C-FLIP degradation mediates sensitization of pancreatic cancer cells to trail-induced apoptosis by the histone deacetylase inhibitor LBH589

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Kauh, John ^a   Fan, Songqing ^a   Xia, Mingjing ^a   Yue, Ping ^a   Yang, Lily ^a   Khuri, Fadlo R ^a   Sun, Shi Yong ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; FLICE INHIBITORY PROTEIN; HISTONE DEACETYLASE INHIBITOR; PANOBINOSTAT; PROTEASOME; PROTEASOME INHIBITOR; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; SURVIVIN; UBIQUITIN; CFLAR PROTEIN, HUMAN; HYDROXAMIC ACID; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIZATION; HUMAN; HUMAN CELL; PANCREAS CANCER; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; UBIQUITINATION; DRUG EFFECT; METABOLISM; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL LINE, TUMOR; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; PANCREATIC NEOPLASMS; PROTEIN STABILITY; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UBIQUITINATION;

EID: 77955584671     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010376     Document Type: Article

References (53)

1. Wong HH, Lemoine NR (2009) Pancreatic cancer: molecular pathogenesis and new therapeutic targets. Nat Rev Gastroenterol Hepatol 6: 412-422.
2. Hamacher R, Schmid RM, Saur D, Schneider G (2008) Apoptotic pathways in pancreatic ductal adenocarcinoma. Mol Cancer 7: 64.
3. Schneider G, Siveke JT, Eckel F, Schmid RM (2005) Pancreatic cancer: basic and clinical aspects. Gastroenterology 128: 1606-1625.
4. Sun SY, Hail N, Jr., Lotan R (2004) Apoptosis as a novel target for cancer chemoprevention. J Natl Cancer Inst 96: 662-672.
5. Fulda S (2009) Apoptosis pathways and their therapeutic exploitation in pancreatic cancer. J Cell Mol Med 13: 1221-1227.
6. Zimmermann KC, Green DR (2001) How cells die: apoptosis pathways. J Allergy Clin Immunol 108: S99-103.
7. Lavrik I, Golks A, Krammer PH (2005) Death receptor signaling. J Cell Sci 118: 265-267.
8. Kelley SK, Ashkenazi A (2004) Targeting death receptors in cancer with Apo2L/TRAIL. Curr Opin Pharmacol 4: 333-339.
9. Rowinsky EK (2005) Targeted induction of apoptosis in cancer management: the emerging role of tumor necrosis factor-related apoptosis-inducing ligand receptor activating agents. J Clin Oncol 23: 9394-9407.
10. Takeda K, Stagg J, Yagita H, Okumura K, Smyth MJ (2007) Targeting deathinducing receptors in cancer therapy. Oncogene 26: 3745-3757.
11. Wu GS, Burns TF, McDonald ER, 3rd, Jiang W, Meng R, et al. (1997) KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet 17: 141-143.
12. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, et al. (2009) Small molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma. Cancer Res 69: 2425-2434.
13. Murtaza I, Saleem M, Adhami VM, Hafeez BB, Mukhtar H (2009) Suppression of cFLIP by lupeol, a dietary triterpene, is sufficient to overcome resistance to TRAIL-mediated apoptosis in chemoresistant human pancreatic cancer cells. Cancer Res 69: 1156-1165.
14. Huang S, Okumura K, Sinicrope FA (2009) BH3 mimetic obatoclax enhances TRAIL-mediated apoptosis in human pancreatic cancer cells. Clin Cancer Res 15: 150-159.
15. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, et al. (2008) Targeting XIAP bypasses Bcl-2-mediated resistance to TRAIL and cooperates with TRAIL to suppress pancreatic cancer growth in vitro and in vivo. Cancer Res 68: 7956-7965.
16. Huang S, Sinicrope FA (2008) BH3 mimetic ABT-737 potentiates TRAILmediated apoptotic signaling by unsequestering Bim and Bak in human pancreatic cancer cells. Cancer Res 68: 2944-2951.
17. Wang P, Zhang J, Bellail A, Jiang W, Hugh J, et al. (2007) Inhibition of RIP and c-FLIP enhances TRAIL-induced apoptosis in pancreatic cancer cells. Cell Signal 19: 2237-2246.
