The plant alkaloid and anti-leukemia drug homoharringtonine sensitizes resistant human colorectal carcinoma cells to TRAIL-induced apoptosis via multiple mechanisms

Apoptosis

Volumn 18, Issue 6, 2013, Pages 739-750

  Beranova, Lenka ^a   Pombinho, Antonio R ^a   Spegarova, Jarmila ^a   Koc, Michal ^a   Klanova, Magdalena ^b   Molinsky, Jan ^b   Klener, Pavel ^b   Bartunek, Petr ^a   Andera, Ladislav ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Apoptosis; cFLIP; Death receptor; Harringtonine; Mcl 1

Indexed keywords

ANTILEUKEMIC AGENT; EFFECTOR CASPASE; FLICE INHIBITORY PROTEIN; HOMOHARRINGTONINE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN MCL 1; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; CANCER CELL; CELL PROLIFERATION; CELL STRAIN HT29; CELL SURVIVAL; COLORECTAL CARCINOMA; DOWN REGULATION; DRUG MECHANISM; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; DRUG RESISTANCE, NEOPLASM; HARRINGTONINES; HT29 CELLS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSPLANTATION, HETEROLOGOUS;

CEPHALOTAXUS; MUS;

EID: 84880571214     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0823-9     Document Type: Article

References (55)

