Transpo-mAb display: Transposition-mediated B cell display and functional screening of full-length IgG antibody libraries

mAbs

Volumn 8, Issue 4, 2016, Pages 726-740

  Waldmeier, Lorenz ^a   Hellmann, Ina ^a   Gutknecht, Chantal K ^a   Wolter, Fabian I ^a   Cook, Skylar C ^b,c   Reddy, Sai T ^b   Grawunder, Ulf ^a   Beerli, Roger R ^a  

^a NBE Therapeutics AG   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c Georgia Institute of Technology   (United States)

Author keywords

Antibody; Antibody drug conjugate; Display; Mammalian; Platform; Screen; Secretion; Therapeutic; Transgene; Transposition

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; MONOCLONAL ANTIBODY; IMMUNOGLOBULIN G;

ALTERNATIVE RNA SPLICING; ANTIBODY LIBRARY; ANTIBODY SCREENING; ANTIGEN PURIFICATION; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CELL SELECTION; CONTROLLED STUDY; DNA TRANSPOSITION; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE CONSTRUCT; GENE EXPRESSION; GENETIC TRANSFECTION; MOLECULAR CLONING; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; OPEN READING FRAME; POLYMERASE CHAIN REACTION; RNA EXTRACTION; ANIMAL; CELL SURFACE DISPLAY; GENE VECTOR; HIGH THROUGHPUT SCREENING; HUMAN; PRECLINICAL STUDY; PROCEDURES; TRANSPOSON;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL SURFACE DISPLAY TECHNIQUES; DNA TRANSPOSABLE ELEMENTS; DRUG EVALUATION, PRECLINICAL; GENETIC VECTORS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; IMMUNOGLOBULIN G;

EID: 84963532713     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2016.1160990     Document Type: Article

References (60)

