Bridging disulfides for stable and defined antibody drug conjugates

Bioconjugate Chemistry

Volumn 25, Issue 6, 2014, Pages 1124-1136

  Badescu, George ^a   Bryant, Penny ^a   Bird, Matthew ^a   Henseleit, Korinna ^a   Swierkosz, Julia ^a   Parekh, Vimal ^a   Tommasi, Rita ^a   Pawlisz, Estera ^a   Jurlewicz, Kosma ^a   Farys, Monika ^a   Camper, Nicolas ^a   Sheng, Xiaobo ^a   Fisher, Martin ^a   Grygorash, Ruslan ^a   Kyle, Andrew ^a   Abhilash, Amrita ^a   Frigerio, Mark ^a   Edwards, Jeff ^a   Godwin, Antony ^a  

^a Antitope Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS; CHEMICAL REACTIONS; COVALENT BONDS; SULFUR COMPOUNDS;

ANTIBODY-DRUG CONJUGATES; ANTIBODY-FRAGMENT; ANTIGEN BINDING; CELL KILLING; DISULPHIDE BONDS; IN-VITRO; PROTEOLYTIC DIGESTION; SITE-SPECIFIC; SULPHUR ATOMS; TRASTUZUMAB;

MONOCLONAL ANTIBODIES;

DISULFIDE; DRUG ANTIBODY; TRASTUZUMAB; VEDOTIN; ANTINEOPLASTIC AGENT; MONOCLONAL ANTIBODY; OLIGOPEPTIDE;

ARTICLE; CELL KILLING; CONJUGATE; CONJUGATION; DISULFIDE BOND; HUMAN; HUMAN CELL; IN VITRO STUDY; PROTEIN DEGRADATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; MCF 7 CELL LINE; STRUCTURE ACTIVITY RELATION; SYNTHESIS; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DISULFIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; MCF-7 CELLS; MOLECULAR STRUCTURE; OLIGOPEPTIDES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84902660348     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc500148x     Document Type: Article

References (40)

