88:11120–23. doi:10.1073/pnas.88.24.11120.
  • Hawkins RE, Russell SJ, Winter G. Selection of phage antibodies by binding affinity. Mimicking affinity maturation. J Mol Biol. 1992;226:889–96. doi:10.1016/0022-2836(92)90639-2.
  • Cannon DA, Shan L, Du Q, Shirinian L, Rickert KW, Rosenthal KL, Korade M, van Vlerken-Ysla LE, Buchanan A, Vaughan TJ, et al. Experimentally guided computational antibody affinity maturation with de novo docking, modelling and rational design. PLoS Comput Biol. 2019;15:e1006980. doi:10.1371/journal.pcbi.1006980.
  • Hu D, Hu S, Wan W, Xu M, Du R, Zhao W, Gao X, Liu J, Liu H, Hong J, et al. Effective optimization of antibody affinity by phage display integrated with high-throughput DNA synthesis and sequencing technologies. PLoS One. 2015;10:e0129125. doi:10.1371/journal.pone.0129125.
  • Frigotto L, Smith M, Brankin C, Sedani A, Cooper S, Kanwar N, Evans D, Svobodova S, Baar C, Glanville J, et al. Codon-Precise, synthetic, antibody fragment libraries built using automated hexamer codon additions and validated through next generation sequencing. Antibodies. 2015;4:88–102. doi:10.3390/antib4020088.
  • Thakkar S, Nanaware-Kharade N, Celikel R, Peterson EC, Varughese KI. Affinity improvement of a therapeutic antibody to methamphetamine and amphetamine through structure-based antibody engineering. Sci Rep. 2014;4:3673. doi:10.1038/srep03673.
  • Votsmeier C, Plittersdorf H, Hesse O, Scheidig A, Strerath M, Gritzan U, Pellengahr K, Scholz P, Eicker A, Myszka D, et al. Femtomolar Fab binding affinities to a protein target by alternative CDR residue co-optimization strategies without phage or cell surface display. MAbs. 2012;4:341–48. doi:10.4161/mabs.19981.
  • Gonzalez-Munoz A, Bokma E, O’Shea D, Minton K, Strain M, Vousden K, et al. Tailored amino acid diversity for the evolution of antibody affinity. MAbs. 2012;4:4. doi:10.4161/mabs.4.1.18821.
  • Yang GH, Yoon SO, Jang MH, Hong HJ. Affinity maturation of an anti-hepatitis B virus PreS1 humanized antibody by phage display. J Microbiol. 2007;45:528–33.
  • Lippow SM, Wittrup KD, Tidor B. Computational design of antibody-affinity improvement beyond in vivo maturation. Nat Biotechnol. 2007;25:1171–76. doi:10.1038/nbt1336.
  • Garcia-Rodriguez C, Levy R, Arndt JW, Forsyth CM, Razai A, Lou J, Geren I, Stevens RC, Marks JD. Molecular evolution of antibody cross-reactivity for two subtypes of type A botulinum neurotoxin. Nat Biotechnol. 2007;25:107–16. doi:10.1038/nbt1269.
  • Lu D, Shen J, Vil MD, Zhang H, Jimenez X, Bohlen P, Witte L, Zhu Z. Tailoring in vitro selection for a picomolar affinity human antibody directed against vascular endothelial growth factor receptor 2 for enhanced neutralizing activity. J Biol Chem. 2003;278:43496–507. doi:10.1074/jbc.M307742200.
  • Rader C, Popkov M, Neves JA, Barbas CF. 3rd. Integrin alpha(v)beta3 targeted therapy for Kaposi’s sarcoma with an in vitro evolved antibody. FASEB J. 2002;16:2000–02. doi:10.1096/fj.02-0281fje.
  • Wu H, Beuerlein G, Nie Y, Smith H, Lee BA, Hensler M, Huse WD, Watkins JD. Stepwise in vitro affinity maturation of Vitaxin, an α v β 3 -specific humanized mAb. Proc Natl Acad Sci U S A. 1998;95:6037–42. doi:10.1073/pnas.95.11.6037.
  • Hemminki A, Niemi S, Hoffren AM, Hakalahti L, Soderlund H, Takkinen K. Specificity improvement of a recombinant anti-testosterone Fab fragment by CDRIII mutagenesis and phage display selection. Protein Eng. 1998;11:311–19. doi:10.1093/protein/11.4.311.
  • Thompson J, Pope T, Tung JS, Chan C, Hollis G, Mark G, et al. Affinity maturation of a high-affinity human monoclonal antibody against the third hypervariable loop of human immunodeficiency virus: use of phage display to improve affinity and broaden strain reactivity. J Mol Biol. 1996;256:77–88. doi:10.1006/jmbi.1996.0069.
  • Jackson JR, Sathe G, Rosenberg M, Sweet R. In vitro antibody maturation. Improvement of a high affinity, neutralizing antibody against IL-1 beta. J Immunol. 1995;154:3310–19.
