Antibody-drug conjugates for cancer therapy

Biomedicines

Volumn 4, Issue 3, 2016, Pages

  Parslow, Adam C ^a   Parakh, Sagun ^a,b   Lee, Fook Thean ^a   Gan, Hui K ^a,b,c   Scott, Andrew M ^a,b,c  

^a OLIVIA NEWTON JOHN CANCER RESEARCH INSTITUTE   (Australia)

^b AUSTIN HEALTH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

ADC; Antibody drug conjugate; Cancer; Immunotherapy; Monoclonal antibodies; Resistance

Indexed keywords

EID: 85024088872     PISSN: None     EISSN: 22279059     Source Type: Journal    
DOI: 10.3390/biomedicines4030014     Document Type: Review

References (98)

1. Schwartz, R.S. Paul Ehrlich's magic bullets. N. Engl. J. Med. 2004, 350, 1079-1080
2. Scott, A.M.;Wolchok, J.D.; Old, L.J. Antibody therapy of cancer. Nat. Rev. Cancer 2012, 12, 278-287
3. Shuptrine, C.W.; Surana, R.; Weiner, L.M. Monoclonal antibodies for the treatment of cancer. Semin. Cancer Biol. 2012, 22, 3-13
4. Kubota, T.; Niwa, R.; Satoh, M.; Akinaga, S.; Shitara, K.; Hanai, N. Engineered therapeutic antibodies with improved effector functions. Cancer Sci. 2009, 100, 1566-1572
5. Sievers, E.L.; Senter, P.D. Antibody-Drug Conjugates in Cancer Therapy. Annu. Rev. Med. 2013, 64, 15-29
6. Panowksi, S.; Bhakta, S.; Raab, H.; Polakis, P.; Junutula, J.R. Site-specific antibody drug conjugates for cancer therapy. mAbs 2014, 6, 34-45
7. Jaracz, S.; Chen, J.; Kuznetsova, L.V.; Ojima, I. Recent advances in tumor-targeting anticancer drug conjugates. Bioorg. Med. Chem. 2005, 13, 5043-5054
8. Chari, R.V.J. Targeted Cancer Therapy: Conferring Specificity to Cytotoxic Drugs. Acc. Chem. Res. 2008, 41, 98-107
9. Shefet-Carasso, L.; Benhar, I. Antibody-targeted drugs and drug resistance-Challenges and solutions. Drug Resist. Updates 2015, 18, 36-46
10. Parakh, S.; Parslow, A.C.; Gan, H.K.; Scott, A.M. Antibody-mediated delivery of therapeutics for cancer therapy. Expert Opin. Drug Deliv. 2016, 13, 401-419
11. Teicher, B.A.; Chari, R.V.J. Antibody Conjugate Therapeutics: Challenges and Potential. Clin. Cancer Res. 2011, 17, 6389-6397
12. Flygare, J.A.; Pillow, T.H.; Aristoff, P. Antibody-Drug Conjugates for the Treatment of Cancer. Chem. Biol. Drug Des. 2013, 81, 113-121
13. Senter, P.D. Potent antibody drug conjugates for cancer therapy. Curr. Opin. Chem. Biol. 2009, 13, 235-244
14. Sochaj, A.M.; Swiderska, K.W.; Otlewski, J. Current methods for the synthesis of homogeneous antibody-drug conjugates. Biotechnol. Adv. 2015, 33, 775-784
15. Krop, I.E.; Beeram, M.; Modi, S.; Jones, S.F.; Holden, S.N.; Yu, W.; Girish, S.; Tibbitts, J.; Yi, J.H.; Sliwkowski, M.X.; et al. Phase I Study of Trastuzumab-DM1, an HER2 Antibody-Drug Conjugate, Given Every 3 Weeks to PatientsWith HER2-Positive Metastatic Breast Cancer. J. Clin. Oncol. 2010, 28, 2698-2704
16. Hamblett, K.J. Effects of Drug Loading on the Antitumor Activity of a Monoclonal Antibody Drug Conjugate. Clin. Cancer Res. 2004, 10, 7063-7070
