Histone deacetylase inhibitor-mediated sensitization to TRAIL-induced apoptosis in childhood malignancies is not associated with upregulation of TRAIL receptor expression, but with potentiated caspase-8 activation

Cancer Biology and Therapy

Volumn 13, Issue 6, 2012, Pages 417-424

  Sonnemann, Jürgen ^a   Trommer, Navina ^a   Becker, Sabine ^a   Wittig, Susan ^a   Grauel, Désirée ^a   Palani, Chithra D ^a   Beck, James F ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Bortezomib; Caspase 8; Childhood tumor; Death receptor; Histone deacetylase inhibitors; TRAIL

Indexed keywords

APICIDIN; CASPASE 8; ENTINOSTAT; ETOPOSIDE; HISTONE DEACETYLASE INHIBITOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; VORINOSTAT;

APOPTOSIS; ARTICLE; CHILDHOOD CANCER; ENZYME ACTIVATION; EWING SARCOMA; MEDULLOBLASTOMA; OSTEOSARCOMA; PROTEIN EXPRESSION; SENSITIZATION; UPREGULATION;

APOPTOSIS; BONE NEOPLASMS; CASPASE 8; CELL LINE, TUMOR; ENZYME ACTIVATION; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MEDULLOBLASTOMA; NEOPLASMS; OSTEOSARCOMA; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SARCOMA, EWING; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84860233044     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.19293     Document Type: Article

References (86)

1. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008; 7:1001-12; PMID:18989337; http://dx.doi.org/10.1038/nrd2637.
2. Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 2009; 27:5459-68; PMID:19826124; http://dx.doi.org/10.1200/JCO.2009. 22.1291.
3. Hernandez A, Thomas R, Smith F, Sandberg J, Kim S, Chung DH, et al. Butyrate sensitizes human colon cancer cells to TRAIL-mediated apoptosis. Surgery 2001; 130:265-72; PMID:11490359; http://dx.doi.org/10.1067/msy.2001. 115897.
4. Inoue H, Shiraki K, Ohmori S, Sakai T, Deguchi M, Yamanaka T, et al. Histone deacetylase inhibitors sensitize human colonic adenocarcinoma cell lines to TNF-related apoptosis inducing ligand-mediated apoptosis. Int J Mol Med 2002; 9:521-5; PMID:11956660.
5. Mitsiades N, Mitsiades CS, Richardson PG, McMullan C, Poulaki V, Fanourakis G, et al. Molecular sequelae of histone deacetylase inhibition in human malignant B cells. Blood 2003; 101:4055-62; PMID:12531799; http://dx.doi.org/10.1182/blood-2002-11-3514.
6. Rosato RR, Almenara JA, Dai Y, Grant S. 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 2003; 2:1273-84; PMID:14707268.
7. L downregulation. Biochem Biophys Res Commun 2004; 314:186-91; PMID:14715264; http://dx.doi.org/10.1016/j.bbrc.2003.12.074.
8. Guo F, Sigua C, Tao J, Bali P, George P, Li Y, et al. 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 2004; 64:2580-9; PMID:15059915; http://dx.doi.org/10.1158/0008-5472.CAN-03-2629.
9. Kim YH, Park JW, Lee JY, Kwon TK. Sodium butyrate sensitizes TRAIL-mediated apoptosis by induction of transcription from the DR5 gene promoter through Sp1 sites in colon cancer cells. Carcinogenesis 2004; 25:1813-20; PMID:15142888; http://dx.doi.org/10.1093/carcin/bgh188.
10. Nakata S, Yoshida T, Horinaka M, Shiraishi T, Wakada M, Sakai T. Histone deacetylase inhibitors upregulate death receptor 5/TRAIL-R2 and sensitize apoptosis induced by TRAIL/APO2-L in human malignant tumor cells. Oncogene 2004; 23:6261-71; PMID:15208660; http://dx.doi.org/10.1038/sj.onc.1207830.
