Exploiting inhibitor of apoptosis proteins as therapeutic targets in hematological malignancies

Leukemia

Volumn 26, Issue 6, 2012, Pages 1155-1165

  Fulda, S ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

apoptosis; hematologic malignancies; IAP proteins; Smac

Indexed keywords

AEG 35156; AEG 40826; ANTISENSE OLIGODEOXYNUCLEOTIDE; AT 406; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; BORTEZOMIB; CYTARABINE; GDC 0917; HGS 1029; IDARUBICIN; INHIBITOR OF APOPTOSIS PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; LBW 242; LCL 161; MELPHALAN; MIDOSTAURIN; NTI 0052; PROTEIN INHIBITOR; SURVIVIN; TL 32711; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MIXED LINEAGE LEUKEMIA; APOPTOSIS; ARTICLE; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL RESEARCH; DRUG TARGETING; HEMATOLOGIC MALIGNANCY; HODGKIN DISEASE; HUMAN; LARGE CELL LYMPHOMA; LEUKEMIA; LYMPHOMA; MOLECULARLY TARGETED THERAPY; MULTIPLE MYELOMA; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; T CELL LEUKEMIA; TREATMENT OUTCOME;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; DRUG DISCOVERY; HEMATOLOGIC NEOPLASMS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS;

EID: 84862011014     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2012.4     Document Type: Article

References (116)