17. Chudasama, V.; Maruani, A.; Caddick, S. Recent advances in the construction of antibody-drug conjugates. Nat. Chem. 2016, 8, 114-119
18. Polson, A.G.; Calemine-Fenaux, J.; Chan, P.; Chang, W.; Christensen, E.; Clark, S.; de Sauvage, F.J.; Eaton, D.; Elkins, K.; Elliott, J.M.; et al. Antibody-Drug Conjugates for the Treatment of Non-Hodgkin's Lymphoma: Target and Linker-Drug Selection. Cancer Res. 2009, 69, 2358-2364
19. Senter, P.D.; Sievers, E.L. The discovery and development of brentuximab vedotin for use in relapsed Hodgkin lymphoma and systemic anaplastic large cell lymphoma. Nat. Biotechnol. 2012, 30, 631-637
20. Jain, N.; Smith, S.W.; Ghone, S.; Tomczuk, B. Current ADC Linker Chemistry. Pharm. Res. 2015, 32, 3526-3540
21. Hamann, P.R.; Hinman, L.M.; Hollander, I.; Beyer, C.F.; Lindh, D.; Holcomb, R.; Hallett, W.; Tsou, H.-R.; Upeslacis, J.; Shochat, D.; et al. Gemtuzumab ozogamicin, a potent and selective anti-CD33 antibody-calicheamicin conjugate for treatment of acute myeloid leukemia. Bioconjug. Chem. 2002, 13, 47-58
22. Kigawa, J.; Minagawa, Y.; Kanamori, Y.; Itamochi, H.; Cheng, X.; Okada, M.; Oishi, T.; Terakawa, N. Glutathione concentration may be a useful predictor of response to second-line chemotherapy in patients with ovarian cancer. Cancer 1998, 82, 697-702
23. Jones, D.P.; Carlson, J.L.; Mody, V.C.; Cai, J.; Lynn, M.J.; Sternberg, P. Redox state of glutathione in human plasma. Free Radic. Biol. Med. 2000, 28, 625-635
24. Saito, G.; Swanson, J.A.; Lee, K.-D. Drug delivery strategy utilizing conjugation via reversible disulfide linkages: role and site of cellular reducing activities. Adv. Drug Deliv. Rev. 2003, 55, 199-215
25. Tothill, R.; Estall, V.; Rischin, D. Merkel Cell Carcinoma: Emerging Biology, Current Approaches, and Future Directions. Am. Soc. Clin. Oncol. 2015, 35, 519-526
26. Doronina, S.O.; Mendelsohn, B.A.; Bovee, T.D.; Cerveny, C.G.; Alley, S.C.; Meyer, D.L.; Oflazoglu, E.; Toki, B.E.; Sanderson, R.J.; Zabinski, R.F.; et al. Enhanced activity of monomethylauristatin F through monoclonal antibody delivery: effects of linker technology on efficacy and toxicity. Bioconjug. Chem. 2006, 17, 114-124
27. LoRusso, P.M.; Weiss, D.; Guardino, E.; Girish, S.; Sliwkowski, M.X. Trastuzumab emtansine: A unique antibody-drug conjugate in development for human epidermal growth factor receptor 2-positive cancer. Clin. Cancer Res. 2011, 17, 6437-6447
28. Erickson, H.K. Antibody-Maytansinoid Conjugates Are Activated in Targeted Cancer Cells by Lysosomal Degradation and Linker-Dependent Intracellular Processing. Cancer Res. 2006, 66, 4426-4433
29. Girish, S.; Gupta, M.; Wang, B.; Lu, D.; Krop, I.E.; Vogel, C.L.; Burris, H.A., III; LoRusso, P.M.; Yi, J.-H.; Saad, O.; et al. Clinical pharmacology of trastuzumab emtansine (T-DM1): an antibody-drug conjugate in development for the treatment of HER2-positive cancer. Cancer Chemother. Pharmacol. 2012, 69, 1229-1240
30. Dumontet, C.; Jordan, M.A. Microtubule-binding agents: A dynamic field of cancer therapeutics. Nat. Rev. Drug Discov. 2010, 9, 790-803
