Targeting ADAM-17 with an inhibitory monoclonal antibody has antitumour effects in triple-negative breast cancer cells

British Journal of Cancer

Volumn 112, Issue 12, 2015, Pages 1895-1903

  Caiazza, F ^a   McGowan, P M ^a   Mullooly, M ^a   Murray, A ^a   Synnott, N ^a   O'Donovan, N ^b   Flanagan, L ^a   Tape, C J ^c,d   Murphy, G ^c   Crown, J ^e   Duffy, M J ^a,e  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b DUBLIN CITY UNIVERSITY   (Ireland)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^e ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

Author keywords

ADAM 17; breast cancer; EGFR; inhibitor; monoclonal antibody; TACE; triple negative

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY D1(A12); PROGESTERONE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG; ADAM PROTEIN; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVE SITE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; TRIPLE NEGATIVE BREAST CANCER; TUMOR INVASION; ANTAGONISTS AND INHIBITORS; CELL MOTION; CELL PROLIFERATION; DISEASE COURSE; DRUG EFFECTS; GENETICS; IMMUNOLOGY; MOLECULARLY TARGETED THERAPY; PATHOLOGY; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

ADAM PROTEINS; ANTIBODIES, MONOCLONAL, HUMANIZED; APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; HUMANS; MOLECULAR TARGETED THERAPY; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84930865948     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2015.163     Document Type: Article

References (39)