1. G.Köhler, C.Milstein. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 1975; 256:495-7; PMID:1172191; http://dx.doi.org/10.1038/256495a0
2. R.R.Beerli, C.Rader. Mining human antibody repertoires. MAbs 2010; 2:365-78; PMID:20505349; http://dx.doi.org/10.4161/mabs.12187
3. H.R.Hoogenboom. Selecting and screening recombinant antibody libraries. Nat Biotechnol 2005; 23:1105-16; PMID:16151404; http://dx.doi.org/10.1038/nbt1126
4. T.Clackson, H.R.Hoogenboom, A.D.Griffiths, G.Winter. Making antibody fragments using phage display libraries. 1991; 352:624-8; PMID:1907718; http://dx.doi.org/10.1038/352624a0
5. A.S.Kang, C.F.Barbas, K.D.Janda, S.J.Benkovic, R.A.Lerner. Linkage of recognition and replication functions by assembling combinatorial antibody Fab libraries along phage surfaces. Proc Natl Acad Sci 1991; 88:4363-6; PMID:1903540; http://dx.doi.org/10.1073/pnas.88.10.4363
6. G.P.Smith. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 1985; 228:1315-7; PMID:4001944; http://dx.doi.org/10.1126/science.4001944
7. G.Chen, A.Hayhurst, J.G.Thomas, B.R.Harvey, B.L.Iverson, G.Georgiou. Isolation of high-affinity ligand-binding proteins by periplasmic expression with cytometric screening (PECS). Nat Biotechnol 2001; 19:537-42; PMID:11385457; http://dx.doi.org/10.1038/89281
8. P.S.Daugherty, M.J.Olsen, B.L.Iverson, G.Georgiou. Development of an optimized expression system for the screening of antibody libraries displayed on the Escherichia coli surface. Protein Engineering 1999; 12:613-21; PMID:10436088; http://dx.doi.org/10.1093/protein/12.7.613
9. J.Hanes, A.Plückthun. In vitro selection and evolution of functional proteins by using ribosome display. Proc Natl Acad Sci 1997; 94:4937-42; PMID:9144168; http://dx.doi.org/10.1073/pnas.94.10.4937
10. M.He, M.J.Taussig. Antibody-ribosome-mRNA (ARM) complexes as efficient selection particles for in vitro display and evolution of antibody combining sites. Nucleic Acids Res 1997; 25:5132-4; PMID:9396828; http://dx.doi.org/10.1093/nar/25.24.5132
11. E.T.Boder, K.D.Wittrup. Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol 1997; 15:553-7; PMID:9181578; http://dx.doi.org/10.1038/nbt0697-553
12. S.A.Gai, K.D.Wittrup. Yeast surface display for protein engineering and characterization. Curr Opin Structural Biol 2007; 17:467-73; http://dx.doi.org/10.1016/j.sbi.2007.08.012
13. M.Ho, S.Nagata, I.Pastan. Isolation of anti-CD22 Fv with high affinity by Fv display on human cells. Proc Natl Acad Sci USA 2006; 103:9637-42; PMID:16763048; http://dx.doi.org/10.1073/pnas.0603653103
14. E.S.Smith, S.Shi, M.Zauderer. Construction of cDNA Libraries in Vaccinia Virus. In: Vaccinia Virus and Poxvirology Totowa, NJ: Humana Press; 2004; 65-75; http://dx.doi.org/10.1385/1-59259-789-0:065
15. R.R.Beerli, M.Bauer, R.B.Buser, M.Gwerder, S.Muntwiler, P.Maurer, P.Saudan, M.F.Bachmann. Isolation of human monoclonal antibodies by mammalian cell display. Proc Natl Acad Sci 2008; 105:14336-41; PMID:18812621; http://dx.doi.org/10.1073/pnas.0805942105
16. E.Breous-Nystrom, K.Schultze, M.Meier, L.Flueck, C.Holzer, M.Boll, V.Seibert, A.Schuster, M.Blanusa, V.Schaefer, et al. Retrocyte Display® technology: generation and screening of a high diversity cellular antibody library. Methods 2014; 65:57-67; PMID:24036249; http://dx.doi.org/10.1016/j.ymeth.2013.09.003
17. Z.Ivics, Z.Izsvák. The expanding universe of transposon technologies for gene and cell engineering. Mob DNA 2010; 1:25; PMID:21138556; http://dx.doi.org/10.1186/1759-8753-1-25