1. Lewis Phillips, G. D., Li, G., Dugger, D. L., Crocker, L. M., Parsons, K. L., Mai, E., Blättler, W. a, Lambert, J. M., Chari, R. V. J., Lutz, R. J., Wong, W. L. T., Jacobson, F. S., Koeppen, H., Schwall, R. H., Kenkare-Mitra, S. R., Spencer, S. D., and Sliwkowski, M. X. (2008) Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody-cytotoxic drug conjugate Cancer Res. 68, 9280-90
2. Wang, L., Amphlett, G., Blättler, W. A., Lambert, J. M., and Zhang, W. (2005) Structural characterization of the maytansinoid-monoclonal antibody immunoconjugate, huN901-DM1, by mass spectrometry Protein Sci. 14, 2436-46
3. Toki, B. E., Cerveny, C. G., Wahl, A. F., and Senter, P. D. (2002) Protease-mediated fragmentation of p-amidobenzyl ethers: a new strategy for the activation of anticancer prodrugs J. Org. Chem. 67, 1866-72
4. Sun, M. M. C., Beam, K. S., Cerveny, C. G., Hamblett, K. J., Blackmore, R. S., Torgov, M. Y., Handley, F. G. M., Ihle, N. C., Senter, P. D., and Alley, S. C. (2005) Reduction-alkylation strategies for the modification of specific monoclonal antibody disulfides Bioconjugate Chem. 16, 1282-90
5. Doronina, S. O., Toki, B. E., Torgov, M. Y., Mendelsohn, B. a, Cerveny, C. G., Chace, D. F., DeBlanc, R. L., Gearing, R. P., Bovee, T. D., Siegall, C. B., Francisco, J. a, Wahl, A. F., Meyer, D. L., and Senter, P. D. (2003) Development of potent monoclonal antibody auristatin conjugates for cancer therapy Nat. Biotechnol. 21, 778-84
6. Hamblett, K. J., Senter, P. D., Chace, D. F., Sun, M. M. C., Lenox, J., Cerveny, C. G., Kissler, K. M., Bernhardt, S. X., Kopcha, A. K., Zabinski, R. F., Meyer, D. L., and Francisco, J. a. (2004) Effects of drug loading on the antitumor activity of a monoclonal antibody drug conjugate Clin. Cancer Res. 10, 7063-70
7. Alley, S. C., Okeley, N. M., and Senter, P. D. (2010) Antibody-drug conjugates: targeted drug delivery for cancer Curr. Opin. Chem. Biol. 14, 529-37
8. Baldwin, A. D. and Kiick, K. L. (2011) Tunable degradation of maleimide-thiol adducts in reducing environments Bioconjugate Chem. 22, 1946-53
9. Shen, B.-Q., Xu, K., Liu, L., Raab, H., Bhakta, S., Kenrick, M., Parsons-Reponte, K. L., Tien, J., Yu, S.-F., Mai, E., Li, D., Tibbitts, J., Baudys, J., Saad, O. M., Scales, S. J., McDonald, P. J., Hass, P. E., Eigenbrot, C., Nguyen, T., Solis, W. a, Fuji, R. N., Flagella, K. M., Patel, D., Spencer, S. D., Khawli, L. a, Ebens, A., Wong, W. L., Vandlen, R., Kaur, S., Sliwkowski, M. X., Scheller, R. H., Polakis, P., and Junutula, J. R. (2012) Conjugation site modulates the in vivo stability and therapeutic activity of antibody-drug conjugates Nat. Biotechnol. 30, 184-9
10. Junutula, J. R., Raab, H., Clark, S., Bhakta, S., Leipold, D. D., Weir, S., Chen, Y., Simpson, M., Tsai, S. P., Dennis, M. S., Lu, Y., Meng, Y. G., Ng, C., Yang, J., Lee, C. C., Duenas, E., Gorrell, J., Katta, V., Kim, A., McDorman, K., Flagella, K., Venook, R., Ross, S., Spencer, S. D., Lee Wong, W., Lowman, H. B., Vandlen, R., Sliwkowski, M. X., Scheller, R. H., Polakis, P., and Mallet, W. (2008) Site-specific conjugation of a cytotoxic drug to an antibody improves the therapeutic index Nat. Biotechnol. 26, 925-32
11. Junutula, J. R., Flagella, K. M., Graham, R. a, Parsons, K. L., Ha, E., Raab, H., Bhakta, S., Nguyen, T., Dugger, D. L., Li, G., Mai, E., Lewis Phillips, G. D., Hiraragi, H., Fuji, R. N., Tibbitts, J., Vandlen, R., Spencer, S. D., Scheller, R. H., Polakis, P., and Sliwkowski, M. X. (2010) Engineered thio-trastuzumab-DM1 conjugate with an improved therapeutic index to target human epidermal growth factor receptor 2-positive breast cancer Clin. Cancer Res. 16, 4769-78
12. Gomez, N., Ouyang, J., Nguyen, M. D. H., Vinson, A. R., Lin, A. a, and Yuk, I. H. (2010) Effect of temperature, pH, dissolved oxygen, and hydrolysate on the formation of triple light chain antibodies in cell culture Biotechnol. Prog. 26, 1438-45
