A high through-put platform for recombinant antibodies to folded proteins

Molecular and Cellular Proteomics

Volumn 14, Issue 10, 2015, Pages 2833-2847

  Hornsby, Michael ^a   Paduch, Marcin ^b   Miersch, Shane ^c   Sääf, Annika ^b   Matsuguchi, Tet ^a   Lee, Brian ^a   Wypisniak, Karolina ^a   Doak, Allison ^a   King, Daniel ^b   Usatyuk, Svitlana ^b   Perry, Kimberly ^b   Lu, Vince ^b   Thomas, William ^b   Luke, Judy ^b   Goodman, Jay ^b   Hoey, Robert J ^b   Lai, Darson ^b   Griffin, Carly ^c   Li, Zhijian ^c   Vizeacoumar, Franco J ^e   Dong, Debbie ^c   Campbell, Elliot ^d   Anderson, Stephen ^d   Zhong, Nan ^f   Gräslund, Susanne ^f   Koide, Shohei ^b   Moffat, Jason ^c   Sidhu, Sachdev ^c   Kossiakoff, Anthony ^b   Wells, James ^a   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d RUTGERS UNIVERSITY   (United States)

^e UNIVERSITY OF SASKATCHEWAN   (Canada)

^f Structural Genomics Consortium   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEOME; RECOMBINANT ANTIBODY; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; ANTIBODY; ANTIGEN; IMMUNOGLOBULIN F(AB) FRAGMENT; RECOMBINANT PROTEIN;

ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; CELL LYSATE; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; ESCHERICHIA COLI; EXERCISE; FLUOROMETRY; GENE EXPRESSION; GENE SILENCING; GENE SYNTHESIS; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMUNOFLUORESCENCE; NONHUMAN; PHAGE DISPLAY; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; ROBOTICS; SEQUENCE ALIGNMENT; SIZE EXCLUSION CHROMATOGRAPHY; VALIDATION STUDY; GENETICS; HIGH THROUGHPUT SCREENING; IMMUNOLOGY;

ANTIBODIES; ANTIGENS; ESCHERICHIA COLI; HIGH-THROUGHPUT SCREENING ASSAYS; IMMUNOGLOBULIN FAB FRAGMENTS; PROTEIN FOLDING; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 84942930536     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.O115.052209     Document Type: Article

References (66)