1. Banerji S, Cibulskis K, Rangel-Escareno C, Brown KK, Carter SL, Frederick AM, Lawrence MS, Sivachenko AY, Sougnez C, Zou L, Cortes ML, Fernandez-Lopez JC, Peng S, Ardlie KG, Auclair D, Bautista-Piña V, Duke F, Francis J, Jung J, Maffuz-Aziz A, Onofrio RC, Parkin M, Pho NH, Quintanar-Jurado V, Ramos AH, Rebollar-Vega R, Rodriguez-Cuevas S, Romero-Cordoba SL, Schumacher SE, Stransky N, Thompson KM, Uribe-Figueroa L, Baselga J, Beroukhim R, Polyak K, Sgroi DC, Richardson AL, Jimenez-Sanchez G, Lander ES, Gabriel SB, Garraway LA, Golub TR, Melendez-Zajgla J, Toker A, Getz G, Hidalgo-Miranda A, Meyerson M (2012) Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 486: 405-409.
2. Blaydon DC, Biancheri P, Di W-L, Plagnol V, Cabral RM, Brooke MA, van Heel DA, Ruschendorf F, Toynbee M, Walne A, O'Toole EA, Martin JE, Lindley K, Vulliamy T, Abrams DJ, MacDonald TT, Harper JI, Kelsell DP (2011) Inflammatory skin and bowel disease linked to ADAM17 deletion. N Engl J Med 365: 1502-1508.
3. Borrell-Pagès M, Rojo F, Albanell J, Baselga J, Arribas J (2003) TACE is required for the activation of the EGFR by TGF-α in tumors. EMBO J 22: 1114-1124.
4. Breslin S, O'Driscoll L (2013) Three-dimensional cell culture: the missing link in drug discovery. Drug Discov Today 18: 240-249.
5. Caiazza F, Elliott L, David F, Sheahan K, Doherty GA, Ryan EJ (2015) Targeting EGFR in metastatic colorectal cancer beyond the limitations of KRAS status: alternative biomarkers and therapeutic strategies. Biomarkers in Medicine 9: 363-375.
6. Cancer Genome Atlas Network (2012) Comprehensive molecular portraits of human breast tumours. Nature 490: 61-70.
7. Clynes RA, Towers TL, Presta LG, Ravetch JV (2000) Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 6: 443-446.
8. Collins DM, O'Donovan N, McGowan PM, O'Sullivan F, Duffy MJ, Crown J (2012) Trastuzumab induces antibody-dependent cell-mediated cytotoxicity (ADCC) in HER-2-non-amplified breast cancer cell lines. Ann Oncol 23: 1788-1795.
9. Duffy MJ, McGowan PM, Crown J (2012) Targeted therapy for triple-negative breast cancer: Where are we? Int J Cancer 131: 2471-2477.
10. Duffy MJ, McKiernan E, O'Donovan N, McGowan PM (2009a) Role of ADAMs in cancer formation and progression. Clin Cancer Res 15: 1140-1144.
11. Duffy MJ, McKiernan E, O'Donovan N, McGowan PM (2009b) The role of ADAMs in disease pathophysiology. Clin Chim Acta 403: 31-36.
12. Dutta B, Pusztai L, Qi Y, Andre F, Lazar V, Bianchini G, Ueno N, Agarwal R, Wang B, Shiang CY, Hortobagyi GN, Mills GB, Symmans WF, Balázsi G (2012) A network-based, integrative study to identify core biological pathways that drive breast cancer clinical subtypes. Br J Cancer 106: 1107-1116.
13. Fridman JS, Caulder E, Hansbury M, Liu X, Yang G, Wang Q, Lo Y, Zhou B-B, Pan M, Thomas SM, Grandis JR, Zhuo J, Yao W, Newton RC, Friedman SM, Scherle PA, Vaddi K (2007a) Selective inhibition of ADAM metalloproteases as a novel approach for modulating ErbB pathways in cancer. Clin Cancer Res 13: 1892-1902.
14. Fridman JS, Scherle PA, Liu X (2007b) Preclinical characterization of INCB7839, a potent and selective inhibitor of ErbB ligand and HER2 receptor shedding: inhibition of ADAM10 and ADAM17 for the treatment of breast cancer. Cancer Res Treat 106: S82.
15. Giricz O, Calvo V, Peterson EA, Abouzeid CM, Kenny PA (2013) TACE-dependent TGFα shedding drives triple-negative breast cancer cell invasion. Int J Cancer 133(11): 2587-2595.
16. Gooz M (2010) ADAM-17: the enzyme that does it all. Crit Rev Biochem Mol Biol 45: 146-169.
17. Ha HC, Snyder SH (1999) Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 96: 13978-13982.
18. Heuckmann JM, Rauh D, Thomas RK (2012) Epidermal growth factor receptor (EGFR) signaling and covalent EGFR inhibition in lung cancer. J Clin Oncol 30: 3417-3420.
19. Hughes L, Malone C, Chumsri S, Burger AM, McDonnell S (2008) Characterisation of breast cancer cell lines and establishment of a novel isogenic subclone to study migration, invasion and tumourigenicity. Clin Exp Metastasis 25: 549-557.
20. Infante J, Burris HA, Lewis N (2007) A multicenter phase Ib study of the safety, pharmacokinetics, biological activity and clinical efficacy of INCB7839, a potent and selective inhibitor of ADAM10 and ADAm17. Breast Cancer Res Treat 106: S269.
21. Jelovac D, Emens LA (2013) HER2-directed therapy for metastatic breast cancer. Oncology (Williston Park) 27: 166-175.
22. Kenny PA, Bissell MJ (2007) Targeting TACE-dependent EGFR ligand shedding in breast cancer. J Clin Invest 117: 337-345.
23. Le Gall SM, Bobé P, Reiss K, Horiuchi K, Niu X-D, Lundell D, Gibb DR, Conrad D, Saftig P, Blobel CP (2009) ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor alpha, L-selectin, and tumor necrosis factor alpha. Mol Biol Cell 20: 1785-1794.
24. Lee GY, Kenny PA, Lee EH, Bissell MJ (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4: 359-365.
25. Ma X, Hu Y (2013) Targeting PI3K/Akt/mTOR cascade: the medicinal potential, updated research highlights and challenges ahead. Curr Med Chem 20(24): 2991-3010.
26. Maltman DJ, Przyborski SA (2010) Developments in three-dimensional cell culture technology aimed at improving the accuracy of in vitro analyses. Biochem Soc Trans 38: 1072-1075.
27. McGowan PM, McKiernan E, Bolster F, Ryan BM, Hill ADK, McDermott EW, Evoy D, O'Higgins N, Crown J, Duffy MJ (2008) ADAM-17 predicts adverse outcome in patients with breast cancer. Ann Oncol 19: 1075-1081.
28. McGowan PM, Mullooly M, Caiazza F, Sukor S, Madden SF, Maguire AA, Pierce A, McDermott EW, Crown J, O'Donovan N, Duffy MJ (2013) ADAM-17: a novel therapeutic target for triple negative breast cancer. Ann Oncol 24: 362-369.
29. McGowan PM, Ryan BM, Hill ADK, McDermott E, O'Higgins N, Duffy MJ (2007) ADAM-17 expression in breast cancer correlates with variables of tumor progression. Clin Cancer Res 13: 2335-2343.
30. Murphy G (2008) The ADAMs: signalling scissors in the tumour microenvironment. Nat Rev Cancer 8: 932-941.
31. Ocaña A, Amir E, Seruga B, Martin M, Pandiella A (2013) The evolving landscape of protein kinases in breast cancer: clinical implications. Cancer Treat Rev 39: 68-76.
32. Richards FM, Tape CJ, Jodrell DI, Murphy G (2012) Anti-tumour effects of a specific anti-ADAM17 antibody in an ovarian cancer model in vivo. PLoS ONE 7: e40597.
33. Roberti MP, Barrio MM, Bravo AI, Rocca YS, Arriaga JM, Bianchini M, Mordoh J, Levy EM (2011) IL-15 and IL-2 increase Cetuximab-mediated cellular cytotoxicity against triple negative breast cancer cell lines expressing EGFR. Breast Cancer Res Treat 130: 465-475.
34. Sahin U, Blobel CP (2007) Ectodomain shedding of the EGF-receptor ligand epigen is mediated by ADAM17. FEBS Lett 581: 41-44.
35. Sahin U, Weskamp G, Kelly K, Zhou H-M, Higashiyama S, Peschon J, Hartmann D, Saftig P, Blobel CP (2004) Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 164: 769-779.
36. Soria J-C, Mok TS, Cappuzzo F, Jänne PA (2012) EGFR-mutated oncogene-addicted non-small cell lung cancer: current trends and future prospects. Cancer Treat Rev 38: 416-430.
37. Tape CJ, Willems SH, Dombernowsky SL, Stanley PL, Fogarasi M, Ouwehand W, McCafferty J, Murphy G (2011) Cross-domain inhibition of TACE ectodomain. Proc Natl Acad Sci USA 108: 5578-5583.
38. Weisenthal LM, Dill PL, Kurnick NB, Lippman ME (1983) Comparison of dye exclusion assays with a clonogenic assay in the determination of drug-induced cytotoxicity. Cancer Res 43: 258-264.
39. Zhang Y, Hegen M, Xu J, Keith JC, Jin G, Du X, Cummons T, Sheppard BJ, Sun L, Zhu Y, Rao VR, Wang Q, Xu W, Cowling R, Nickerson-Nutter CL, Gibbons J, Skotnicki J, Lin L-L, Levin J (2004) Characterization of (2 R, 3 S)-2-([[4-(2-butynyloxy)phenyl]sulfonyl]amino)-N,3-dihydroxybutanamide, a potent and selective inhibitor of TNF-alpha converting enzyme. Int Immunopharmacol 4: 1845-1857.