1. Lockshin RA, Zakeri Z. Cell death in health and disease. J Cell Mol Med 2007; 11: 1214-1224.
2. Reed JC, Pellecchia M. Apoptosis-based therapies for hematologic malignancies. Blood 2005; 106: 408-418. (Pubitemid 40981231)
3. Fulda S, Debatin KM. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006; 25: 4798-4811. (Pubitemid 44187627)
4. Fulda S. Tumor resistance to apoptosis. Int J Cancer 2009; 124: 511-515.
5. LaCasse EC, Mahoney DJ, Cheung HH, Plenchette S, Baird S, Korneluk RG. IAP-targeted therapies for cancer. Oncogene 2008; 27: 6252-6275.
6. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008; 7: 1001-1012.
7. Fulda S, Galluzzi L, Kroemer G. Targeting mitochondria for cancer therapy. Nat Rev Drug Discov 2010; 9: 447-464.
8. Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 2008; 8: 61-70.
9. Altieri DC. New wirings in the survivin networks. Oncogene 2008; 27: 6276-6284.
10. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011; 12: 439-452.
11. Eckelman BP, Salvesen GS, Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 2006; 7: 988-994. (Pubitemid 44480512)
12. Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES et al. Structural basis of caspase-7 inhibition by XIAP. Cell 2001; 104: 769-780. (Pubitemid 32241026)
13. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW et al. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001; 104: 791-800. (Pubitemid 32241028)
14. Huang Y, Park YC, Rich RL, Segal D, Myszka DG, Wu H. Structural basis of caspase inhibition by XIAP: differential roles of the linker versus the BIR domain. Cell 2001; 104: 781-790. (Pubitemid 32241027)
15. Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J et al. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001; 410: 112-116. (Pubitemid 32225846)
16. Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM et al. Mechanism of XIAP-mediated inhibition of caspase-9. Mol Cell 2003; 11: 519-527. (Pubitemid 36293842)
17. Lu M, Lin S-C, Huang Y, Kang YJ, Rich R, Lo Y-C et al. XIAP induces NF-kappaB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol Cell 2007; 26: 689-702. (Pubitemid 46856243)
18. Levkau B, Garton KJ, Ferri N, Kloke K, Nofer JR, Baba HA et al. xIAP induces cell-cycle arrest and activates nuclear factor-kappaB: new survival pathways disabled by caspase-mediated cleavage during apoptosis of human endothelial cells. Circ Res 2001; 88: 282-290. (Pubitemid 32173751)
19. Lewis J, Burstein E, Reffey SB, Bratton SB, Roberts AB, Duckett CS. Uncoupling of the signaling and caspase-inhibitory properties of X-linked inhibitor of apoptosis. J Biol Chem 2004; 279: 9023-9029. (Pubitemid 38295965)
20. Birkey Reffey S, Wurthner JU, Parks WT, Roberts AB, Duckett CS. X-linked inhibitor of apoptosis protein functions as a cofactor in transforming growth factor-beta signaling. J Biol Chem 2001; 276: 26542-26549.
21. Hofer-Warbinek R, Schmid JA, Stehlik C, Binder BR, Lipp J, de Martin R. Activation of NF-kappa B by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1. J Biol Chem 2000; 275: 22064-22068. (Pubitemid 30621784)
22. Huang H, Joazeiro CA, Bonfoco E, Kamada S, Leverson JD, Hunter T. The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7. J Biol Chem 2000; 275: 26661-26664.
23. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 2008; 30: 689-700. (Pubitemid 351818251)
24. Varfolomeev E, Goncharov T, Fedorova AV, Dynek JN, Zobel K, Deshayes K et al. 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.
25. Mahoney DJ, Cheung HH, Mrad RL, Plenchette S, Simard C, Enwere E et al. Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc Natl Acad Sci USA 2008; 105: 11778-11783.
26. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 2008; 9: 1364-1370.
27. Zarnegar BJ, Wang Y, Mahoney DJ, Dempsey PW, Cheung HH, He J et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 2008; 9: 1371-1378.
28. Xu L, Zhu J, Hu X, Zhu H, Kim HT, LaBaer J et al. c-IAP1 cooperates with Myc by acting as a ubiquitin ligase for Mad1. Mol Cell 2007; 28: 914-922. (Pubitemid 350217057)
29. Kasof GM, Gomes BC. Livin, a novel inhibitor of apoptosis protein family member. J Biol Chem 2001; 276: 3238-3246.
30. Vucic D, Stennicke HR, Pisabarro MT, Salvesen GS, Dixit VM. ML-IAP, a novel inhibitor of apoptosis that is preferentially expressed in human melanomas. Curr Biol 2000; 10: 1359-1366.
