Smac mimetic and glucocorticoids synergize to induce apoptosis in childhood ALL by promoting ripoptosome assembly

Blood

Volumn 124, Issue 2, 2014, Pages 240-250

  Belz, Katharina ^a   Schoeneberger, Hannah ^a   Wehner, Sibylle ^b   Weigert, Andreas ^a   Bönig, Halvard ^a   Klingebiel, Thomas ^b   Fichtner, Iduna ^c   Fulda, Simone ^a  

^a GOETHE UNIVERSITY   (Germany)

^b Children's Hospital   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTILEUKEMIC AGENT; BORTEZOMIB; CASPASE 3; CASPASE 8; CASPASE 9; CD34 ANTIGEN; CYTOCHROME C; DEXAMETHASONE; FAS LIGAND; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; LEXATUMUMAB; REACTIVE OXYGEN METABOLITE; SMAC MIMETIC BV6; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ACUTE LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CHILDHOOD LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG INTERACTION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; JURKAT CELL LINE; LEUKEMIA CELL; MESENCHYMAL STROMA CELL; MONOTHERAPY; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN EXPRESSION; TREATMENT DURATION; TUMOR XENOGRAFT;

ANIMALS; APOPTOSIS; CASPASE 8; CELLS, CULTURED; CHILD; DRUG SYNERGISM; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; GLUCOCORTICOIDS; GTPASE-ACTIVATING PROTEINS; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; OLIGOPEPTIDES; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN MULTIMERIZATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904104369     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-05-500918     Document Type: Article

References (49)