11. Chopin V, Slomianny C, Hondermarck H, Le Bourhis X. Synergistic induction of apoptosis in breast cancer cells by cotreatment with butyrate and TNFalpha, TRAIL or anti-Fas agonist antibody involves enhancement of death receptors' signaling and requires p21(waf1). Exp Cell Res 2004; 298:560-73; PMID:15265702; http://dx.doi.org/10.1016/j.yexcr.2004.04.038.
12. Inoue S, MacFarlane M, Harper N, Wheat LM, Dyer MJ, Cohen GM. Histone deacetylase inhibitors potentiate TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in lymphoid malignancies. Cell Death Differ 2004; 11:193-206; PMID:15608694; http://dx.doi.org/10.1038/sj.cdd.4401535.
13. Watanabe K, Okamoto K, Yonehara S. Sensitization of osteosarcoma cells to death receptor-mediated apoptosis by HDAC inhibitors through downregulation of cellular FLIP. Cell Death Differ 2005; 12:10-8; PMID:15540114; http://dx.doi.org/10.1038/sj.cdd.4401507.
14. Sonnemann J, Gänge J, Kumar KS, Müller C, Bader P, Beck JF. Histone deacetylase inhibitors interact synergistically with tumor necrosis factor-related apoptosisinducing ligand (TRAIL) to induce apoptosis in carcinoma cell lines. Invest New Drugs 2005; 23:99-109; PMID:15744585; http://dx.doi.org/10.1007/s10637-005-5854-9.
15. Vanoosten RL, Moore JM, Ludwig AT, Griffith TS. Depsipeptide (FR901228) enhances the cytotoxic activity of TRAIL by redistributing TRAIL receptor to membrane lipid rafts. Mol Ther 2005; 11:542-52; PMID:15771957; http://dx.doi.org/10.1016/j.ymthe.2004.12.008.
16. Taghiyev AF, Guseva NV, Sturm MT, Rokhlin OW, Cohen MB. Trichostatin A (TSA) sensitizes the human prostatic cancer cell line DU145 to death receptor ligands treatment. Cancer Biol Ther 2005; 4:382-90; PMID:15846101; http://dx.doi.org/10.4161/cbt.4.4.1615.
17. MacFarlane M, Inoue S, Kohlhaas SL, Majid A, Harper N, Kennedy DB, et al. Chronic lymphocytic leukemic cells exhibit apoptotic signaling via TRAIL-R1. Cell Death Differ 2005; 12:773-82; PMID:15861184; http://dx.doi.org/10.1038/sj. cdd.4401649.
18. Singh TR, Shankar S, Srivastava RK. HDAC inhibitors enhance the apoptosis-inducing potential of TRAIL in breast carcinoma. Oncogene 2005; 24:4609-23; PMID:15897906; http://dx.doi.org/10.1038/sj.onc.1208585.
19. Shetty S, Graham BA, Brown JG, Hu X, Vegh-Yarema N, Harding G, et al. Transcription factor NFkappaB differentially regulates death receptor 5 expression involving histone deacetylase 1. Mol Cell Biol 2005; 25:5404-16; PMID:15964798; http://dx.doi.org/10.1128/MCB.25.13.5404-16.2005.
20. Kim EH, Kim HS, Kim SU, Noh EJ, Lee JS, Choi KS. Sodium butyrate sensitizes human glioma cells to TRAIL-mediated apoptosis through inhibition of Cdc2 and the subsequent downregulation of survivin and XIAP. Oncogene 2005; 24:6877-89; PMID:16007142; http://dx.doi.org/10.1038/sj.onc.1208851.
21. Fandy TE, Shankar S, Ross DD, Sausville E, Srivastava RK. Interactive effects of HDAC inhibitors and TRAIL on apoptosis are associated with changes in mitochondrial functions and expressions of cell cycle regulatory genes in multiple myeloma. Neoplasia 2005; 7:646-57; PMID:16026644; http://dx.doi.org/10. 1593/neo.04655.