1. Pasqualini, R., and Arap, W. (2004) Hybridoma-free generation of monoclonal antibodies. Proc. Natl. Acad. Sci. U.S.A. 101, 257-259
2. Harlow, E., and Lane, D. Using antibodies : a laboratory manual. 1999, Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press. xiv, 495 p.
3. Berglund, L., Bjorling, E., Oksvold, P., Fagerberg, L., Asplund, A., Szigyarto, C. A., Persson, A., Ottosson, J., Wernerus, H., Nilsson, P., Lundberg, E., Sivertsson, A., Navani, S., Wester, K., Kampf, C., Hober, S., Ponten, F., and Uhlen, M. (2008) A genecentric Human Protein Atlas for expression profiles based on antibodies. Mol. Cell. Proteomics 7, 2019-2027
4. Bordeaux, J., Welsh, A., Agarwal, S., Killiam, E., Baquero, M., Hanna, J., Anagnostou, V., and Rimm, D. (2010) Antibody validation. BioTechniques 48, 197-209
5. Bradbury, A., and Pluckthun, A. (2015) Reproducibility: standardize antibodies used in research. Nature 518, 27-29
6. Gloriam, D. E., Orchard, S., Bertinetti, D., Bjorling, E., Bongcam-Rudloff, E., Borrebaeck, C. A., Bourbeillon, J., Bradbury, A. R., de Daruvar, A., Dubel, S., Frank, R., Gibson, T. J., Gold, L., Haslam, N., Herberg, F. W., Hiltke, T., Hoheisel, J. D., Kerrien, S., Koegl, M., Konthur, Z., Korn, B., Landegren, U., Montecchi-Palazzi, L., Palcy, S., Rodriguez, H., Schweinsberg, S., Sievert, V., Stoevesandt, O., Taussig, M. J., Ueffing, M., Uhlen, M., van der Maarel, S., Wingren, C., Woollard, P., Sherman, D. J., and Hermjakob, H. (2010) A community standard format for the representation of protein affinity reagents. Mol. Cell. Proteomics 9, 1-10
7. Schofield, D. J., Pope, A. R., Clementel, V., Buckell, J., Chapple, S., Clarke, K. F., Conquer, J. S., Crofts, A. M., Crowther, S. R., Dyson, M. R., Flack, G., Griffin, G. J., Hooks, Y., Howat, W. J., Kolb-Kokocinski, A., Kunze, S., Martin, C. D., Maslen, G. L., Mitchell, J. N., O'Sullivan, M., Perera, R. L., Roake, W., Shadbolt, S. P., Vincent, K. J., Warford, A., Wilson, W. E., Xie, J., Young, J. L., and McCafferty, J. (2007) Application of phage display to high throughput antibody generation and characterization. Genome Biol. 8, R254
8. Turunen, L., Takkinen, K., Soderlund, H., and Pulli, T. (2009) Automated panning and screening procedure on microplates for antibody generation from phage display libraries. J. Biomol. Screen. 14, 282-293
9. Pershad, K., Pavlovic, J. D., Graslund, S., Nilsson, P., Colwill, K., Karatt-Vellatt, A., Schofield, D. J., Dyson, M. R., Pawson, T., Kay, B. K., and McCafferty, J. (2010) Generating a panel of highly specific antibodies to 20 human SH2 domains by phage display. Protein Eng. Des. Sel. 23, 279-288
10. Colwill, K., and Graslund, S. (2011) A roadmap to generate renewable protein binders to the human proteome. Nat. Methods 8, 551-558
11. Vaquerizas, J. M., Kummerfeld, S. K., Teichmann, S. A., and Luscombe, N. M. (2009) A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 10, 252-263
12. Spolar, R. S., and Record, M. T., Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science 263, 777-784
13. Frankel, A. D., and Kim, P. S. (1991) Modular structure of transcription factors: implications for gene regulation. Cell 65, 717-719
14. Bradbury, A. R., Sidhu, S., Dubel, S., and McCafferty, J. (2011) Beyond natural antibodies: the power of in vitro display technologies. Nat. Biotechnol. 29, 245-254
15. Persson, H., Ye, W., Wernimont, A., Adams, J. J., Koide, A., Koide, S., Lam, R., and Sidhu, S. S. (2013) CDR-H3 diversity is not required for antigen recognition by synthetic antibodies. J. Mol. Biol. 425, 803-811
16. Koerber, J. T., Thomsen, N. D., Hannigan, B. T., Degrado, W. F., and Wells, J. A. (2013) Nature-inspired design of motif-specific antibody scaffolds. Nat. Biotechnol. 31, 916-921