18. B.Chénais. Vectors for gene therapy: A place for DNA transposon. Open J Genetics 2013; 03:1; http://dx.doi.org/10.4236/ojgen.2013.32A1001; http://dx.doi.org/10.4236/ojgen.2013.32A1001
19. M.Munoz-Lopez, J.Garcia-Perez. DNA Transposons: Nature and Applications in Genomics. CG 2010; 11:115-28; http://dx.doi.org/10.2174/138920210790886871; http://dx.doi.org/10.2174/138920210790886871
20. K.Yusa, L.Zhou, M.A.Li, A.Bradley. A hyperactive piggyBac transposase for mammalian applications. Proc Natl Acad Sci 2011; 108:1531-1536; PMID:21205896; http://dx.doi.org/10.1073/pnas.1008322108
21. M.-P.Cayer, M.Drouin, S.-P.Sea, A.Forest, S.Côté, C.Simard, L.Boyer, A.Jacques, N.Pineault, D.Jung. Comparison of promoter activities for efficient expression into human B cells and haematopoietic progenitors with adenovirus Ad5/F35. J Immunol Methods 2007; 322:118-27; PMID:17397859; http://dx.doi.org/10.1016/j.jim.2007.02.008
22. W.Cushley, B.Coupar, C.A.Mickelson. A common mechanism for the synthesis of membrane and secreted immunoglobulin α, γ and μ chains. Nature 1982; 298:77-9; PMID:6806665; http://dx.doi.org/10.1038/298077a0
23. F.W.Alt, A.L.M.Bothwell, M.Knapp, E.Siden, E.Mather, M.Koshland, D.Baltimore. Synthesis of secreted and membrane-bound immunoglobulin mu heavy chains is directed by mRNAs that differ at their 3′ ends. Cell 1980; 20:293-301; PMID:6771018; http://dx.doi.org/10.1016/0092-8674(80)90615-7
24. Y.Shinkai, G.Rathbun, K.P.Lam, E.M.Oltz, V.Stewart, M.Mendelsohn, J.Charron, M.Datta, F.Young, A.M.Stall. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 1992; 68:855-67; PMID:1547487; http://dx.doi.org/10.1016/0092-8674(92)90029-C
25. A.F.Wahl, K.Klussman, J.D.Thompson, J.H.Chen, L.V.Francisco, G.Risdon, D.F.Chace, C.B.Siegall, J.A.Francisco. The anti-CD30 monoclonal antibody SGN-30 promotes growth arrest and DNA fragmentation in vitro and affects antitumor activity in models of Hodgkin's disease. Cancer Res 2002; 62:3736-42; PMID:12097283
26. Y.T.Chen, K.Furushima, P.S.Hou, A.T.Ku, J.M.Deng, C.W.Jang, H.Fang, H.P.Adams, M.L.Kuo, H.N.Ho, et al. PiggyBac transposon-mediated, reversible gene transfer in human embryonic stem cells. Stem Cells Dev 2010; 19:763-71; PMID:19740021; http://dx.doi.org/10.1089/scd.2009.0118
27. M.H.Wilson, C.J.Coates, A.L.George. PiggyBac transposon-mediated gene transfer in human cells. Mol Ther 2007; 15:139-45; PMID:17164785; http://dx.doi.org/10.1038/sj.mt.6300028
28. S.Baskar, A.Wiestner, W.H.Wilson, I.Pastan, C.Rader. Targeting malignant B cells with an immunotoxin against ROR1. MAbs 2012; 4:349-61; PMID:22531447; http://dx.doi.org/10.4161/mabs.19870
29. A.H.Daneshmanesh, M.Hojjat-Farsangi, A.S.Khan, M.Jeddi-Tehrani, M.M.Akhondi, A.A.Bayat, R.Ghods, A.-R.Mahmoudi, R.Hadavi, A.Österborg, et al. Monoclonal antibodies against ROR1 induce apoptosis of chronic lymphocytic leukemia (CLL) cells. Leukemia 2012; 26:1348-55; PMID:22289919; http://dx.doi.org/10.1038/leu.2011.362
30. N.Borcherding, D.Kusner, G.-H.Liu, W.Zhang. ROR1, an embryonic protein with an emerging role in cancer biology. Protein Cell 2014; 5:496-502; PMID:24752542; http://dx.doi.org/10.1007/s13238-014-0059-7
31. H.Karasuyama, A.Rolink, F.Melchers. A complex of glycoproteins is associated with VpreB/lambda 5 surrogate light chain on the surface of mu heavy chain-negative early precursor B cell lines. J Exp Med 1993; 178:469-78; PMID:8340754; http://dx.doi.org/10.1084/jem.178.2.469
32. H.Le Hir, A.Nott, M.J.Moore. How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 2003; 28:215-20; PMID:12713906; http://dx.doi.org/10.1016/S0968-0004(03)00052-5