18. Hylander BL, Pitoniak R, Penetrante RB, Gibbs JF, Oktay D, et al. (2005) The anti-tumor effect of Apo2L/TRAIL on patient pancreatic adenocarcinomas grown as xenografts in SCID mice. J Transl Med 3: 22.
19. Xu ZW, Kleeff J, Friess H, Buchler MW, Solioz M (2003) Synergistic cytotoxic effect of TRAIL and gemcitabine in pancreatic cancer cells. Anticancer Res 23: 251-258.
20. Matsuzaki H, Schmied BM, Ulrich A, Standop J, Schneider MB, et al. (2001) Combination of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and actinomycin D induces apoptosis even in TRAIL-resistant human pancreatic cancer cells. Clin Cancer Res 7: 407-414.
21. Krueger A, Baumann S, Krammer PH, Kirchhoff S (2001) FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol Cell Biol 21: 8247-8254.
22. Budd RC, Yeh WC, Tschopp J (2006) cFLIP regulation of lymphocyte activation and development. Nat Rev Immunol 6: 196-204.
23. Kim Y, Suh N, Sporn M, Reed JC (2002) An inducible pathway for degradation of FLIP protein sensitizes tumor cells to TRAIL-induced apoptosis. J Biol Chem 277: 22320-22329.
24. Poukkula M, Kaunisto A, Hietakangas V, Denessiouk K, Katajamaki T, et al. (2005) Rapid turnover of c-FLIPshort is determined by its unique C-terminal tail. J Biol Chem 280: 27345-27355.
25. Chang L, Kamata H, Solinas G, Luo JL, Maeda S, et al. (2006) The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover. Cell 124: 601-613.
26. Wajant H (2003) Targeting the FLICE Inhibitory Protein (FLIP) in cancer therapy. Mol Interv 3: 124-127.
27. Atadja P (2009) Development of the pan-DAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett 280: 233-241.
28. Haefner M, Bluethner T, Niederhagen M, Moebius C, Wittekind C, et al. (2008) Experimental treatment of pancreatic cancer with two novel histone deacetylase inhibitors. World J Gastroenterol 14: 3681-3692.
29. Liu X, Yue P, Schonthal AH, Khuri FR, Sun SY (2006) Cellular FLICEinhibitory protein down-regulation contributes to celecoxib-induced apoptosis in human lung cancer cells. Cancer Res 66: 11115-11119.
30. Lin Y, Liu X, Yue P, Benbrook DM, Berlin KD, et al. (2008) Involvement of c- FLIP and survivin down-regulation in flexible heteroarotinoid-induced apoptosis and enhancement of TRAIL-initiated apoptosis in lung cancer cells. Mol Cancer Ther 7: 3556-3565.
31. Sun SY, Yue P, Dawson MI, Shroot B, Michel S, et al. (1997) Differential effects of synthetic nuclear retinoid receptor-selective retinoids on the growth of human non-small cell lung carcinoma cells. Cancer Res 57: 4931-4939.
32. Sun SY, Yue P, Wu GS, El-Deiry WS, Shroot B, et al. (1999) Mechanisms of apoptosis induced by the synthetic retinoid CD437 in human non-small cell lung carcinoma cells. Oncogene 18: 2357-2365.
33. Liu X, Yue P, Zhou Z, Khuri FR, Sun SY (2004) Death receptor regulation and celecoxib-induced apoptosis in human lung cancer cells. J Natl Cancer Inst 96: 1769-1780.
34. Chen S, Liu X, Yue P, Schonthal AH, Khuri FR, et al. (2007) CHOP-dependent DR5 induction and ubiquitin/proteasome-mediated c-FLIP downregulation contribute to enhancement of TRAIL-induced apoptosis by dimethyl-celecoxib in human non-small cell lung cancer cells. Mol Pharmacol 72: 1269-1279.
35. Zhang L, Fang B (2005) Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther 12: 228-237.
36. Chawla-Sarkar M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, et al. (2004) Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 11: 915-923.
37. Vogler M, Durr K, Jovanovic M, Debatin KM, Fulda S (2007) Regulation of TRAIL-induced apoptosis by XIAP in pancreatic carcinoma cells. Oncogene 26: 248-257.
