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Antibody humanization by structure-based computational protein design

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Pages 1045-1057 | Received 19 Mar 2015, Accepted 20 Jul 2015, Published online: 11 Sep 2015

References

  • Brooks M. Top 100 selling drugs of 2013. Medscape Medical News, 2014. Available at http://www.medscape.com/viewarticle/820011
  • Carter PJ. Potent antibody therapeutics by design. Nat Rev Immunol 2006; 6:343-57; PMID:16622479; http://dx.doi.org/10.1038/nri1837
  • Jones PT, Dear PH, Foote J, Neuberger MS, Winter G. Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 1986; 321:522–5; PMID:3713831
  • Roguska MA, Pedersen JT, Keddy CA, Henry AH, Searle SJ, Lambert JM, Goldmacher VS, Blättler WA, Rees AR, Guild BC. Humanization of murine monoclonal antibodies through variable domain resurfacing. Proc Natl Acad Sci 1994; 91:969-73; PMID:8302875
  • Gonzales NR, Padlan EA, De Pascalis R, Schuck P, Schlom J, Kashmiri SV. SDR grafting of a murine antibody using multiple human germline templates to minimize its immunogenicity. Mol Immunol 2004; 41:863-72; PMID:15261458; http://dx.doi.org/10.1016/j.molimm.2004.03.041
  • Khee Hwang WY, Almagro JC, Buss TN, Tan P, Foote J. Use of human germline genes in a CDR homology-based approach to antibody humanization. Methods 2005; 36:35-42; PMID:15848073; http://dx.doi.org/10.1016/j.ymeth.2005.01.004
  • Lazar GA, Desjarlais JR, Jacinto J, Karki S, Hammond PW. A molecular immunology approach to antibody humanization and functional optimization. Mol Immunol 2007; 44:1986-98; PMID:17079018; http://dx.doi.org/10.1016/j.molimm.2006.09.029
  • Baca M, Presta LG, O'Connor SJ, Wells JA. Antibody humanization using monovalent phage display. J Biol Chem 1997; 272:10678-84; PMID:9099717; http://dx.doi.org/10.1074/jbc.272.16.10678
  • Dall'Acqua WF, Damschroder MM, Zhang J, Woods RM, Widjaja L, Yu J, Wu H. Antibody humanization by framework shuffling. Methods 2005; 36:43-60; PMID:15848074; http://dx.doi.org/10.1016/j.ymeth.2005.01.005
  • Dennis MS. CDR repair: A novel approach to antibody humanization. In Shire SJ, Gombotz W, Bechtold-Peters K, Andya J (Eds.), Current Trends in Monoclonal Antibody Development and Manufacturing. New York: Springer-Verlag, 2010; 9-28.
  • Osbourn J, Groves M, Vaughan T. From rodent reagents to human therapeutics using antibody guided selection. Methods 2005; 36:61-8; PMID:15848075; http://dx.doi.org/10.1016/j.ymeth.2005.01.006
  • Hwang WYK, Foote J. Immunogenicity of engineered antibodies. Methods 2005; 36:3-10; PMID:15848070; http://dx.doi.org/10.1016/j.ymeth.2005.01.001
  • McCafferty J, Griffiths AD, Winter G, Chiswell DJ. Phage antibodies: filamentous phage displaying antibody variable domains. Nat 1990; 348:552-4; PMID:2247164; http://dx.doi.org/10.1038/348552a0
  • Feldhaus MJ, Siegel RW, Opresko LK, Coleman JR, Feldhaus JMW, Yeung YA, Cochran JR, Heinzelman P, Colby D, Swers J, et al. Flow-cytometric isolation of human antibodies from a nonimmune Saccharomyces cerevisiae surface display library. Nat Biotechnol 2003; 21:163-70; PMID:12536217; http://dx.doi.org/10.1038/nbt785
  • Lee E-C, Liang Q, Ali H, Bayliss L, Beasley A, Bloomfield-Gerdes T, Bonoli L, Brown R, Campbell J, Carpenter A, et al. Complete humanization of the mouse immunoglobulin loci enables efficient therapeutic antibody discovery. Nat Biotechnol 2014; 32:356-63; PMID:24633243; http://dx.doi.org/10.1038/nbt.2825
  • Lonberg N. In Chernajovsky Y, Nissim A (Eds.), Human monoclonal antibodies from transgenic mice. Therapeutic Antibodies. Berlin: Springer-Verlag; 2008; 69-97.
