Antibody–drug conjugates for cancer therapy

The Lancet Oncology

Volumn 17, Issue 6, 2016, Pages e254-e262

  Thomas, Anish ^a   Teicher, Beverly A ^a   Hassan, Raffit ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANETUMAB RAVTANSINE; ANTIBODY DRUG CONJUGATE; BRENTUXIMAB VEDOTIN; CALICHEAMICIN; CAPECITABINE; CD22 ANTIGEN; CD30 ANTIGEN; CYTOTOXIC AGENT; DOCETAXEL; DOLASTATIN 10; DUOCARMYCIN DERIVATIVE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLEMBATUMUMAB VEDOTIN; INOTUZUMAB OZOGAMICIN; LAPATINIB; MAYTANSINE; MESOTHELIN; MONOCLONAL ANTIBODY; ROVALPITUZUMAB TESIRINE; SACITUZUMAB GOVITECAN; TRASTUZUMAB; TRASTUZUMAB EMTANSINE; UNCLASSIFIED DRUG; ANTIBODY CONJUGATE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANEMIA; ANTIGEN BINDING; ARTHRALGIA; AUTOLOGOUS STEM CELL TRANSPLANTATION; BREAST CANCER; BREAST METASTASIS; CANCER IMMUNOTHERAPY; CANCER THERAPY; CAPILLARY LEAK SYNDROME; COMBINATION CHEMOTHERAPY; CONJUGATION; CONSTIPATION; COUGHING; CUTANEOUS T CELL LYMPHOMA; DIARRHEA; DRUG SELECTIVITY; DRUG STRUCTURE; DRUG TARGETING; DRUG TOLERABILITY; EPISTAXIS; EPITHELIUM TUMOR; FATIGUE; FEVER; HEADACHE; HEART LEFT VENTRICLE EJECTION FRACTION; HODGKIN DISEASE; HUMAN; HYPERTRANSAMINASEMIA; INTERNALIZATION; KERATITIS; LARGE CELL LYMPHOMA; LIVER DYSFUNCTION; LIVER FAILURE; LIVER TOXICITY; LYMPHOMA; MAXIMUM TOLERATED DOSE; MELANOMA; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; MUSCULOSKELETAL PAIN; MYALGIA; NAUSEA; NEUROPATHY; NEUTROPENIA; NONHUMAN; OSTEOSARCOMA; OVERALL SURVIVAL; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; PROSTATE CANCER; RASH; RECOMMENDED DRUG DOSE; REVIEW; SENSORY NEUROPATHY; SIDE EFFECT; SMALL CELL LUNG CANCER; SOLID TUMOR; STEVENS JOHNSON SYNDROME; STOMACH CANCER; T CELL LYMPHOMA; THROMBOCYTOPENIA; TRANSITIONAL CELL CARCINOMA; TRIPLE NEGATIVE BREAST CANCER; TUMOR LYSIS SYNDROME; UNSPECIFIED SIDE EFFECT; UPPER RESPIRATORY TRACT INFECTION; VOMITING; XEROSTOMIA; NEOPLASMS;

ANTIBODIES, MONOCLONAL; HUMANS; IMMUNOCONJUGATES; NEOPLASMS;

EID: 84976870682     PISSN: 14702045     EISSN: 14745488     Source Type: Journal    
DOI: 10.1016/S1470-2045(16)30030-4     Document Type: Review

References (73)

1. 1 Pastan, I, Hassan, R, Fitzgerald, DJ, Kreitman, RJ, Immunotoxin therapy of cancer. Nat Rev Cancer 6 (2006), 559–565.
2. 2 Olsen, E, Duvic, M, Frankel, A, et al. Pivotal phase III trial of two dose levels of denileukin diftitox for the treatment of cutaneous T-cell lymphoma. J Clin Oncol 19 (2001), 376–388.
3. 3 Kreitman, RJ, Tallman, MS, Robak, T, et al. Phase I trial of anti-CD22 recombinant immunotoxin moxetumomab pasudotox (CAT-8015 or HA22) in patients with hairy cell leukemia. J Clin Oncol 30 (2012), 1822–1828.
