Mining Naïve Rabbit Antibody Repertoires by Phage Display for Monoclonal Antibodies of Therapeutic Utility

Journal of Molecular Biology

Volumn 429, Issue 19, 2017, Pages 2954-2973

  Peng, Haiyong ^a   Nerreter, Thomas ^b   Chang, Jing ^a   Qi, Junpeng ^a   Li, Xiuling ^a   Karunadharma, Pabalu ^a   Martinez, Gustavo J ^a,e   Fallahi, Mohammad ^a   Soden, Jo ^c   Freeth, Jim ^c   Beerli, Roger R ^d   Grawunder, Ulf ^d   Hudecek, Michael ^b   Rader, Christoph ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^c Retrogenix   (United Kingdom)

^d NBE Therapeutics AG   (Switzerland)

^e ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

antibody engineering; cancer therapy; chimeric antigen receptors; ROR1; ROR2

Indexed keywords

CD3 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN RET; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE ROR1; PROTEIN TYROSINE KINASE ROR2; RABBIT ANTISERUM; UNCLASSIFIED DRUG; CYTOKINE; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOLOGIC FACTOR; MONOCLONAL ANTIBODY; PEPTIDE LIBRARY; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; RECOMBINANT PROTEIN; ROR1 PROTEIN, HUMAN; ROR2 PROTEIN, HUMAN; TUMOR ANTIGEN;

ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ARTICLE; CELL ENGINEERING; CONTROLLED STUDY; GENETIC VARIABILITY; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; NEW ZEALAND WHITE (RABBIT); NEXT GENERATION SEQUENCING; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE; VALIDATION PROCESS; ANIMAL; CELL PROLIFERATION; CYTOTOXICITY TEST; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; ISOLATION AND PURIFICATION; LEPORIDAE; PEPTIDE LIBRARY; PROCEDURES; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; CYTOTOXICITY TESTS, IMMUNOLOGIC; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; PEPTIDE LIBRARY; RABBITS; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; RECOMBINANT PROTEINS; T-LYMPHOCYTES;

EID: 85028328597     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2017.08.003     Document Type: Article

References (58)