  • Duvall M, Bradley N, Fiorini RN. A novel platform to produce human monoclonal antibodies: The next generation of therapeutic human monoclonal antibodies discovery. mAbs 2011; 3(2):203-8; PMID:21285537
  • Li J, Sai T, Berger M, Chao Q, Davidson D, Deshmukh G, Drozdowski B, Ebel W, Harley S, Henry M, et al. Human antibodies for immunotherapy development generated via a human B cell hybridoma technology. Proc Natl Acad Sci U S A 2006; 103:3557-62; PMID:16505368; http://dx.doi.org/10.1073/pnas.0511285103
  • Clark M. Antibody humanization: a case of the ‘Emperor's new clothes’? Immunology Today 2000; 21:397-402; PMID:10916143; http://dx.doi.org/10.1016/S0167-5699(00)01680-7
  • Hansel TT, Kropshofer H, Singer T, Mitchell JA, George AJ. The safety and side effects of monoclonal antibodies. Nat Rev Drug Dis 2010; 9:325-38; PMID:20305665; http://dx.doi.org/10.1038/nrd3003
  • Almagro JC, Fransson J. Humanization of antibodies. Front Biosci 2008; 13:1619-33; PMID:17981654
  • Nelson AL, Dhimolea E, Reichert JM. Development trends for human monoclonal antibody therapeutics. Nat Rev Drug Dis 2010; 9:767-74; PMID:20811384; http://dx.doi.org/10.1038/nrd3229
  • Lu Z-J, Deng S-J, Huang D-G, He Y, Lei M, Zhou L, Jin P. Frontier of therapeutic antibody discovery: the challenges and how to face them. World J Biol Chem 2012; 3:187; PMID:23275803; http://dx.doi.org/10.4331/wjbc.v3.i12.187
  • Bogen B, Ruffini P. Review: to what extent are T cells tolerant to immunoglobulin variable regions? Scandinavian J Immunol 2009; 70:526-30; PMID:19906193; http://dx.doi.org/10.1111/j.1365-3083.2009.02340.x
  • Chames P, Van Regenmortel M, Weiss E, Baty D. Therapeutic antibodies: successes, limitations and hopes for the future. Br J Pharmacol 2009; 157:220-33; PMID:19459844; http://dx.doi.org/10.1111/j.1476-5381.2009.00190.x
  • Pavlinkova G, Colcher D, Booth BJ, Goel A, Wittel UA, Batra SK. Effects of humanization and gene shuffling on immunogenicity and antigen binding of anti-tag-72 single-chain Fvs. Inter J Cancer 2001; 94:717-26; PMID:11745468; http://dx.doi.org/10.1002/ijc.1523
  • Jawa V, Cousens LP, Awwad M, Wakshull E, Kropshofer H, De Groot AS. T-cell dependent immunogenicity of protein therapeutics: preclinical assessment and mitigation. Clin Immunol 2013; 149:534-55; PMID:24263283; http://dx.doi.org/10.1016/j.clim.2013.09.006
  • Marcatili P, Rosi A, Tramontano A. PIGS: automatic prediction of antibody structures. Bioinformatics 2008; 24:1953-4; PMID:18641403; http://dx.doi.org/10.1093/bioinformatics/btn341
  • Shirai H, Ikeda K, Yamashita K, Tsuchiya Y, Sarmiento J, Liang S, Morokata T, Mizuguchi K, Higo J, Standley DM, et al. High-resolution modeling of antibody structures by a combination of bioinformatics, expert knowledge, and molecular simulations. Proteins 2014; 82:1624-35; PMID:24756852
  • Sivasubramanian A, Sircar A, Chaudhury S, Gray JJ. Toward high-resolution homology modeling of antibody Fv regions and application to antibody-antigen docking. Proteins 2009; 74:497-514; PMID:19062174; http://dx.doi.org/10.1002/prot.22309
  • Zhu K, Day T, Warshaviak D, Murrett C, Friesner R, Pearlman D. Antibody structure determination using a combination of homology modeling, energy-based refinement, and loop prediction. Proteins 2014; 82:1646-55; PMID:24619874
  • Choi Y, Deane CM. Predicting antibody complementarity determining region structures without classification. Mol Biosys 2011; 7:3327-34; PMID:22011953; http://dx.doi.org/10.1039/c1mb05223c