4. 4 Hassan, R, Miller, AC, Sharon, E, et al. Major cancer regressions in mesothelioma after treatment with an anti-mesothelin immunotoxin and immune suppression. Sci Transl Med, 5, 2013, 208ra147.
5. 5 Hassan, R, Alewine, C, Pastan, I, New life for immunotoxin cancer therapy. Clin Cancer Res 22 (2016), 1055–1058.
6. 6 Sliwkowski, MX, Mellman, I, Antibody therapeutics in cancer. Science 341 (2013), 1192–1198.
7. 7 Sievers, EL, Senter, PD, Antibody–drug conjugates in cancer therapy. Annu Rev Med 64 (2013), 15–29.
8. 8 Teicher, BA, Chari, RV, Antibody conjugate therapeutics: challenges and potential. Clin Cancer Res 17 (2011), 6389–6397.
9. 9 Chari, RV, Targeted delivery of chemotherapeutics: tumor-activated prodrug therapy. Adv Drug Deliv Rev 31 (1998), 89–104.
10. 10 Dombret, H, Gardin, C, An update of current treatments for adult acute myeloid leukemia. Blood 127 (2016), 53–61.
11. 11 Petersdorf, SH, Kopecky, KJ, Slovak, M, et al. A phase 3 study of gemtuzumab ozogamicin during induction and postconsolidation therapy in younger patients with acute myeloid leukemia. Blood 121 (2013), 4854–4860.
12. 12 Teicher, BA, Antibody-drug conjugate targets. Curr Cancer Drug Targets 9 (2009), 982–1004.
13. 13 Chari, RV, Targeted cancer therapy: conferring specificity to cytotoxic drugs. Acc Chem Res 41 (2008), 98–107.
14. 14 Schrama, D, Reisfeld, RA, Becker, JC, Antibody targeted drugs as cancer therapeutics. Nat Rev Drug Discov 5 (2006), 147–159.
15. 15 Carter, PJ, Senter, PD, Antibody-drug conjugates for cancer therapy. Cancer J 14 (2008), 154–169.
16. 16 Beck, A, Haeuw, JF, Wurch, T, Goetsch, L, Bailly, C, Corvaia, N, The next generation of antibody-drug conjugates comes of age. Discov Med 10 (2010), 329–339.
17. 17 Lopus, M, Oroudjev, E, Wilson, L, et al. Maytansine and cellular metabolites of antibody-maytansinoid conjugates strongly suppress microtubule dynamics by binding to microtubules. Mol Cancer Ther 9 (2010), 2689–2699.
18. 18 Vaishampayan, U, Glode, M, Du, W, et al. Phase II study of dolastatin-10 in patients with hormone-refractory metastatic prostate adenocarcinoma. Clin Cancer Res 6 (2000), 4205–4208.
19. 19 Issell, BF, Crooke, ST, Maytansine. Cancer Treat Rev 5 (1978), 199–207.
20. 20 MacMillan, KS, Boger, DL, Fundamental relationships between structure, reactivity, and biological activity for the duocarmycins and CC-1065. J Med Chem 52 (2009), 5771–5780.
21. 21 Small, EJ, Figlin, R, Petrylak, D, et al. A phase II pilot study of KW-2189 in patients with advanced renal cell carcinoma. Invest New Drugs 18 (2000), 193–197.
22. 22 Thorson, JS, Sievers, EL, Ahlert, J, et al. Understanding and exploiting nature's chemical arsenal: the past, present and future of calicheamicin research. Curr Pharm Des 6 (2000), 1841–1879.
23. 23 Damle, NK, Frost, P, Antibody-targeted chemotherapy with immunoconjugates of calicheamicin. Curr Opin Pharmacol 3 (2003), 386–390.
24. 24 Anderl, J, Faulstich, H, Hechler, T, Kulke, M, Antibody–drug conjugate payloads. Methods Mol Biol 1045 (2013), 51–70.