22. VanOosten RL, Moore JM, Karacay B, Griffith TS. Histone deacetylase inhibitors modulate renal cell carcinoma sensitivity to TRAIL/Apo-2L-induced apoptosis by enhancing TRAIL-R2 expression. Cancer Biol Ther 2005; 4:1104-12; PMID:16096370; http://dx.doi.org/10.4161/cbt.4.10.2022.
23. Mitsiades CS, Poulaki V, McMullan C, Negri J, Fanourakis G, Goudopoulou A, et al. Novel histone deacetylase inhibitors in the treatment of thyroid cancer. Clin Cancer Res 2005; 11:3958-65; PMID:15897598; http://dx.doi.org/10. 1158/1078-0432.CCR-03-0776.
24. El-Zawahry A, Lu P, White SJ, Voelkel-Johnson C. In vitro efficacy of AdTRAIL gene therapy of bladder cancer is enhanced by trichostatin A-mediated restoration of CAR expression and downregulation of cFLIP and Bcl-XL. Cancer Gene Ther 2006; 13:281-9; PMID:16167063; http://dx.doi.org/10.1038/sj.cgt. 7700905.
25. Shankar S, Singh TR, Fandy TE, Luetrakul T, Ross DD, Srivastava RK. Interactive effects of histone deacetylase inhibitors and TRAIL on apoptosis in human leukemia cells: involvement of both death receptor and mitochondrial pathways. Int J Mol Med 2005; 16:1125-38; PMID:16273296.
26. Schuchmann M, Schulze-Bergkamen H, Fleischer B, Schattenberg JM, Siebler J, Weinmann A, et al. Histone deacetylase inhibition by valproic acid downregulates c-FLIP/CASH and sensitizes hepatoma cells towards CD95- and TRAIL receptor-mediated apoptosis and chemotherapy. Oncol Rep 2006; 15:227-30; PMID:16328060.
27. Earel JK Jr, VanOosten RL, Griffith TS. Histone deacetylase inhibitors modulate the sensitivity of tumor necrosis factor-related apoptosis-inducing ligand-resistant bladder tumor cells. Cancer Res 2006; 66:499-507; PMID:16397266; http://dx.doi.org/10.1158/0008-5472.CAN-05-3017.
28. Lakshmikanthan V, Kaddour-Djebbar I, Lewis RW, Kumar MV. SAHA-sensitized prostate cancer cells to TNFalpha-related apoptosis-inducing ligand (TRAIL): mechanisms leading to synergistic apoptosis. Int J Cancer 2006; 119:221-8; PMID:16450389; http://dx.doi.org/10.1002/ijc.21824.
29. VanOosten RL, Earel JK Jr, Griffith TS. Enhancement of Ad5-TRAIL cytotoxicity against renal cell carcinoma with histone deacetylase inhibitors. Cancer Gene Ther 2006; 13:628-32; PMID:16456549; http://dx.doi.org/10.1038/sj. cgt.7700939.
30. Sonnemann J, Kumar KS, Heesch S, Müller C, Hartwig C, Maass M, et al. Histone deacetylase inhibitors induce cell death and enhance the susceptibility to ionizing radiation, etoposide, and TRAIL in medulloblastoma cells. Int J Oncol 2006; 28:755-66; PMID:16465382.
31. Butler LM, Liapis V, Bouralexis S, Welldon K, Hay S, Thai M, et al. The histone deacetylase inhibitor, suberoylanilide hydroxamic acid, overcomes resistance of human breast cancer cells to Apo2L/TRAIL. Int J Cancer 2006; 119:944-54; PMID:16550602; http://dx.doi.org/10.1002/ijc.21939.
32. Pathil A, Armeanu S, Venturelli S, Mascagni P, Weiss TS, Gregor M, et al. HDAC inhibitor treatment of hepatoma cells induces both TRAIL-independent apoptosis and restoration of sensitivity to TRAIL. Hepatology 2006; 43:425-34; PMID:16583461; http://dx.doi.org/10.1002/hep.21054.