1. Mage, R.G., Lanning, D., Knight, K.L., B cell and antibody repertoire development in rabbits: the requirement of gut-associated lymphoid tissues. Dev. Comp. Immunol. 30 (2006), 137–153.
2. Knight, K.L., Winstead, C.R., Generation of antibody diversity in rabbits. Curr. Opin. Immunol. 9 (1997), 228–232.
3. Winstead, C.R., Zhai, S.K., Sethupathi, P., Knight, K.L., Antigen-induced somatic diversification of rabbit IgH genes: gene conversion and point mutation. J. Immunol. 162 (1999), 6602–6612.
4. Ridder, R., Schmitz, R., Legay, F., Gram, H., Generation of rabbit monoclonal antibody fragments from a combinatorial phage display library and their production in the yeast Pichia pastoris. Biotechnology 13 (1995), 255–260.
5. Lang, I.M., Barbas, C.F. 3rd, Schleef, R.R., Recombinant rabbit Fab with binding activity to type-1 plasminogen activator inhibitor derived from a phage-display library against human alpha-granules. Gene 172 (1996), 295–298.
6. Popkov, M., Mage, R.G., Alexander, C.B., Thundivalappil, S., Barbas, C.F. III, Rader, C., Rabbit immune repertoires as sources for therapeutic monoclonal antibodies: the impact of kappa allotype-correlated variation in cysteine content on antibody libraries selected by phage display. J. Mol. Biol. 325 (2003), 325–335.
7. Spieker-Polet, H., Sethupathi, P., Yam, P.C., Knight, K.L., Rabbit monoclonal antibodies: generating a fusion partner to produce rabbit–rabbit hybridomas. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 9348–9352.
8. Rader, C., Generation and selection of rabbit antibody libraries by phage display. Methods Mol. Biol. 525 (2009), 101–128.
9. Rader, C., Ritter, G., Nathan, S., Elia, M., Gout, I., Jungbluth, A.A., Cohen, L.S., Welt, S., Old, L.J., Barbas, C.F. 3rd, The rabbit antibody repertoire as a novel source for the generation of therapeutic human antibodies. J. Biol. Chem. 275 (2000), 13668–13676.
10. Steinberger, P., Sutton, J.K., Rader, C., Elia, M., Barbas, C.F. 3rd, Generation and characterization of a recombinant human CCR5-specific antibody. A phage display approach for rabbit antibody humanization. J. Biol. Chem. 275 (2000), 36073–36078.
11. Borras, L., Gunde, T., Tietz, J., Bauer, U., Hulmann-Cottier, V., Grimshaw, J.P., Urech, D.M., Generic approach for the generation of stable humanized single-chain Fv fragments from rabbit monoclonal antibodies. J. Biol. Chem. 285 (2010), 9054–9066.
12. Jendreyko, N., Popkov, M., Beerli, R.R., Chung, J., McGavern, D.B., Rader, C., Barbas, C.F. 3rd, Intradiabodies, bispecific, tetravalent antibodies for the simultaneous functional knockout of two cell surface receptors. J. Biol. Chem. 278 (2003), 47812–47819.
13. Popkov, M., Jendreyko, N., Gonzalez-Sapienza, G., Mage, R.G., Rader, C., Barbas, C.F. 3rd, Human/mouse cross-reactive anti-VEGF receptor 2 recombinant antibodies selected from an immune b9 allotype rabbit antibody library. J. Immunol. Methods 288 (2004), 149–164.
14. Popkov, M., Jendreyko, N., McGavern, D.B., Rader, C., Barbas, C.F. 3rd, Targeting tumor angiogenesis with adenovirus-delivered anti-Tie-2 intrabody. Cancer Res. 65 (2005), 972–981.
15. Popkov, M., Rader, C., Barbas, C.F. 3rd, Isolation of human prostate cancer cell reactive antibodies using phage display technology. J. Immunol. Methods 291 (2004), 137–151.
16. Jendreyko, N., Popkov, M., Rader, C., Barbas, C.F. 3rd, Phenotypic knockout of VEGF-R2 and Tie-2 with an intradiabody reduces tumor growth and angiogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 8293–8298.
17. Hofer, T., Tangkeangsirisin, W., Kennedy, M.G., Mage, R.G., Raiker, S.J., Venkatesh, K., Lee, H., Giger, R.J., Rader, C., Chimeric rabbit/human Fab and IgG specific for members of the Nogo-66 receptor family selected for species cross-reactivity with an improved phage display vector. J. Immunol. Methods 318 (2007), 75–87.
18. Stahl, S.J., Watts, N.R., Rader, C., DiMattia, M.A., Mage, R.G., Palmer, I., Kaufman, J.D., Grimes, J.M., Stuart, D.I., Steven, A.C., Wingfield, P.T., Generation and characterization of a chimeric rabbit/human Fab for co-crystallization of HIV-1 Rev. J. Mol. Biol. 397 (2010), 697–708.
19. DiMattia, M.A., Watts, N.R., Stahl, S.J., Rader, C., Wingfield, P.T., Stuart, D.I., Steven, A.C., Grimes, J.M., Implications of the HIV-1 Rev dimer structure at 3.2 Å resolution for multimeric binding to the Rev response element. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 5810–5814.