17. Xiao, R., Anderson, S., Aramini, J., Belote, R., Buchwald, W. A., Ciccosanti, C., Conover, K., Everett, J. K., Hamilton, K., Huang, Y. J., Janjua, H., Jiang, M., Kornhaber, G. J., Lee, D. Y., Locke, J. Y., Ma, L. C., Maglaqui, M., Mao, L., Mitra, S., Patel, D., Rossi, P., Sahdev, S., Sharma, S., Shastry, R., Swapna, G. V., Tong, S. N., Wang, D., Wang, H., Zhao, L., Montelione, G. T., and Acton, T. B. (2010) The high-throughput protein sample production platform of the Northeast Structural Genomics Consortium. J. Struct. Biol. 172, 21-33
18. Acton, T. B., Xiao, R., Anderson, S., Aramini, J., Buchwald, W. A., Ciccosanti, C., Conover, K., Everett, J., Hamilton, K., Huang, Y. J., Janjua, H., Kornhaber, G., Lau, J., Lee, D. Y., Liu, G., Maglaqui, M., Ma, L., Mao, L., Patel, D., Rossi, P., Sahdev, S., Shastry, R., Swapna, G. V., Tang, Y., Tong, S., Wang, D., Wang, H., Zhao, L., and Montelione, G. T. (2011) Preparation of protein samples for NMR structure, function, and smallmolecule screening studies. Methods Enzymol. 493, 21-60
19. Harrison, S. C. (1991) A structural taxonomy of DNA-binding domains. Nature 353, 715-719
20. Zhang, Y., Werling, U., and Edelmann, W. (2012) SLiCE: a novel bacterial cell extract-based DNA cloning method. Nucleic Acids Res. 40, e55
21. Aslanidis, C., and Pde Jong, P. J. (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res. 18, 6069-6074
22. Keates, T., Cooper, C. D., Savitsky, P., Allerston, C. K., Phillips, C., Hammarstrom, M., Daga, N., Berridge, G., Mahajan, P., Burgess-Brown, N. A., Muller, S., Graslund, S., and Gileadi, O. (2012) Expressing the human proteome for affinity proteomics: optimizing expression of soluble protein domains and in vivo biotinylation. N. Biotechnol. 29, 515-525
23. Structural Genomics, C., China Structural Genomics, C., Northeast Structural Genomics, C., Graslund, S., Nordlund, P., Weigelt, J., Hallberg, B. M., Bray, J., Gileadi, O., Knapp, S., Oppermann, U., Arrowsmith, C., Hui, R., Ming, J., dhe-Paganon, S., Park, H. W., Savchenko, A., Yee, A., Edwards, A., Vincentelli, R., Cambillau, C., Kim, R., Kim, S. H., Rao, Z., Shi, Y., Terwilliger, T. C., Kim, C. Y., Hung, L. W., Waldo, G. S., Peleg, Y., Albeck, S., Unger, T., Dym, O., Prilusky, J., Sussman, J. L., Stevens, R. C., Lesley, S. A., Wilson, I. A., Joachimiak, A., Collart, F., Dementieva, I., Donnelly, M. I., Eschenfeldt, W. H., Kim, Y., Stols, L., Wu, R., Zhou, M., Burley, S. K., Emtage, J. S., Sauder, J. M., Thompson, D., Bain, K., Luz, J., Gheyi, T., Zhang, F., Atwell, S., Almo, S. C., Bonanno, J. B., Fiser, A., Swaminathan, S., Studier, F. W., Chance, M. R., Sali, A., Acton, T. B., Xiao, R., Zhao, L., Ma, L. C., Hunt, J. F., Tong, L., Cunningham, K., Inouye, M., Anderson, S., Janjua, H., Shastry, R., Ho, C. K., Wang, D., Wang, H., Jiang, M., Montelione, G. T., Stuart, D. I., Owens, R. J., Daenke, S., Schutz, A., Heinemann, U., Yokoyama, S., Bussow, K., and Gunsalus, K. C. (2008) Protein production and purification. Nat. Methods 5, 135-146
24. Miersch, S., Li, Z., Hanna, R., McLaughlin, M. E., Hornsby, M., Matsuguchi, T., Paduch, M., Saaf, A., Wells, J., Koide, S., Kossiakoff, A., and Sidhu, S. S. (2015) Scalable high throughput selection from phage-display synthetic antibody libraries. J. Vis. Exp. 95, 51492
25. Yin, G., Garces, E. D., Yang, J., Zhang, J., Tran, C., Steiner, A. R., Roos, C., Bajad, S., Hudak, S., Penta, K., Zawada, J., Pollitt, S., and Murray, C. J. (2012) Aglycosylated antibodies and antibody fragments produced in a scalable in vitro transcription-translation system. MAbs 4, 217-225
26. Paduch, M., Koide, A., Uysal, S., Rizk, S. S., Koide, S., and Kossiakoff, A. A. (2013) Generating conformation-specific synthetic antibodies to trap proteins in selected functional states. Methods 60, 3-14
27. Boder, E. T., and Wittrup, K. D. (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat. Biotechnol. 15, 553-557
28. Weaver-Feldhaus, J. M., Lou, J., Coleman, J. R., Siegel, R. W., Marks, J. D., and Feldhaus, M. J. (2004) Yeast mating for combinatorial Fab library generation and surface display. FEBS Lett. 564, 24-34