  • North B, Lehmann A, Dunbrack Jr RL. A new clustering of antibody CDR loop conformations. J Mol Biol 2011; 406:228-56; PMID:21035459; http://dx.doi.org/10.1016/j.jmb.2010.10.030
  • Weitzner BD, Kuroda D, Marze N, Xu J, Gray JJ. Blind prediction performance of RosettaAntibody 3.0: Grafting, relaxation, kinematic loop modeling, and full CDR optimization. Proteins 2014; 82:1611-23; PMID:24519881; http://dx.doi.org/10.1002/prot.24534
  • Damborsky J, Brezovsky J. Computational tools for designing and engineering enzymes. Curr Opin Chem Biol 2014; 19:8-16; PMID:24780274; http://dx.doi.org/10.1016/j.cbpa.2013.12.003
  • Kazlauskas RJ, Bornscheuer UT. Finding better protein engineering strategies. Nat Chem Biol 2009; 5:526-9; PMID:19620988; http://dx.doi.org/10.1038/nchembio0809-526
  • Kries H, Blomberg R, Hilvert D. De novo enzymes by computational design. Curr Opin Chem Biol 2013; 17:221-8; PMID:23498973; http://dx.doi.org/10.1016/j.cbpa.2013.02.012
  • Dunbar J, Fuchs A, Shi J, Deane C. ABangle: characterising the VH-VL orientation in antibodies. Protein Engineering Design and Selection 2013; 26:611-20; http://dx.doi.org/10.1093/protein/gzt020
  • Kunik V, Ashkenazi S, Ofran Y. Paratome: an online tool for systematic identification of antigen-binding regions in antibodies based on sequence or structure. Nucl Acids Res 2012; 40:W521-W4; PMID:22675071; http://dx.doi.org/10.1093/nar/gks480
  • Olimpieri PP, Chailyan A, Tramontano A, Marcatili P. Prediction of site-specific interactions in antibody-antigen complexes: the proABC method and server. Bioinformatics 2013; 29:2285-91; PMID:23803466
  • Olimpieri PP, Marcatili P, Tramontano A. Tabhu: Tools for antibody humanization. Bioinformatics 2015; 31:434-5; PMID:25304777
  • Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TE, DeBolt S, Ferguson D, Seibel G, Kollman P. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun 1995; 91:1-41; http://dx.doi.org/10.1016/0010-4655(95)00041-D
  • Parker AS, Choi Y, Griswold KE, Bailey-Kellogg C. Structure-guided deimmunization of therapeutic proteins. J Comput Biol 2013; 20:152-65; PMID:23384000; http://dx.doi.org/10.1089/cmb.2012.0251
  • Zhang T, Wu M-R, Sentman CL. An NKp30-based chimeric antigen receptor promotes T cell effector functions and antitumor efficacy in vivo. J Immunol 2012; 189:2290-9; PMID:22851709; http://dx.doi.org/10.4049/jimmunol.1103495
  • Rammensee H-G, Friede T, Stevanović S. MHC ligands and peptide motifs: first listing. Immunogenetics 1995; 41:178-228; PMID:7890324; http://dx.doi.org/10.1007/BF00172063
  • Ehrenmann F, Lefranc M-P. IMGT/3Dstructure-DB: querying the IMGT database for 3D structures in immunology and immunoinformatics (IG or antibodies, TR, MH, RPI, and FPIA). Cold Spring Harbor Protocols 2011; 2011:750-61 pdb-prot5637
  • Poiron C, Wu Y, Ginestoux C, Ehrenmann F, Patrice D, Lefranc M-P. IMGT/mAb-DB: the IMGT database for therapeutic monoclonal antibodies. JOBIM 2010; 13
  • Giudicelli V, Chaume D, Lefranc M-P. IMGT/V-QUEST, an integrated software program for immunoglobulin and T cell receptor V-J and V-D-J rearrangement analysis. Nucl Acids Res 2004; 32:W435-W40; PMID:15215425; http://dx.doi.org/10.1093/nar/gkh412
  • Retter I, Althaus HH, Munch R, Muller W. VBASE2, an integrative V gene database. Nucl Acids Res 2005; 33:D671-D4; PMID:15608286; http://dx.doi.org/10.1093/nar/gki088
  • Tomlinson I, Williams S, Corbett S, Cox J, Winter G. V BASE sequence directory. Cambridge, UK: MRC Centre for protein engineering; 1996.