33. M.Onda. New Monoclonal Antibodies to Mesothelin Useful for Immunohistochemistry, Fluorescence-Activated Cell Sorting, Western Blotting, and ELISA. Clin Cancer Res 2005; 11:5840-6; PMID:16115924; http://dx.doi.org/10.1158/1078-0432.CCR-05-0578
34. K.Chang, I.Pastan. Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci USA 1996; 93:136-40; PMID:8552591; http://dx.doi.org/10.1073/pnas.93.1.136
35. R.J.Kelly, E.Sharon, I.Pastan, R.Hassan. Mesothelin-targeted agents in clinical trials and in preclinical development. Mol Cancer Ther 2012; 11:517-25; PMID:22351743; http://dx.doi.org/10.1158/1535-7163.MCT-11-0454
36. M.-P.Lefranc. IMGT, the International ImMunoGeneTics Information System for Immunoinformatics: methods for querying IMGT databases, tools, and web resources in the context of immunoinformatics. Mol Biotechnol 2008; 40:101-11; PMID:18463990; http://dx.doi.org/10.1007/s12033-008-9062-7
37. J.Yang, S.Baskar, K.Y.Kwong, M.G.Kennedy, A.Wiestner, C.Rader. Therapeutic potential and challenges of targeting receptor tyrosine kinase ROR1 with monoclonal antibodies in B-cell malignancies. PLoS One 2011; 6:e21018; PMID:21698301; http://dx.doi.org/10.1371/journal.pone.0021018
38. H.Dave, M.R.Anver, D.O.Butcher, P.Brown, J.Khan, A.S.Wayne, S.Baskar, C.Rader. Restricted Cell Surface Expression of Receptor Tyrosine Kinase ROR1 in Pediatric B-Lineage Acute Lymphoblastic Leukemia Suggests Targetability with Therapeutic Monoclonal Antibodies. PLoS One 2012; 7:e52655; PMID:23285131; http://dx.doi.org/10.1371/journal.pone.0052655
39. A.Doerner, L.Rhiel, S.Zielonka, H.Kolmar. Therapeutic antibody engineering by high efficiency cell screening. FEBS Letters 2014; 588:278-87; PMID:24291259; http://dx.doi.org/10.1016/j.febslet.2013.11.025
40. D.J.King, P.M.Bowers, M.R.Kehry, R.A.Horlick. Mammalian cell display and somatic hypermutation in vitro for human antibody discovery. Curr Drug Discov Technol 2014; 11:56-64; PMID:23978037; http://dx.doi.org/10.2174/15701638113109990037
41. P.M.Bowers, R.A.Horlick, M.R.Kehry, T.Y.Neben, G.L.Tomlinson, L.Altobell, X.Zhang, J.L.Macomber, I.P.Krapf, B.F.Wu, et al. Mammalian cell display for the discovery and optimization of antibody therapeutics. Methods 2014; 65:44-56; PMID:23792919; http://dx.doi.org/10.1016/j.ymeth.2013.06.010
42. C.Zhou, F.W.Jacobsen, L.Cai, Q.Chen, W.D.Shen. Development of a novel mammalian cell surface antibody display platform. MAbs 2010; 2:508-18; PMID:20716968; http://dx.doi.org/10.4161/mabs.2.5.12970
43. R.A.Horlick, J.L.Macomber, P.M.Bowers, T.Y.Neben, G.L.Tomlinson, I.P.Krapf, J.L.Dalton, P.Verdino, D.J.King. Simultaneous surface display and secretion of proteins from mammalian cells facilitate efficient in vitro selection and maturation of antibodies. J Biol Chem 2013; 288:19861-9; PMID:23689374; http://dx.doi.org/10.1074/jbc.M113.452482
44. L.S.Collier, D.A.Largaespada. Transposons for cancer gene discovery: Sleeping Beauty and beyond. Genome Biol 2007; 8 Suppl 1:S15; PMID:18047692; http://dx.doi.org/10.1186/gb-2007-8-s1-s15
45. J.Ni, K.J.Clark, S.C.Fahrenkrug, S.C.Ekker. Transposon tools hopping in vertebrates. Briefings Functional Genomics Proteomics 2008; 7:444-53; ; http://dx.doi.org/10.1093/bfgp/eln049; http://dx.doi.org/10.1093/bfgp/eln049
46. M.A.Li, D.J.Turner, Z.Ning, K.Yusa, Q.Liang, S.Eckert, L.Rad, T.W.Fitzgerald, N.L.Craig, A.Bradley. Mobilization of giant piggyBac transposons in the mouse genome. Nucleic Acids Res 2011; 39:e148-8; PMID:21948799; http://dx.doi.org/10.1093/nar/gkr764