31. Ashhab Y, Alian A, Polliack A, Panet A, Ben Yehuda D. Two splicing variants of a new inhibitor of apoptosis gene with different biological properties and tissue distribution pattern. FEBS Lett 2001; 495: 56-60. (Pubitemid 32367973)
32. Vucic D, Deshayes K, Ackerly H, Pisabarro MT, Kadkhodayan S, Fairbrother WJ et al. SMAC negatively regulates the anti-apoptotic activity of melanoma inhibitor of apoptosis (ML-IAP). J Biol Chem 2002; 277: 12275-12279. (Pubitemid 34952796)
33. Vucic D, Franklin MC, Wallweber HJA, Das K, Eckelman BP, Shin H et al. Engineering ML-IAP to produce an extraordinarily potent caspase 9 inhibitor: implications for Smac-dependent anti-apoptotic activity of ML-IAP. Biochem J 2005; 385: 11-20.
34. Nachmias B, Ashhab Y, Bucholtz V, Drize O, Kadouri L, Lotem M et al. Caspase-mediated cleavage converts Livin from an antiapoptotic to a proapoptotic factor: implications for drug-resistant melanoma. Cancer Res 2003; 63: 6340-6349. (Pubitemid 37255182)
35. Nachmias B, Lazar I, Elmalech M, Abed-El-Rahaman I, Asshab Y, Mandelboim O et al. Subcellular localization determines the delicate balance between the anti-and pro-apoptotic activity of Livin. Apoptosis 2007; 12: 1129-1142. (Pubitemid 46890380)
36. Imoto I, Yang ZQ, Pimkhaokham A, Tsuda H, Shimada Y, Imamura M et al. Identification of cIAP1 as a candidate target gene within an amplicon at 11q22 in esophageal squamous cell carcinomas. Cancer Res 2001; 61: 6629-6634. (Pubitemid 32896476)
37. Bashyam MD, Bair R, Kim YH, Wang P, Hernandez-Boussard T, Karikari CA et al. Array-based comparative genomic hybridization identifies localized DNA amplifications and homozygous deletions in pancreatic cancer. Neoplasia 2005; 7: 556-562. (Pubitemid 40967756)
38. Dierlamm J, Baens M, Wlodarska I, Stefanova-Ouzounova M, Hernandez JM, Hossfeld DK et al. The apoptosis inhibitor gene API2 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21) associated with mucosa-associated lymphoid tissue lymphomas. Blood 1999; 93: 3601-3609. (Pubitemid 29249804)
39. Akagi T, Motegi M, Tamura A, Suzuki R, Hosokawa Y, Suzuki H et al. A novel gene, MALT1 at 18q21, is involved in t(11;18) (q21;q21) found in low-grade B-cell lymphoma of mucosa-associated lymphoid tissue. Oncogene 1999; 18: 5785-5794. (Pubitemid 29507432)
40. Morgan JA, Yin Y, Borowsky AD, Kuo F, Nourmand N, Koontz JI et al. Breakpoints of the t(11;18)(q21;q21) in mucosa-associated lymphoid tissue (MALT) lymphoma lie within or near the previously undescribed gene MALT1 in chromosome 18. Cancer Res 1999; 59: 6205-6213. (Pubitemid 30035644)
41. Ye H, Liu H, Attygalle A, Wotherspoon AC, Nicholson AG, Charlotte F et al. Variable frequencies of t(11;18)(q21;q21) in MALT lymphomas of different sites: significant association with CagA strains of H pylori in gastric MALT lymphoma. Blood 2003; 102: 1012-1018. (Pubitemid 36917798)
42. Snipas SJ, Wildfang E, Nazif T, Christensen L, Boatright KM, Bogyo M et al. Characteristics of the caspase-like catalytic domain of human paracaspase. Biol Chem 2004; 385: 1093-1098. (Pubitemid 39600319)
43. Zhou H, Wertz I, O'Rourke K, Ultsch M, Seshagiri S, Eby M et al. Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 2004; 427: 167-171. (Pubitemid 38094958)
44. Varfolomeev E, Wayson SM, Dixit VM, Fairbrother WJ, Vucic D. The inhibitor of apoptosis protein fusion c-IAP2. MALT1 stimulates NF-kappaB activation independently of TRAF1 AND TRAF2. J Biol Chem 2006; 281: 29022-29029. (Pubitemid 44507046)
45. Waldele K, Silbermann K, Schneider G, Ruckes T, Cullen BR, Grassmann R. Requirement of the human T-cell leukemia virus (HTLV-1) tax-stimulated HIAP-1 gene for the survival of transformed lymphocytes. Blood 2006; 107: 4491-4499. (Pubitemid 43801377)
46. Tamm I, Kornblau SM, Segall H, Krajewski S, Welsh K, Kitada S et al. Expression and prognostic significance of IAP-family genes in human cancers and myeloid leukemias. Clin Cancer Res 2000; 6: 1796-1803. (Pubitemid 30305074)
47. Tamm I, Richter S, Scholz F, Schmelz K, Oltersdorf D, Karawajew L et al. XIAP expression correlates with monocytic differentiation in adult de novo AML: impact on prognosis. Hematol J 2004; 5: 489-495. (Pubitemid 40045282)
48. Carter BZ, Kornblau SM, Tsao T, Wang RY, Schober WD, Milella M et al. Caspase-independent cell death in AML: caspase inhibition in vitro with pancaspase inhibitors or in vivo by XIAP or Survivin does not affect cell survival or prognosis. Blood 2003; 102: 4179-4186. (Pubitemid 37487005)
