Combining TRAIL with PI3 kinase or HSP90 inhibitors enhances apoptosis in colorectal cancer cells via suppression of survival signaling

Oncotarget

Volumn 4, Issue 8, 2013, Pages 1185-1198

  Saturno, Grazia ^a,b   Valenti, Melanie ^a   De Haven Brandon, Alexis ^a   Thomas, George V ^a,c   Eccles, Suzanne ^a   Clarke, Paul A ^a   Workman, Paul ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Apoptosis; Colorectal cancer; Hsp90; Pi3 Kinase mTOR; TRAIL

Indexed keywords

2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; CASPASE 3; CASPASE 8; CASPASE 9; DEATH RECEPTOR 4; DEATH RECEPTOR 5; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HEAT SHOCK PROTEIN 90 INHIBITOR; I KAPPA B KINASE ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; TANESPIMYCIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL SURVIVAL; CHEMOSENSITIVITY; COLON MUCOSA; COLORECTAL CANCER; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME ACTIVITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; INHIBITION KINETICS; MORNING DOSAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BENZOQUINONES; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DRUG SCREENING ASSAYS, ANTITUMOR; FURANS; HCT116 CELLS; HSP90 HEAT-SHOCK PROTEINS; HT29 CELLS; HUMANS; LACTAMS, MACROCYCLIC; MICE; MICE, NUDE; PHOSPHATIDYLINOSITOL 3-KINASES; PYRIDINES; PYRIMIDINES; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84884341253     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1162     Document Type: Article

References (53)

