Selection strategies for anticancer antibody discovery: Searching off the beaten path

Trends in Biotechnology

Volumn 33, Issue 5, 2015, Pages 292-301

  Sánchez Martín, David ^a   Sørensen, Morten Dræby ^b,c   Lykkemark, Simon ^c   Sanz, Laura ^d   Kristensen, Peter ^c   Ruoslahti, Erkki ^e,f   Álvarez Vallina, Luis ^c,d  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Structural Biology and Biocomputing Programme   (Spain)

^c AARHUS UNIVERSITY   (Denmark)

^d HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^e BURNHAM INSTITUTE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Advanced phage selections; Phage display; Therapeutic antibodies; Tumor associated antigens

Indexed keywords

ANTIGENS; ONCOLOGY; PHAGE DISPLAY; TUMORS;

ANTIBODY LIBRARY; ANTIBODY THERAPY; PHAGE SELECTION; THERAPEUTIC ANTIBODIES; TUMOR MARKERS; VARIOUS TECHNOLOGIES;

ANTIBODIES;

ANTINEOPLASTIC AGENT; MONOCLONAL ANTIBODY; TUMOR ANTIGEN; TUMOR MARKER; CANCER ANTIBODY;

ANTIBODY LIBRARY; CANCER THERAPY; DRUG TARGETING; EX VIVO STUDY; HUMAN; IN VIVO STUDY; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; REVIEW; TECHNOLOGY; ANIMAL; CELL SURFACE DISPLAY; CHEMISTRY; DRUG DEVELOPMENT; IMMUNOLOGY; NEOPLASMS; ONCOLOGY; TRENDS; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEOPLASM; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; CELL SURFACE DISPLAY TECHNIQUES; DRUG DISCOVERY; HUMANS; MEDICAL ONCOLOGY; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84928049044     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2015.02.008     Document Type: Review

References (91)

