Targeting FLIP and Mcl-1 using a combination of aspirin and sorafenib sensitizes colon cancer cells to TRAIL

Journal of Pathology

Volumn 229, Issue 3, 2013, Pages 410-421

  Pennarun, Bodvael ^a   Kleibeuker, Jan H ^a   Van Ek, Wytske Boersma ^a   Kruyt, Frank Ae ^a   Hollema, Harry ^a   De Vries, Elisabeth Ge ^a   De Jong, Steven ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

aspirin; FLIP; Mcl 1; sorafenib; TRAIL

Indexed keywords

ACETYLSALICYLIC ACID; BEVACIZUMAB; CARBOPLATIN; DULANERMIN; FLICE INHIBITORY PROTEIN; MAPATUMUMAB; PACLITAXEL; PROTEIN MCL 1; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; SORAFENIB;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE ARREST; COLON ADENOMA; COLON CANCER; COLON CARCINOMA; CONTROLLED STUDY; DRUG POTENCY; DRUG POTENTIATION; DRUG SENSITIZATION; DRUG TARGETING; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MITOSIS INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOCARCINOMA; ADENOMA; ANTINEOPLASTIC AGENTS; APOPTOSIS; ASPIRIN; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; DRUG THERAPY, COMBINATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTESTINAL MUCOSA; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECOMBINANT PROTEINS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR STEM CELL ASSAY;

EID: 84872928550     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4138     Document Type: Article

References (61)