1. Cancer Research UK, http://www.cancerresearchuk.org/
2. NCI, http://www.cancer.gov/
3. Cunningham D, Atkin W, Lenz HJ, Lynch HT, Minsky B, Nordlinger B, Starling N. Colorectal cancer. Lancet. 2010; 375: 1030-1047.
4. Benson AB 3rd, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, Cooper HS, Engstrom PF, Enzinger PC, Fakih MG, Fenton MJ, Fuchs CS, Grem JL, Hunt S, Kamel A, Leong LA, Lin E, et al. Metastatic colon cancer, version 3. 2013: featured updates to the NCCN Guidelines. J Natl Compr Canc Netw. 2013; 11: 141-152.
5. Prenen H, Vecchione L, Van Cutsem E. Role of targeted agents in metastatic colorectal cancer. Target Oncol. 2013; 8: 83-96.
6. Fulda S. Novel insights into the synergistic interaction ofBortezomib and TRAIL: tBid provides the link. Oncotarget. 2011; 2: 418-421.
7. Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer. 2002; 2: 420-430.
8. Wilson TR, McLaughlin KM, McEwan M, Sakai H, Rogers KM, Redmond KM, Johnston PG, Longley DB. c-FLIP: a key regulator of colorectal cancer cell death. Cancer Res. 2007; 67: 5754-5762.
9. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov. 2008; 7: 1001-1012.
10. Yang A, Wilson NS, Ashkenazi A. Proapoptotic DR4 and DR5 signaling in cancer cells: toward clinical translation. Curr Opin Cell Biol. 2010; 22: 837-844
11. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med. 1999; 5: 157- 163.
12. Ashkenazi A, Holland P, Eckhardt SG. Ligand-based targeting of apoptosis in cancer: the potential of recombinant human apoptosis ligand 2/Tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J Clin Oncol. 2008; 26: 3621-3630.
13. Pan Y, Xu R, Peach M, Huang CP, Branstetter D, Novotny W, Herbst RS, Eckhardt SG, Holland PM. Evaluation of pharmacodynamic biomarkers in a Phase 1a trial of dulanermin (rhApo2L/TRAIL) in patients with advanced tumours. Br J Cancer. 2011; 105: 1830-1838.
14. Wiezorek J, Holland P, Graves J. Death receptor agonists as a targeted therapy for cancer. Clin Cancer Res. 2010; 16: 1701-1708.
15. Dimberg LY, Anderson CK, Camidge R, Behbakht K, Thorburn A, Ford HL. On the TRAIL to successful cancer therapy?. Predicting and counteracting resistance against TRAIL-based therapeutics. Oncogene. 2013; 32: 1341- 1350.
16. Bellail AC, Hao C. The roadmap of TRAIL apoptotic pathway-targeted cancer therapies: what is next? Expert Rev Anticancer Ther. 2012; 12: 547-549.
17. Song JJ, An JY, Kwon YT, Lee YJ. Evidence for two modes of development of acquired tumor necrosis factorrelated apoptosis-inducing ligand resistance. Involvement of Bcl-xL. J Biol Chem. 2007; 282: 319-328.
18. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer. 2008; 8: 782-798.
19. Kim J, Kang D, Sun BK, Kim JH, Song JJ. TRAIL/ MEKK4/p38/HSP27/Akt survival network is biphasically modulated by the Src/CIN85/c-Cbl complex. Cell Signal. 2013; 25: 372-379.
20. Yap TA, Workman P. Exploiting the cancer genome: strategies for the discovery and clinical development of targeted molecular therapeutics. Annu Rev Pharmacol Toxicol. 2012; 52: 549-573.
21. Workman P, Clarke PA, Raynaud FI, van Montfort RL. Drugging the PI3 kinome: from chemical tools to drugs in the clinic. Cancer Res. 2010; 70: 2146-2157.
22. Clarke PA, Workman P. Phosphatidylinositide-3-kinase inhibitors: addressing questions of isoform selectivity and pharmacodynamic/predictive biomarkers in early clinical trials. J Clin Oncol. 2012; 30: 331-333.
23. Shuttleworth SJ, Silva FA, Cecil AR, Tomassi CD, Hill TJ, Raynaud FI, Clarke PA, Workman P. Progress in the preclinical discovery and clinical development of class I and dual class I/IV phosphoinositide 3-kinase (PI3K) inhibitors. Curr Med Chem. 2011; 18: 2686-2714.
24. Neckers L, Workman P. Hsp90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res. 2012; 18: 64-76.
25. Martins AS, Davies FE, Workman P. Inhibiting the molecular evolution of cancer through HSP90. Oncotarget. 2012; 3: 1054-1056.
26. Travers J, Sharp S, Workman P. HSP90 inhibition: twopronged exploitation of cancer dependencies. Drug Discov Today. 2012; 17: 242-252.
27. Miyata Y, Nakamoto H, Neckers L. The therapeutic target Hsp90 and cancer hallmarks. Curr Pharm Des. 2013; 19: 347-365.
28. Walsby E, Pearce L, Burnett AK, Fegan C, Pepper C. The Hsp90 inhibitor NVP-AUY922-AG inhibits NF-κB signaling, overcomes microenvironmental cytoprotection and is highly synergistic with fludarabine in primary CLL cells. Oncotarget. 2012; 3: 525-534.
29. Chawla-Sarkar M, Bauer JA, Lupica JA, Morrison BH, Tang Z, Oates RK, Almasan A, DiDonato JA, Borden EC, Lindner DJ. Suppression of NF-kappa B survival signaling by nitrosylcobalamin sensitizes neoplasms to the anti-tumor effects of Apo2L/TRAIL. J Biol Chem. 2003; 278: 39461- 39469.
30. Vasilevskaya IA, O'Dwyer PJ. 17-Allylamino-17- demethoxygeldanamycin overcomes TRAIL resistance in colon cancer cell lines. Biochem Pharmacol. 2005; 70: 580- 589.
31. Stolfi C, Pallone F, Monteleone G. Molecular Targets of TRAIL-Sensitizing Agents in Colorectal Cancer. Int J Mol Sci. 2012; 13:7886-7901.