20. Yang, J., Baskar, S., Kwong, K.Y., Kennedy, M.G., Wiestner, A., Rader, C., Therapeutic potential and challenges of targeting receptor tyrosine kinase ROR1 with monoclonal antibodies in B-cell malignancies. PLoS One, 6, 2011, e21018.
21. Forrester, W.C., The Ror receptor tyrosine kinase family. Cell. Mol. Life Sci. 59 (2002), 83–96.
22. Rebagay, G., Yan, S., Liu, C., Cheung, N.K., ROR1 and ROR2 in human malignancies: potentials for targeted therapy. Front. Oncol., 2, 2012, 34.
23. Debebe, Z., Rathmell, W.K., Ror2 as a therapeutic target in cancer. Pharmacol. Ther. 150 (2015), 143–148.
24. Borcherding, N., Kusner, D., Liu, G.H., Zhang, W., ROR1, an embryonic protein with an emerging role in cancer biology. Protein Cell 5 (2014), 496–502.
25. Zhang, S., Chen, L., Cui, B., Chuang, H.Y., Yu, J., Wang-Rodriguez, J., Tang, L., Chen, G., Basak, G.W., Kipps, T.J., ROR1 is expressed in human breast cancer and associated with enhanced tumor-cell growth. PLoS One, 7, 2012, e31127.
26. Cui, B., Zhang, S., Chen, L., Yu, J., Widhopf, G.F. 2nd, Fecteau, J.F., Rassenti, L.Z., Kipps, T.J., Targeting ROR1 inhibits epithelial–mesenchymal transition and metastasis. Cancer Res. 73 (2013), 3649–3660.
27. Bos, P.D., Zhang, X.H., Nadal, C., Shu, W., Gomis, R.R., Nguyen, D.X., Minn, A.J., van de Vijver, M.J., Gerald, W.L., Foekens, J.A., Massagué, J., Genes that mediate breast cancer metastasis to the brain. Nature 459 (2009), 1005–1009.
28. Yamaguchi, T., Yanagisawa, K., Sugiyama, R., Hosono, Y., Shimada, Y., Arima, C., Kato, S., Tomida, S., Suzuki, M., Osada, H., Takahashi, T., NKX2-1/TITF1/TTF-1-induced ROR1 is required to sustain EGFR survival signaling in lung adenocarcinoma. Cancer Cell 21 (2012), 348–361.
29. McCartney-Francis, N., Skurla, R.M. Jr., Mage, R.G., Bernstein, K.E., Kappa-chain allotypes and isotypes in the rabbit: cDNA sequences of clones encoding b9 suggest an evolutionary pathway and possible role of the interdomain disulfide bond in quantitative allotype expression. Proc. Natl. Acad. Sci. U. S. A. 81 (1984), 1794–1798.
30. Carneiro, M., Rubin, C.J., Di Palma, F., Albert, F.W., Alföldi, J., Barrio, A.M., Pielberg, G., Rafati, N., Sayyab, S., Turner-Maier, J., Younis, S., Afonso, S., Aken, B., Alves, J.M., Barrell, D., Bolet, G., Boucher, S., Burbano, H.A., Campos, R., Chang, J.L., Duranthon, V., Fontanesi, L., Garreau, H., Heiman, D., Johnson, J., Mage, R.G., Peng, Z., Queney, G., Rogel-Gaillard, C., Ruffier, M., Searle, S., Villafuertem, R., Xiong, A., Young, S., Forsberg-Nilsson, K., Good, J.M., Lander, E.S., Ferrand, N., Lindblad-Toh, K., Andersson, L., Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science 345 (2014), 1074–1079.
31. Pinheiro, A., Neves, F., Lemos de Matos, A., Abrantes, J., van der Loo, W., Mage, R., Esteves, P.J., An overview of the lagomorph immune system and its genetic diversity. Immunogenetics 68 (2016), 83–107.
32. de Haard, H.J., van Neer, N., Reurs, A., Hufton, S.E., Roovers, R.C., Henderikx, P., de Bruïne, A.P., Arends, J.W., Hoogenboom, H.R., A large non-immunized human Fab fragment phage library that permits rapid isolation and kinetic analysis of high affinity antibodies. J. Biol. Chem. 274 (1999), 18218–18230.
33. Fellouse, F.A., Wiesmann, C., Sidhu, S.S., Synthetic antibodies from a four-amino-acid code: a dominant role for tyrosine in antigen recognition. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 12467–12472.
34. Rothe, C., Urlinger, S., Löhning, C., Prassler, J., Stark, Y., Jäger, U., Hubner, B., Bardroff, M., Pradel, I., Boss, M., Bittlingmaier, R., Bataa, T., Frisch, C., Brocks, B., Honegger, A., Urban, M., The human combinatorial antibody library HuCAL GOLD combines diversification of all six CDRs according to the natural immune system with a novel display method for efficient selection of high-affinity antibodies. J. Mol. Biol. 376 (2008), 1182–1200.
35. Glanville, J., D'Angelo, S., Khan, T.A., Reddy, S.T., Naranjo, L., Ferrara, F., Bradbury, A.R., Deep sequencing in library selection projects: what insight does it bring?. Curr. Opin. Struct. Biol. 33 (2015), 146–160.
36. Lavinder, J.J., Hoi, K.H., Reddy, S.T., Wine, Y., Georgiou, G., Systematic characterization and comparative analysis of the rabbit immunoglobulin repertoire. PLoS One, 9, 2014, e101322.
37. Ravn, U., Didelot, G., Venet, S., Ng, K.T., Gueneau, F., Rousseau, F., Calloud, S., Kosco-Vilbois, M., Fischer, N., Deep sequencing of phage display libraries to support antibody discovery. Methods 60 (2013), 99–110.
