Prognostic and therapeutic relevance of c-FLIP in acute myeloid leukaemia

British Journal of Haematology

Volumn 160, Issue 2, 2013, Pages 188-198

  Mclornan, Donal ^a,b   Hay, Jodie ^a   Mclaughlin, Kirsty ^a   Holohan, Caitriona ^a   Burnett, Alan K ^c   Hills, Robert K ^c   Johnston, Patrick G ^a   Mills, Ken I ^a   Mcmullin, Mary Frances ^a   Longley, Daniel B ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b KING'S COLLEGE HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

AML; Apoptosis; C FLIP; Prognostic biomarker; TRAIL

Indexed keywords

ACY 775; ANTHRACYCLINE; ENTINOSTAT; FLICE INHIBITORY PROTEIN; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VORINOSTAT;

ACUTE GRANULOCYTIC LEUKEMIA; ADOLESCENT; ADULT; AGED; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CFLAR GENE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENCY; DRUG SENSITIVITY; DRUG SENSITIZATION; ENZYME INHIBITION; FEMALE; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS;

ADOLESCENT; ADULT; AGED; ALTERNATIVE SPLICING; APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL LINE, TUMOR; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, LEUKEMIC; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; KAPLAN-MEIER ESTIMATE; LEUKEMIA, MYELOID, ACUTE; LEUKEMIA, MYELOMONOCYTIC, ACUTE; MALE; MIDDLE AGED; NEOPLASM PROTEINS; PROGNOSIS; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA, MESSENGER; RNA, NEOPLASM; RNA, SMALL INTERFERING; TNF-RELATED APOPTOSIS-INDUCING LIGAND; YOUNG ADULT;

EID: 84872261651     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12108     Document Type: Article

References (43)

