Smac mimetic primes apoptosis-resistant acute myeloid leukaemia cells for cytarabine-induced cell death by triggering necroptosis

Cancer Letters

Volumn 344, Issue 1, 2014, Pages 101-109

  Chromik, Joerg ^a   Safferthal, Charlotta ^a   Serve, Hubert ^a   Fulda, Simone ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Apoptosis; IAP proteins; Leukaemia; Necroptosis; Smac

Indexed keywords

BV 6; CASPASE; CYTARABINE; ETANERCEPT; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG POTENTIATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; NECROPTOSIS; PARACRINE SIGNALING; PRIORITY JOURNAL;

ACUTE MYELOID LEUKAEMIA; AML; APOPTOSIS; ARAC; BACULOVIRUS IAP REPEAT; BIR; CBF; CELLULAR INHIBITOR OF APOPTOSIS PROTEIN 1; CI; CIAP1; COMBINATION INDEX; CORE-BINDING FACTOR; CYTARABINE; FACS; FADD; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; FLUORESCENCE-ACTIVATED CELL-SORTING; IAP; IAP PROTEINS; INHIBITOR OF APOPTOSIS; LEUKAEMIA; MITOCHONDRIAL MEMBRANE POTENTIAL; MIXED LINEAGE KINASE DOMAIN-LIKE PROTEIN; MLKL; MMP; N-BENZYLOXYCARBONYL-VAL-ALA-ASP-FLUOROMETHYLKETONE; NEC; NECROPTOSIS; NECROSTATIN-1; NF-ΚB; NUCLEAR FACTOR KAPPAB; PI; PROPIDIUM IODIDE; REALLY INTERESTING NEW GENE; RECEPTOR-INTERACTING PROTEIN 1; RING; RIP1; SECOND MITOCHONDRIA-DERIVED ACTIVATOR OF CASPASES; SMAC; TNF; TNFR1; TUMOUR NECROSIS FACTOR; TUMOUR NECROSIS FACTOR RECEPTOR 1; X-LINKED INHIBITOR OF APOPTOSIS; XIAP; ZVAD.FMK;

ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; BIOMIMETICS; BLOTTING, WESTERN; CELL LINE, TUMOR; CYTARABINE; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKEMIA, MYELOID, ACUTE; MITOCHONDRIAL PROTEINS; OLIGOPEPTIDES;

EID: 84893682835     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.10.018     Document Type: Article

References (44)