13. Gomez, N., Vinson, A. R., Ouyang, J., Nguyen, M. D. H., Chen, X.-N., Sharma, V. K., and Yuk, I. H. (2010) Triple light chain antibodies: factors that influence its formation in cell culture Biotechnol. Bioeng. 105, 748-60
14. Axup, J. Y., Bajjuri, K. M., Ritland, M., Hutchins, B. M., Kim, C. H., Kazane, S. a, Halder, R., Forsyth, J. S., Santidrian, A. F., Stafin, K., Lu, Y., Tran, H., Seller, A. J., Biroc, S. L., Szydlik, A., Pinkstaff, J. K., Tian, F., Sinha, S. C., Felding-Habermann, B., Smider, V. V., and Schultz, P. G. (2012) Synthesis of site-specific antibody-drug conjugates using unnatural amino acids Proc. Natl. Acad. Sci. U. S. A. 109, 16101-6
15. Kiick, K. L., Saxon, E., Tirrell, D. a, and Bertozzi, C. R. (2002) Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation Proc. Natl. Acad. Sci. U. S. A. 99, 19-24
16. Del Rosario, R. B., Wahl, R. L., Brocchini, S. J., Lawton, R. G., and Smith, R. H. Sulfhydryl site-specific cross-linking and labeling of monoclonal antibodies by a fluorescent equilibrium transfer alkylation cross-link reagent. Bioconjugate Chem. 1, 51-9.
17. Khalili, H., Godwin, A., Choi, J., Lever, R., and Brocchini, S. (2012) Comparative binding of disulfide-bridged PEG-Fabs Bioconjugate Chem. 23, 2262-77
18. Balan, S., Choi, J.-W., Godwin, A., Teo, I., Laborde, C. M., Heidelberger, S., Zloh, M., Shaunak, S., and Brocchini, S. (2007) Site-specific PEGylation of protein disulfide bonds using a three-carbon bridge Bioconjugate Chem. 18, 61-76
19. Brocchini, S., Balan, S., Godwin, A., Choi, J.-W., Zloh, M., and Shaunak, S. (2006) PEGylation of native disulfide bonds in proteins Nat. Protoc. 1, 2241-52
20. Zloh, M., Shaunak, S., Balan, S., and Brocchini, S. (2007) Identification and insertion of 3-carbon bridges in protein disulfide bonds: a computational approach Nat. Protoc. 2, 1070-83
21. Willner, D., Trail, P. A., Hofstead, S. J., King, H. D., Lasch, S. J., Braslawsky, G. R., Greenfield, R. S., Kaneko, T., and Firestone, R. A. (1993) (6-Maleimidocaproyl)hydrazone of doxorubicin-a new derivative for the preparation of immunoconjugates of doxorubicin Bioconjugate Chem. 4, 521-527
22. Pitot, H. C., McElroy, E. A., Reid, J. M., Windebank, A. J., Sloan, J. A., Erlichman, C., Bagniewski, P. G., Walker, D. L., Rubin, J., Goldberg, R. M., Adjei, A. A., and Ames, M. M. (1999) Phase I trial of dolastatin-10 (NSC 376128) in patients with advanced solid tumors Clin. Cancer Res. 5, 525-31
23. Madden, T., Tran, H. T., Beck, D., Huie, R., Newman, R. A., Pusztai, L., Wright, J. J., and Abbruzzese, J. L. (2000) Novel marine-derived anticancer agents: a phase I clinical, pharmacological, and pharmacodynamic study of dolastatin 10 (NSC 376128) in patients with advanced solid tumors Clin. Cancer Res. 6, 1293-301
24. Ravry, M. J., Omura, G. A., and Birch, R. (1985) Phase II evaluation of maytansine (NSC 153858) in advanced cancer. A Southeastern Cancer Study Group trial Am. J. Clin. Oncol. 8, 148-50
25. Thigpen, J. T., Ehrlich, C. E., Conroy, J., and Blessing, J. A. (1983) Phase II study of maytansine in the treatment of advanced or recurrent squamous cell carcinoma of the cervix. A Gynecologic Oncology Group study Am. J. Clin. Oncol. 6, 427-30
26. Ratanatharathorn, V., Gad-el-Mawla, N., Wilson, H. E., Bonnet, J. D., Rivkin, S. E., and Mass, R. (1982) Phase II evaluation of maytansine in refractory non-Hodgkin's lymphoma: a Southwest Oncology Group study Cancer Treat. Rep. 66, 1687-8
27. Pro, B., Advani, R., Brice, P., Bartlett, N. L., Rosenblatt, J. D., Illidge, T., Matous, J., Ramchandren, R., Fanale, M., Connors, J. M., Yang, Y., Sievers, E. L., Kennedy, D. A., and Shustov, A. (2012) Brentuximab vedotin (SGN-35) in patients with relapsed or refractory systemic anaplastic large-cell lymphoma: results of a phase II study J. Clin. Oncol. 30, 2190-6