1. Jemal A, Siegel R, Ward E, et al,. Cancer Statistics, 2008. CA Cancer J Clin 2008; 58: 71-96. (Pubitemid 351521864)
2. Baron JA, Cole BF, Sandler RS, et al,. A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med 2003; 348: 891-899. (Pubitemid 36297997)
3. Jalving M, Koornstra JJ, de Jong S, et al,. Review article: the potential of combinational regimen with non-steroidal anti-inflammatory drugs in the chemoprevention of colorectal cancer. Aliment Pharmacol Ther 2005; 21: 321-339. (Pubitemid 40313936)
4. Chan AT, Cook NR,. Are we ready to recommend aspirin for cancer prevention? Lancet 2012; 379: 1569-1571.
5. Rothwell PM, Wilson M, Price JF, et al,. Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet 2012; 379: 1591-601.
6. de Groot DJ, de Vries EGE, Groen HJ, et al,. Non-steroidal anti-inflammatory drugs to potentiate chemotherapy effects: from lab to clinic. Crit Rev Oncol Hematol 2007; 61: 52-69. (Pubitemid 44880148)
7. Wilhelm S, Carter C, Tang L, et al,. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004; 64: 7099-7109. (Pubitemid 39331023)
8. Plastaras JP, Kim SH, Liu YY, et al,. Cell cycle dependent and schedule-dependent antitumor effects of sorafenib combined with radiation. Cancer Res 2007; 67: 9443-9454. (Pubitemid 47535934)
9. Yu C, Bruzek LM, Meng XW, et al,. The role of Mcl-1 downregulation in the proapoptotic activity of the multikinase inhibitor BAY 43-9006. Oncogene 2005; 24: 6861-6869. (Pubitemid 41509409)
10. 1 cell cycle arrest in human pancreatic cancer cell lines. J Gastrointest Surg 2000; 4: 24-32.
11. Iglesias-Serret D, Pique M, Gil J, et al,. Transcriptional and translational control of Mcl-1 during apoptosis. Arch Biochem Biophys 2003; 417: 141-152. (Pubitemid 36993789)
12. Johnstone RW, Frew AJ, Smyth MJ,. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008; 8: 782-798.
13. Koornstra JJ, Kleibeuker JH, van Geelen CMM, et al,. Expression of TRAIL (TNF-related apoptosis-inducing ligand) and its receptors in normal colonic mucosa, adenomas, and carcinomas. J Pathol 2003; 200: 327-335. (Pubitemid 36827307)
14. Hague A, Hicks DJ, Hasan F, et al,. Increased sensitivity to TRAIL-induced apoptosis occurs during the adenoma to carcinoma transition of colorectal carcinogenesis. Br J Cancer 2005; 92: 736-742. (Pubitemid 40460611)
15. Jalving M, de Jong S, Koornstra JJ, et al,. TRAIL induces apoptosis in human colorectal adenoma cell lines and human colorectal adenomas. Clin Cancer Res 2006; 12: 4350-4356.
16. Oldenhuis CNAM, Stegehuis JH, Walenkamp AME, et al,. Targeting TRAIL death receptors. Curr Opin Pharmacol 2008; 8: 433-439.
17. Soria J, Smit E, Khayat D, et al,. Phase 1b study of dulanermin (recombinant human Apo2L/TRAIL) in combination with paclitaxel, carboplatin, and bevacizumab in patients with advanced non-squamous non-small-cell lung cancer. J Clin Oncol 2010; 28: 1527-1533.
18. Kim KM, Song JJ, An JY, et al,. Pretreatment of acetylsalicylic acid promotes tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by down-regulating BCL-2 gene expression. J Biol Chem 2005; 280: 41047-41056. (Pubitemid 41780600)
19. Ricci MS, Kim SH, Ogi K, et al,. Reduction of TRAIL-induced Mcl-1 and cIAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 2007; 12: 66-80. (Pubitemid 47001783)
20. van Geelen CMM, de Vries EGE, Le TKP, et al,. Differential modulation of the TRAIL receptors and the CD95 receptor in colon carcinoma cell lines. Br J Cancer 2003; 89: 363-373. (Pubitemid 36976328)
21. Heijink DM, Kleibeuker JH, Jalving M, et al,. Independent induction of caspase-8 and cFLIP expression during colorectal carcinogenesis in sporadic and HNPCC adenomas and carcinomas. Cell Oncol 2007; 29: 409-419. (Pubitemid 47255979)
22. Chou TC,. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2012; 58: 621-681.
23. Clark JW, Eder JP, Ryan D, et al,. Safety and pharmacokinetics of the dual action Raf kinase and vascular endothelial growth factor receptor inhibitor, BAY 43-9006, in patients with advanced, refractory solid tumors. Clin Cancer Res 2005; 11: 5472-5480. (Pubitemid 41060823)
24. Calleros L, Sanchez-Hernandez I, Baquero P, et al,. Oncogenic Ras, but not V600EB-RAF, protects from cholesterol depletion-induced apoptosis through the PI3K/AKT pathway in colorectal cancer cells. Carcinogenesis 2009; 30: 1670-1677.
25. Hao H, Muniz-Medina V, Mehta H, et al,. Context-dependent roles of mutant B-Raf signaling in melanoma and colorectal carcinoma cell growth. Mol Cancer Ther 2007; 6: 2220-2229. (Pubitemid 47294750)
26. Rosato RR, Almenara JA, Coe S, et al,. The multikinase inhibitor sorafenib potentiates TRAIL lethality in human leukemia cells in association with Mcl-1 and cFLIPL down-regulation. Cancer Res 2007; 67: 9490-9500. (Pubitemid 47535939)
27. Krueger A, Baumann S, Krammer PH, et al,. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol Cell Biol 2001; 21: 8247-8254. (Pubitemid 33108586)
28. Willis SN, Chen L, Dewson G, et al,. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 2005; 19: 1294-1305. (Pubitemid 41003019)
29. Tait SW, Green DR,. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11: 621-632.
30. Deng Y, Lin Y, Wu X,. TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev 2002; 16: 33-45. (Pubitemid 34049636)
31. Maas C, Verbrugge I, de VE, et al. Smac/DIABLO release from mitochondria and XIAP inhibition are essential to limit clonogenicity of type I tumor cells after TRAIL receptor stimulation. Cell Death Differ 2010; 17: 1613-1623.