  • Julian MC, Li L, Garde S, Wilen R, Tessier PM. Efficient affinity maturation of antibody variable domains requires co-selection of compensatory mutations to maintain thermodynamic stability. Sci Rep. 2017;7:45259. doi:10.1038/srep45259.
  • Kosuri S, Church GM. Large-scale de novo DNA synthesis: technologies and applications. Nat Methods. 2014;11:499–507. doi:10.1038/nmeth.2918.
  • Kosuri S, Eroshenko N, Leproust EM, Super M, Way J, Li JB, Church GM. Scalable gene synthesis by selective amplification of DNA pools from high-fidelity microchips. Nat Biotechnol. 2010;28:1295–99. doi:10.1038/nbt.1716.
  • 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;114:944–49. doi:10.1073/pnas.1616408114.
  • Tiller KE, Li L, Kumar S, Julian MC, Garde S, Tessier PM. Arginine mutations in antibody complementarity-determining regions display context-dependent affinity/specificity trade-offs. J Biol Chem. 2017;292:16638–52. doi:10.1074/jbc.M117.783837.
  • Pepinsky RB, Silvian L, Berkowitz SA, Farrington G, Lugovskoy A, Walus L, Eldredge J, Capili A, Mi S, Graff C, et al. Improving the solubility of anti-LINGO-1 monoclonal antibody Li33 by isotype switching and targeted mutagenesis. Protein Sci. 2010;19:954–66. doi:10.1002/pro.372.
  • Rosenfeld R, Alcalay R, Mechaly A, Lapidoth G, Epstein E, Kronman C, J Fleishman S, Mazor O. Improved antibody-based ricin neutralization by affinity maturation is correlated with slower off-rate values. Protein Eng Des Sel. 2017;30:611–17. doi:10.1093/protein/gzx028.
  • Hurlburt NK, Seydoux E, Wan YH, Edara SsVV, AB, Feng J, Feng J, Suthar MS, McGuire AT, Stamatatos L, Pancera M, et al. Structural basis for potent neutralization of SARS-CoV-2 and role of antibody affinity maturation. Nat Commun. 2020;11:5413. doi:10.1038/s41467-020-19231-9.
  • Akbar R, Robert PA, Pavlovic M, Jeliazkov JR, Snapkov I, Slabodkin A, Weber CR, Scheffer L, Miho E, Haff IH, et al. A compact vocabulary of paratope-epitope interactions enables predictability of antibody-antigen binding. Cell Rep. 2021;34:108856. doi:10.1016/j.celrep.2021.108856.
  • Xu JL, Davis MM. Diversity in the CDR3 region of V(H) is sufficient for most antibody specificities. Immunity. 2000;13:37–45. doi:10.1016/S1074-7613(00)00006-6.
  • Hemminki A, Niemi S, Hautoniemi L, Söderlund H, Takkinen K. Fine tuning of an anti-testosterone antibody binding site by stepwise optimisation of the CDRs. Immunotechnology. 1998;4:59–69. doi:10.1016/S1380-2933(98)00002-5.
  • Traxlmayr MW, Shusta EV. Directed evolution of protein thermal stability using yeast surface display. Methods Mol Biol. 2017;1575:45–65.
  • Darling RJ, Brault PA. Kinetic exclusion assay technology: characterization of molecular interactions. Assay Drug Dev Technol. 2004;2:647–57. doi:10.1089/adt.2004.2.647.
  • Kovaltsuk A, Leem J, Kelm S, Snowden J, Deane CM, Krawczyk K. Observed antibody space: a resource for data mining next-generation sequencing of antibody repertoires. J Immunol. 2018;201:2502–09. doi:10.4049/jimmunol.1800708.
  • Ye J, Ma N, Madden TL, Ostell JM. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 2013;41:W34–40. doi:10.1093/nar/gkt382.
  • Giudicelli V, Brochet X, Lefranc MP. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb Protoc. 2011;2011:695–715. doi:10.1101/pdb.prot5633.
  • Kabat EA, Wu TT, Bilofsky H. Evidence supporting somatic assembly of the DNA segments (minigenes), coding for the framework, and complementarity-determining segments of immunoglobulin variable regions. J Exp Med. 1979;149:1299–313. doi:10.1084/jem.149.6.1299.
  • Benatuil L, Perez JM, Belk J, Hsieh CM. An improved yeast transformation method for the generation of very large human antibody libraries. Protein Eng Des Sel. 2010;23:155–59. doi:10.1093/protein/gzq002.
  • Ferrara F, Naranjo LA, Kumar S, Gaiotto T, Mukundan H, Swanson B, et al. Using phage and yeast display to select hundreds of monoclonal antibodies: application to antigen 85, a tuberculosis biomarker. PLoS One. 2012;7:e49535. doi:10.1371/journal.pone.0049535.