1. Allen, W.L., Stevenson, L., Coyle, V.M., Jithesh, P.V., Proutski, I., Carson, G., Gordon, M.A., Lenz, H.J., Van Schaeybroeck, S., Longley, D.B. & Johnston, P.G. (2011) A systems biology approach identifies SART1 as a novel determinant of both 5-fluorouracil and SN38 drug resistance in colorectal cancer. Molecular Cancer Therapeutics, 11, 119-131.
2. Ashkenazi, A. & Dixit, V.M. (1999) Apoptosis control by death and decoy receptors. Current Opinion in Cell Biology, 11, 255-260.
3. Balsas, P., Lopez-Royuela, N., Galan-Malo, P., Anel, A., Marzo, I. & Naval, J. (2009) Cooperation between Apo2L/TRAIL and bortezomib in multiple myeloma apoptosis. Biochemical Pharmacology, 77, 804-812.
4. Bradner, J.E., West, N., Grachan, M.L., Greenberg, E.F., Haggarty, S.J., Warnow, T. & Mazitschek, R. (2010) Chemical phylogenetics of histone deacetylases. Nature Chemical Biology, 6, 238-243.
5. Carlisi, D., Lauricella, M., D'Anneo, A., Emanuele, S., Angileri, L., Di Fazio, P., Santulli, A., Vento, R. & Tesoriere, G. (2009) The histone deacetylase inhibitor suberoylanilide hydroxamic acid sensitises human hepatocellular carcinoma cells to TRAIL-induced apoptosis by TRAIL-DISC activation. European Journal of Cancer, 45, 2425-2438.
6. Cheson, B.D., Bennett, J.M., Kopecky, K.J., Buchner, T., Willman, C.L., Estey, E.H., Schiffer, C.A., Doehner, H., Tallman, M.S., Lister, T.A., Lo-Coco, F., Willemze, R., Biondi, A., Hiddemann, W., Larson, R.A., Lowenberg, B., Sanz, M.A., Head, D.R., Ohno, R. & Bloomfield, C.D. (2003) Revised recommendations of the International Working Group for Diagnosis, Standardization of Response Criteria, Treatment Outcomes, and Reporting Standards for Therapeutic Trials in Acute Myeloid Leukemia. Journal of Clinical Oncology, 21, 4642-4649.
7. Elrod, H.A., Lin, Y.D., Yue, P., Wang, X., Lonial, S., Khuri, F.R. & Sun, S.Y. (2007) The alkylphospholipid perifosine induces apoptosis of human lung cancer cells requiring inhibition of Akt and activation of the extrinsic apoptotic pathway. Molecular Cancer Therapeutics, 6, 2029-2038.
8. Frew, A.J., Lindemann, R.K., Martin, B.P., Clarke, C.J., Sharkey, J., Anthony, D.A., Banks, K.M., Haynes, N.M., Gangatirkar, P., Stanley, K., Bolden, J.E., Takeda, K., Yagita, H., Secrist, J.P., Smyth, M.J. & Johnstone, R.W. (2008) Combination therapy of established cancer using a histone deacetylase inhibitor and a TRAIL receptor agonist. Proc Natl Acad Sci U S A, 105, 11317-11322.
9. Garcia-Manero, G., Yang, H., Bueso-Ramos, C., Ferrajoli, A., Cortes, J., Wierda, W.G., Faderl, S., Koller, C., Morris, G., Rosner, G., Loboda, A., Fantin, V.R., Randolph, S.S., Hardwick, J.S., Reilly, J.F., Chen, C., Ricker, J.L., Secrist, J.P., Richon, V.M., Frankel, S.R. & Kantarjian, H.M. (2008a) Phase 1 study of the histone deacetylase inhibitor vorinostat (suberoylanilide hydroxamic acid [SAHA]) in patients with advanced leukemias and myelodysplastic syndromes. Blood, 111, 1060-1066.
10. Garcia-Manero, G., Assouline, S., Cortes, J., Estrov, Z., Kantarjian, H., Yang, H., Newsome, W.M., Miller, W.H., Rousseau, Jr, C., Kalita, A., Bonfils, C., Dubay, M., Patterson, T.A., Li, Z., Besterman, J.M., Reid, G., Laille, E., Martell, R.E. & Minden, M. (2008b) Phase 1 study of the oral isotype specific histone deacetylase inhibitor MGCD0103 in leukemia. Blood, 112, 981-989.
11. Gediya, L.K., Belosay, A., Khandelwal, A., Purushottamachar, P. & Njar, V.C. (2008) Improved synthesis of histone deacetylase inhibitors (HDIs) (MS-275 and CI-994) and inhibitory effects of HDIs alone or in combination with RAMBAs or retinoids on growth of human LNCaP prostate cancer cells and tumor xenografts. Bioorganic & Medicinal Chemistry, 16, 3352-3360.