31. Oroudjev, E.; Lopus, M.; Wilson, L.; Audette, C.; Provenzano, C.; Erickson, H.; Kovtun, Y.; Chari, R.; Jordan, M.A. Maytansinoid-antibody conjugates induce mitotic arrest by suppressing microtubule dynamic instability. Mol. Cancer Ther. 2010, 9, 2700-2713
32. Komlodi-Pasztor, E.; Sackett, D.;Wilkerson, J.; Fojo, T. Mitosis is not a key target of microtubule agents in patient tumors. Nat. Rev. Clin. Oncol. 2011, 8, 244-250
33. Poruchynsky, M.S.; Komlodi-Pasztor, E.; Trostel, S.; Wilkerson, J.; Regairaz, M.; Pommier, Y.; Zhang, X.; Kumar Maity, T.; Robey, R.; Burotto, M.; et al. Microtubule-targeting agents augment the toxicity of DNA-damaging agents by disrupting intracellular trafficking of DNA repair proteins. Proc. Natl. Acad. Sci. USA 2015, 112, 1571-1576
34. Hartley, J.A. The development of pyrrolobenzodiazepines as antitumour agents. Expert Opin. Investig. Drugs 2011, 20, 733-744
35. Sutherland, M.S.K.;Walter, R.B.; Jeffrey, S.C.; Burke, P.J.; Yu, C.; Kostner, H.; Stone, I.; Ryan, M.C.; Sussman, D.; Lyon, R.P. SGN-CD33A: A novel CD33-targeting antibody-drug conjugate using a pyrrolobenzodiazepine dimer is active in models of drug-resistant AML. Blood 2013, 122, 1455-1463
36. Elgersma, R.C.; Coumans, R.G.E.; Huijbregts, T.; Menge, W.M.P.B.; Joosten, J.A.F.; Spijker, H.J.; de Groot, F.M.H.; van der Lee, M.M.C.; Ubink, R.; van den Dobbelsteen, D.J.; et al. Design, Synthesis, and Evaluation of Linker-Duocarmycin Payloads: Toward Selection of HER2-Targeting Antibody-Drug Conjugate SYD985. Mol. Pharm. 2015, 12, 1813-1835
37. Van der Lee, M.M.C.; Groothuis, P.G.; Ubink, R.; van der Vleuten, M.A.J.; van Achterberg, T.A.; Loosveld, E.M.; Damming, D.; Jacobs, D.C.H.; Rouwette, M.; Egging, D.F.; et al. The Preclinical Profile of the Duocarmycin-Based HER2-Targeting ADC SYD985 Predicts for Clinical Benefit in Low HER2-Expressing Breast Cancers. Mol. Cancer Ther. 2015, 14, 692-703
38. Yu, S.-F.; Zheng, B.; Go, M.; Lau, J.; Spencer, S.; Raab, H.; Soriano, R.; Jhunjhunwala, S.; Cohen, R.; Caruso, M.; et al. A Novel Anti-CD22 Anthracycline-Based Antibody-Drug Conjugate (ADC) That Overcomes Resistance to Auristatin-Based ADCs. Clin. Cancer Res. 2015, 21, 3298-3306
39. Moldenhauer, G.; Salnikov, A.V.; Luttgau, S.; Herr, I.; Anderl, J.; Faulstich, H. Therapeutic Potential of Amanitin-Conjugated Anti-Epithelial Cell Adhesion Molecule Monoclonal Antibody Against Pancreatic Carcinoma. J. Natl. Cancer Inst. 2012, 104, 622-634
40. Sachdev, J.; Edelman, M.; Harb, W.; Matei, D.; Nguyen, B.; Burgess, S. P1.08. A phase 1 study of 3 different schedules of the folic acid-tubulysin small-molecule drug conjugate EC1456 in pts with advanced solid tumors. Ann. Oncol. 2015, 26
41. Sahin, U.; Hartmann, F.; Senter, P.; Pohl, C.; Engert, A.; Diehl, V.; Pfreundschuh, M. Specific activation of the prodrug mitomycin phosphate by a bispecific anti-CD30/anti-alkaline phosphatase monoclonal antibody. Cancer Res. 1990, 50, 6944-6948