33. Thai M, Labrinidis A, Hay S, Liapis V, Bouralexis S, Welldon K, et al. Apo2l/Tumor necrosis factor-related apoptosis-inducing ligand prevents breast cancer-induced bone destruction in a mouse model. Cancer Res 2006; 66:5363-70; PMID:16707463; http://dx.doi.org/10.1158/0008-5472.CAN-05-4386.
34. Inoue S, Twiddy D, Dyer MJ, Cohen GM. Upregulation of TRAIL-R2 is not involved in HDACi mediated sensitization to TRAIL-induced apoptosis. Cell Death Differ 2006; 13:2160-2; PMID:16729023; http://dx.doi.org/10.1038/sj.cdd.4401977.
35. Inoue S, Mai A, Dyer MJ, Cohen GM. Inhibition of histone deacetylase class I but not class II is critical for the sensitization of leukemic cells to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. Cancer Res 2006; 66:6785-92; PMID:16818655; http://dx.doi.org/10.1158/0008-5472. CAN-05-4563.
36. Ziauddin MF, Yeow WS, Maxhimer JB, Baras A, Chua A, Reddy RM, et al. Valproic acid, an antiepileptic drug with histone deacetylase inhibitory activity, potentiates the cytotoxic effect of Apo2L/TRAIL on cultured thoracic cancer cells through mitochondria-dependent caspase activation. Neoplasia 2006; 8:446-57; PMID:16820090; http://dx.doi.org/10.1593/neo.05823.
37. Lundqvist A, Abrams SI, Schrump DS, Alvarez G, Suffredini D, Berg M, et al. Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: a novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Res 2006; 66:7317-25; PMID:16849582; http://dx.doi.org/10.1158/0008-5472.CAN-06-0680.
38. Mühlethaler-Mottet A, Flahaut M, Bourloud KB, Auderset K, Meier R, Joseph JM, et al. Histone deacetylase inhibitors strongly sensitise neuroblastoma cells to TRAIL-induced apoptosis by a caspases-dependent increase of the pro- to anti-apoptotic proteins ratio. BMC Cancer 2006; 6:214; PMID:16930472; http://dx.doi.org/10.1186/1471-2407-6-214.
39. Fandy TE, Srivastava RK. Trichostatin A sensitizes TRAIL-resistant myeloma cells by downregulation of the antiapoptotic Bcl-2 proteins. Cancer Chemother Pharmacol 2006; 58:471-7; PMID:16435155; http://dx.doi.org/10.1007/ s00280-005-0184-3.
40. Gillespie S, Borrow J, Zhang XD, Hersey P. Bim plays a crucial role in synergistic induction of apoptosis by the histone deacetylase inhibitor SBHA and TRAIL in melanoma cells. Apoptosis 2006; 11:2251-65; PMID:17051334; http://dx.doi.org/10.1007/s10495-006-0283-6.
41. Kasman L, Lu P, Voelkel-Johnson C. The histone deacetylase inhibitors depsipeptide and MS-275, enhance TRAIL gene therapy of LNCaP prostate cancer cells without adverse effects in normal prostate epithelial cells. Cancer Gene Ther 2007; 14:327-34; PMID:17186014; http://dx.doi.org/10.1038/sj.cgt.7701017.
42. Reddy RM, Yeow WS, Chua A, Nguyen DM, Baras A, Ziauddin MF, et al. Rapid and profound potentiation of Apo2L/TRAIL-mediated cytotoxicity and apoptosis in thoracic cancer cells by the histone deacetylase inhibitor Trichostatin A: the essential role of the mitochondria-mediated caspase activation cascade. Apoptosis 2007; 12:55-71; PMID:17136498; http://dx.doi.org/10.1007/s10495-006- 0484-z.