12. Grimwade, D., Walker, H., Oliver, F., Wheatley, K., Harrison, C., Harrison, G., Rees, J., Hann, I., Stevens, R., Burnett, A. & Goldstone, A. (1998) The importance of diagnostic cytogenetics on outcome in AML: analysis of 1, 612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood, 92, 2322-2333.
13. Hyer, M.L., Croxton, R., Krajewska, M., Krajewski, S., Kress, C.L., Lu, M., Suh, N., Sporn, M.B., Cryns, V.L., Zapata, J.M. & Reed, J.C. (2005) Synthetic triterpenoids cooperate with tumor necrosis factor-related apoptosis-inducing ligand to induce apoptosis of breast cancer cells. Cancer Research, 65, 4799-4808.
14. Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J.L., Schroter, M., Burns, K., Mattmann, C., Rimoldi, D., French, L.E. & Tschopp, J. (1997) Inhibition of death receptor signals by cellular FLIP. Nature, 388, 190-195.
15. Itoh, Y., Suzuki, T., Kouketsu, A., Suzuki, N., Maeda, S., Yoshida, M., Nakagawa, H. & Miyata, N. (2007) Design, synthesis, structure-selectivity relationship, and effect on human cancer cells of a novel series of histone deacetylase 6-selective inhibitors. Journal of Medicinal Chemistry, 50, 5425-5438.
16. Johnstone, R.W., Frew, A.J. & Smyth, M.J. (2008) The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nature Reviews Cancer, 8, 782-798.
17. Jones, D.T., Ganeshaguru, K., Mitchell, W.A., Foroni, L., Baker, R.J., Prentice, H.G., Mehta, A.B. & Wickremasinghe, R.G. (2003) Cytotoxic drugs enhance the ex vivo sensitivity of malignant cells from a subset of acute myeloid leukaemia patients to apoptosis induction by tumour necrosis factor receptor-related apoptosis-inducing ligand. British Journal of Haematology, 121, 713-720.
18. Kerr, E., Holohan, C., McLaughlin, K.M., Majkut, J., Dolan, S., Redmond, K., Riley, J., McLaughlin, K., Stasik, I., Crudden, M., Van Schaeybroeck, S., Fenning, C., O'Connor, R., Kiely, P., Sgobba, M., Haigh, D., Johnston, P.G. & Longley, D.B. (2012) Identification of an acetylation-dependant Ku70/FLIP complex that regulates FLIP expression and HDAC inhibitor-induced apoptosis. Cell Death and Differentiation, 19, 1317-1327.
19. Krueger, A., Baumann, S., Krammer, P.H. & Kirchhoff, S. (2001) FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Molecular and Cellular Biology, 21, 8247-8254.
20. Lane, A.A. & Chabner, B.A. (2009) Histone deacetylase inhibitors in cancer therapy. Journal of Clinical Oncology, 27, 5459-5468.
21. Lane, S.W., Scadden, D.T. & Gilliland, D.G. (2009) The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood, 114, 1150-1157.
22. Longley, D.B. & Johnston, P.G. (2005) Molecular mechanisms of drug resistance. The Journal of pathology., 205, 275-292.
23. Longley, D.B., Wilson, T.R., McEwan, M., Allen, W.L., McDermott, U., Galligan, L. & Johnston, P.G. (2006) c-FLIP inhibits chemotherapy-induced colorectal cancer cell death. Oncogene, 25, 838-848.
24. Lowenberg, B., Downing, J.R. & Burnett, A. (1999) Acute myeloid leukemia. New England Journal of Medicine, 341, 1051-1062.
25. Luo, J., Solimini, N.L. & Elledge, S.J. (2009) Principles of cancer therapy: oncogene and non-oncogene addiction. Cell, 136, 823-837.
26. McLornan, D.P., McMullin, M.F., Johnston, P. & Longley, D.B. (2007) Molecular mechanisms of drug resistance in acute myeloid leukaemia. Expert opinion on drug metabolism & toxicology., 3, 363-377.
27. McLornan, D.P., Barrett, H.L., Cummins, R., McDermott, U., McDowell, C., Conlon, S.J., Coyle, V.M., Van Schaeybroeck, S., Wilson, R., Kay, E.W., Longley, D.B. & Johnston, P.G. (2010) Prognostic significance of TRAIL signaling molecules in stage II and III colorectal cancer. Clinical Cancer Research, 16, 3442-3451.