42. Deng, C.; Pan, B.; O'Connor, O.A. Brentuximab vedotin. Clin. Cancer Res. 2013, 19, 22-27
43. Fromm, J.R.; McEarchern, J.A.; Kennedy, D.; Thomas, A.; Shustov, A.R.; Gopal, A.K. Clinical binding properties, internalization kinetics, and clinicopathologic activity of brentuximab vedotin: An antibody-drug conjugate for CD30-positive lymphoid neoplasms. Clin. Lymphoma Myeloma Leuk. 2012, 12, 280-283
44. Junttila, M.R.; Mao, W.; Wang, X.; Wang, B.-E.; Pham, T.; Flygare, J.; Yu, S.-F.; Yee, S.; Goldenberg, D.; Fields, C.; et al. Targeting LGR5+ cells with an antibody-drug conjugate for the treatment of colon cancer. Sci. Transl. Med. 2015, 7
45. Bross, P.F.; Beitz, J.; Chen, G.; Chen, X.H.; Duffy, E.; Kieffer, L.; Roy, S.; Sridhara, R.; Rahman, A.; Williams, G.; et al. Approval summary: gemtuzumab ozogamicin in relapsed acute myeloid leukemia. Clin. Cancer Res. 2001, 7, 1490-1496
46. Petersdorf, S.H.; Kopecky, K.J.; Slovak, M.;Willman, C.; Nevill, T.; Brandwein, J.; Larson, R.A.; Erba, H.P.; Stiff, P.J.; Stuart, R.K.; et al. A phase 3 study of gemtuzumab ozogamicin during induction and postconsolidation therapy in younger patients with acute myeloid leukemia. Blood 2013, 121, 4854-4860
47. Burnett, A.K.; Hills, R.K.; Milligan, D.; Kjeldsen, L.; Kell, J.; Russell, N.H.; Yin, J.A.L.; Hunter, A.; Goldstone, A.H.; Wheatley, K. Identification of Patients With Acute Myeloblastic Leukemia Who Benefit From the Addition of Gemtuzumab Ozogamicin: Results of the MRC AML15 Trial. J. Clin. Oncol. 2011, 29, 369-377
48. Burnett, A.K.; Russell, N.H.; Hills, R.K.; Kell, J.; Freeman, S.; Kjeldsen, L.; Hunter, A.E.; Yin, J.; Craddock, C.F.; Dufva, I.H.; et al. Addition of Gemtuzumab Ozogamicin to Induction Chemotherapy Improves Survival in Older Patients With Acute Myeloid Leukemia. J. Clin. Oncol. 2012, 30, 3924-3931
49. Delaunay, J.; Recher, C.; Pigneux, A.; Witz, F.; Vey, N.; Blanchet, O.; Lefebvre, P.; Luquet, I.; Guillerme, I.; Volteau, C. Addition of gemtuzumab ozogamycin to chemotherapy improves event-free survival but not overall survival of AML patients with intermediate cytogenetics not eligible for allogeneic transplantation. Results of the GOELAMS AML 2006 IR study. Blood 2011, 118, 79
50. Castaigne, S.; Pautas, C.; Terré, C.; Raffoux, E.; Bordessoule, D.; Bastie, J.-N.; Legrand, O.; Thomas, X.; Turlure, P.; Reman, O.; et al. Effect of gemtuzumab ozogamicin on survival of adult patients with de-novo acute myeloid leukaemia (ALFA-0701): A randomised, open-label, phase 3 study. Lancet 2012, 379, 1508-1516
51. Ravandi, F.; Estey, E.H.; Appelbaum, F.R.; Lo-Coco, F.; Schiffer, C.A.; Larson, R.A.; Burnett, A.K.; Kantarjian, H.M. Gemtuzumab Ozogamicin: Time to Resurrect? J. Clin. Oncol. 2012, 30, 3921-3923
52. Estey, E. Treatment of AML: Resurrection for gemtuzumab ozogamicin? Lancet 2012, 379, 1468-1469
53. Dang, N.H.; Ogura, M.; Castaigne, S.; Fayad, L.; Jerkeman, M.; Radford, J.A.; Pezzutto, A.; Bondarenko, I.; Stewart, D.A.; Shnaidman, M. Randomized, phase 3 trial of inotuzumab ozogamicin plus rituximab (R-InO) versus chemotherapy for relapsed/refractory aggressive B-cell non-Hodgkin lymphoma (B-NHL). J. Clin. Oncol. 2014, 32, 8529