1. Venugopal B, Evans TR (2011) Developing histone deacetylase inhibitors as anti-cancer therapeutics. Curr Med Chem 18:1658-1671
2. Schumacher M, Kelkel M, Dicato M, Diederich M (2011) A survey of marine natural compounds and their derivatives with anti-cancer activity reported in 2010. Molecules 16:5629-5646
3. Scheinberg DA, Villa CH, Escorcia FE, McDevitt MR (2010) Conscripts of the infinite armada: systemic cancer therapy using nanomaterials. Nat Rev Clin Oncol 7:266-276
4. Biasutto L, Dong LF, Zoratti M, Neuzil J (2010) Mitochondrially targeted anti-cancer agents. Mitochondrion 10:670-681
5. Deckert PM (2009) Current constructs and targets in clinical development for antibody-based cancer therapy. Curr Drug Targets 10:158-175
6. Yerbes R, Palacios C, Lopez-Rivas A (2011) The therapeutic potential of TRAIL receptor signalling in cancer cells. Clin Transl Oncol 13:839-847
7. Bernardi S, Secchiero P, Zauli G (2012) State of art and recent developments of anti-cancer strategies based on TRAIL. Recent Pat Anticancer Drug Discov 7:207-217
8. Abdulghani J, El-Deiry WS (2010) TRAIL receptor signaling and therapeutics. Expert Opin Ther Targets 14:1091-1108
9. Pennarun B, Meijer A, de Vries EG, Kleibeuker JH, Kruyt F, de Jong S (2010) Playing the DISC: turning on TRAIL death receptor-mediated apoptosis in cancer. Biochim Biophys Acta 1805:123-140
10. Gonzalvez F, Ashkenazi A (2010) New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 29:4752-4765
11. Fu K, Ren H, Wang Y, Fei E, Wang H, Wang G (2011) DJ-1 inhibits TRAIL-induced apoptosis by blocking pro-caspase-8 recruitment to FADD. Oncogene 31:1311-1322
12. Cao X, Pobezinskaya YL, Morgan MJ, Liu ZG (2011) The role of TRADD in TRAIL-induced apoptosis and signaling. Faseb J 25:1353-1358
13. Sun M, Song L, Li Y, Zhou T, Jope RS (2008) Identification of an antiapoptotic protein complex at death receptors. Cell Death Differ 15:1887-1900
14. Mulherkar N, Prasad KV, Prabhakar BS (2007) MADD/DENN splice variant of the IG20 gene is a negative regulator of caspase-8 activation. Knockdown enhances TRAIL-induced apoptosis of cancer cells. J Biol Chem 282:11715-11721
15. Xiao C, Yang BF, Asadi N, Beguinot F, Hao C (2002) Tumor necrosis factor-related apoptosis-inducing ligand-induced death-inducing signaling complex and its modulation by c-FLIP and PED/PEA-15 in glioma cells. J Biol Chem 277:25020-25025
16. Castro Alves C, Terziyska N, Grunert M et al (2012) Leukemia-initiating cells of patient-derived acute lymphoblastic leukemia xenografts are sensitive towards TRAIL. Blood 119(18):4224-4227
17. Piggott L, Omidvar N, Perez SM, Eberl M, Clarkson RW (2011) Suppression of apoptosis inhibitor c-FLIP selectively eliminates breast cancer stem cell activity in response to the anti-cancer agent, TRAIL. Breast Cancer Res 13:R88
18. Zhang L, Fang B (2005) Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther 12:228-237
19. Ehrhardt H, Fulda S, Schmid I, Hiscott J, Debatin KM, Jeremias I (2003) TRAIL induced survival and proliferation in cancer cells resistant towards TRAIL-induced apoptosis mediated by NF-kappaB. Oncogene 22:3842-3852
20. Amm HM, Oliver PG, Lee CH, Li Y, Buchsbaum DJ (2011) Combined modality therapy with TRAIL or agonistic death receptor antibodies. Cancer Biol Ther 11:431-449
21. Fulda S (2012) Histone deacetylase (HDAC) inhibitors and regulation of TRAIL-induced apoptosis. Exp Cell Res 318(11):1208-1212
22. Sayers TJ (2011) Targeting the extrinsic apoptosis signaling pathway for cancer therapy. Cancer Immunol Immunother 60:1173-1180
23. Ding J, Polier G, Kohler R, Giaisi M, Krammer PH, Li-Weber M (2012) Wogonin and related natural flavones overcome tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) protein resistance of tumors by down-regulation of c-FLIP protein and up-regulation of TRAIL receptor 2 expression. J Biol Chem 287:641-649
24. Gupta SC, Reuter S, Phromnoi K et al (2011) Nimbolide sensitizes human colon cancer cells to TRAIL through reactive oxygen species- and ERK-dependent up-regulation of death receptors, p53, and Bax. J Biol Chem 286:1134-1146
25. Whitson EL, Sun H, Thomas CL et al (2012) Synergistic TRAIL sensitizers from barleria alluaudii and diospyros maritima. J Nat Prod 75:394-399
26. Kim TD, Frick M, le Coutre P (2011) Omacetaxine mepesuccinate for the treatment of leukemia. Expert Opin Pharmacother 12:2381-2392
27. Klag T, Hartel N, Erben P et al (2012) Omacetaxine mepesuccinate prevents cytokine-dependent resistance to nilotinib in vitro: potential role of the common beta-subunit c of cytokine receptors. Leukemia 26:1321-1328
28. Meng H, Yang C, Jin J, Zhou Y, Qian W (2008) Homoharringtonine inhibits the AKT pathway and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Leuk Lymphoma 49:1954-1962
29. Eckelbarger JD, Wilmot JT, Epperson MT et al (2008) Synthesis of antiproliferative Cephalotaxus esters and their evaluation against several human hematopoietic and solid tumor cell lines: uncovering differential susceptibilities to multidrug resistance. Chemistry 14:4293-4306