25. 25 Starodub, AN, Ocean, AJ, Shah, MA, et al. First-in-human trial of a novel anti-Trop-2 antibody-SN-38 conjugate, sacituzumab govitecan, for the treatment of diverse metastatic solid tumors. Clin Cancer Res 21 (2015), 3870–3878.
26. 26 Letschert, K, Faulstich, H, Keller, D, Keppler, D, Molecular characterization and inhibition of amanitin uptake into human hepatocytes. Toxicol Sci 91 (2006), 140–149.
27. 27 Younes, A, Bartlett, NL, Leonard, JP, et al. Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas. N Engl J Med 363 (2010), 1812–1821.
28. 28 Ansell, SM, Brentuximab vedotin. Blood 124 (2014), 3197–3200.
29. 29 Burris, HA III, Rugo, HS, Vukelja, SJ, 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 29 (2011), 398–405.
30. 30 Polson, AG, Ho, WY, Ramakrishnan, V, Investigational antibody-drug conjugates for hematological malignancies. Expert Opin Investig Drugs 20 (2011), 75–85.
31. 31 Kellogg, BA, Garrett, L, Kovtun, Y, et al. Disulfide-linked antibody-maytansinoid conjugates: optimization of in vivo activity by varying the steric hindrance at carbon atoms adjacent to the disulfide linkage. Bioconjug Chem 22 (2011), 717–727.
32. 32 Zhao, RY, Wilhelm, SD, Audette, C, et al. Synthesis and evaluation of hydrophilic linkers for antibody-maytansinoid conjugates. J Med Chem 54 (2011), 3606–3623.
33. 33 Kovtun, YV, Audette, CA, Mayo, MF, et al. Antibody–maytansinoid conjugates designed to bypass multidrug resistance. Cancer Res 70 (2010), 2528–2537.
34. 34 Hamblett, KJ, Senter, PD, Chace, DF, et al. Effects of drug loading on the antitumor activity of a monoclonal antibody drug conjugate. Clin Cancer Res 10 (2004), 7063–7070.
35. 35 Tian, F, Lu, Y, Manibusan, A, et al. A general approach to site-specific antibody drug conjugates. Proc Natl Acad Sci USA 111 (2014), 1766–1771.
36. 36 Mahapatra, K, Darbonne, W, Bumbaca, D, et al. Abstract A135: T-DM1-induced thrombocytopenia results from impaired platelet production in a HER2-independent manner. Mol Cancer Ther, 10(11 suppl), 2011, A135.
37. 37 Younes, A, Bartlett, NL, Leonard, JP, et al. Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas. N Engl J Med 363 (2010), 1812–1821.
38. 38 Katz, J, Janik, JE, Younes, A, Brentuximab vedotin (SGN-35). Clin Cancer Res 17 (2011), 6428–6436.
39. 39 Pro, B, Advani, R, Brice, P, et al. 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 (2012), 2190–2196.
40. 40 Younes, A, Gopal, AK, Smith, SE, et al. Results of a pivotal phase II study of brentuximab vedotin for patients with relapsed or refractory Hodgkin's lymphoma. J Clin Oncol 30 (2012), 2183–2189.
41. 41 de Claro, RA, McGinn, K, Kwitkowski, V, et al. US 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 18 (2012), 5845–5849.
42. 42 LoRusso, PM, Weiss, D, Guardino, E, Girish, S, Sliwkowski, MX, Trastuzumab emtansine: a unique antibody-drug conjugate in development for human epidermal growth factor receptor 2-positive cancer. Clin Cancer Res 17 (2011), 6437–6447.
43. 43 Lambert, JM, Chari, RV, Ado-trastuzumab emtansine (T-DM1): an antibody-drug conjugate (ADC) for HER2-positive breast cancer. J Med Chem 57 (2014), 6949–6964.
44. 44 Amiri-Kordestani, L, Blumenthal, GM, Xu, QC, et al. FDA approval: ado-trastuzumab emtansine for the treatment of patients with HER2-positive metastatic breast cancer. Clin Cancer Res 20 (2014), 4436–4441.