29. Kay, B. K., Thai, S., and Volgina, V. V. (2009) High-throughput biotinylation of proteins. Methods Mol. Biol. 498, 185-196
30. Ackerman, M., Levary, D., Tobon, G., Hackel, B., Orcutt, K. D., and Wittrup, K. D. (2009) Highly avid magnetic bead capture: an efficient selection method for de novo protein engineering utilizing yeast surface display. Biotechnol. Prog. 25, 774-783
31. Rakestraw, J. A., Aird, D., Aha, P. M., Baynes, B. M., and Lipovsek, D. (2011) Secretion-and-capture cell-surface display for selection of targetbinding proteins. Protein Eng. Des. Sel. 24, 525-530
32. Koerber, J. T., Hornsby, M. J., and Wells, J. A. (2015) An improved singlechain fab platform for efficient display and recombinant expression. J. Mol. Biol. 427, 576-586
33. Garrard, L. J., Yang, M., O'Connell, M. P., Kelley, R. F., and Henner, D. J. (1991) Fab assembly and enrichment in a monovalent phage display system. Biotechnology 9, 1373-1377
34. Bass, S., Greene, R., and Wells, J. A.(1990) Hormone phage: an enrichment method for variant proteins with altered binding properties. Proteins 8, 309-314
35. Lee, C. V., Sidhu, S. S., and Fuh, G. (2004) Bivalent antibody phage display mimics natural immunoglobulin. J. Immunol. Methods 284, 119-132
36. Los, M., Roodhart, J. M. and Voest, E. E. (2007) Target practice: lessons from phase III trials with bevacizumab and vatalanib in the treatment of advanced colorectal cancer. Oncologist 12, 443-450
37. Schulman, E. S. (2001) Development of a monoclonal anti-immunoglobulin E antibody (omalizumab) for the treatment of allergic respiratory disorders. Am. J. Respir. Crit. Care Med. 164, S6-11
38. Hudis, C. A. (2007) Trastuzumab-mechanism of action and use in clinical practice. N. Engl. J. Med. 357, 39-51
39. Fellouse, F. A., Esaki, K., Birtalan, S., Raptis, D., Cancasci, V. J., Koide, A., Jhurani, P., Vasser, M., Wiesmann, C., Kossiakoff, A. A., Koide, S., and Sidhu, S. S. (2007) High-throughput generation of synthetic antibodies from highly functional minimalist phage-displayed libraries. J. Mol. Biol. 373, 924-940
40. Miller, K. R., Koide, A., Leung, B., Fitzsimmons, J., Yoder, B., Yuan, H., Jay, M., Sidhu, S. S., Koide, S., and Collins, E. J. (2012) T cell receptor-like recognition of tumor in vivo by synthetic antibody fragment. PLoS One 7, e43746
41. Kaneko, T., Huang, H., Cao, X., Li, X., Li, C., Voss, C., Sidhu, S. S., and Li, S. S. (2012) Superbinder SH2 domains act as antagonists of cell signaling. Sci. Signal. 5, ra68
42. Gao, J., Sidhu, S. S., and Wells, J. A. (2009) Two-state selection of conformation-specific antibodies. Proc. Natl. Acad. Sci. U.S.A. 106, 3071-3076
43. Thomsen, N. D., Koerber, J. T., and Wells, J. A. (2013) Structural snapshots reveal distinct mechanisms of procaspase-3 and-7 activation. Proc. Natl. Acad. Sci. U.S.A. 110, 8477-8482
44. Ye, J. D., Tereshko, V., Frederiksen, J. K., Koide, A., Fellouse, F. A., Sidhu, S. S., Koide, S., Kossiakoff, A. A., and Piccirilli, J. A. (2008) Synthetic antibodies for specific recognition and crystallization of structured RNA. Proc. Natl. Acad. Sci. U.S.A. 105, 82-87
45. Schwab, C., and Bosshard, H. R. (1992) Caveats for the use of surfaceadsorbed protein antigen to test the specificity of antibodies. J. Immunol. Methods 147, 125-134
46. Smith, G. P. (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228, 1315-1317
47. Starovasnik, M. A., O'Connell, M. P., Fairbrother, W. J., and Kelley, R. F. (1999) Antibody variable region binding by Staphylococcal protein A: thermodynamic analysis and location of the Fv binding site on E-domain. Protein Sci. 8, 1423-1431
48. Niesen, F. H., Berglund, H., and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2, 2212-2221
49. Hotzel, I., Theil, F. P., Bernstein, L. J., Prabhu, S., Deng, R., Quintana, L., Lutman, J., Sibia, R., Chan, P., Bumbaca, D., Fielder, P., Carter, P. J., and Kelley, R. F. (2012) A strategy for risk mitigation of antibodies with fast clearance. MAbs 4, 753-760