43. Garofalo M, Romano G, Quintavalle C, Romano MF, Chiurazzi F, Zanca C, et al. Selective inhibition of PED protein expression sensitizes B-cell chronic lymphocytic leukaemia cells to TRAIL-induced apoptosis. Int J Cancer 2007; 120:1215-22; PMID:17192900; http://dx.doi.org/10.1002/ijc.22495.
44. VanOosten RL, Earel JK Jr, Griffith TS. Histone deacetylase inhibitors enhance Ad5-TRAIL killing of TRAIL-resistant prostate tumor cells through increased caspase-2 activity. Apoptosis 2007; 12:561-71; PMID:17195089; http://dx.doi.org/10.1007/s10495-006-0009-9.
45. Lillehammer T, Engesaeter BO, Prasmickaite L, Maelandsmo GM, Fodstad O, Engebraaten O. Combined treatment with Ad-hTRAIL and DTIC or SAHA is associated with increased mitochondrial-mediated apoptosis in human melanoma cell lines. J Gene Med 2007; 9:440-51; PMID:17410615; http://dx.doi.org/10.1002/jgm.1036.
46. Gómez-Benito M, Martinez-Lorenzo MJ, Anel A, Marzo I, Naval J. Membrane expression of DR4, DR5 and caspase-8 levels, but not Mcl-1, determine sensitivity of human myeloma cells to Apo2L/TRAIL. Exp Cell Res 2007; 313:2378-88; PMID:17462628; http://dx.doi.org/10.1016/j.yexcr.2007.03.018.
47. Sonnemann J, Dreyer L, Hartwig M, Palani CD, Hong TT, Klier U, et al. Histone deacetylase inhibitors induce cell death and enhance the apoptosis-inducing activity of TRAIL in Ewing's sarcoma cells. J Cancer Res Clin Oncol 2007; 133:847-58; PMID:17486365; http://dx.doi.org/10.1007/s00432-007- 0227-8.
48. Cip1-dependent decrease in survivin levels. Cancer Res 2007; 67:6987-94; PMID:17638911; http://dx.doi.org/10.1158/0008-5472.CAN-07-0812.
49. Lagneaux L, Gillet N, Stamatopoulos B, Delforge A, Dejeneffe M, Massy M, et al. Valproic acid induces apoptosis in chronic lymphocytic leukemia cells through activation of the death receptor pathway and potentiates TRAIL response. Exp Hematol 2007; 35:1527-37; PMID:17697742; http://dx.doi.org/10.1016/j. exphem.2007.06.014.
50. Inoue S, Walewska R, Dyer MJ, Cohen GM. Downregulation of Mcl-1 potentiates HDACi-mediated apoptosis in leukemic cells. Leukemia 2008; 22:819-25; PMID:18239621; http://dx.doi.org/10.1038/leu.2008.1.
51. Stieglmaier J, Bremer E, Kellner C, Liebig TM, ten Cate B, Peipp M, et al. Selective induction of apoptosis in leukemic B-lymphoid cells by a CD19-specific TRAIL fusion protein. Cancer Immunol Immunother 2008; 57:233-46; PMID:17665197; http://dx.doi.org/10.1007/s00262-007-0370-8.
52. Iacomino G, Medici MC, Russo GL. Valproic acid sensitizes K562 erythroleukemia cells to TRAIL/Apo2L-induced apoptosis. Anticancer Res 2008; 28:855-64; PMID:18507029.
53. Feng R, Ma H, Hassig CA, Payne JE, Smith ND, Mapara MY, et al. KD5170, a novel mercaptoketone-based histone deacetylase inhibitor, exerts antimyeloma effects by DNA damage and mitochondrial signaling. Mol Cancer Ther 2008; 7:1494-505; PMID:18566220; http://dx.doi.org/10.1158/1535-7163.MCT-08-0183.
54. Frew AJ, Lindemann RK, Martin BP, Clarke CJP, Sharkey J, Anthony DA, et al. Combination therapy of established cancer using a histone deacetylase inhibitor and a TRAIL receptor agonist. Proc Natl Acad Sci USA 2008; 105:11317-22; PMID:18685088; http://dx.doi.org/10.1073/pnas.0801868105.