1. Weiner L.M., et al. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat. Rev. Immunol. 2010, 10:317-327.
2. Cuesta A.M., et al. Multivalent antibodies: when design surpasses evolution. Trends Biotechnol. 2010, 28:355-362.
3. Reichert J.M. Antibodies to watch in 2014: mid-year update. MAbs 2014, 6:799-802.
4. Vacchelli E., et al. Trial Watch: tumor-targeting monoclonal antibodies in cancer therapy. Oncoimmunology 2014, 3:e27048.
5. Aranda F., et al. Trial Watch: immunostimulatory monoclonal antibodies in cancer therapy. Oncoimmunology 2014, 3:e27297.
6. Carter P., et al. Identification and validation of cell surface antigens for antibody targeting in oncology. Endocr. Relat. Cancer 2004, 11:659-687.
7. Uva P., et al. Comparative membranome expression analysis in primary tumors and derived cell lines. PLoS ONE 2010, 5:e11742.
8. Sanz L., et al. Differential transplantability of human endothelial cells in colorectal cancer and renal cell carcinoma primary xenografts. Lab. Invest. 2009, 89:91-97.
9. Swartz M.A., et al. Tumor microenvironment complexity: emerging roles in cancer therapy. Cancer Res. 2012, 72:2473-2480.
10. Heine M., et al. High interstitial fluid pressure is associated with low tumour penetration of diagnostic monoclonal antibodies applied for molecular imaging purposes. PLoS ONE 2012, 7:e36258.
11. Junttila M.R., de Sauvage F.J. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 2013, 501:346-354.
12. Bradbury A.R., et al. Beyond natural antibodies: the power of in vitro display technologies. Nat. Biotechnol. 2011, 29:245-254.
13. Rust S., et al. Combining phenotypic and proteomic approaches to identify membrane targets in a 'triple negative' breast cancer cell type. Mol. Cancer 2013, 12:11.
14. Kurosawa G., et al. Comprehensive screening for antigens overexpressed on carcinomas via isolation of human mAbs that may be therapeutic. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:7287-7292.
15. Heitner T., et al. Selection of cell binding and internalizing epidermal growth factor receptor antibodies from a phage display library. J. Immunol. Methods 2001, 248:17-30.
16. Ayat H., et al. Isolation of scFv antibody fragments against HER2 and CEA tumor antigens from combinatorial antibody libraries derived from cancer patients. Biologicals 2013, 41:345-354.
17. Mazuet C., et al. Breast carcinoma specific antibody selection combining phage display and immunomagnetic cell sorting. Biochem. Biophys. Res. Commun. 2006, 348:550-559.
18. Shukla G.S., Krag D.N. Phage display selection for cell-specific ligands: development of a screening procedure suitable for small tumor specimens. J. Drug Target. 2005, 13:7-18.
19. Goenaga A.L., et al. Identification and characterization of tumor antigens by using antibody phage display and intrabody strategies. Mol. Immunol. 2007, 44:3777-3788.
20. Hauptschein R.S., et al. Functional proteomic screen identifies a modulating role for CD44 in death receptor-mediated apoptosis. Cancer Res. 2005, 65:1887-1896.
21. Sui J., et al. Identification of CD4 and transferrin receptor antibodies by CXCR4 antibody-guided Pathfinder selection. Eur. J. Biochem. 2003, 270:4497-4506.
22. Xie J., et al. Prevention of cell death by antibodies selected from intracellular combinatorial libraries. Chem. Biol. 2014, 21:274-283.
23. Sorensen M.D., et al. Raising antibodies against circulating foetal cells from maternal peripheral blood. Prenat. Diagn. 2013, 33:284-291.
24. Yea K., et al. Converting stem cells to dendritic cells by agonist antibodies from unbiased morphogenic selections. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:14966-14971.
25. Sanchez-Martin D., et al. Proteasome activator complex PA28 identified as an accessible target in prostate cancer by in vivo selection of human antibodies. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:13791-13796.
26. Boess F., et al. Gene expression in two hepatic cell lines, cultured primary hepatocytes, and liver slices compared to the in vivo liver gene expression in rats: possible implications for toxicogenomics use of in vitro systems. Toxicol. Sci. 2003, 73:386-402.
27. Pan C., et al. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol. Cell. Proteomics 2009, 8:443-450.
28. Sun Y., et al. Biopanning phage-display libraries on small tissue sections captured by laser capture microdissection. J. Biotech Res. 2009, 1:55-63.
29. Sun Y., et al. Phage-display selection on tumor histological specimens with laser capture microdissection. J. Immunol. Methods 2009, 347:46-53.
30. Yao V.J., et al. Targeting pancreatic islets with phage display assisted by laser pressure catapult microdissection. Am. J. Pathol. 2005, 166:625-636.
31. Ruan W., et al. Identification of clinically significant tumor antigens by selecting phage antibody library on tumor cells in situ using laser capture microdissection. Mol. Cell. Proteomics 2006, 5:2364-2373.
32. Sorensen M.D., et al. Microselection - affinity selecting antibodies against a single rare cell in a heterogeneous population. J. Cell. Mol. Med. 2010, 14:1953-1961.