54. 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.; et al. Results of a pivotal phase II study of brentuximab vedotin for patients with relapsed or refractory Hodgkin's lymphoma. J. Clin. Oncol. 2012, 30, 2183-2189
55. Berdeja, J.G.; Hernandez-Ilizaliturri, F.; Chanan-Khan, A.; Patel, M.; Kelly, K.R.; Running, K.L.; Murphy, M.; Guild, R.; Carrigan, C.; Ladd, S. Phase I study of lorvotuzumab mertansine (LM, IMGN901) in combination with lenalidomide (Len) and dexamethasone (Dex) in patients with CD56-positive relapsed or relapsed/refractory multiple myeloma (MM). Blood 2012, 120, 728
56. Kelly, K.R.; Chanan-Khan, A.; Somlo, G.; Heffner, L.T. Indatuximab Ravtansine (BT062) in Combination with Lenalidomide and Low-Dose Dexamethasone in Patients with Relapsed and/or Refractory Multiple. Blood 2014, 124, 4736
57. Verma, S.; Miles, D.; Gianni, L.; Krop, I.E.; Welslau, M.; Baselga, J.; Pegram, M.; Oh, D.-Y.; Diéras, V.; Guardino, E.; et al. Trastuzumab Emtansine for HER2-Positive Advanced Breast Cancer. N. Engl. J. Med. 2012, 367, 1783-1791
58. Boni, V.; Rixe, O.; Rasco, D.; Gomez-Roca, C.; Calvo, E.; Morris, J.C.; Tolcher, A.W.; Assadourian, S.; Guillemin, H.; Delord, J.-P. Abstract A73: A Phase I first-in-human (FIH) study of SAR566658, an anti CA6-antibody drug conjugate (ADC), in patients (Pts) with CA6-positive advanced solid tumors (STs) (NCT01156870). Mol. Cancer Ther. 2013, 12
59. Morschhauser, F.; Flinn, I. Preliminary results of a phase II randomized study (ROMULUS) of polatuzumab vedotin (PoV) or pinatuzumab vedotin (PiV) plus rituximab (RTX) in patients (Pts) with relapsed/refractory (R/R) non-Hodgkin lymphoma (NHL). In Proceedings of the 50th Annual Meeting of American Society Of Clinical Oncology, Chicago, IL, USA, 30 May-3 June 2014
60. Ott, P.A.; Hamid, O.; Pavlick, A.C.; Kluger, H.; Kim, K.B.; Boasberg, P.D.; Simantov, R.; Crowley, E.; Green, J.A.; Hawthorne, T.; et al. Phase I/II Study of the Antibody-Drug Conjugate Glembatumumab Vedotin in Patients With Advanced Melanoma. J. Clin. Oncol. 2014, 32, 3659-3666
61. Petrylak, D.P.; Smith, D.C.; Appleman, L.J.; Fleming, M.T.; Hussain, A.; Dreicer, R.; Sartor, A.O.; Shore, N.D.; Vogelzang, N.J.; Youssoufian, H. A phase 2 trial of prostate-specific membrane antigen antibody drug conjugate (PSMA ADC) in taxane-refractory metastatic castration-resistant prostate cancer (mCRPC). Blood 2014, 32, 5023
62. Gan, H.K.; Papadopoulos, K.P.; Fichtel, L.; Lassman, A.B.; Merrell, R.; Van Den Bent, M.J.; Kumthekar, P.; Scott, A.M.; Pedersen, M.; Gomez, E.J.; et al. Phase I study of ABT-414 mono-or combination therapy with temozolomide (TMZ) in recurrent glioblastoma (GBM). In Proceedings of the ASCO Annual Meeting, Chicago, IL, USA, 29 May-2 June 2015