45. 45 Verma, S, Miles, D, Gianni, L, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 367 (2012), 1783–1791.
46. 46 Krop, IE, Kim, SB, Gonzalez-Martin, A, et al. Trastuzumab emtansine versus treatment of physician's choice for pretreated HER2-positive advanced breast cancer (TH3RESA): a randomised, open-label, phase 3 trial. Lancet Oncol 15 (2014), 689–699.
47. 47 Cardillo, TM, Govindan, SV, Sharkey, RM, Trisal, P, Goldenberg, DM, Humanized anti-Trop-2 IgG-SN-38 conjugate for effective treatment of diverse epithelial cancers: preclinical studies in human cancer xenograft models and monkeys. Clin Cancer Res 17 (2011), 3157–3169.
48. 48 Wagner-Johnston, ND, Goy, A, Rodriguez, MA, et al. A phase 2 study of inotuzumab ozogamicin and rituximab, followed by autologous stem cell transplant in patients with relapsed/refractory diffuse large B-cell lymphoma. Leuk Lymphoma 56 (2015), 2863–2869.
49. 49 Golfier, S, Kopitz, C, Kahnert, A, et al. Anetumab ravtansine: a novel mesothelin-targeting antibody-drug conjugate cures tumors with heterogeneous target expression favored by bystander effect. Mol Cancer Ther 13 (2014), 1537–1548.
50. 50 Daver, N, Kantarjian, H, Ravandi, F, et al. A phase II study of decitabine and gemtuzumab ozogamicin in newly diagnosed and relapsed acute myeloid leukemia and high-risk myelodysplastic syndrome. Leukemia 30 (2016), 268–273.
51. 51 Gan, HK, Fichtel, L, Lassman, AB, et al. A phase 1 study evaluating ABT-414 in combination with temozolomide (TMZ) for subjects with recurrent or unresectable glioblastoma (GBM). Proc Am Soc Clin Oncol, 32(5 suppl), 2014 abstr 2021.
52. 52 Bendell, J, Saleh, M, Rose, AA, et al. Phase I/II study of the antibody-drug conjugate glembatumumab vedotin in patients with locally advanced or metastatic breast cancer. J Clin Oncol 32 (2014), 3619–3625.
53. 53 Borghaei, H, O'Malley, DM, Seward, SM, et al. Phase 1 study of IMGN853, a folate receptor alpha (FRα)-targeting antibody-drug conjugate (ADC) in patients (Pts) with epithelial ovarian cancer (EOC) and other FRA-positive solid tumors. Proc Am Soc Clin Oncol, 33(suppl), 2015 abstr 5558.
54. 54 Thompson, JA, Motzer, R, Molina, AM, et al. Phase I studies of anti-ENPP3 antibody drug conjugates (ADCs) in advanced refractory renal cell carcinomas (RRCC). Proc Am Soc Clin Oncol, 33(suppl), 2015 abstr 2503.
55. 55 Saunders, LR, Bankovich, AJ, Anderson, WC, et al. A DLL3-targeted antibody-drug conjugate eradicates high-grade pulmonary neuroendocrine tumor-initiating cells in vivo. Sci Transl Med, 7, 2015, 302ra136.
56. 56 Rudin, CM, Pietanza, MC, Spigel, DR, et al. A DLL3-targeted ADC, rovalpituzumab tesirine, demonstrates substantial activity in a phase I study in relapsed and refractory SCLC. J Thorac Oncol, 10(9 suppl 2), 2015 oral 10.1.
57. 57 Dotan, E, Berlin, J, Starodub, A, et al. Activity of IMMU-130 anti-CEACAM5-SN-38 antibody-drug conjugate (ADC) on metastatic colorectal cancer (mCRC) having relapsed after CPT-11: phase I study. Proc Am Soc Clin Oncol, 32(5 suppl), 2014 abstr 3106.