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403-10; PMID:2231712; http://dx.doi.org/10.1016/S0022-2836(05)80360-2
  • Narayanan A, Sellers BD, Jacobson MP. Energy-based analysis and prediction of the orientation between light-and heavy-chain antibody variable domains. J Mol Biol 2009; 388:941-53; PMID:19324053; http://dx.doi.org/10.1016/j.jmb.2009.03.043
  • Foote J, Winter G. Antibody framework residues affecting the conformation of the hypervariable loops. J Mol Biol 1992; 224:487-99; PMID:1560463; http://dx.doi.org/10.1016/0022-2836(92)91010-M
  • Safdari Y, Farajnia S, Asgharzadeh M, Khalili M. Antibody humanization methods-a review and update. Biotechnol Genet Eng Rev 2013; 29:175-86; PMID:24568279; http://dx.doi.org/10.1080/02648725.2013.801235
  • Abhinandan K, Martin AC. Analyzing the “degree of humanness” of antibody sequences. J Mol Biol 2007; 369:852-62; PMID:17442342; http://dx.doi.org/10.1016/j.jmb.2007.02.100
  • Gao SH, Huang K, Tu H, Adler AS. Monoclonal antibody humanness score and its applications. BMC Biotechnol 2013; 13:55; PMID:23826749; http://dx.doi.org/10.1186/1472-6750-13-55
  • Thullier P, Huish O, Pelat T, Martin AC. The humanness of macaque antibody sequences. J Mol Biol 2010; 396:1439-50; PMID:20043919; http://dx.doi.org/10.1016/j.jmb.2009.12.041
  • Harding FA, Stickler MM, Razo J, DuBridge RB. The immunogenicity of humanized and fully human antibodies. MAbs 2010; 2:256-65; PMID:20400861
  • King C, Garza EN, Mazor R, Linehan JL, Pastan I, Pepper M, Baker D. Removing T-cell epitopes with computational protein design. Proc Natl Acad Sci 2014; 111:8577-82; PMID:24843166; http://dx.doi.org/10.1073/pnas.1321126111
  • Mazor R, Eberle JA, Hu X, Vassall AN, Onda M, Beers R, Lee EC, Kreitman RJ, Lee B, Baker D, et al. Recombinant immunotoxin for cancer treatment with low immunogenicity by identification and silencing of human T-cell epitopes. Proc Natl Acad Sci 2014; 111:8571-6; PMID:24799704; http://dx.doi.org/10.1073/pnas.1405153111
  • Salvat RS, Choi Y, Bishop A, Bailey-Kellogg C, Griswold KE. Protein deimmunization via structure-based design enables efficient epitope deletion at high mutational loads. Biotechnol Bioeng 2015; PMID:25655032
  • Salvat RS, Parker AS, Choi Y, Bailey-Kellogg C, Griswold KE. Mapping the Pareto Optimal Design Space for a Functionally Deimmunized Biotherapeutic Candidate. PLoS Comput Biol 2015; 11:e1003988; PMID:25568954; http://dx.doi.org/10.1371/journal.pcbi.1003988
  • Salvat RS, Parker AS, Guilliams A, Choi Y, Bailey-Kellogg C, Griswold KE. Computationally driven deletion of broadly distributed T cell epitopes in a biotherapeutic candidate. Cell Mol Life Sci 2014; 71:4869-80; PMID:24880662; http://dx.doi.org/10.1007/s00018-014-1652-x
  • Kumar A, Blum KA, Fung HC, Smith MR, Foster PA, Younes A. A phase 1 dose-escalation study of XmAb® 2513 in patients with relapsed or refractory Hodgkin lymphoma. Br J Haematol 2014; PMID:AMBIGUOUS
  • Parham P, Ohta T. Population biology of antigen presentation by MHC class I molecules. Science 1996; 272:67-74; PMID:8600539; http://dx.doi.org/10.1126/science.272.5258.67
  • Reche PA, Reinherz EL. Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol 2003; 331:623-41; PMID:12899833; http://dx.doi.org/10.1016/S0022-2836(03)00750-2
  • Lovell SC, Word JM, Richardson JS, Richardson DC. The penultimate rotamer library. Proteins 2000; 40:389-408; PMID:10861930; http://dx.doi.org/10.1002/1097-0134(20000815)40:3%3c389::AID-PROT50%3e3.0.CO;2-2