50. Nishikori, S., Hattori, T., Fuchs, S. M., Yasui, N., Wojcik, J., Koide, A., Strahl, B. D., and Koide, S. (2012) Broad ranges of affinity and specificity of antihistone antibodies revealed by a quantitative peptide immunoprecipitation assay. J. Mol. Biol. 424, 391-399
51. Lamboy, J. A., Arter, J. A., Knopp, K. A., Der, D., Overstreet, C. M., Palermo, E. F., Urakami, H., Yu, T. B., Tezgel, O., Tew, G. N., Guan, Z., Kuroda, K., and Weiss, G. A. (2009) Phage wrapping with cationic polymers eliminates nonspecific binding between M13 phage and high pI target proteins. J. Am. Chem. Soc. 131, 16454-16460
52. Reich, N. C. (2013) STATs get their move on. JAKSTAT 2, e27080
53. Marcon, E., Jain, H., Bhattacharya, A., Guo, H., Phanse, S., Pu, S., Byram, G., Collins, B. C., Dowdell, E., Fenner, M., Guo, X., Hutchinson, A., Kennedy, J. J., Krastins, B., Larsen, B., Lin, Z. Y., Lopez, M. F., Loppnau, P., Miersch, S., Nguyen, T., Olsen, J. B., Paduch, M., Ravichandran, M., Seitova, A., Vadali, G., Vogelsang, M. S., Whiteaker, J. R., Zhong, G., Zhong, N., Zhao, L., Aebersold, R., Arrowsmith, C. H., Emili, A., Frappier, L., Gingras, A. C., Gstaiger, M., Paulovich, A. G., Koide, S., Kossiakoff, A. A., Sidhu, S. S., Wodak, S. J., Graslund, S., Greenblatt, J. F., and Edwards, A. M. (2015) Assessment of a method to characterize antibody selectivity and specificity for use in immunoprecipitation. Nat. Methods 12, 725-731
54. Uhlen, M., Oksvold, P., Fagerberg, L., Lundberg, E., Jonasson, K., Forsberg, M., Zwahlen, M., Kampf, C., Wester, K., Hober, S., Wernerus, H., Bjorling, L., and Ponten, F. (2010) Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 28, 1248-1250
55. Hober, S., and Uhlen, M. (2008) Human protein atlas and the use of microarray technologies. Curr. Opin. Biotechnol. 19, 30-35
56. Mersmann, M., Meier, D., Mersmann, J., Helmsing, S., Nilsson, P., Graslund, S., Colwill, K., Hust, M., and Dubel, S. (2010) Towards proteome scale antibody selections using phage display. N. Biotechnol. 27, 118-128
57. Lipman, N. S., Jackson, L. R., Trudel, L. J., and Weis-Garcia, F. (2005) Monoclonal versus polyclonal antibodies: distinguishing characteristics, applications, and information resources. ILAR J. 46, 258-268
58. Konthur, Z., Hust, M., and Dubel, S. (2005) Perspectives for systematic in vitro antibody generation. Gene, 364, 19-29
59. Kehoe, J. W., Velappan, N., Walbolt, M., Rasmussen, J., King, D., Lou, J., Knopp, K., Pavlik, P., Marks, J. D., Bertozzi, C. R., and Bradbury, A. R. (2006) Using phage display to select antibodies recognizing post-translational modifications independently of sequence context. Mol. Cell. Proteomics 5, 2350-2363
60. Kierny, M. R., Cunningham, T. D., and Kay, B. K. (2012) Detection of biomarkers using recombinant antibodies coupled to nanostructured platforms. Nano Rev. 3, online only
61. Schilling, J., Schoppe, J., and Pluckthun, A. (2014) From DARPins to LoopDARPins: novel LoopDARPin design allows the selection of low picomolar binders in a single round of ribosome display. J. Mol. Biol. 426, 691-721
62. Elsliger, M. A., Deacon, A. M., Godzik, A., Lesley, S. A., Wooley, J., Wuthrich, K., and Wilson, I. A. (2010) The JCSG high-throughput structural biology pipeline. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 1137-1142
63. Letunic, I., Doerks, T., and Bork, P. (2015) SMART: recent updates, new developments, and status in 2015. Nucleic Acids Res. 43, D257-D260
64. Katoh, K., and Standley, D. M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780
65. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., and Barton, G. J. (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191
66. Zhang, H., Gao, S., Lercher, M. J., Hu, S., and Chen, W. H. (2012) EvolView, an online tool for visualizing, annotating, and managing phylogenetic trees. Nucleic Acids Res. 40, W569-W572.