Dacarbazine and the Agonistic TRAIL Receptor-2 Antibody Lexatumumab Induce Synergistic Anticancer Effects in Melanoma

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Engesæter, Birgit ^a   Engebraaten, Olav ^a,b   Flørenes, Vivi Ann ^a   Mælandsmo, Gunhild Mari ^a,c  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; DACARBAZINE; DEATH RECEPTOR 5; INHIBITOR OF APOPTOSIS PROTEIN; LEXATUMUMAB; LIVIN; MAPATUMUMAB; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL XL; PROTEIN BID; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL DEATH; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENTIATION; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MELANOMA; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASES; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; DACARBAZINE; DRUG SYNERGISM; FEMALE; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MELANOMA; MICE; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR STEM CELL ASSAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84866701492     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045492     Document Type: Article

References (46)

1. Garbe C, Eigentler TK, (2007) Diagnosis and treatment of cutaneous melanoma: state of the art 2006. Melanoma Res 17: 117-127.
2. Eigentler TK, Caroli UM, Radny P, Garbe C, (2003) Palliative therapy of disseminated malignant melanoma: a systematic review of 41 randomised clinical trials. Lancet Oncol 4: 748-759.
3. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, et al. (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: 2507-2516.
4. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, et al. (2010) Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 363: 809-819.
5. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, et al. (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363: 711-723.
6. Dai DL, Wang Y, Liu M, Martinka M, Li G, (2008) Bim expression is reduced in human cutaneous melanomas. J Invest Dermatol 128: 403-407.
7. Eberle J, Hossini AM, (2008) Expression and function of bcl-2 proteins in melanoma. Curr Genomics 9: 409-419.
8. Kurbanov BM, Fecker LF, Geilen CC, Sterry W, Eberle J, (2007) Resistance of melanoma cells to TRAIL does not result from upregulation of antiapoptotic proteins by NF-kappaB but is related to downregulation of initiator caspases and DR4. Oncogene 26: 3364-3377.
9. Satyamoorthy K, Chehab NH, Waterman MJ, Lien MC, El-Deiry WS, et al. (2000) Aberrant regulation and function of wild-type p53 in radioresistant melanoma cells. Cell Growth Differ 11: 467-474.
10. Zhuang L, Lee CS, Scolyer RA, McCarthy SW, Zhang XD, et al. (2007) Mcl-1, Bcl-XL and Stat3 expression are associated with progression of melanoma whereas Bcl-2, AP-2 and MITF levels decrease during progression of melanoma. Mod Pathol 20: 416-426.
11. Kluger HM, McCarthy MM, Alvero AB, Sznol M, Ariyan S, et al. (2007) The X-linked inhibitor of apoptosis protein (XIAP) is up-regulated in metastatic melanoma, and XIAP cleavage by Phenoxodiol is associated with Carboplatin sensitization. J Transl Med 5: 6.
12. Chen N, Gong J, Chen X, Meng W, Huang Y, et al. (2009) Caspases and inhibitor of apoptosis proteins in cutaneous and mucosal melanoma: expression profile and clinicopathologic significance. Hum Pathol 40: 950-956.
13. Gong J, Chen N, Zhou Q, Yang B, Wang Y, et al. (2005) Melanoma inhibitor of apoptosis protein is expressed differentially in melanoma and melanocytic naevus, but similarly in primary and metastatic melanomas. J Clin Pathol 58: 1081-1085.
14. Falschlehner C, Ganten TM, Koschny R, Schaefer U, Walczak H, (2009) TRAIL and other TRAIL receptor agonists as novel cancer therapeutics. Adv Exp Med Biol 647: 195-206.
15. Daniel PT, Wieder T, Sturm I, Schulze-Osthoff K, (2001) The kiss of death: promises and failures of death receptors and ligands in cancer therapy. Leukemia 15: 1022-1032.