30. Efferth T, Sauerbrey A, Halatsch ME, Ross DD, Gebhart E (2003) Molecular modes of action of cephalotaxine and homoharringtonine from the coniferous tree Cephalotaxus hainanensis in human tumor cell lines. Naunyn Schmiedebergs Arch Pharmacol 367:56-67
31. Dimberg LY, Anderson CK, Camidge R, Behbakht K, Thorburn A, Ford HL (2012) On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics. Oncogene. doi: 10.1038/onc.2012.164
32. Siegemund M, Pollak N, Seifert O et al (2012) Superior antitumoral activity of dimerized targeted single-chain TRAIL fusion proteins under retention of tumor selectivity. Cell Death Dis 3:e295
33. Frese S, Schuller A, Frese-Schaper M, Gugger M, Schmid RA (2009) Cytotoxic effects of camptothecin and cisplatin combined with tumor necrosis factor-related apoptosis-inducing ligand (Apo2L/TRAIL) in a model of primary culture of non-small cell lung cancer. Anticancer Res 29:2905-2911
34. Chen LH, Jiang CC, Kiejda KA et al (2007) Thapsigargin sensitizes human melanoma cells to TRAIL-induced apoptosis by up-regulation of TRAIL-R2 through the unfolded protein response. Carcinogenesis 28:2328-2336
35. Chen R, Guo L, Chen Y, Jiang Y, Wierda WG, Plunkett W (2011) Homoharringtonine reduced Mcl-1 expression and induced apoptosis in chronic lymphocytic leukemia. Blood 117:156-164
36. Sah NK, Munshi A, Kurland JF, McDonnell TJ, Su B, Meyn RE (2003) Translation inhibitors sensitize prostate cancer cells to apoptosis induced by tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) by activating c-Jun N-terminal kinase. J Biol Chem 278:20593-20602
37. Kantarjian HM, Talpaz M, Santini V, Murgo A, Cheson B, O'Brien SM (2001) Homoharringtonine: history, current research, and future direction. Cancer 92:1591-1605
38. Kim SH, Ricci MS, El-Deiry WS (2008) Mcl-1: a gateway to TRAIL sensitization. Cancer Res 68:2062-2064
39. Bagnoli M, Canevari S, Mezzanzanica D (2011) Cellular FLICE-inhibitory protein (c-FLIP) signalling: a key regulator of receptor-mediated apoptosis in physiologic context and in cancer. Int J Biochem Cell Biol 42:210-213
40. Sharp DA, Lawrence DA, Ashkenazi A (2005) Selective knockdown of the long variant of cellular FLICE inhibitory protein augments death receptor-mediated caspase-8 activation and apoptosis. J Biol Chem 280:19401-19409
41. Haag C, Stadel D, Zhou S et al (2011) Identification of c-FLIP(L) and c-FLIP(S) as critical regulators of death receptor-induced apoptosis in pancreatic cancer cells. Gut 60:225-237
42. Thome M, Schneider P, Hofmann K et al (1997) Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517-521
43. Pop C, Oberst A, Drag M et al (2011) FLIP(L) induces caspase 8 activity in the absence of interdomain caspase 8 cleavage and alters substrate specificity. Biochem J 433:447-457
44. Fricker N, Beaudouin J, Richter P, Eils R, Krammer PH, Lavrik IN (2011) Model-based dissection of CD95 signaling dynamics reveals both a pro- and antiapoptotic role of c-FLIPL. J Cell Biol 190:377-389
45. Micheau O, Thome M, Schneider P et al (2002) The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem 277:45162-45171
46. Tromp JM, Geest CR, Breij EC et al (2012) Tipping the Noxa/Mcl-1 balance overcomes ABT-737 resistance in chronic lymphocytic leukemia. Clin Cancer Res 18:487-498
47. Jacquemin G, Granci V, Gallouet AS et al (2012) Quercetin-mediated Mcl-1 and survivin downregulation restores TRAIL-induced apoptosis in non-Hodgkin's lymphoma B cells. Haematologica 97:38-46
48. Leitch AE, Riley NA, Sheldrake TA et al (2010) The cyclin-dependent kinase inhibitor R-roscovitine down-regulates Mcl-1 to override pro-inflammatory signalling and drive neutrophil apoptosis. Eur J Immunol 40:1127-1138
49. Pennarun B, Kleibeuker JH, Boersma-van Ek W et al (2012) Targeting FLIP and Mcl-1 using a combination of aspirin and sorafenib sensitizes colon cancer cells to TRAIL. J Pathol 229(3):410-421
50. Ricci MS, Kim SH, Ogi K et al (2007) Reduction of TRAIL-induced Mcl-1 and cIAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 12:66-80
51. Jennewein C, Karl S, Baumann B, Micheau O, Debatin KM, Fulda S (2012) Identification of a novel pro-apoptotic role of NF-kappaB in the regulation of TRAIL- and CD95-mediated apoptosis of glioblastoma cells. Oncogene 31:1468-1474
52. Koschny R, Ganten TM, Sykora J et al (2007) TRAIL/bortezomib cotreatment is potentially hepatotoxic but induces cancer-specific apoptosis within a therapeutic window. Hepatology 45:649-658
53. Lecis D, Drago C, Manzoni L et al (2010) Novel SMAC-mimetics synergistically stimulate melanoma cell death in combination with TRAIL and bortezomib. Br J Cancer 102:1707-1716
54. Menke C, Bin L, Thorburn J, Behbakht K, Ford HL, Thorburn A (2011) Distinct TRAIL resistance mechanisms can be overcome by proteasome inhibition but not generally by synergizing agents. Cancer Res 71:1883-1892
55. Unterkircher T, Cristofanon S, Vellanki SH et al (2011) Bortezomib primes glioblastoma, including glioblastoma stem cells, for TRAIL by increasing tBid stability and mitochondrial apoptosis. Clin Cancer Res 17:4019-4030