55. Dzieran J, Beck JF, Sonnemann J. Differential responsiveness of human hepatoma cells versus normal hepatocytes to TRAIL in combination with either histone deacetylase inhibitors or conventional cytostatics. Cancer Sci 2008; 99:1685-92; PMID:18754884; http://dx.doi.org/10.1111/j.1349-7006.2008.00868.x.
56. Aguilera DG, Das CM, Sinnappah-Kang ND, Joyce C, Taylor PH, Wen S, et al. Reactivation of death receptor 4 (DR4) expression sensitizes medulloblastoma cell lines to TRAIL. J Neurooncol 2009; 93:303-18; PMID:19148581; http://dx.doi.org/10.1007/s11060-008-9788-x.
57. Symanowski J, Vogelzang N, Zawel L, Atadja P, Pass H, Sharma S. A histone deacetylase inhibitor LBH589 downregulates XIAP in mesothelioma cell lines which is likely responsible for increased apoptosis with TRAIL. J Thorac Oncol 2009; 4:149-60; PMID:19179889; http://dx.doi.org/10.1097/JTO.0b013e318194f991.
58. Park SJ, Kim MJ, Kim HB, Sohn HY, Bae JH, Kang CD, et al. Cotreatment with apicidin overcomes TRAIL resistance via inhibition of Bcr-Abl signaling pathway in K562 leukemia cells. Exp Cell Res 2009; 315:1809-18; PMID:19268463; http://dx.doi.org/10.1016/j.yexcr.2009.02.024.
59. Park SJ, Kim MJ, Kim HB, Sohn HY, Bae JH, Kang CD, et al. Trichostatin A sensitizes human ovarian cancer cells to TRAIL-induced apoptosis by downregulation of c-FLIPL via inhibition of EGFR pathway. Biochem Pharmacol 2009; 77:1328-36; PMID:19426671; http://dx.doi.org/10.1016/j.bcp.2008.12.027.
60. Shankar S, Davis R, Singh KP, Kurzrock R, Ross DD, Srivastava RK. Suberoylanilide hydroxamic acid (Zolinza/vorinostat) sensitizes TRAIL-resistant breast cancer cells orthotopically implanted in BALB/c nude mice. Mol Cancer Ther 2009; 8:1596-605; PMID:19509267; http://dx.doi.org/10.1158/1535-7163.MCT- 08-1004.
61. Norian LA, Kucaba TA, Earel JK, Knutson T, Vanoosten RL, Griffith TS. Synergistic induction of apoptosis in primary B-CLL cells after treatment with recombinant tumor necrosis factor-related apoptosis-inducing ligand and histone deacetylase inhibitors. J Oncol 2009; 2009:408038; PMID:19547714; http://dx.doi.org/10.1155/2009/408038.
62. Häcker S, Dittrich A, Mohr A, Schweitzer T, Rutkowski S, Krauss J, et al. Histone deacetylase inhibitors cooperate with IFNgamma to restore caspase-8 expression and overcome TRAIL resistance in cancers with silencing of caspase-8. Oncogene 2009; 28:3097-110; PMID:19597472; http://dx.doi.org/10.1038/ onc.2009.161.
63. Carlisi D, Lauricella M, D'Anneo A, Emanuele S, Angileri L, Di Fazio P, et al. The histone deacetylase inhibitor suberoylanilide hydroxamic acid sensitises human hepatocellular carcinoma cells to TRAIL-induced apoptosis by TRAIL-DISC activation. Eur J Cancer 2009; 45:2425-38; PMID:19643600; http://dx.doi.org/10.1016/j.ejca.2009.06.024.
64. Yeh CC, Deng YT, Sha DY, Hsiao M, Kuo MY. Suberoylanilide hydroxamic acid sensitizes human oral cancer cells to TRAIL-induced apoptosis through increase DR5 expression. Mol Cancer Ther 2009; 8:2718-25; PMID:19737941; http://dx.doi.org/10.1158/1535-7163.MCT-09-0211.