  • Chen C-Y, Georgiev I, Anderson AC, Donald BR. Computational structure-based redesign of enzyme activity. Proc Natl Acad Sci 2009; 106:3764-9; PMID:19228942; http://dx.doi.org/10.1073/pnas.0900266106
  • Gainza P, Roberts KE, Donald BR. Protein design using continuous rotamers. PLoS Comput Biol 2012; 8:e1002335; PMID:22279426; http://dx.doi.org/10.1371/journal.pcbi.1002335
  • Goldstein RF. Efficient rotamer elimination applied to protein side-chains and related spin glasses. Biophys J 1994; 66:1335-40; PMID:8061189; http://dx.doi.org/10.1016/S0006-3495(94)80923-3
  • Abhinandan K, Martin AC. Analysis and improvements to Kabat and structurally correct numbering of antibody variable domains. Mol Immunol 2008; 45:3832-9; PMID:18614234; http://dx.doi.org/10.1016/j.molimm.2008.05.022
  • He L, Friedman AM, Bailey-Kellogg C. A divide-and-conquer approach to determine the Pareto frontier for optimization of protein engineering experiments. Proteins 2012; 80:790-806; PMID:22180081; http://dx.doi.org/10.1002/prot.23237
  • Krivov GG, Shapovalov MV, Dunbrack RL. Improved prediction of protein side-chain conformations with SCWRL4. Proteins 2009; 77:778-95; PMID:19603484; http://dx.doi.org/10.1002/prot.22488
  • Choi Y, Deane CM. FREAD revisited: accurate loop structure prediction using a database search algorithm. Proteins 2010; 78:1431-40; PMID:20034110
  • Kelm S, Vangone A, Choi Y, Ebejer J-P, Shi J, Deane CM. Fragment-based modeling of membrane protein loops: Successes, failures, and prospects for the future. Proteins 2014; 82:175-86; PMID:23589399; http://dx.doi.org/10.1002/prot.24299
  • Ponder JW. TINKER: Software tools for molecular design (Ver. 6.0). Saint Louis, MO: Washington University School of Medicine; 2004; 3.
  • Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 2006; 65:712-25; PMID:16981200; http://dx.doi.org/10.1002/prot.21123
  • Qiu D, Shenkin PS, Hollinger FP, Still WC. The GB/SA continuum model for solvation. A fast analytical method for the calculation of approximate Born radii. J Phys Chem 1997; 101:3005-14; http://dx.doi.org/10.1021/jp961992r
  • Eswar N, Webb B, Marti-Renom MA, Madhusudhan M, Eramian D, Shen M-Y, Pieper U, Sali A. Comparative protein structure modeling using Modeller. Curr Protoc Bioinformat 2006:5-6; PMID:18428767
  • Shen M-y, Sali A. Statistical potential for assessment and prediction of protein structures. Protein Sci 2006; 15:2507-24; PMID:17075131; http://dx.doi.org/10.1110/ps.062416606
  • Al-Lazikani B, Lesk AM, Chothia C. Standard conformations for the canonical structures of immunoglobulins. J Mol Biol 1997; 273:927-48; PMID:9367782; http://dx.doi.org/10.1006/jmbi.1997.1354
  • Chothia C, Lesk AM. Canonical structures for the hypervariable regions of immunoglobulins. J Mol Biol 1987; 196:901-17; PMID:3681981; http://dx.doi.org/10.1016/0022-2836(87)90412-8
  • Chothia C, Lesk AM, Tramontano A, Levitt M, Smith-Gill SJ, Air G, Sheriff S, Padlan EA, Davies D, Tulip WR, et al. Conformations of immunoglobulin hypervariable regions. Nature 1989; 342:877-83; PMID:2687698; http://dx.doi.org/10.1038/342877a0
  • Deane CM, Blundell TL. CODA: a combined algorithm for predicting the structurally variable regions of protein models. Protein Sci 2001; 10:599-612; PMID:11344328; http://dx.doi.org/10.1110/ps.37601
  • Boesch AW, Brown EP, Cheng HD, Ofori MO, Normandin E, Nigrovic PA, Alter G, Ackerman ME. Highly parallel characterization of IgG Fc binding interactions. mAbs 2014; 6(4):915-27; PMID:24927273; http://dx.doi.org/10.4161/mabs.28808

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