Bispecific antibodies and antibody-drug conjugates (ADCs) bridging HER2 and prolactin receptor improve efficacy of HER2 ADCs

Molecular Cancer Therapeutics

Volumn 16, Issue 4, 2017, Pages 681-693

  Andreev, Julian ^a   Thambi, Nithya ^a   Perez Bay, Andres E ^a   Delfino, Frank ^a   Martin, Joel ^a   Kelly, Marcus P ^a   Kirshner, Jessica R ^a   Rafique, Ashique ^a   Kunz, Arthur ^a   Nittoli, Thomas ^a   MacDonald, Douglas ^a   Daly, Christopher ^a   Olson, William ^a   Thurston, Gavin ^a  

^a REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY DRUG CONJUGATE; BISPECIFIC ANTIBODY; CELL SURFACE RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HUMAN MONOCLONAL ANTIBODY; PROLACTIN RECEPTOR; PROLACTIN RECEPTOR ANTIBODY; TRASTUZUMAB EMTANSINE; UNCLASSIFIED DRUG; ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; ERBB2 PROTEIN, HUMAN; MAYTANSINE; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER CELL LINE; CELL KILLING; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; DRUG CONJUGATION; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG TARGETING; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; COMPARATIVE STUDY; DRUG EFFECTS; DRUG POTENTIATION; FEMALE; METABOLISM; PROTEIN TRANSPORT; TUMOR CELL LINE;

ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DRUG SYNERGISM; FEMALE; HUMANS; IMMUNOCONJUGATES; MAYTANSINE; PROTEIN TRANSPORT; RECEPTOR, ERBB-2; RECEPTORS, PROLACTIN;

EID: 85016980262     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-16-0658     Document Type: Article

References (48)