16. Fodstad O, Kjonniksen I, Aamdal S, Nesland JM, Boyd MR, et al. (1988) Extrapulmonary, tissue-specific metastasis formation in nude mice injected with FEMX-I human melanoma cells. Cancer Res 48: 4382-4388.
17. Fodstad O, Aamdal S, McMenamin M, Nesland JM, Pihl A, (1988) A new experimental metastasis model in athymic nude mice, the human malignant melanoma LOX. Int J Cancer 41: 442-449.
18. Herlyn M, (1990) Human melanoma: development and progression. Cancer Metastasis Rev 9: 101-112.
19. Eggermont AM, Kirkwood JM, (2004) Re-evaluating the role of dacarbazine in metastatic melanoma: what have we learned in 30 years? Eur J Cancer 40: 1825-1836.
20. Lillehammer T, Engesaeter BO, Prasmickaite L, Maelandsmo GM, Fodstad O, et al. (2007) Combined treatment with Ad-hTRAIL and DTIC or SAHA is associated with increased mitochondrial-mediated apoptosis in human melanoma cell lines. J Gene Med 9: 440-451.
21. Wakelee HA, Patnaik A, Sikic BI, Mita M, Fox NL, 7et al (2010) Phase I and pharmacokinetic study of lexatumumab (HGS-ETR2) given every 2 weeks in patients with advanced solid tumors. Ann Oncol 21: 376-381.
22. Plummer R, Attard G, Pacey S, Li L, Razak A, et al. (2007) Phase 1 and pharmacokinetic study of lexatumumab in patients with advanced cancers. Clin Cancer Res 13: 6187-6194.
23. Tolcher AW, Mita M, Meropol NJ, von Mehren M, Patnaik A, et al. (2007) Phase I pharmacokinetic and biologic correlative study of mapatumumab, a fully human monoclonal antibody with agonist activity to tumor necrosis factor-related apoptosis-inducing ligand receptor-1. J Clin Oncol 25: 1390-1395.
24. Greco FA, Bonomi P, Crawford J, Kelly K, Oh Y, et al. (2008) Phase 2 study of mapatumumab, a fully human agonistic monoclonal antibody which targets and activates the TRAIL receptor-1, in patients with advanced non-small cell lung cancer. Lung Cancer 61: 82-90.
25. Leong S, Cohen RB, Gustafson DL, Langer CJ, Camidge DR, et al. (2009) Mapatumumab, an antibody targeting TRAIL-R1, in combination with paclitaxel and carboplatin in patients with advanced solid malignancies: results of a phase I and pharmacokinetic study. J Clin Oncol 27: 4413-4421.
26. Mom CH, Verweij J, Oldenhuis CN, Gietema JA, Fox NL, et al. (2009) Mapatumumab, a fully human agonistic monoclonal antibody that targets TRAIL-R1, in combination with gemcitabine and cisplatin: a phase I study. Clin Cancer Res 15: 5584-5590.
27. Berger A, Quast SA, Plotz M, Hein M, Kunz M, et al. (2011) Sensitization of melanoma cells for death ligand-induced apoptosis by an indirubin derivative-Enhancement of both extrinsic and intrinsic apoptosis pathways. Biochem Pharmacol 81: 71-81.
28. Hornle M, Peters N, Thayaparasingham B, Vorsmann H, Kashkar H, et al. (2011) Caspase-3 cleaves XIAP in a positive feedback loop to sensitize melanoma cells to TRAIL-induced apoptosis. Oncogene 30: 575-587.
29. Zhang XD, Zhang XY, Gray CP, Nguyen T, Hersey P, (2001) Tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis of human melanoma is regulated by smac/DIABLO release from mitochondria. Cancer Res 61: 7339-7348.
30. Franco AV, Zhang XD, Van Berkel E, Sanders JE, Zhang XY, et al. (2001) The role of NF-kappa B in TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis of melanoma cells. J Immunol 166: 5337-5345.