58. 58 Almhanna, K, Messersmith, WA, Ahnert, JR, et al. MLN0264, an investigational, first-in-class antibody-drug conjugate (ADC) targeting guanylyl cyclase C (GCC): phase I, first-in-human study in patients (pts) with advanced gastrointestinal (GI) malignancies expressing GCC. Proc Am Soc Clin Oncol, 31(suppl), 2013 abstr TPS3646.
59. 59 Chang, K, Pastan, I, Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci USA 93 (1996), 136–140.
60. 60 Hassan, R, Bendell, JC, Blumenschein, G, et al. Phase I study of anti-mesothelin antibody drug conjugate anetumab ravtansine. J Thorac Oncol, 10(9 suppl 2), 2015 oral 11.02.
61. 61 DiJoseph, JF, Armellino, DC, Boghaert, ER, et al. Antibody-targeted chemotherapy with CMC-544: a CD22-targeted immunoconjugate of calicheamicin for the treatment of B-lymphoid malignancies. Blood 103 (2004), 1807–1814.
62. 62 Shor, B, Gerber, HP, Sapra, P, Preclinical and clinical development of inotuzumab-ozogamicin in hematological malignancies. Mol Immunol 67 (2015), 107–116.
63. 63 Vaickus, L, Ball, ED, Foon, KA, Immune markers in hematologic malignancies. Crit Rev Oncol Hematol 11 (1991), 267–297.
64. 64 Advani, A, Coiffier, B, Czuczman, MS, et al. Safety, pharmacokinetics, and preliminary clinical activity of inotuzumab ozogamicin, a novel immunoconjugate for the treatment of B-cell non-Hodgkin's lymphoma: results of a phase I study. J Clin Oncol 28 (2010), 2085–2093.
65. 65 Kantarjian, H, Thomas, D, Jorgensen, J, et al. Inotuzumab ozogamicin, an anti-CD22-calecheamicin conjugate, for refractory and relapsed acute lymphocytic leukaemia: a phase 2 study. Lancet Oncol 13 (2012), 403–411.
66. 66 Shvartsur, A, Bonavida, B, Trop2 and its overexpression in cancers: regulation and clinical/therapeutic implications. Genes Cancer 6 (2015), 84–105.
67. 67 Faltas, B, Goldenberg, DM, Ocean, AJ, et al. Sacituzumab govitecan, a novel antibody–drug conjugate, in patients with metastatic platinum-resistant urothelial carcinoma. Clin Genitourin Cancer 14 (2016), e75–e79.
68. 68 Bardia, A, Vahdat, LT, Robinson Diamond, J, et al. Therapy of refractory/relapsed metastatic triple-negative breast cancer (TNBC) with an anti-Trop-2-SN-38 antibody-drug conjugate (ADC), sacituzumab govitecan (IMMU-132): phase I/II clinical experience. Proc Am Soc Clin Oncol, 33(suppl), 2015 abstr 1016.
69. 69 Geffers, I, Serth, K, Chapman, G, et al. Divergent functions and distinct localization of the Notch ligands DLL1 and DLL3 in vivo. J Cell Biol 178 (2007), 465–476.
70. 70 Ott, PA, Hamid, O, Pavlick, AC, et al. Phase I/II study of the antibody-drug conjugate glembatumumab vedotin in patients with advanced melanoma. J Clin Oncol 32 (2014), 3659–3666.
71. 71 Yardley, DA, Weaver, R, Melisko, ME, et al. EMERGE: a randomized phase II study of the antibody-drug conjugate glembatumumab vedotin in advanced glycoprotein NMB-expressing breast cancer. J Clin Oncol 33 (2015), 1609–1619.
72. 72 Muller, P, Kreuzaler, M, Khan, T, et al. Trastuzumab emtansine (T-DM1) renders HER2+ breast cancer highly susceptible to CTLA-4/PD-1 blockade. Sci Transl Med, 7, 2015, 315ra188.
73. 73 Gardai, SJ, Epp, A, Law, C-L, Abstract 2469: brentuximab vedotin-mediated immunogenic cell death. Cancer Res, 75(15 suppl), 2015, 2469.