38. Kim EH, Kim HS, Kim SU, Noh EJ, Lee JS, et al. (2005) Sodium butyrate sensitizes human glioma cells to TRAIL-mediated apoptosis through inhibition of Cdc2 and the subsequent downregulation of survivin and XIAP. Oncogene 24: 6877-6889.
39. Guo F, Sigua C, Tao J, Bali P, George P, et al. (2004) Cotreatment with histone deacetylase inhibitor LAQ824 enhances Apo-2L/tumor necrosis factor-related apoptosis inducing ligand-induced death inducing signaling complex activity and apoptosis of human acute leukemia cells. Cancer Res 64: 2580-2589.
40. Symanowski J, Vogelzang N, Zawel L, Atadja P, Pass H, et al. (2009) A histone deacetylase inhibitor LBH589 downregulates XIAP in mesothelioma cell lineswhich is likely responsible for increased apoptosis with TRAIL. J Thorac Oncol 4: 149-160.
41. Singh TR, Shankar S, Srivastava RK (2005) HDAC inhibitors enhance the apoptosis-inducing potential of TRAIL in breast carcinoma. Oncogene 24: 4609-4623.
42. Neuzil J, Swettenham E, Gellert N (2004) Sensitization of mesothelioma to TRAIL apoptosis by inhibition of histone deacetylase: role of Bcl-xL downregulation. Biochem Biophys Res Commun 314: 186-191.
43. Rosato RR, Almenara JA, Dai Y, Grant S (2003) Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Mol Cancer Ther 2: 1273-1284.
44. Zhang XD, Gillespie SK, Borrow JM, Hersey P (2003) The histone deacetylase inhibitor suberic bishydroxamate: a potential sensitizer of melanoma to TNFrelated apoptosis-inducing ligand (TRAIL) induced apoptosis. Biochem Pharmacol 66: 1537-1545.
45. Elrod HA, Sun SY (2007) Modulation of death receptors by cancer therapeutic agents. Cancer Biol Ther 7: 163-173.
46. Pathil A, Armeanu S, Venturelli S, Mascagni P, Weiss TS, et al. (2006) HDAC inhibitor treatment of hepatoma cells induces both TRAIL-independent apoptosis and restoration of sensitivity to TRAIL. Hepatology 43: 425-434.
47. Schuchmann M, Schulze-Bergkamen H, Fleischer B, Schattenberg JM, Siebler J, et al. (2006) Histone deacetylase inhibition by valproic acid down-regulates c- FLIP/CASH and sensitizes hepatoma cells towards CD95- and TRAIL receptor-mediated apoptosis and chemotherapy. Oncol Rep 15: 227-230.
48. Darvas K, Rosenberger S, Brenner D, Fritsch C, Gmelin N, et al. (2010) Histone deacetylase inhibitor-induced sensitization to TNFalpha/TRAIL-mediated apoptosis in cervical carcinoma cells is dependent on HPV oncogene expression. Int J Cancer.
49. Wood TE, Dalili S, Simpson CD, Sukhai MA, Hurren R, et al. (2010) Selective inhibition of histone deacetylases sensitizes malignant cells to death receptor ligands. Mol Cancer Ther 9: 246-256.
50. Sanda T, Okamoto T, Uchida Y, Nakagawa H, Iida S, et al. (2007) Proteome analyses of the growth inhibitory effects of NCH-51, a novel histone deacetylase inhibitor, on lymphoid malignant cells. Leukemia 21: 2344-2353.
51. Watanabe K, Okamoto K, Yonehara S (2005) Sensitization of osteosarcoma cells to death receptor-mediated apoptosis by HDAC inhibitors through downregulation of cellular FLIP. Cell Death Differ 12: 10-18.
52. Lucas DM, Davis ME, Parthun MR, Mone AP, Kitada S, et al. (2004) The histone deacetylase inhibitor MS-275 induces caspase-dependent apoptosis in Bcell chronic lymphocytic leukemia cells. Leukemia 18: 1207-1214.
53. Giles F, Fischer T, Cortes J, Garcia-Manero G, Beck J, et al. (2006) A phase I study of intravenous LBH589, a novel cinnamic hydroxamic acid analogue histone deacetylase inhibitor, in patients with refractory hematologic malignancies. Clin Cancer Res 12: 4628-4635.