33. Lu H., et al. Application of laser capture microdissection to phage display peptide library screening. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2004, 98:692-697.
34. Kubo N., et al. Identification of oligopeptide binding to colon cancer cells separated from patients using laser capture microdissection. J. Drug Target. 2008, 16:396-404.
35. Tanaka T., et al. In situ phage screening. A method for identification of subnanogram tissue components in situ. J. Biol. Chem. 2002, 277:30382-30387.
36. Sorensen M.D., Kristensen P. Selection of antibodies against a single rare cell present in a heterogeneous population using phage display. Nat. Protoc. 2011, 6:509-522.
37. Ross A.A., et al. Detection and viability of tumor cells in peripheral blood stem cell collections from breast cancer patients using immunocytochemical and clonogenic assay techniques. Blood 1993, 82:2605-2610.
38. Kristensen P., Winter G. Proteolytic selection for protein folding using filamentous bacteriophages. Fold. Des. 1998, 3:321-328.
39. de Wildt R.M., et al. Antibody arrays for high-throughput screening of antibody-antigen interactions. Nat. Biotechnol. 2000, 18:989-994.
40. Subkhankulova T., et al. Modelling and measuring single cell RNA expression levels find considerable transcriptional differences among phenotypically identical cells. BMC Genomics 2008, 9:268.
41. Pasqualini R., Ruoslahti E. Organ targeting in vivo using phage display peptide libraries. Nature 1996, 380:364-366.
42. Teesalu T., et al. Mapping of vascular ZIP codes by phage display. Methods Enzymol. 2012, 503:35-56.
43. Arap W., et al. Steps toward mapping the human vasculature by phage display. Nat. Med. 2002, 8:121-127.
44. Krag D.N., et al. Selection of tumor-binding ligands in cancer patients with phage display libraries. Cancer Res. 2006, 66:7724-7733.
45. Ruoslahti E. Peptides as targeting elements and tissue penetration devices for nanoparticles. Adv. Mater. 2012, 24:3747-3756.
46. Ruoslahti E., et al. Targeting of drugs and nanoparticles to tumors. J. Cell Biol. 2010, 188:759-768.
47. Shukla G.S., et al. Intravenous infusion of phage-displayed antibody library in human cancer patients: enrichment and cancer-specificity of tumor-homing phage-antibodies. Cancer Immunol. Immunother. 2013, 62:1397-1410.
48. Deramchia K., et al. In vivo phage display to identify new human antibody fragments homing to atherosclerotic endothelial and subendothelial tissues [corrected]. Am. J. Pathol. 2012, 180:2576-2589.
49. Liu Y., et al. Controlling the selection stringency of phage display using a microfluidic device. Lab Chip 2009, 9:1033-1036.
50. Ho M., Pastan I. Mammalian cell display for antibody engineering. Methods Mol. Biol. 2009, 525:337-352.
51. Alonso-Camino V., et al. Lymphocyte display: a novel antibody selection platform based on T cell activation. PLoS ONE 2009, 4:e7174.
52. Alonso-Camino V., et al. CARbodies: human antibodies against cell surface tumor antigens selected from repertoires displayed on T cell chimeric antigen receptors. Mol. Ther. Nucleic Acids 2013, 2:e93.
53. Barbas C.F., et al. High-affinity self-reactive human antibodies by design and selection: targeting the integrin ligand binding site. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:10003-10007.
54. Smith J.W., et al. Building synthetic antibodies as adhesive ligands for integrins. J. Biol. Chem. 1994, 269:32788-32795.
55. Zhu X., et al. Identification of internalizing human single-chain antibodies targeting brain tumor sphere cells. Mol. Cancer Ther. 2010, 9:2131-2141.
56. Rossig C., et al. Selection of human antitumor single-chain Fv antibodies from the B-cell repertoire of patients immunized against autologous neuroblastoma. Med. Pediatr. Oncol. 2000, 35:692-695.
57. Wong C., et al. Human scFv antibody fragments specific for the epithelial tumour marker MUC-1, selected by phage display on living cells. Cancer Immunol. Immunother. 2001, 50:93-101.
58. Rothe A., et al. Construction of phage display libraries from reactive lymph nodes of breast carcinoma patients and selection for specifically binding human single chain Fv on cell lines. Int. J. Mol. Med. 2004, 14:729-735.
59. Araujo T.G., et al. A novel highly reactive Fab antibody for breast cancer tissue diagnostics and staging also discriminates a subset of good prognostic triple-negative breast cancers. Cancer Lett. 2014, 343:275-285.
60. Jakobsen C.G., et al. Phage display derived human monoclonal antibodies isolated by binding to the surface of live primary breast cancer cells recognize GRP78. Cancer Res. 2007, 67:9507-9517.
61. Rubinstein D.B., et al. Receptor for the globular heads of C1q (gC1q-R, p33, hyaluronan-binding protein) is preferentially expressed by adenocarcinoma cells. Int. J. Cancer 2004, 110:741-750.
62. Gur D., et al. Identification of single chain antibodies to breast cancer stem cells using phage display. Biotechnol. Prog. 2009, 25:1780-1787.
63. Wiiger M.T., et al. A novel human recombinant single-chain antibody targeting CD166/ALCAM inhibits cancer cell invasion in vitro and in vivo tumour growth. Cancer Immunol. Immunother. 2010, 59:1665-1674.
64. Groot A.J., et al. Reverse proteomic antibody screening identifies anti adhesive VHH targeting VLA-3. Mol. Immunol. 2009, 46:2022-2028.