65. Wood TE, Dalili S, Simpson CD, Sukhai MA, Hurren R, Anyiwe K, et al. Selective inhibition of histone deacetylases sensitizes malignant cells to death receptor ligands. Mol Cancer Ther 2010; 9:246-56; PMID:20053768; http://dx.doi.org/10.1158/1535-7163.MCT-09-0495.
66. Inoue S, Harper N, Walewska R, Dyer MJ, Cohen GM. Enhanced Fas-associated death domain recruitment by histone deacetylase inhibitors is critical for the sensitization of chronic lymphocytic leukemia cells to TRAIL-induced apoptosis. Mol Cancer Ther 2009; 8:3088-97; PMID:19887558; http://dx.doi.org/10.1158/1535- 7163.MCT-09-0451.
67. Darvas K, Rosenberger S, Brenner D, Fritsch C, Gmelin N, Krammer PH, et al. Histone deacetylase inhibitor-induced sensitization to TNFalpha/TRAIL- mediated apoptosis in cervical carcinoma cells is dependent on HPV oncogene expression. Int J Cancer 2010; 127:1384-92; PMID:20087862; http://dx.doi.org/10. 1002/ijc.25170.
68. D'Acunto CW, Carratù A, Rodriquez M, Taddei M, Parente L, Petrella A. LGP1, A histone deacetylase inhibitor analogue of FR235222, sensitizes promyelocytic leukaemia U937 cells to TRAIL-mediated apoptosis. Anticancer Res 2010; 30:887-94; PMID:20393011.
69. Schüler S, Fritsche P, Diersch S, Arlt A, Schmid RM, Saur D, et al. HDAC2 attenuates TRAIL-induced apoptosis of pancreatic cancer cells. Mol Cancer 2010; 9:80; PMID:20398369; http://dx.doi.org/10.1186/1476-4598-9-80.
70. Kauh J, Fan S, Xia M, Yue P, Yang L, Khuri FR, et al. c-FLIP degradation mediates sensitization of pancreatic cancer cells to TRAIL-induced apoptosis by the histone deacetylase inhibitor LBH589. PLoS One 2010; 5:10376; PMID:20442774; http://dx.doi.org/10.1371/journal.pone.0010376.
71. Lucas DM, Alinari L, West DA, Davis ME, Edwards RB, Johnson AJ, et al. The novel deacetylase inhibitor AR-42 demonstrates pre-clinical activity in B-cell malignancies in vitro and in vivo. PLoS One 2010; 5:10941; PMID:20532179; http://dx.doi.org/10.1371/journal.pone.0010941.
72. Morales JC, Ruiz-Magaña MJ, Carranza D, Ortiz-Ferrón G, Ruiz-Ruiz C. HDAC inhibitors with different gene regulation activities depend on the mitochondrial pathway for the sensitization of leukemic T cells to TRAIL-induced apoptosis. Cancer Lett 2010; 297:91-100; PMID:20580868; http://dx.doi.org/10.1016/j.canlet.2010.04.029.
73. Sung ES, Kim A, Park JS, Chung J, Kwon MH, Kim YS. Histone deacetylase inhibitors synergistically potentiate death receptor 4-mediated apoptotic cell death of human T-cell acute lymphoblastic leukemia cells. Apoptosis 2010; 15:1256-69; PMID:20582477; http://dx.doi.org/10.1007/s10495-010-0521-9.
74. Srivastava RK, Kurzrock R, Shankar S. MS-275 sensitizes TRAIL-resistant breast cancer cells, inhibits angiogenesis and metastasis, and reverses epithelial-mesenchymal transition in vivo. Mol Cancer Ther 2010; 9:3254-66; PMID:21041383; http://dx.doi.org/10.1158/1535-7163.MCT-10-0582.