63. Starodub, A.; Ocean, A.J.; Messersmith, W.A.; Picozzi, V.J.; Guarino, M.J.; Thomas, S.S.; Bardia, A.; Shah, M.A.; Govindan, S.V.; Maliakal, P.P. Phase I/II trial of IMMU-132 (isactuzumab govitecan), an anti-Trop-2-SN-38 antibody drug conjugate (ADC): Results in patients with metastatic gastrointestinal (GI) cancers. Blood 2015, 33, 703-747
64. De Claro, R.A.; McGinn, K.; Kwitkowski, V.; Bullock, J.; Khandelwal, A.; Habtemariam, B.; Ouyang, Y.; Saber, H.; Lee, K.; Koti, K.; et al. U.S. Food and Drug Administration Approval Summary: Brentuximab Vedotin for the Treatment of Relapsed Hodgkin Lymphoma or Relapsed Systemic Anaplastic Large-Cell Lymphoma. Clin. Cancer Res. 2012, 18, 5845-5849
65. Moskowitz, C.H.; Nademanee, A.; Masszi, T.; Agura, E.; Holowiecki, J.; Abidi, M.H.; Chen, A.I.; Stiff, P.; Gianni, A.M.; Carella, A. Brentuximab vedotin as consolidation therapy after autologous stem-cell transplantation in patients with Hodgkin's lymphoma at risk of relapse or progression (AETHERA): A randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 2015, 385, 1853-1862
66. Amiri-Kordestani, L.; Blumenthal, G.M.; Xu, Q.C.; Zhang, L.; Tang, S.W.; Ha, L.; Weinberg, W.C.; Chi, B.; Candau-Chacon, R.; Hughes, P.; et al. FDA approval: ado-trastuzumab emtansine for the treatment of patients with HER2-positive metastatic breast cancer. Clin. Cancer Res. 2014, 20, 4436-4441
67. Lewis Phillips, G.D.; Li, G.; Dugger, D.L.; Crocker, L.M.; Parsons, K.L.; Mai, E.; Blattler, W.A.; Lambert, J.M.; Chari, R.V.J.; Lutz, R.J.; et al. Targeting HER2-Positive Breast Cancer with Trastuzumab-DM1, an Antibody-Cytotoxic Drug Conjugate. Cancer Res. 2008, 68, 9280-9290
68. Barok, M.; Tanner, M.; Koninki, K.; Isola, J. Trastuzumab-DM1 causes tumour growth inhibition by mitotic catastrophe in trastuzumab-resistant breast cancer cells in vivo. Breast Cancer Res. 2011, 13, R46
69. Hurvitz, S.A.; Dirix, L.; Kocsis, J.; Bianchi, G.V.; Lu, J.; Vinholes, J.; Guardino, E.; Song, C.; Tong, B.; Ng, V.; et al. Phase II Randomized Study of Trastuzumab Emtansine Versus Trastuzumab Plus Docetaxel in Patients With Human Epidermal Growth Factor Receptor 2-Positive Metastatic Breast Cancer. J. Clin. Oncol. 2013, 31, 1157-1163
70. Dieras, V.; Harbeck, N.; Albain, K.; Burris, H.; Awada, A.; Crivellari, D.; Andre, F.; Choi, Y. J.; Huang, J.; Miller, K.D. Abstract P3-14-01: A phase Ib/II trial of trastuzumab-DM1 with pertuzumab for patients with HER2-positive, locally advanced or metastatic breast cancer: interim efficacy and safety results. Cancer Res. 2010, 70
71. Burris, H.A.; Rugo, H.S.; Vukelja, S.J.; Vogel, C.L.; Borson, R.A.; Limentani, S.; Tan-Chiu, E.; Krop, I.E.; Michaelson, R.A.; Girish, 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
72. Hughes, B. Antibody-drug conjugates for cancer: poised to deliver? Nat. Rev. Drug Discov. 2010, 9, 665-667
73. Krop, I.E.; LoRusso, P.; Miller, K.D.; Modi, S.; Yardley, D.; Rodriguez, G.; Guardino, E.; Lu, M.; Zheng, M.; Girish, S.; 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, 3234-3241