1. Estey E., Dohner H. Acute myeloid leukaemia. Lancet 2006, 368:1894-1907.
2. Schimmer A.D. Apoptosis in leukemia: from molecular pathways to targeted therapies. Best Pract. Res. Clin. Haematol. 2008, 21:5-11.
3. Fulda S. Cell death in hematological tumors. Apoptosis 2009, 14:409-423.
4. Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., Dawson T.M., Dawson V.L., El-Deiry W.S., Fulda S., Gottlieb E., Green D.R., Hengartner M.O., Kepp O., Knight R.A., Kumar S., Lipton S.A., Lu X., Madeo F., Malorni W., Mehlen P., Nunez G., Peter M.E., Piacentini M., Rubinsztein D.C., Shi Y., Simon H.U., Vandenabeele P., White E., Yuan J., Zhivotovsky B., Melino G., Kroemer G. Molecular definitions of cell death subroutines: recommendations of the nomenclature committee on cell death. Cell Death Differ. 2012, 19(2012):107-120.
5. Fulda S., Debatin K.M. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006, 25:4798-4811.
6. Ashkenazi A. Targeting the extrinsic apoptosis pathway in cancer. Cytokine Growth Factor Rev. 2008, 19:325-331.
7. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
8. Vandenabeele P., Galluzzi L., Vanden Berghe T., Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11:700-714.
9. Sun L., Wang H., Wang Z., He S., Chen S., Liao D., Wang L., Yan J., Liu W., Lei X., Wang X. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012, 148:213-227.
10. Oberst A., Dillon C.P., Weinlich R., McCormick L.L., Fitzgerald P., Pop C., Hakem R., Salvesen G.S., Green D.R. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011, 471:363-367.
11. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
12. Eckelman B.P., Salvesen G.S., Scott F.L. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep. 2006, 7:988-994.
13. Bertrand M.J., Milutinovic S., Dickson K.M., Ho W.C., Boudreault A., Durkin J., Gillard J.W., Jaquith J.B., Morris S.J., Barker P.A. CIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 2008, 30:689-700.
14. Varfolomeev E., Goncharov T., Fedorova A.V., Dynek J.N., Zobel K., Deshayes K., Fairbrother W.J., Vucic D. C-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J. Biol. Chem. 2008, 283:24295-24299.
15. Fulda S., Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov. 2012, 11:109-124.
16. Tamm I., Kornblau S.M., Segall H., Krajewski S., Welsh K., Kitada S., Scudiero D.A., Tudor G., Qui Y.H., Monks A., Andreeff M., Reed J.C. Expression and prognostic significance of IAP-family genes in human cancers and myeloid leukemias. Clin. Cancer Res. 2000, 6:1796-1803.
17. Tamm I., Richter S., Scholz F., Schmelz K., Oltersdorf D., Karawajew L., Schoch C., Haferlach T., Ludwig W.D., Wuchter C. XIAP expression correlates with monocytic differentiation in adult de novo AML: impact on prognosis. Hematol. J. 2004, 5:489-495.
18. Hess C.J., Berkhof J., Denkers F., Ossenkoppele G.J., Schouten J.P., Oudejans J.J., Waisfisz Q., Schuurhuis G.J. Activated intrinsic apoptosis pathway is a key related prognostic parameter in acute myeloid leukemia. J. Clin. Oncol. 2007, 25:1209-1215.
19. Bullinger L., Rucker F.G., Kurz S., Du J., Scholl C., Sander S., Corbacioglu A., Lottaz C., Krauter J., Frohling S., Ganser A., Schlenk R.F., Dohner K., Pollack J.R., Dohner H. Gene-expression profiling identifies distinct subclasses of core binding factor acute myeloid leukemia. Blood 2007, 110:1291-1300.
20. Luck S.C., Russ A.C., Botzenhardt U., Paschka P., Schlenk R.F., Dohner H., Fulda S., Dohner K., Bullinger L. Deregulated apoptosis signaling in core-binding factor leukemia differentiates clinically relevant, molecular marker-independent subgroups. Leukemia 2011, 25:1728-1738.
21. Varfolomeev E., Blankenship J.W., Wayson S.M., Fedorova A.V., Kayagaki N., Garg P., Zobel K., Dynek J.N., Elliott L.O., Wallweber H.J., Flygare J.A., Fairbrother W.J., Deshayes K., Dixit V.M., Vucic D. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007, 131:669-681.
22. Vince J.E., Wong W.W., Khan N., Feltham R., Chau D., Ahmed A.U., Benetatos C.A., Chunduru S.K., Condon S.M., McKinlay M., Brink R., Leverkus M., Tergaonkar V., Schneider P., Callus B.A., Koentgen F., Vaux D.L., Silke J. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007, 131:682-693.
23. Wang L., Du F., Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008, 133:693-703.
24. Fakler M., Loeder S., Vogler M., Schneider K., Jeremias I., Debatin K.M., Fulda S. Small molecule XIAP inhibitors cooperate with TRAIL to induce apoptosis in childhood acute leukemia cells and overcome Bcl-2-mediated resistance. Blood 2009, 113:1710-1722.
25. Loeder S., Zenz T., Schnaiter A., Mertens D., Winkler D., Dohner H., Debatin K.M., Stilgenbauer S., Fulda S. A novel paradigm to trigger apoptosis in chronic lymphocytic leukemia. Cancer Res. 2009, 69:8977-8986.