31. Ivanov VN, Hei TK, (2006) Sodium arsenite accelerates TRAIL-mediated apoptosis in melanoma cells through upregulation of TRAIL-R1/R2 surface levels and downregulation of cFLIP expression. Exp Cell Res 312: 4120-4138.
32. Sloot AMVD, Tur V, Szegezdi E, Mullally MM, Cool RH, et al. (2006) Designed tumor necrosis factor-related apoptosis-inducing ligand variants initiating apoptosis exclusively via the DR5 receptor. Proc Natl Acad Sci U S A 103: 8634-8639.
33. Ding B, Wu X, Fan W, Wu Z, Gao J, et al. (2011) Anti-DR5 monoclonal antibody-mediated DTIC-loaded nanoparticles combining chemotherapy and immunotherapy for malignant melanoma: target formulation development and in vitro anticancer activity. Int J Nanomedicine 6: 1991-2005.
34. Roy S, Bayly CI, Gareau Y, Houtzager VM, Kargman S, et al. (2001) Maintenance of caspase-3 proenzyme dormancy by an intrinsic "safety catch" regulatory tripeptide. Proc Natl Acad Sci U S A 98: 6132-6137.
35. Eckelman BP, Salvesen GS, Scott FL, (2006) Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 7: 988-994.
36. Duckett CS, (2005) IAP proteins: sticking it to Smac. Biochem J 385: e1-2.
37. Vucic D, Franklin MC, Wallweber HJ, Das K, Eckelman BP, et al. (2005) Engineering ML-IAP to produce an extraordinarily potent caspase 9 inhibitor: implications for Smac-dependent anti-apoptotic activity of ML-IAP. Biochem J 385: 11-20.
38. Engesaeter BO, Sathermugathevan M, Hellenes T, Engebraten O, Holm R, et al. (2011) Targeting inhibitor of apoptosis proteins in combination with dacarbazine or TRAIL in melanoma cells. Cancer Biol Ther 12: 47-58.
39. Nachmias B, Ashhab Y, Bucholtz V, Drize O, Kadouri L, et al. (2003) Caspase-mediated cleavage converts Livin from an antiapoptotic to a proapoptotic factor: implications for drug-resistant melanoma. Cancer Res 63: 6340-6349.
40. Nachmias B, Mizrahi S, Elmalech M, Lazar I, Ashhab Y, et al. (2007) Manipulation of NK cytotoxicity by the IAP family member Livin. Eur J Immunol 37: 3467-3476.
41. Gyrd-Hansen M, Darding M, Miasari M, Santoro MM, Zender L, et al. (2008) IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat Cell Biol 10: 1309-1317.
42. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, et al. (2008) Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 9: 1364-1370.
43. Corazza N, Jakob S, Schaer C, Frese S, Keogh A, et al. (2006) TRAIL receptor-mediated JNK activation and Bim phosphorylation critically regulate Fas-mediated liver damage and lethality. J Clin Invest 116: 2493-2499.
44. Schneider-Jakob S, Corazza N, Badmann A, Sidler D, Stuber-Roos R, et al. (2010) Synergistic induction of cell death in liver tumor cells by TRAIL and chemotherapeutic drugs via the BH3-only proteins Bim and Bid. Cell Death Dis 1: e86.
45. Marini P, Denzinger S, Schiller D, Kauder S, Welz S, et al. (2006) Combined treatment of colorectal tumours with agonistic TRAIL receptor antibodies HGS-ETR1 and HGS-ETR2 and radiotherapy: enhanced effects in vitro and dose-dependent growth delay in vivo. Oncogene 25: 5145-5154.
46. von Haefen C, Gillissen B, Hemmati PG, Wendt J, Guner D, et al. (2004) Multidomain Bcl-2 homolog Bax but not Bak mediates synergistic induction of apoptosis by TRAIL and 5-FU through the mitochondrial apoptosis pathway. Oncogene 23: 8320-8332.