32. Wilson TR, McEwan M, McLaughlin K, et al,. Combined inhibition of FLIP and XIAP induces Bax-independent apoptosis in type II colorectal cancer cells. Oncogene 2009; 28: 63-72.
33. Haag C, Stadel D, Zhou S, et al,. Identification of c-FLIPL and c-FLIPS as critical regulators of death receptor-induced apoptosis in pancreatic cancer cells. Gut 2010; 60: 225-237.
34. Seal S, Hockenbery DM, Spaulding EY, et al,. Differential responses of FLIPLong and FLIPShort-overexpressing human myeloid leukemia cells to TNF-α- and TRAIL-initiated apoptotic signals. Exp Hematol 2008; 36: 1660-1672.
35. Rampino N, Yamamoto H, Ionov Y, et al,. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 1997; 275: 967-969. (Pubitemid 27087710)
36. Desagher S, Osen-Sand A, Nichols A, et al,. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 1999; 144: 891-901. (Pubitemid 29238966)
37. Wei MC, Lindsten T, Mootha VK, et al,. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 2000; 14: 2060-2071. (Pubitemid 30637355)
38. Barnhart BC, Alappat EC, Peter ME,. The CD95 type I/type II model. Semin Immunol 2003; 15: 185-193. (Pubitemid 38155825)
39. Hector S, Prehn J,. Apoptosis signaling proteins as prognostic biomarkers in colorectal cancer: a review. Biochim Biophys Acta Rev Cancer 2009; 1795: 117-129.
40. Zhou W, Hu J, Tang H, et al,. Small interfering RNA targeting mcl-1 enhances proteasome inhibitor-induced apoptosis in various solid malignant tumors. BMC Cancer 2011; 11: 485.
41. Shirley S, Micheau O,. Targeting c-FLIP in cancer. Cancer Lett 2010; in press. doi: 10.1016/j.canlet.2010.10.009.
42. Chen F, Zhu HH, Zhou LF, et al,. Inhibition of c-FLIP expression by miR-512-3p contributes to taxol-induced apoptosis in hepatocellular carcinoma cells. Oncol Rep 2010; 23: 1457-1462.
43. Longley DB, Wilson TR, McEwan M, et al,. c-FLIP inhibits chemotherapy-induced colorectal cancer cell death. Oncogene 2006; 25: 838-848. (Pubitemid 43237702)
44. Wilson TR, McLaughlin KM, McEwan M, et al,. c-FLIP: a key regulator of colorectal cancer cell death. Cancer Res 2007; 67: 5754-5762. (Pubitemid 46985008)
45. Krajewska M, Moss SF, Krajewski S, et al,. Elevated expression of Bcl-X and reduced Bak in primary colorectal adenocarcinomas. Cancer Res 1996; 56: 2422-2427. (Pubitemid 26154093)
46. Schulze-Bergkamen H, Ehrenberg R, Hickmann L, et al,. Bcl-x(L) and myeloid cell leukaemia-1 contribute to apoptosis resistance of colorectal cancer cells. World J Gastroenterol 2008; 14: 3829-3840.
47. Koornstra JJ, de Jong S, Hollema H, et al,. Changes in apoptosis during the development of colorectal cancer: a systematic review of the literature. Crit Rev Oncol Hematol 2003; 45: 37-53. (Pubitemid 35449787)
48. LeBlanc H, Lawrence D, Varfolomeev E, et al,. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med 2002; 8: 274-281. (Pubitemid 34250106)
49. Mott J, Bronk S, Mesa R, et al,. BH3-only protein mimetic obatoclax sensitizes cholangiocarcinoma cells to Apo2L/TRAIL-induced apoptosis. Mol Cancer Ther 2008; 7: 2339-2347.
50. Wei MC, Zong WX, Cheng EH, et al,. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730. (Pubitemid 32385543)
51. von Haefen C, Gillissen B, Hemmati PG, et al,. Multidomain Bcl-2 homolog Bax but not Bak mediates synergistic induction of apoptosis by TRAIL and 5-FU through the mitochondrial apoptosis pathway. Oncogene 2004; 23: 8320-8332. (Pubitemid 39531843)
52. Wang S, El Deiry WS,. Requirement of p53 targets in chemosensitization of colonic carcinoma to death ligand therapy. Proc Natl Acad Sci USA 2003; 100: 15095-15100. (Pubitemid 37518022)
53. Wang SH, Mezosi E, Wolf JM, et al,. IFN-γ sensitization to TRAIL-induced apoptosis in human thyroid carcinoma cells by upregulating Bak expression. Oncogene 2004; 23: 928-935. (Pubitemid 38250938)
54. Sherr C, McCormick F,. The RB and p53 pathways in cancer. Cancer Cell 2002; 2: 103-112. (Pubitemid 41039110)
55. Takada Y, Bhardwaj A, Potdar P, et al,. Nonsteroidal anti-inflammatory agents differ in their ability to suppress NF-κB activation, inhibition of expression of cyclooxygenase-2 and cyclin D1, and abrogation of tumor cell proliferation. Oncogene 2004; 23: 9247-9258. (Pubitemid 40069695)
56. Heijink DM, Jalving M, Oosterhuis D, et al,. TNF-related apoptosis-inducing ligand cooperates with NSAIDs via activated Wnt signalling in (pre)malignant colon cells. J Pathol 2011; 223: 378-389.
57. van Geelen CMM, de Vries EGE, de Jong S,. Lessons from TRAIL-resistance mechanisms in colorectal cancer cells: paving the road to patient-tailored therapy. Drug Resist Updat 2004; 7: 345-358. (Pubitemid 40341956)
58. Soria JC, Márk Z, Zatloukal P, et al,. Randomized phase II study of dulanermin in combination with paclitaxel, carboplatin, and bevacizumab in advanced non-small-cell lung cancer. J Clin Oncol 2011; 29: 4442-4451.
59. Sun W, Nelson D, Alberts SR, et al,. Phase Ib study of mapatumumab in combination with sorafenib in patients with advanced hepatocellular carcinoma (HCC) and chronic viral hepatitis. J Clin Oncol 2011; 29: no 4, suppl 261.
60. Hellwig CT, Rehm M,. TRAIL Signaling and synergy mechanisms used in TRAIL-based combination therapies. Mol Cancer Ther 2012; 11: 3-13.
61. den Hollander MW, Gietema JA, de Jong S, et al,. Translating TRAIL-receptor targeting agents to the clinic. Cancer Lett 2012; in press. doi: 10.1016/j.canlet.2012.04.007.