26. Loeder S., Fakler M., Schoeneberger H., Cristofanon S., Leibacher J., Vanlangenakker N., Bertrand M.J., Vandenabeele P., Jeremias I., Debatin K.M., Fulda S. RIP1 is required for IAP inhibitor-mediated sensitization of childhood acute leukemia cells to chemotherapy-induced apoptosis. Leukemia 2012, 26:1020-1029.
27. Fulda S., Wick W., Weller M., Debatin K.M. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 2002, 8:808-815.
28. Vogler M., Walczak H., Stadel D., Haas T.L., Genze F., Jovanovic M., Bhanot U., Hasel C., Moller P., Gschwend J.E., Simmet T., Debatin K.M., Fulda S. Small molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma. Cancer Res. 2009, 69:2425-2434.
29. Abhari B.A., Cristofanon S., Kappler R., von Schweinitz D., Humphreys R., Fulda S. RIP1 is required for IAP inhibitor-mediated sensitization for TRAIL-induced apoptosis via a RIP1/FADD/caspase-8 cell death complex. Oncogene 2013, 32:3263-3273.
30. Basit F., Humphreys R., Fulda S. RIP1 Protein-dependent Assembly of a cytosolic cell death complex is required for Inhibitor of apoptosis (IAP) inhibitor-mediated sensitization to lexatumumab-induced apoptosis. J. Biol. Chem. 2012, 287:38767-38777.
31. Wagner L., Marschall V., Karl S., Cristofanon S., Zobel K., Deshayes K., Vucic D., Debatin K.M., Fulda S. Smac mimetic sensitizes glioblastoma cells to Temozolomide-induced apoptosis in a RIP1- and NF-kappaB-dependent manner. Oncogene 2013, 32:988-997.
32. Roboz G.J. Current treatment of acute myeloid leukemia. Curr. Opin. Oncol. 2012, 24:711-719.
33. Fulda S., Strauss G., Meyer E., Debatin K.M. Functional CD95 ligand and CD95 death-inducing signaling complex in activation-induced cell death and doxorubicin-induced apoptosis in leukemic T cells. Blood 2000, 95:301-308.
34. Chou T.C. The median-effect principle and the combination index for quantitation of synergism and antagonism. Synergism and antagonism in chemotherapy 1991, 61-102. Academic Press, San Diego, USA. T.C. Chou (Ed.).
35. Petersen S.L., Wang L., Yalcin-Chin A., Li L., Peyton M., Minna J., Harran P., Wang X. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer cell 2007, 12:445-456.
36. Biton S., Ashkenazi A. NEMO and RIP1 control cell fate in response to extensive DNA damage via TNF-alpha feedforward signaling. Cell 2011, 145:92-103.
37. Laukens B., Jennewein C., Schenk B., Vanlangenakker N., Schier A., Cristofanon S., Zobel K., Deshayes K., Vucic D., Jeremias I., Bertrand M.J., Vandenabeele P., Fulda S. smac mimetic bypasses apoptosis resistance in FADD- or caspase-8-deficient cells by priming for tumor necrosis factor alpha-induced necroptosis. Neoplasia 2011, 13:971-979.
38. Vanlangenakker N., Vanden Berghe T., Bogaert P., Laukens B., Zobel K., Deshayes K., Vucic D., Fulda S., Vandenabeele P., Bertrand M.J. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 2011, 18:656-665.
39. Carter B.Z., Gronda M., Wang Z., Welsh K., Pinilla C., Andreeff M., Schober W.D., Nefzi A., Pond G.R., Mawji I.A., Houghten R.A., Ostresh J., Brandwein J., Minden M.D., Schuh A.C., Wells R.A., Messner H., Chun K., Reed J.C., Schimmer A.D. Small-molecule XIAP inhibitors derepress downstream effector caspases and induce apoptosis of acute myeloid leukemia cells. Blood 2005, 105:4043-4050.
40. Servida F., Lecis D., Scavullo C., Drago C., Seneci P., Carlo-Stella C., Manzoni L., Polli E., Lambertenghi Deliliers G., Delia D., Onida F. Novel second mitochondria-derived activator of caspases (Smac) mimetic compounds sensitize human leukemic cell lines to conventional chemotherapeutic drug-induced and death receptor-mediated apoptosis. Invest. New Drugs 2011, 29:1264-1275.
41. Weisberg E., Kung A.L., Wright R.D., Moreno D., Catley L., Ray A., Zawel L., Tran M., Cools J., Gilliland G., Mitsiades C., McMillin D.W., Jiang J., Hall-Meyers E., Griffin J.D. Potentiation of antileukemic therapies by Smac mimetic, LBW242: effects on mutant FLT3-expressing cells. Mol. Cancer Ther. 2007, 6:1951-1961.
42. Weisberg E., Ray A., Barrett R., Nelson E., Christie A.L., Porter D., Straub C., Zawel L., Daley J.F., Lazo-Kallanian S., Stone R., Galinsky I., Frank D., Kung A.L., Griffin J.D. Smac mimetics: implications for enhancement of targeted therapies in leukemia. Leukemia 2010, 24:2100-2109.
43. Horita H., Frankel A.E., Thorburn A. Acute myeloid leukemia-targeted toxin activates both apoptotic and necroptotic death mechanisms. PLoS One 2008, 3:e3909.
44. Fulda S. Exploiting inhibitor of apoptosis proteins as therapeutic targets in hematological malignancies. Leukemia 2012, 26:1155-1165.