74. De Goeij, B.E.; Lambert, J.M. New developments for antibody-drug conjugate-based therapeutic approaches. Curr. Opin. Immunol. 2016, 40, 14-23
75. Younes, A.; Kim, S.; Romaguera, J.; Copeland, A.; Farial, S.D.C.; Kwak, L.W.; Fayad, L.; Hagemeister, F.; Fanale, M.; Neelapu, S.; et al. Phase I Multidose-Escalation Study of the Anti-CD19 Maytansinoid Immunoconjugate SAR3419 Administered by Intravenous Infusion Every 3 Weeks to Patients with Relapsed/Refractory B-Cell Lymphoma. J. Clin. Oncol. 2012, 30, 2776-2782
76. Thompson, J.A.; Motzer, R. Phase I studies of anti-ENPP3 antibody drug conjugates (ADCs) in advanced refractory renal cell carcinomas (RRCC). In Proceedings of the ASCO Annual Meeting, Chicago, IL, USA, 29 May-2 June 2015
77. Goff, L.W.; Papadopoulos, K.; Posey, J.A.; Phan, A.T.; Patnaik, A.; Miller, J.G.; Zildjian, S.; O'Leary, J.J.; Qin, A.; Tolcher, A. A phase II study of IMGN242 (huC242-DM4) in patients with CanAg-positive gastric or gastroesophageal (GE) junction cancer. In Proceedings of the 45th ASCO Annual Meeting, Orlando, IL, USA, 29 May-2 June 2009
78. Bendell, J.; Blumenschein, G.; Zinner, R.; Hong, D.; Jones, S.; Infante, J.; Burris, H.; Rajagopalan, P.; Kornacker, M.; Henderson, D.; et al. Abstract LB-291: First-in-human phase I dose escalation study of a novel anti-mesothelin antibody drug conjugate (ADC), BAY 94-9343, in patients with advanced solid tumors. Cancer Res. 2014, 73
79. Moore, K.; Ponte, J.; LoRusso, P.; Birrer, M.; Bauer, T.M.; Borghei, H.; O'Malley, D.; Ruiz-Soto, R.; Lutz, R.J.; Malik, L. Relationship of pharmacokinetics (PK), toxicity and initial evidence of clinical activity with IMGN853, a folate receptor alpha (FRα)-targeting antibody drug conjugate in patients with epithelial ovarian cancer and other FRα-positive solid tumors. J. Clin. Oncol. 2014, 32, 5571
80. Oak, E.; Bartlett, N.L. A safety evaluation of brentuximab vedotin for the treatment of Hodgkin lymphoma. Expert Opin. Drug Saf. 2016, 15, 875-882
81. Goy, A.; Forero, A.;Wagner-Johnston, N.; Christopher Ehmann, W.; Tsai, M.; Hatake, K.; Ananthakrishnan, R.; Volkert, A.; Vandendries, E.; Ogura, M. A phase 2 study of inotuzumab ozogamicin in patients with indolent B-cell non-Hodgkin lymphoma refractory to rituximab alone, rituximab and chemotherapy, or radioimmunotherapy. Br. J. Haematol. 2016
82. Onitilo, A.A.; Engel, J.M.; Stankowski, R.V. Cardiovascular toxicity associated with adjuvant trastuzumab therapy: Prevalence, patient characteristics, and risk factors. Ther. Adv. Drug Saf. 2014, 5, 154-166
83. Uppal, H.; Doudement, E.; Mahapatra, K.; Darbonne, W.C.; Bumbaca, D.; Shen, B.-Q.; Du, X.; Saad, O.; Bowles, K.; Olsen, S.; et al. Potential mechanisms for thrombocytopenia development with trastuzumab emtansine (T-DM1). Clin. Cancer Res. 2015, 21, 123-133
84. Dosio, F.; Brusa, P.; Cattel, L. Immunotoxins and Anticancer Drug Conjugate Assemblies: The Role of the Linkage between Components. Toxins 2011, 3, 848-883