49. Hess CJ, Berkhof J, Denkers F, Ossenkoppele GJ, Schouten JP, Oudejans JJ et al. Activated intrinsic apoptosis pathway is a key related prognostic parameter in acute myeloid leukemia. J Clin Oncol 2007; 25: 1209-1215. (Pubitemid 46640566)
50. Luck SC, Russ AC, Botzenhardt U, Paschka P, Schlenk RF, Dohner H et al. Deregulated apoptosis signaling in core-binding factor leukemia differentiates clinically relevant, molecular marker-independent subgroups. Leukemia 2011; 25: 1728-1738.
51. Bullinger L, Rucker FG, Kurz S, Du J, Scholl C, Sander S et al. Gene-expression profiling identifies distinct subclasses of core binding factor acute myeloid leukemia. Blood 2007; 110: 1291-1300. (Pubitemid 47281428)
52. Sung KW, Choi J, Hwang YK, Lee SJ, Kim HJ, Kim JY et al. Overexpression of X-linked inhibitor of apoptosis protein (XIAP) is an independent unfavorable prognostic factor in childhood de novo acute myeloid leukemia. J Korean Med Sci 2009; 24: 605-613.
53. Tamm I, Richter S, Oltersdorf D, Creutzig U, Harbott J, Scholz F et al. High expression levels of x-linked inhibitor of apoptosis protein and survivin correlate with poor overall survival in childhood de novo acute myeloid leukemia. Clin Cancer Res 2004; 10: 3737-3744. (Pubitemid 38697607)
54. 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: 260-266.
55. Holcik M, Lefebvre C, Yeh C, Chow T, Korneluk RG. A new internal-ribosomeentry-site motif potentiates XIAP-mediated cytoprotection. Nat Cell Biol 1999; 1: 190-192. (Pubitemid 129656025)
56. Grzybowska-Izydorczyk O, Cebula B, Robak T, Smolewski P. Expression and prognostic significance of the inhibitor of apoptosis protein (IAP) family and its antagonists in chronic lymphocytic leukaemia. Eur J Cancer 2010; 46: 800-810.
57. Frenzel LP, Patz M, Pallasch CP, Brinker R, Claasen J, Schulz A et al. Novel X-linked inhibitor of apoptosis inhibiting compound as sensitizer for TRAIL-mediated apoptosis in chronic lymphocytic leukaemia with poor prognosis. Br J Haematol 2011; 152: 191-200.
58. Vallat L, Magdelenat H, Merle-Beral H, Masdehors P, Potocki de Montalk G, Davi F et al. The resistance of B-CLL cells to DNA damage-induced apoptosis defined by DNA microarrays. Blood 2003; 101: 4598-4606. (Pubitemid 36857833)
59. Silva KL, Vasconcellos DV, Castro ED, Coelho AM, Linden R, Maia RC. Apoptotic effect of fludarabine is independent of expression of IAPs in B-cell chronic lymphocytic leukemia. Apoptosis 2006; 11: 277-285. (Pubitemid 43291027)
60. De Graaf AO, van Krieken JH, Tonnissen E, Wissink W, van de Locht L, Overes I et al. Expression of C-IAP1, C-IAP2 and SURVIVIN discriminates different types of lymphoid malignancies. Br J Haematol 2005; 130: 852-859. (Pubitemid 43899726)
61. Nakagawa Y, Hasegawa M, Kurata M, Yamamoto K, Abe S, Inoue M et al. Expression of IAP-family proteins in adult acute mixed lineage leukemia (AMLL). Am J Hematol 2005; 78: 173-180. (Pubitemid 40316493)
62. Hussain AR, Uddin S, Ahmed M, Bu R, Ahmed SO, Abubaker J et al. Prognostic significance of XIAP expression in DLBCL and effect of its inhibition on AKT signalling. J Pathol 2010; 222: 180-190.
63. Hasegawa T, Suzuki K, Sakamoto C, Ohta K, Nishiki S, Hino M et al. Expression of the inhibitor of apoptosis (IAP) family members in human neutrophils: up-regulation of cIAP2 by granulocyte colony-stimulating factor and overexpression of cIAP2 in chronic neutrophilic leukemia. Blood 2003; 101: 1164-1171. (Pubitemid 36139392)
64. Kashkar H, Haefs C, Shin H, Hamilton-Dutoit SJ, Salvesen GS, Kronke M et al. XIAP-mediated caspase inhibition in Hodgkin's lymphoma-derived B cells. J Exp Med 2003; 198: 341-347. (Pubitemid 36987859)
65. Keats JJ, Fonseca R, Chesi M, Schop R, Baker A, Chng WJ et al. Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 2007; 12: 131-144. (Pubitemid 47208626)
66. Annunziata CM, Davis RE, Demchenko Y, Bellamy W, Gabrea A, Zhan F et al. Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 2007; 12: 115-130. (Pubitemid 47199123)
67. El-Mesallamy HO, Hegab HM, Kamal AM. Expression of inhibitor of apoptosis protein (IAP) livin/BIRC7 in acute leukemia in adults: correlation with prognostic factors and outcome. Leuk Res 2011; 35: 1616-1622.
68. Choi J, Hwang YK, Sung KW, Lee SH, Yoo KH, Jung HL et al. Expression of Livin, an antiapoptotic protein, is an independent favorable prognostic factor in childhood acute lymphoblastic leukemia. Blood 2007; 109: 471-477. (Pubitemid 46105940)