28. Younes, A., Gopal, A. K., Smith, S. E., Ansell, S. M., Rosenblatt, J. D., Savage, K. J., Ramchandren, R., Bartlett, N. L., Cheson, B. D., de Vos, S., Forero-Torres, A., Moskowitz, C. H., Connors, J. M., Engert, A., Larsen, E. K., Kennedy, D. a, Sievers, E. L., and Chen, R. (2012) Results of a pivotal phase II study of brentuximab vedotin for patients with relapsed or refractory Hodgkin's lymphoma J. Clin. Oncol. 30, 2183-9
29. Verma, S., Miles, D., Gianni, L., Krop, I. E., Welslau, M., Baselga, J., Pegram, M., Oh, D.-Y., Diéras, V., Guardino, E., Fang, L., Lu, M. W., Olsen, S., and Blackwell, K. (2012) Trastuzumab emtansine for HER2-positive advanced breast cancer N. Engl. J. Med. 367, 1783-91
30. King, H. D., Yurgaitis, D., Willner, D., Firestone, R. A., Yang, M. B., Lasch, S. J., Hellström, K. E., and Trail, P. A. (1999) Monoclonal antibody conjugates of doxorubicin prepared with branched linkers: A novel method for increasing the potency of doxorubicin immunoconjugates Bioconjugate Chem. 10, 279-88
31. Francisco, J. a, Cerveny, C. G., Meyer, D. L., Mixan, B. J., Klussman, K., Chace, D. F., Rejniak, S. X., Gordon, K. a, DeBlanc, R., Toki, B. E., Law, C.-L., Doronina, S. O., Siegall, C. B., Senter, P. D., and Wahl, A. F. (2003) cAC10-vcMMAE, an anti-CD30-monomethyl auristatin E conjugate with potent and selective antitumor activity Blood 102, 1458-65
32. Schmidt, M. M. and Wittrup, K. D. (2009) A modeling analysis of the effects of molecular size and binding affinity on tumor targeting Mol. Cancer Ther. 8, 2861-71
33. Kim, K. M., Charlotte, F., McDonagh, C. F., Westendorf, L., Brown, L. L., Sussman, D., Feist, T., Lyon, R., Alley, S. C., Okeley, N. M., Zhang, X., Thompson, M. C., Stone, I., Gerber, H. P., and Carter, P. J. (2008) Anti-CD30 diabody-drug conjugates with potent antitumor activity Mol. Cancer Ther. 7, 2486-97
34. Wu, A. M. and Senter, P. D. (2005) Arming antibodies: prospects and challenges for immunoconjugates Nat. Biotechnol. 23, 1137-1146
35. Li, L., Crow, D., Turatti, F., Bading, J. R., Anderson, A. L., Poku, E., Yazaki, P. J., Carmichael, J., Leong, D., Wheatcroft, M. P., Raubitschek, A. A., Hudson, P. J., Colcher, D., and Shively, J. E. (2011) Site-specific conjugation of monodispersed DOTA-PEGn to a thiolated diabody reveals the effect of increasing PEG size on kidney clearance and tumor uptake with improved 64-copper PET imaging Bioconjugate Chem. 22, 709-716
36. Rudnick, S. I., Lou, J., Shaller, C. C., Tang, Y., Klein-Szanto, A. J. P., Weiner, L. M., Marks, J. D., and Adams, G. P. (2011) Influence of affinity and antigen internalization on the uptake and penetration of Anti-HER2 antibodies in solid tumors Cancer Res. 71, 2250-9
37. Pacchiana, G., Chiriaco, C., Stella, M. C., Petronzelli, F., De Santis, R., Galluzzo, M., Carminati, P., Comoglio, P. M., Michieli, P., and Vigna, E. (2010) Monovalency unleashes the full therapeutic potential of the DN-30 anti-Met antibody J. Biol. Chem. 285, 36149-57
38. Farys, M., Ginn, C., Badescu, G., Peciak, K., Pawlisz, E., Khalili, H., and Brocchini, S. (2013) Chemical and Genetic Modification, in Biological Drug Products: Development and Strategies (Wang, W. and Singh, M., Eds.) pp 233-284, Wiley.
39. Pasut, G. and Veronese, F. M. (2012) State of the art in PEGylation: the great versatility achieved after forty years of research J. Controlled Release 161, 461-72
40. Merchant, M., Ma, X., Maun, H. R., Zheng, Z., Peng, J., Romero, M., Huang, A., Yang, N. Y., Nishimura, M., Greve, J., Santell, L., Zhang, Y. W., Su, Y., Kaufman, D. W., Billeci, K. L., Mai, E., Moffat, B., Lim, A., Duenas, E. T., Phillips, H. S., Xiang, H., Young, J. C., Vande Woude, G. F., Dennis, M. S., Reilly, D. E., Schwall, R. H., Starovasnik, M. A., Lazarus, R. A., and Yansura, D. G. (2013) Monovalent antibody design and mechanism of action of onartuzumab, a MET antagonist with anti-tumor activity as a therapeutic agent Proc. Natl. Acad. Sci. U. S. A. 110, E2987-E2996