85. Bracci, L.; Schiavoni, G.; Sistigu, A.; Belardelli, F. Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer. Cell Death Differ. 2014, 21, 15-25
86. Müller, P.; Martin, K.; Theurich, S.; Schreiner, J.; Savic, S.; Terszowski, G.; Lardinois, D.; Heinzelmann-Schwarz, V.A.; Schlaak, M.; Kvasnicka, H.-M.; et al. Microtubule-depolymerizing agents used in antibody-drug conjugates induce antitumor immunity by stimulation of dendritic cells. Cancer Immunol. Res. 2014, 2, 741-755
87. Müller, P.; Kreuzaler, M.; Khan, T.; Thommen, D.S.; Martin, K.; Glatz, K.; Savic, S.; Harbeck, N.; Nitz, U.; Gluz, O.; et al. Trastuzumab emtansine (T-DM1) renders HER2+ breast cancer highly susceptible to CTLA-4/PD-1 blockade. Sci. Transl. Med. 2015, 7
88. Barok, M.; Joensuu, H.; Isola, J. Trastuzumab emtansine: mechanisms of action and drug resistance. Breast Cancer Res. 2014, 16, 1
89. Ritchie, M.; Tchistiakova, L.; Scott, N. Implications of receptor-mediated endocytosis and intracellular trafficking dynamics in the development of antibody drug conjugates. mAbs 2014, 5, 13-21
90. Loganzo, F.; Tan, X.; Sung, M.; Jin, G.; Myers, J.S.; Melamud, E.; Wang, F.; Diesl, V.; Follettie, M.T.; Musto, S.; et al. Tumor cells chronically treated with a trastuzumab-maytansinoid antibody-drug conjugate develop varied resistance mechanisms but respond to alternate treatments. Mol. Cancer Ther. 2015, 14, 952-963
91. Helman, E.; Wick, M.J.; Clark, M.J.; Gamez, L.; Boyle, S.; Papadopoulos, K.P.; Luo, S.; Tolcher, A.W.; Sripakdeevong, P.; Karbelashvili, M.; et al. Abstract 1457: Genomic characterization of a PDX model of T-DM1-resistant HER2+ invasive ductal carcinoma using augmented exome sequencing. Cancer Res. 2015, 75, 1457
92. O'Brien, C.; Cavet, G.; Pandita, A.; Hu, X.; Haydu, L.; Mohan, S.; Toy, K.; Rivers, C.S.; Modrusan, Z.; Amler, L.C.; et al. Functional genomics identifies ABCC3 as a mediator of taxane resistance in HER2-amplified breast cancer. Cancer Res. 2008, 68, 5380-5389
93. Szakács, G.; Paterson, J.K.; Ludwig, J.A.; Booth-Genthe, C.; Gottesman, M.M. Targeting multidrug resistance in cancer. Nat. Rev. Drug Discov. 2006, 5, 219-234
94. Gottesman, M.M. Mechanisms of Cancer Drug Resistance. Annu. Rev. Med. 2002, 53, 615-627
95. Sammet, B.; Steinkühler, C.; Sewald, N. Antibody-drug conjugates in tumor therapy. Pharm. Pat. Anal. 2012, 1, 65-73
96. Loo, T.W.; Clarke, D.M. Recent progress in understanding the mechanism of P-glycoprotein-mediated drug efflux. J. Membr. Boil. 2005, 206, 173-185
97. Kovtun, Y.V.; Audette, C.A.; Mayo, M.F.; Jones, G.E.; Doherty, H.; Maloney, E.K.; Erickson, H.K.; Sun, X.; Wilhelm, S.; Ab, O.; et al. Antibody-Maytansinoid Conjugates Designed to Bypass Multidrug Resistance. Cancer Res. 2010, 70, 2528-2537
98. Chen, R.; Hou, J.; Newman, E.; Kim, Y.; Donohue, C.; Liu, X.; Thomas, S.H.; Forman, S.J.; Kane, S.E. CD30 Downregulation, MMAE Resistance, and MDR1 Upregulation Are All Associated with Resistance to Brentuximab Vedotin. Mol. Cancer Ther. 2015, 14, 1376-1384