1. Pui CH, Relling MV, Downing JR. Acute lymphoblastic leukemia. N Engl J Med. 2004;350(15):1535-1548.
2. Stanulla M, Cario G, Meissner B, et al. Integrating molecular information into treatment of childhood acute lymphoblastic leukemia-a perspective from the BFM Study Group. Blood Cells Mol Dis. 2007;39(2):160-163.
3. Tissing WJ, Meijerink JP, den Boer ML, Pieters R. Molecular determinants of glucocorticoid sensitivity and resistance in acute lymphoblastic leukemia. Leukemia. 2003;17(1):17-25.
4. Sionov RV, Spokoini R, Kfir-Erenfeld S, Cohen O, Yefenof E. Mechanisms regulating the susceptibility of hematopoietic malignancies to glucocorticoid-induced apoptosis. Adv Cancer Res. 2008;101:127-248.
5. Lockshin RA, Zakeri Z. Cell death in health and disease. J Cell Mol Med. 2007;11(6):1214-1224.
6. Schimmer AD. Apoptosis in leukemia: from molecular pathways to targeted therapies. Best Pract Res Clin Haematol. 2008;21(1):5-11.
7. Fulda S. Cell death in hematological tumors. Apoptosis. 2009;14(4):409-423.
8. Fulda S, Debatin KM. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene. 2006;25(34):4798-4811.
9. Fulda S, Galluzzi L, Kroemer G. Targeting mitochondria for cancer therapy. Nat Rev Drug Discov. 2010;9(6):447-464.
10. Fulda S, Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat Rev Drug Discov. 2012;11(2):109-124.
11. Fulda S. Tumor resistance to apoptosis. Int J Cancer. 2009;124(3):511-515.
12. Hundsdoerfer P, Dietrich I, Schmelz K, Eckert C, Henze G. XIAP expression is post-transcriptionally upregulated in childhood ALL and is associated with glucocorticoid response in T-cell ALL. Pediatr Blood Cancer. 2010;55(2):260-266.
13. Wuchter C, Richter S, Oltersdorf D, Karawajew L, Ludwig WD, Tamm I. Differences in the expression pattern of apoptosis-related molecules between childhood and adult de novo acute myeloid leukemia. Haematologica. 2004;89(3):363-364.
14. Eckelman BP, Salvesen GS, Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep. 2006;7(10):988-994.
15. Festjens N, Vanden Berghe T, Cornelis S, Vandenabeele P. RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ. 2007;14(3):400-410.
16. Feoktistova M, Geserick P, Kellert B, et al. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell. 2011;43(3):449-463.
17. Tenev T, Bianchi K, Darding M, et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell. 2011;43(3):432-448.
18. Geserick P, Hupe M, Moulin M, et al. Cellular IAPs inhibit a cryptic CD95-induced cell death by limiting RIP1 kinase recruitment. J Cell Biol. 2009;187(7):1037-1054.
19. Varfolomeev E, Blankenship JW, Wayson SM, et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalphadependent apoptosis. Cell. 2007;131(4):669-681.
20. Vince JE, Wong WW, Khan N, et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell. 2007;131(4):682-693.
21. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell. 2008;133(4):693-703.
22. Fulda S. Molecular pathways: targeting inhibitor of apoptosis proteins in cancer-from molecular mechanism to therapeutic application. Clin Cancer Res. 2014;20(2):289-295.
23. Fakler M, Loeder S, Vogler M, et al. Small molecule XIAP inhibitors cooperate with TRAIL to induce apoptosis in childhood acute leukemia cells and overcome Bcl-2-mediated resistance. Blood. 2009;113(8):1710-1722.
24. Loeder S, Drensek A, Jeremias I, Debatin KM, Fulda S. Small molecule XIAP inhibitors sensitize childhood acute leukemia cells for CD95-induced apoptosis. Int J Cancer. 2010;126(9):2216-2228.
25. Löder S, Fakler M, Schoeneberger H, et al. RIP1 is required for IAP inhibitor-mediated sensitization of childhood acute leukemia cells to chemotherapy-induced apoptosis. Leukemia. 2012;26(5):1020-1029.
26. Gonzalez P, Mader I, Tchoghandjian A, et al. Impairment of lysosomal integrity by B10, a glycosylated derivative of betulinic acid, leads to lysosomal cell death and converts autophagy into a detrimental process. Cell Death Differ. 2012;19(8):1337-1346.
27. Fulda S, Strauss G, Meyer E, Debatin KM. 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(1):301-308.
28. Häcker S, Dittrich A, Mohr A, et al. Histone deacetylase inhibitors cooperate with IFN-gamma to restore caspase-8 expression and overcome TRAIL resistance in cancers with silencing of caspase-8. Oncogene. 2009;28(35):3097-3110.
29. Borgmann A, Baldy C, von Stackelberg A, et al. Childhood all blasts retain phenotypic and genotypic characteristics upon long-term serial passage in NOD/SCID mice. Pediatr Hematol Oncol. 2000;17(8):635-650.
30. Workman P, Aboagye EO, Balkwill F, et al Committee of the National Cancer Research Institute. Guidelines for the welfare and use of animals in cancer research. Br J Cancer. 2010;102(11):1555-1577.
31. Chou TC. The median-effect principle and the combination index for quantitation of synergism and antagonism. In: Chou TC, ed. Synergism and antagonism in chemotherapy. San Diego, USA: Academic Press; 1991:61-102.
32. Müller-Sienerth N, Dietz L, Holtz P, et al. SMAC mimetic BV6 induces cell death in monocytes and maturation of monocyte-derived dendritic cells. PLoS ONE. 2011;6(6):e21556.
33. Batinić-Haberle I, Cuzzocrea S, Rebouças JS, et al. Pure MnTBAP selectively scavenges peroxynitrite over superoxide: comparison of pure and commercial MnTBAP samples to MnTE-2-PyP in two models of oxidative stress injury, an SOD-specific Escherichia coli model and carrageenan-induced pleurisy. Free Radic Biol Med. 2009;46(2):192-201.
34. Bertrand MJ, Milutinovic S, Dickson KM, et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell. 2008;30(6):689-700.
35. Runnebaum IB, Brüning A. Glucocorticoids inhibit cell death in ovarian cancer and up-regulate caspase inhibitor cIAP2. Clin Cancer Res. 2005;11(17):6325-6332.
36. Webster JC, Huber RM, Hanson RL, et al. Dexamethasone and tumor necrosis factor-alpha act together to induce the cellular inhibitor of apoptosis-2 gene and prevent apoptosis in a variety of cell types. Endocrinology. 2002;143(10):3866-3874.
37. Petersen SL, Wang L, Yalcin-Chin A, et al. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell. 2007;12(5):445-456.
38. Wagner L, Marschall V, Karl S, et al. Smac mimetic sensitizes glioblastoma cells to Temozolomide-induced apoptosis in a RIP1-and NF-κB-dependent manner. Oncogene. 2013;32(8):988-997.
39. Fulda S. Therapeutic opportunities for counteracting apoptosis resistance in childhood leukaemia. Br J Haematol. 2009;145(4):441-454.
40. Abhari BA, 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(27):3263-3273.
41. 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(46):38767-38777.
42. Stadel D, Cristofanon S, Abhari BA, et al. Requirement of nuclear factor kB for Smac mimetic-mediated sensitization of pancreatic carcinoma cells for gemcitabine-induced apoptosis. Neoplasia. 2011;13(12):1162-1170.
43. Berger R, Jennewein C, Marschall V, et al. NF-κB is required for Smac mimetic-mediated sensitization of glioblastoma cells for γ-irradiation-induced apoptosis. Mol Cancer Ther. 2011;10(10):1867-1875.
44. Dueber EC, Schoeffler AJ, Lingel A, et al. Antagonists induce a conformational change in cIAP1 that promotes autoubiquitination. Science. 2011;334(6054):376-380.
45. Feltham R, Bettjeman B, Budhidarmo R, et al. Smac mimetics activate the E3 ligase activity of cIAP1 protein by promoting RING domain dimerization. J Biol Chem. 2011;286(19):17015-17028.
46. Yang Y, Fang S, Jensen JP, Weissman AM, Ashwell JD. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science. 2000;288(5467):874-877.
47. Biton S, Ashkenazi A. NEMO and RIP1 control cell fate in response to extensive DNA damage via TNF-α feedforward signaling. Cell. 2011;145(1):92-103.
48. Vince JE, Chau D, Callus B, et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J Cell Biol. 2008;182(1):171-184.
49. Bauer M, Goldstein M, Christmann M, Becker H, Heylmann D, Kaina B. Human monocytes are severely impaired in base and DNA double-strand break repair that renders them vulnerable to oxidative stress. Proc Natl Acad Sci USA. 2011;108(52):21105-21110.