65. Staneloudi C., et al. Development and characterization of novel photosensitizer: scFv conjugates for use in photodynamic therapy of cancer. Immunology 2007, 120:512-517.
66. Liebman M.A., et al. Generation and preliminary characterization of an antibody library with preferential reactivity to human colorectal cancer cells as compared to normal human blood cells. Immunol. Lett. 2004, 91:179-188.
67. Huls G.A., et al. A recombinant, fully human monoclonal antibody with antitumor activity constructed from phage-displayed antibody fragments. Nat. Biotechnol. 1999, 17:276-281.
68. Williams B.R., Sharon J. Polyclonal anti-colorectal cancer Fab phage display library selected in one round using density gradient centrifugation to separate antigen-bound and free phage. Immunol. Lett. 2002, 81:141-148.
69. Xu M.Y., et al. Production of a human single-chain variable fragment antibody against esophageal carcinoma. World J. Gastroenterol. 2004, 10:2619-2623.
70. Geuijen C.A., et al. A proteomic approach to tumour target identification using phage display, affinity purification and mass spectrometry. Eur. J. Cancer 2005, 41:178-187.
71. Bakker A.B., et al. C-type lectin-like molecule-1: a novel myeloid cell surface marker associated with acute myeloid leukemia. Cancer Res. 2004, 64:8443-8450.
72. Shadidi M., Sioud M. An anti-leukemic single chain Fv antibody selected from a synthetic human phage antibody library. Biochem. Biophys. Res. Commun. 2001, 280:548-552.
73. Baskar S., et al. A human monoclonal antibody drug and target discovery platform for B-cell chronic lymphocytic leukemia based on allogeneic hematopoietic stem cell transplantation and phage display. Blood 2009, 114:4494-4502.
74. Delcommenne M., Klingemann H.G. Detection and characterization of syndecan-1-associated heparan sulfate 6-O-sulfated motifs overexpressed in multiple myeloma cells using single chain antibody variable fragments. Hum. Antibodies 2012, 21:29-30.
75. Shen Y., et al. Generation and selection of immunized Fab phage display library against human B cell lymphoma. Cell Res. 2007, 17:650-660.
76. Jarutat T., et al. Selection of vimentin-specific antibodies from the HuCAL phage display library by subtractive panning on formalin-fixed, paraffin-embedded tissue. Biol. Chem. 2007, 388:651-658.
77. Shui X., et al. Construction and selection of human Fab antibody phage display library of liver cancer. Hybridoma (Larchmt) 2009, 28:341-347.
78. Yu B., et al. Human scFv antibody fragments specific for hepatocellular carcinoma selected from a phage display library. World J. Gastroenterol. 2005, 11:3985-3989.
79. Reiersen H., et al. Screening human antibody libraries against carcinoma cells by affinity purification and polymerase chain reaction. J. Immunol. Methods 2008, 330:44-56.
80. Zhang J., et al. A pentavalent single-domain antibody approach to tumor antigen discovery and the development of novel proteomics reagents. J. Mol. Biol. 2004, 341:161-169.
81. Luo Y., et al. Production and radioimmunoimaging of novel fully human phage display recombinant antibodies and growth inhibition of lung adenocarcinoma cell line overexpressing Prx I. Cancer Biol. Ther. 2009, 8:1369-1377.
82. Douguchi J., et al. Construction of human monoclonal single-chain Fv antibodies against small-cell lung cancer by phage display libraries derived from cell-immunized SCID mice engrafted with human peripheral blood lymphocytes. Proteomics Clin. Appl. 2009, 3:1265-1272.
83. An F., et al. Targeted drug delivery to mesothelioma cells using functionally selected internalizing human single-chain antibodies. Mol. Cancer Ther. 2008, 7:569-578.
84. Sharma S., et al. Characterization of a putative ovarian oncogene, elongation factor 1α, isolated by panning a synthetic phage display single-chain variable fragment library with cultured human ovarian cancer cells. Clin. Cancer Res. 2007, 13:5889-5896.
85. Gao C., et al. De novo identification of tumor-specific internalizing human antibody-receptor pairs by phage-display methods. J. Immunol. Methods 2003, 274:185-197.
86. Conrad F., et al. Human antibodies targeting cell surface antigens overexpressed by the hormone refractory metastatic prostate cancer cells: ICAM-1 is a tumor antigen that mediates prostate cancer cell invasion. J. Mol. Med. (Berl.) 2009, 87:507-514.
87. Eustace B.K., et al. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat. Cell Biol. 2004, 6:507-514.
88. Dantas-Barbosa C., et al. Isolation of osteosarcoma-associated human antibodies from a combinatorial Fab phage display library. J. Biomed. Biotechnol. 2009, 2009:157531.
89. Orecchia P., et al. A novel human anti-syndecan-1 antibody inhibits vascular maturation and tumour growth in melanoma. Eur. J. Cancer 2013, 49:2022-2033.
90. Cai X., Garen A. Anti-melanoma antibodies from melanoma patients immunized with genetically modified autologous tumor cells: selection of specific antibodies from single-chain Fv fusion phage libraries. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:6537-6541.
91. Sánchez-Martin D., et al. In vivo selection of tumor-specific antibodies. Oncotarget 2013, 4:1547.