1. American Cancer Society. Cancer facts & figures 2015. Atlanta, GA: American Cancer Society; 2015.
2. Chari RVJ, Miller ML, Widdison WC. Antibody-drug conjugates: an emerging concept in cancer therapy. Angewandte Chemie International Edition 2014;53:3796-827.
3. Sievers EL, Senter PD. Antibody-drug conjugates in cancer therapy. Ann Rev Med 2013;64:15-29.
4. Bander NH. Antibody-drug conjugate target selection: critical factors. Met Mol Biol 2013;1045:29-40.
5. Burris HA 3rd, Rugo HS, Vukelja SJ, Vogel CL, Borson RA, Limentani S, et al. Phase II study of the antibody drug conjugate trastuzumab-DM1 for the treatment of human epidermal growth factor receptor 2 (HER2)-positive breast cancer after prior HER2-directed therapy. J Clin Oncol 2011;29:398-405.
6. Krop IE, LoRusso P, Miller KD, Modi S, Yardley D, Rodriguez G, et al. A phase II study of trastuzumab emtansine in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer who were previously treated with trastuzumab, lapatinib, an anthracycline, a taxane, and capecitabine. J Clin Oncol 2012;30:3234-41.
7. Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol 2013;31:3997-4013.
8. Owens MA, Horten BC, Da Silva MM. HER2 amplification ratios by fluorescence in situ hybridization and correlation with immunohistochemistry in a cohort of 6556 breast cancer tissues. Clin Breast Cancer 2004;5:63-9.
9. Press MF, Sauter G, Bernstein L, Villalobos IE, Mirlacher M, Zhou JY, et al. Diagnostic evaluation of HER-2 as a molecular target: an assessment of accuracy and reproducibility of laboratory testing in large, prospective, randomized clinical trials. Clin Cancer Res 2005;11:6598-607.
10. Faupel-Badger JM, Duggan MA, Sherman ME, Garcia-Closas M, Yang XR, Lissowska J, et al. Prolactin receptor expression and breast cancer: relationships with tumor characteristics among pre- and post-menopausal women in a population-based case-control study from Poland. Horm Cancer 2014;5:42-50.
11. Galsgaard ED, Rasmussen BB, Folkesson CG, Rasmussen LM, Berchtold MW, Christensen L, et al. Re-evaluation of the prolactin receptor expression in human breast cancer. J Endocrinol 2009;201:115-28.
12. Goffin V, Touraine P. The prolactin receptor as a therapeutic target in human diseases: browsing new potential indications. Expert Opinion Ther Targets 2015;19:1229-44.
13. Damiano JS, Wasserman E. Molecular pathways: blockade of the PRLR signaling pathway as a novel antihormonal approach for the treatment of breast and prostate cancer. Clin Cancer Res 2013;19:1644-50.
14. Sorkin A, Goh LK. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 2008;314:3093-106.
15. Austin CD, De Maziere AM, Pisacane PI, van Dijk SM, Eigenbrot C, Sliwkowski MX, et al. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin. Mol Biol Cell 2004;15:5268-82.
16. Macdonald LE, Karow M, Stevens S, Auerbach W, Poueymirou WT, Yasenchak J, et al. Precise and in situ genetic humanization of 6 Mb of mouse immunoglobulin genes. Proc Nat Acad Sci U S A 2014;111: 5147-52.
17. Murphy AJ, Macdonald LE, Stevens S, Karow M, Dore AT, Pobursky K, et al. Mice with megabase humanization of their immunoglobulin genes generate antibodies as efficiently as normal mice. Proc Nat Acad Sci U S A 2014;111:5153-8.
18. Carter P, Presta L, Gorman CM, Ridgway JB, Henner D, Wong WL, et al. Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc Nat Acad Sci U S A 1992;89:4285-9.
19. Carter PJ, Presta LG. Immunoglobulin variants. Google Patents, assignee; 1998.
20. Merchant AM, Zhu Z, Yuan JQ, Goddard A, Adams CW, Presta LG, et al. An efficient route to human bispecific IgG. Nat Biotechnology 1998;16: 677-81.
21. McWhirter J, MacDonald L, Stevens S, Davis S, Buckler DR, Hosiawa KA, et al. Humanized universal light chain mice. Google Patents; 2013.
22. Smith EJ, Olson K, Haber LJ, Varghese B, Duramad P, Tustian AD, et al. A novel, native-format bispecific antibody triggering T-cell killing of B-cells is robustly active in mouse tumor models and cynomolgus monkeys. Sci Rep 2015;5:17943.
23. Schneider-Poetsch T, Ju J, Eyler DE, Dang Y, Bhat S, Merrick WC, et al. Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat Chem Biol 2010;6:209-17.
24. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 1991;266:17707-12.
25. Slater AFG. Chloroquine: mechanism of drug action and resistance in plasmodium falciparum. Pharmacol Ther 1993;57:203-35.