32. Ma Y, Lakshmikanthan V, Lewis RW, Kumar MV. Sensitization of TRAIL-resistant cells by inhibition of heat shock protein 90 with low-dose geldanamycin. Mol Cancer Ther. 2006; 5: 170-178.
33. Hayakawa M, Kaizawa H, Kawaguchi K, et al. Synthesis and biological evaluation of pyrido[3',2':4,5]furo[3,2-d] pyrimidine derivatives as novel PI3 kinase p110a inhibitors. Bioorg Med Chem Lett. 2007; 17: 2438-2442.
34. Raynaud FI, Eccles S, Clarke PA, Hayes A, Nutley B, AlixS, Henley A, Di-Stefano F, Ahmad Z, Guillard S, Bjerke LM, Kelland L, Valenti M, Patterson L, Gowan S, de Haven Brandon A et al. Pharmacologic characterization of a potent inhibitor of class I phosphatidylinositide 3-kinases. Cancer Res. 2007; 67: 5840-5850.
35. Lane D, Robert V, Grondin R, Rancourt C, Piché A. Malignant ascites protect against TRAIL-induced apoptosis by activating the PI3K/Akt pathway in human ovarian carcinoma cells. Int J Cancer. 2007; 121: 1227-1237.
36. Opel D, Westhoff MA, Bender A, Braun V, Debatin KM, Fulda S. Phosphatidylinositol 3-kinase inhibition broadly sensitizes glioblastoma cells to death receptor- and druginduced apoptosis. Cancer Res. 2008; 68: 6271-6280.
37. Gharbi SI, Zvelebil MJ, Shuttleworth SJ, Hancox T, Saghir N, Timms JF, Waterfield MD. Exploring the specificity of the PI3K family inhibitor LY294002. Biochem J. 2007; 404: 15-21.
38. Bagci-Onder T, Wakimoto H, Anderegg M, Cameron C, Shah K. A dual PI3K/mTOR inhibitor, PI-103, cooperates with stem cell delivered TRAIL in experimental glioma models. Cancer Res. 2011; 71: 154-163.
39. Opel D, Naumann I, Schneider M, Bertele D, Debatin KM, Fulda S. Targeting Aberrant PI3K/Akt Activation by PI103 Restores Sensitivity to TRAIL-Induced Apoptosis in Neuroblastoma. Clin Cancer Res. 2011; 17: 3233-3247.
40. Griffith TS, Chin WA, Jackson GC, Lynch DH, Kubin MZ. Intracellular regulation of TRAIL-induced apoptosis in human melanoma cells. J Immunol. 1998; 161: 2833-2840.
41. Galligan L, Longley DB, McEwan M, Wilson TR, McLaughlin K, Johnston PG. Chemotherapy and TRAILmediated colon cancer cell death: the roles of p53, TRAIL receptors, and c-FLIP. Mol Cancer Ther. 2005; 4: 2026- 2036.
42. Folkes AJ, Ahmadi K, Alderton WK, Alix S, Baker SJ, Box G, Chuckowree IS, Clarke PA, Depledge P, Eccles SA, Friedman LS, Hayes A, Hancox TC, Kugendradas A, Lensun L, Moore P et al. The identification of 2-(1H-indazol-4-yl)-6-(4-methanesulfonyl-piperazin- 1-ylmethyl)-4-morpholin-4-yl-thieno[3,2-d]pyrimidine (GDC-0941) as a potent, selective, orally bioavailable inhibitor of class I PI3 kinase for the treatment of cancer. J Med Chem. 2008; 51: 5522-5532.
43. Raynaud FI, Eccles SA, Patel S, Alix S, Box G, Chuckowree I, Folkes A, Gowan S, De Haven Brandon A, Di Stefano F, Hayes A, Henley AT, Lensun L, Pergl-Wilson G, Robson A, et al. Biological properties of potent inhibitors of class I phosphatidylinositide 3-kinases: from PI-103 through PI- 540, PI-620 to the oral agent GDC-0941. Mol Cancer Ther. 2009; 8: 1725-1738.
44. Herbst RS, Eckhardt SG, Kurzrock R, Ebbinghaus S, O'Dwyer PJ, Gordon MS, Novotny W, Goldwasser MA, Tohnya TM, Lum BL, Ashkenazi A, Jubb AM, Mendelson DS. Phase I dose-escalation study of recombinant human Apo2L/TRAIL, a dual proapoptotic receptor agonist, in patients with advanced cancer. J Clin Oncol. 2010; 28: 2839-2846.
45. Mahalingam D, Szegezdi E, Keane M, Jong S, Samali A. TRAIL receptor signalling and modulation: Are we on the right TRAIL? Cancer Treat Rev. 2009; 35: 280-288.
46. Sartore-Bianchi A, Bencardino K, Cassingena A, Venturini F, Funaioli C, Cipani T, Amatu A, Pietrogiovanna L, Schiavo R, Di Nicolantonio F, Artale S, Bardelli A, Siena S. Therapeutic implications of resistance to molecular therapies in metastatic colorectal cancer. Cancer Treat Rev. 2010; 36 Suppl 3: S1-5.
47. Amm HM, Oliver PG, Lee CH, Li Y, Buchsbaum DJ. Combined modality therapy with TRAIL or agonistic death receptor antibodies. Cancer Biol Ther. 2011; 11: 431-449.
48. Bauer JA, Lupica JA, Schmidt H, Morrison BH, Haney RM, Masci RK, Lee RM, Didonato JA, Lindner DJ. Nitrosylcobalamin potentiates the anti-neoplastic effects of chemotherapeutic agents via suppression of survival signaling. PLoS One. 2007; 2: e1313.
49. de Wilt LH, Kroon J, Jansen G, de Jong S, Peters GJ, Kruyt FA. Bortezomib and TRAIL: A perfect match for apoptotic elimination of tumour cells? Crit Rev Oncol Hematol. 2013; 85: 363-372.
50. Varfolomeev E, Alicke B, Elliott JM, et al. X chromosomelinked inhibitor of apoptosis regulates cell death induction by proapoptotic receptor agonists. J Biol Chem. 2009; 284: 34553-34560.
51. Chou TC. Preclinical versus clinical drug combination studies. Leuk Lymphoma. 2008; 49: 2059-2080.
52. Hucl T, Gallmeier E, Kern SE. Distinguishing rational from irrational applications of pharmacogenetic synergies from the bench to clinical trials. Cell Cycle. 2007; 6: 1336-1341.
53. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, Double JA, Everitt J, Farningham DA, Glennie MJ, Kelland LR, Robinson V, Stratford IJ, Tozer GM, Watson S, Wedge SR, et al. Guidelines for the welfare and use of animals in cancer research. Br J Cancer. 2010; 102: 1555-1577.