47. S.Ding, X.Wu, G.Li, M.Han, Y.Zhuang, T.Xu. Efficient Transposition of the piggyBac (PB) Transposon in Mammalian Cells and Mice. Cell 2005; 122:473-83; PMID:16096065; http://dx.doi.org/10.1016/j.cell.2005.07.013
48. Z.Izsvák, Z.Ivics, R.H.Plasterk. Sleeping Beauty, a wide host-range transposon vector for genetic transformation in vertebrates. J Mol Biol 2000; 302:93-102; http://dx.doi.org/10.1006/jmbi.2000.4047
49. W.Walther, U.Stein. Viral vectors for gene transfer: a review of their use in the treatment of human diseases. Drugs 2000; 60:249-71; PMID:10983732; http://dx.doi.org/10.2165/00003495-200060020-00002
50. I.Grabundzija, M.Irgang, L.Mátés, E.Belay, J.Matrai, A.Gogol-Döring, K.Kawakami, W.Chen, P.Ruiz, M.K.L.Chuah, et al. Comparative Analysis of Transposable Element Vector Systems in Human Cells. Mol Ther 2009; 18:1200-9; http://dx.doi.org/10.1038/mt.2010.47
51. Y.Zhou, J.Wang, I.Zhou, H.Lou, C.Z.Li, Z.R.Chen, Z.H.Zhang, S.Liu, S.Wu, W.Tan, et al. Simultaneous expression of displayed and secreted antibodies for antibody screen. PLoS One 2013; 8:e80005; PMID:24244593; http://dx.doi.org/10.1371/journal.pone.0080005
52. S.C.-Y.Wu, Y.-J.J.Meir, C.J.Coates, A.M.Handler, P.Pelczar, S.Moisyadi, J.M.Kaminski. piggyBac is a flexible and highly active transposon as compared to sleeping beauty, Tol2, and Mos1 in mammalian cells. Proc Natl Acad Sci USA 2006; 103:15008-13; PMID:17005721; http://dx.doi.org/10.1073/pnas.0606979103
53. K.A.Skipper, P.R.Andersen, N.Sharma, J.G.Mikkelsen. DNA transposon-based gene vehicles - scenes from an evolutionary drive. J Biomedical Sci 2013; 20:92; http://dx.doi.org/10.1186/1423-0127-20-92; http://dx.doi.org/10.1186/1423-0127-20-92
54. J.C.Almagro, J.Fransson. Humanization of antibodies. Front Biosci 2008; 13:1619-33; PMID:17981654
55. C.R.Wood. Antibody Drug Discovery. In: C.R.Wood, ed. Antibody Drug Discovery London, UK: Imperial College Press, 2011; http://dx.doi.org/10.1142/9781848166295
56. M.H.Kershaw, J.A.Westwood, P.K.Darcy. Gene-engineered T cells for cancer therapy. Nat Rev Cancer 2013; 13:525-41; PMID:23880905; http://dx.doi.org/10.1038/nrc3565
57. S.Ramanayake, I.Bilmon, D.Bishop, M.-C.Dubosq, E.Blyth, L.Clancy, D.Gottlieb, K.Micklethwaite. Low-cost generation of Good Manufacturing Practice–grade CD19-specific chimeric antigen receptor–expressing T cells using piggyBac gene transfer and patient-derived materials. Cytotherapy 2015; 17:1251-67; PMID:26212611; http://dx.doi.org/10.1016/j.jcyt.2015.05.013
58. S.Saito, Y.Nakazawa, A.Sueki, K.Matsuda, M.Tanaka, R.Yanagisawa, Y.Maeda, Y.Sato, S.Okabe, T.Inukai, et al. Anti-leukemic potency of piggyBac-mediated CD19-specific T cells against refractory Philadelphia chromosome–positive acute lymphoblastic leukemia. Cytotherapy 2014; 16:1257-69; PMID:25108652; http://dx.doi.org/10.1016/j.jcyt.2014.05.022
59. P.V.R.Manuri, M.H.Wilson, S.N.Maiti, T.Mi, H.Singh, S.Olivares, M.J.Dawson, H.Huls, D.A.Lee, P.H.Rao, et al. piggyBac Transposon/Transposase System to Generate CD19-Specific T Cells for the Treatment of B-Lineage Malignancies. Human Gene Therapy 2010; 21:427-37; PMID:19905893; http://dx.doi.org/10.1089/hum.2009.114
60. M.Onda, M.Willingham, S.Nagata, T.K.Bera, R.Beers, M.Ho, R.Hassan, R.J.Kreitman, I.Pastan. New monoclonal antibodies to mesothelin useful for immunohistochemistry, fluorescence-activated cell sorting, Western blotting, and ELISA. Clin Cancer Res 2005; 11:5840-6; PMID:16115924; http://dx.doi.org/10.1158/1078-0432.CCR-05-0578