38. Kwong, K.Y., Rader, C., E. coli expression and purification of Fab antibody fragments. Curr. Protoc. Protein Sci., 2009 (Chapter 6, Unit 6.10).
39. Balakrishnan, A., Goodpaster, T., Randolph-Habecker, J., Hoffstrom, B.G., Jalikis, F.G., Koch, L.K., Berger, C., Kosasih, P.L., Rajan, A., Sommermeyer, D., Porter, P.L., Riddell, S.R., Analysis of ROR1 protein expression in human cancer and normal tissues. Clin. Cancer Res. 23 (2017), 3061–3071.
40. Schwabe, G.C., Tinschert, S., Buschow, C., Meinecke, P., Wolff, G., Gillessen-Kaesbach, G., Oldridge, M., Wilkie, A.O., Kömec, R., Mundlos, S., Distinct mutations in the receptor tyrosine kinase gene ROR2 cause brachydactyly type B. Am. J. Hum. Genet. 67 (2000), 822–831.
41. Hudecek, M., Lupo-Stanghellini, M.T., Kosasih, P.L., Sommermeyer, D., Jensen, M.C., Rader, C., Riddell, S.R., Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells. Clin. Cancer Res. 19 (2013), 3153–3164.
42. Wang, X., Chang, W.C., Wong, C.W., Colcher, D., Sherman, M., Ostberg, J.R., Forman, S.J., Riddell, S.R., Jensen, M.C., A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood 118 (2011), 1255–1263.
43. Bradbury, A., Plückthun, A., Reproducibility: standardize antibodies used in research. Nature 518 (2015), 27–29.
44. Bradbury, A.R., Plückthun, A., Getting to reproducible antibodies: the rationale for sequenced recombinant characterized reagents. Protein Eng. Des. Sel. 28 (2015), 303–305.
45. Weber, J., Peng, H., Rader, C., From rabbit antibody repertoires to rabbit monoclonal antibodies. Exp. Mol. Med., 49, 2017, e305.
46. Berger, C., Sommermeyer, D., Hudecek, M., Berger, M., Balakrishnan, A., Paszkiewicz, P.J., Kosasih, P.L., Rader, C., Riddell, S.R., Safety of targeting ROR1 in primates with chimeric antigen receptor-modified T cells. Cancer Immunol. Res. 3 (2015), 206–216.
47. Shinkai, Y., Rathbun, G., Lam, K.P., Oltz, E.M., Stewart, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., Stall, A.M., Alt, F.W., RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68 (1992), 855–867.
48. Waldmeier, L., Hellmann, I., Gutknecht, C.K., Wolter, F.I., Cook, S.C., Reddy, S.T., Grawunder, U., Beerli, R.R., Transpo-mAb display: transposition-mediated B cell display and functional screening of full-length IgG antibody libraries. MAbs 8 (2016), 726–740.
49. Hudecek, M., Schmitt, T.M., Baskar, S., Lupo-Stanghellini, M.T., Nishida, T., Yamamoto, T.N., Bleakley, M., Turtle, C.J., Chang, W.C., Greisman, H.A., Wood, B., Maloney, D.G., Jensen, M.C., Rader, C., Riddell, S.R., The B-cell tumor-associated antigen ROR1 can be targeted with T cells modified to express a ROR1-specific chimeric antigen receptor. Blood 116 (2010), 4532–4541.
50. Hofer, T., Thomas, J.D., Burke, T.R. Jr., Rader, C., An engineered selenocysteine defines a unique class of antibody derivatives. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 12451–12456.
51. Merchant, A.M., Zhu, Z., Yuan, J.Q., Goddard, A., Adams, C.W., Presta, L.G., Carter, P., An efficient route to human bispecific IgG. Nat. Biotechnol. 16 (1998), 677–681.
52. Rader, C., Generation of human Fab libraries for phage display. Methods Mol. Biol. 901 (2012), 53–79.
53. Sidhu, S.S., Lowman, H.B., Cunningham, B.C., Wells, J.A., Phage display for selection of novel binding peptides. Methods Enzymol. 328 (2000), 333–363.
54. Kwong, K.Y., Baskar, S., Zhang, H., Mackall, C.L., Rader, C., Generation, affinity maturation, and characterization of a human anti-human NKG2D monoclonal antibody with dual antagonistic and agonistic activity. J. Mol. Biol. 384 (2008), 1143–1156.
55. Rader, C., Popkov, M., Neves, J.A., Barbas, C.F. 3rd, Integrin alpha(v)beta3 targeted therapy for Kaposi's sarcoma with an in vitro evolved antibody. FASEB J. 16 (2002), 2000–2002.
56. Yang, J., Rader, C., Cloning, expression, and purification of monoclonal antibodies in scFv-Fc format. Methods Mol. Biol. 901 (2012), 209–232.
57. Turner, L., Lavstsen, T., Berger, S.S., Wang, C.W., Petersen, J.E., Avril, M., Brazier, A.J., Freeth, J., Jespersen, J.S., Nielsen, M.A., Magistrado, P., Lusingu, J., Smith, J.D., Higgins, M.K., Theander, T.G., Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498 (2013), 502–505.
58. Brown, C.E., Wright, C.L., Naranjo, A., Vishwanath, R.P., Chang, W.C., Olivares, S., Wagner, J.R., Bruins, L., Raubitschek, A., Cooper, L.J., Jensen, M.C., Biophotonic cytotoxicity assay for high-throughput screening of cytolytic killing. J. Immunol. Methods 297 (2005), 39–52.