28. Menzin, J., Lang, K., Earle, C.C., Kerney, D. & Mallick, R. (2002) The outcomes and costs of acute myeloid leukemia among the elderly. Archives of Internal Medicine, 162, 1597-1603.
29. Nagata, S. (1999) Fas ligand-induced apoptosis. Annual Review of Genetics, 33, 29-55.
30. Petronelli, A., Saulle, E., Pasquini, L., Petrucci, E., Mariani, G., Biffoni, M., Ferretti, G., Scambia, G., Benedetti-Panici, P., Greggi, S., Cognetti, F., Russo, M.A., Sporn, M. & Testa, U. (2009) High sensitivity of ovarian cancer cells to the synthetic triterpenoid CDDO-Imidazolide. Cancer Letters, 282, 214-228.
31. Riccioni, R., Pasquini, L., Mariani, G., Saulle, E., Rossini, A., Diverio, D., Pelosi, E., Vitale, A., Chierichini, A., Cedrone, M., Foa, R., Lo Coco, F., Peschle, C. & Testa, U. (2005) TRAIL decoy receptors mediate resistance of acute myeloid leukemia cells to TRAIL. Haematologica, 90, 612-624.
32. Rogers, K.M., Thomas, M., Galligan, L., Wilson, T.R., Allen, W.L., Sakai, H., Johnston, P.G. & Longley, D.B. (2007) Cellular FLICE-inhibitory protein regulates chemotherapy-induced apoptosis in breast cancer cells. Molecular Cancer Therapeutics, 6, 1544-1551.
33. Scaffidi, C., Schmitz, I., Krammer, P.H. & Peter, M.E. (1999) The role of c-FLIP in modulation of CD95-induced apoptosis. Journal of Biological Chemistry, 274, 1541-1548.
34. Schaefer, E.W., Loaiza-Bonilla, A., Juckett, M., DiPersio, J.F., Roy, V., Slack, J., Wu, W., Laumann, K., Espinoza-Delgado, I. & Gore, S.D. (2009) A phase 2 study of vorinostat in acute myeloid leukemia. Haematologica, 94, 1375-1382.
35. Sharp, D.A., Lawrence, D.A. & Ashkenazi, A. (2005) Selective knockdown of the long variant of cellular FLICE inhibitory protein augments death receptor-mediated caspase-8 activation and apoptosis. Journal of Biological Chemistry, 280, 19401-19409.
36. Shirley, S. & Micheau, O. (2010) Targeting c-FLIP in cancer. Cancer letters, Nov 9. [Epub ahead of print]. doi.org/10.1016/j.canlet.2010.10009.
37. Smith, M., Barnett, M., Bassan, R., Gatta, G., Tondini, C. & Kern, W. (2004) Adult acute myeloid leukaemia. Critical Reviews in Oncology Hematology, 50, 197-222.
38. Steele, N.L., Plumb, J.A., Vidal, L., Tjornelund, J., Knoblauch, P., Rasmussen, A., Ooi, C.E., Buhl-Jensen, P., Brown, R., Evans, T.R. & DeBono, J.S. (2008) A phase 1 pharmacokinetic and pharmacodynamic study of the histone deacetylase inhibitor belinostat in patients with advanced solid tumors. Clinical Cancer Research, 14, 804-810.
39. Tallman, M.S. (2005) New strategies for the treatment of acute myeloid leukemia including antibodies and other novel agents. Hematology/ the Education Program of the American Society of Hematology., 14, 3-150.
40. Thiede, C., Steudel, C., Mohr, B., Schaich, M., Schakel, U., Platzbecker, U., Wermke, M., Bornhauser, M., Ritter, M., Neubauer, A., Ehninger, G. & Illmer, T. (2002) Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: association with FAB subtypes and identification of subgroups with poor prognosis. Blood, 99, 4326-4335.
41. Wilson, T.R., McLaughlin, K.M., McEwan, M., Sakai, H., Rogers, K.M., Redmond, K.M., Johnston, P.G. & Longley, D.B. (2007) c-FLIP: a key regulator of colorectal cancer cell death. Cancer Research, 67, 5754-5762.
42. Wilson, T.R., Redmond, K.M., McLaughlin, K.M., Crawford, N., Gately, K., O'Byrne, K., Le-Clorrenec, C., Holohan, C., Fennell, D.A., Johnston, P.G. & Longley, D.B. (2009) Procaspase 8 overexpression in non-small-cell lung cancer promotes apoptosis induced by FLIP silencing. Cell Death and Differentiation, 16, 1352-1361.
43. Zhang, X., Li, W. & Olumi, A.F. (2007) Low-dose 12-O-tetradecanoylphorbol-13-acetate enhances tumor necrosis factor related apoptosis-inducing ligand induced apoptosis in prostate cancer cells. Clinical Cancer Research, 13, 7181-7190.