75. Martin BP, Frew AJ, Bots M, Fox S, Long F, Takeda K, et al. Antitumor activities and on-target toxicities mediated by a TRAIL receptor agonist following cotreatment with panobinostat. Int J Cancer 2011; 128:2735-47; PMID:20715169; http://dx.doi.org/10.1002/ijc.25594.
76. Menke C, Bin L, Thorburn J, Behbakht K, Ford HL, Thorburn A. Distinct TRAIL resistance mechanisms can be overcome by proteasome inhibition but not generally by synergizing agents. Cancer Res 2011; 71:1883-92; PMID:21363923; http://dx.doi.org/10.1158/0008-5472.CAN-10-2252.
77. Kim DR, Park MY, Lee CS, Shim SH, Yoon HI, Lee JH, et al. Combination of vorinostat and adenovirus-TRAIL exhibits a synergistic antitumor effect by increasing transduction and transcription of TRAIL in lung cancer cells. Cancer Gene Ther 2011; 18:467-77; PMID:21455254; http://dx.doi.org/10.1038/cgt.2011.11.
78. Yerbes R, López-Rivas A. Itch/AIP4-independent proteasomal degradation of cFLIP induced by the histone deacetylase inhibitor SAHA sensitizes breast tumour cells to TRAIL. Invest New Drugs 2010; In press; PMID:21107885; http://dx.doi.org/10.1007/s10637-010-9597-x.
79. Kaminskyy VO, Surova OV, Vaculova A, Zhivotovsky B. Combined inhibition of DNA methyltransferase and histone deacetylase restores caspase-8 expression and sensitizes SCLC cells to TRAIL. Carcinogenesis 2011; 32:1450-8; PMID:21771726; http://dx.doi.org/10.1093/carcin/bgr135.
80. Lauricella M, Ciraolo A, Carlisi D, Vento R, Tesoriere G. SAHA/TRAIL combination induces detachment and anoikis of MDA-MB231 and MCF-7 breast cancer cells. Biochimie 2011; In press; PMID:21835222.
81. Liu X, Yue P, Chen S, Hu L, Lonial S, Khuri FR, et al. The proteasome inhibitor PS-341 (bortezomib) upregulates DR5 expression leading to induction of apoptosis and enhancement of TRAIL-induced apoptosis despite upregulation of c-FLIP and survivin expression in human NSCLC cells. Cancer Res 2007; 67:4981-8; PMID:17510429; http://dx.doi.org/10.1158/0008-5472.CAN-06-4274.
82. Mitsiades N, Poulaki V, Mitsiades C, Tsokos M. Ewing's sarcoma family tumors are sensitive to tumor necrosis factor-related apoptosis-inducing ligand and express death receptor 4 and death receptor 5. Cancer Res 2001; 61:2704-12; PMID:11289151.
83. Seki N, Toh U, Sayers TJ, Fujii T, Miyagi M, Akagi Y, et al. Bortezomib sensitizes human esophageal squamous cell carcinoma cells to TRAIL-mediated apoptosis via activation of both extrinsic and intrinsic apoptosis pathways. Mol Cancer Ther 2010; 9:1842-51; PMID:20515944; http://dx.doi.org/10.1158/1535- 7163.MCT-09-0918.
84. Lu G, Punj V, Chaudhary PM. Proteasome inhibitor Bortezomib induces cell cycle arrest and apoptosis in cell lines derived from Ewing's sarcoma family of tumors and synergizes with TRAIL. Cancer Biol Ther 2008; 7:603-8; PMID:18223318; http://dx.doi.org/10.4161/cbt.7.4.5564.
85. Kontny HU, Hämmerle K, Klein R, Shayan P, Mackall CL, Niemeyer CM. Sensitivity of Ewing's sarcoma to TRAIL-induced apoptosis. Cell Death Differ 2001; 8:506-14; PMID:11423911; http://dx.doi.org/10.1038/sj.cdd.4400836.
86. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 2009; 459:428-32; PMID:19363473; http://dx.doi.org/10.1038/nature08012.