26. Grinde B. Effect of carboxylic ionophores on lysosomal protein degradation in rat hepatocytes. Experimental Cell Res 1983;149:27-35.
27. Boccadoro M, Morgan G, Cavenagh J. Preclinical evaluation of the proteasome inhibitor bortezomib in cancer therapy. Cancer Cell Int 2005;5:18.
28. Fenteany G, Schreiber SL. Lactacystin, proteasome function, and cell fate. J Biol Chem 1998;273:8545-8.
29. Chan GKY, Kleinheinz TL, Peterson D, Moffat JG. A simple high-content cell cycle assay reveals frequent discrepancies between cell number and ATP and MTS proliferation assays. PLoS ONE 2013;8:e63583.
30. Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, et al. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 1999; 274:25543-9.
31. Dunn KW, Kamocka MM, McDonald JH. A practical guide to evaluating colocalization in biological microscopy. Am J Physiol Cell Physiol 2011; 300:C723-42.
32. Varghese B, Barriere H, Carbone CJ, Banerjee A, Swaminathan G, Plotnikov A, et al. Polyubiquitination of prolactin receptor stimulates its internalization, postinternalization sorting, and degradation via the lysosomal pathway. Mol Cell Biol 2008;28:5275-87.
33. Piazza TM, Lu JC, Carver KC, Schuler LA. SRC family kinases accelerate prolactin receptor internalization, modulating trafficking and signaling in breast cancer cells. Mol Endocrinol 2009;23:202-12.
34. Lu JC, Scott P, Strous GJ, Schuler LA. Multiple internalization motifs differentially used by prolactin receptor isoforms mediate similar endocytic pathways. Mol Endocrinol 2002;16:2515-27.
35. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004;5:121-32
36. Ogawa M, Kosaka N, Regino CA, Mitsunaga M, Choyke PL, Kobayashi H. High sensitivity detection of cancer in vivo using a dual-controlled activation fluorescent imaging probe based on H-dimer formation and pH activation. Mol BioSystems 2010;6:888-93.
37. Li John Y, Perry Samuel R, Muniz-Medina V, Wang X, Wetzel Leslie K, Rebelatto Marlon C, et al. A biparatopic HER2-targeting antibody-drug conjugate induces tumor regression in primary models refractory to or ineligible for HER2-targeted therapy. Cancer Cell 2016;29:117-29.
38. Bien-Ly N, Yu YJ, Bumbaca D, Elstrott J, Boswell CA, Zhang Y, et al. Transferrin receptor (TfR) trafficking determines brain uptake of TfR antibody affinity variants. J Exp Med 2014;211:233-44.
39. St. Pierre CA, Leonard D, Corvera S, Kurt-Jones EA, Finberg RW. Antibodies to cell surface proteins redirect intracellular trafficking pathways. Exp Mol Pathol 2011;91:723-32.
40. Ben-Kasus T, Schechter B, Lavi S, Yarden Y, Sela M. Persistent elimination of ErbB-2/HER2-overexpressing tumors using combinations of monoclonal antibodies: relevance of receptor endocytosis. Proc Nat Acad Sci U S A 2009;106:3294-9.
41. Rock BM, Tometsko ME, Patel SK, Hamblett KJ, Fanslow WC, Rock DA. Intracellular catabolism of an antibody drug conjugate with a noncleavable linker. Drug Metab Dispos 2015;43:1341-4.
42. Leal M, Sapra P, Hurvitz SA, Senter P, Wahl A, Schutten M, et al. Antibody-drug conjugates: an emerging modality for the treatment of cancer. Ann NY Acad Sci 2014;1321:41-54.
43. Ritchie M, Tchistiakova L, Scott N. Implications of receptor-mediated endocytosis and intracellular trafficking dynamics in the development of antibody drug conjugates. mAbs 2013;5:13-21.
44. de Goeij BE, Satijn D, Freitag CM, Wubbolts R, Bleeker WK, Khasanov A, et al. High turnover of tissue factor enables efficient intracellular delivery of antibody-drug conjugates. Mol Cancer Ther 2015;14: 1130-40.
45. Breij EC, de Goeij BE, Verploegen S, Schuurhuis DH, Amirkhosravi A, Francis J, et al. An antibody-drug conjugate that targets tissue factor exhibits potent therapeutic activity against a broad range of solid tumors. Cancer Res 2014;74:1214-26.
46. Brack S, Attinger-Toller I, Schade B, Mourlane F, Klupsch K, Woods R, et al. A bispecific HER2-targeting FynomAb with superior antitumor activity and novel mode of action. Mol Cancer Ther 2014;13: 2030-9.
47. de Goeij BE, Vink T, Ten Napel H, Breij EC, Satijn D, Wubbolts R, et al. Efficient payload delivery by a bispecific antibody-drug conjugate targeting HER2 and CD63. Mol Cancer Ther 2016;15:2688-97
48. Kontermann RE. Dual targeting strategies with bispecific antibodies. mAbs 2012;4:182-97.