69. Pluta A, Wrzesien-Kus A, Cebula-Obrzut B, Wolska A, Szmigielska-Kaplon A, Czemerska M et al. Influence of high expression of Smac/DIABLO protein on the clinical outcome in acute myeloid leukemia patients. Leuk Res 2010; 34: 1308-1313.
70. Ren Y, Akyurek N, Schlette E, Rassidakis GZ, Medeiros LJ. Expression of Smac/DIABLO in B-cell non-Hodgkin and Hodgkin lymphomas. Hum Pathol 2006; 37: 1407-1413. (Pubitemid 44584334)
71. Chai J, Du C, Wu JW, Kyin S, Wang X, Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 2000; 406: 855-862. (Pubitemid 30664254)
72. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAILor anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002; 8: 808-815.
73. Arnt CR, Chiorean MV, Heldebrant MP, Gores GJ, Kaufmann SH. Synthetic Smac/DIABLO peptides enhance the effects of chemotherapeutic agents by binding XIAP and cIAP1 in situ. J Biol Chem 2002; 277: 44236-44243. (Pubitemid 36157856)
74. Yang L, Mashima T, Sato S, Mochizuki M, Sakamoto H, Yamori T et al. Predominant suppression of apoptosome by inhibitor of apoptosis protein in non-small cell lung cancer H460 cells: therapeutic effect of a novel polyarginineconjugated Smac peptide. Cancer Res 2003; 63: 831-837. (Pubitemid 36231984)
75. Oost TK, Sun C, Armstrong RC, Al-Assaad AS, Betz SF, Deckwerth TL et al. Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer. J Med Chem 2004; 47: 4417-4426. (Pubitemid 39096830)
76. Sharma SK, Straub C, Zawel L. Development of peptidomimetics targeting IAPs. Int J Pept Res Ther 2006; 12: 21-32.
77. Kipp RA, Case MA, Wist AD, Cresson CM, Carrell M, Griner E et al. Molecular targeting of inhibitor of apoptosis proteins based on small molecule mimics of natural binding partners. Biochemistry (Mosc) 2002; 41: 7344-7349. (Pubitemid 34602451)
78. Flygare JA, Fairbrother WJ. Small-molecule pan-IAP antagonists: a patent review. Expert Opin Ther Pat 2010; 20: 251-267.
79. Zobel K, Wang L, Varfolomeev E, Franklin MC, Elliott LO, Wallweber HJ et al. Design, synthesis, and biological activity of a potent Smac mimetic that sensitizes cancer cells to apoptosis by antagonizing IAPs. ACS Chem Biol 2006; 1: 525-533.
80. Sun H, Nikolovska-Coleska Z, Yang CY, Qian D, Lu J, Qiu S et al. Design of small-molecule peptidic and nonpeptidic Smac mimetics. Acc Chem Res 2008; 41: 1264-1277.
81. Gaither A, Porter D, Yao Y, Borawski J, Yang G, Donovan J et al. A Smac mimetic rescue screen reveals roles for inhibitor of apoptosis proteins in tumor necrosis factor-alpha signaling. Cancer Res 2007; 67: 11493-11498.
82. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007; 131: 669-681. (Pubitemid 350087204)
83. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007; 131: 682-693. (Pubitemid 350103599)
84. Sun H, Nikolovska-Coleska Z, Lu J, Meagher JL, Yang CY, Qiu S et al. Design, synthesis, and characterization of a potent, nonpeptide, cell-permeable, bivalent Smac mimetic that concurrently targets both the BIR2 and BIR3 domains in XIAP. J Am Chem Soc 2007; 129: 15279-15294. (Pubitemid 350247811)
85. Jansen B, Zangemeister-Wittke U. Antisense therapy for cancer-the time of truth. Lancet Oncol 2002; 3: 672-683. (Pubitemid 35314910)
86. LaCasse EC, Cherton-Horvat GG, Hewitt KE, Jerome LJ, Morris SJ, Kandimalla ER et al. Preclinical characterization of AEG35156/GEM 640, a second-generation antisense oligonucleotide targeting X-linked inhibitor of apoptosis. Clin Cancer Res 2006; 12: 5231-5241. (Pubitemid 44453353)
87. Carter BZ, Gronda M, Wang Z, Welsh K, Pinilla C, Andreeff M et al. Small-molecule XIAP inhibitors derepress downstream effector caspases and induce apoptosis of acute myeloid leukemia cells. Blood 2005; 105: 4043-4050. (Pubitemid 40656154)
88. Weisberg E, Kung AL, Wright RD, Moreno D, Catley L, Ray A et al. Potentiation of antileukemic therapies by Smac mimetic, LBW242: effects on mutant FLT3-expressing cells. Mol Cancer Ther 2007; 6: 1951-1961. (Pubitemid 47052485)
89. Weisberg E, Ray A, Barrett R, Nelson E, Christie AL, Porter D et al. Smac mimetics: implications for enhancement of targeted therapies in leukemia. Leukemia 2010; 24: 2100-2109.
90. Fakler M, Loeder S, Vogler M, Schneider K, Jeremias I, Debatin KM 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: 1710-1722.
91. 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: 2216-2228.
92. Loeder S, Fakler M, Schoeneberger H, Cristofanon S, Vanlangenakker N, Bertrand M et al. RIP is required for IAP inhibitor-mediated sensitization of childhood acute leukemia cells to chemotherapy-induced apoptosis. Leukemia 2011; e-pub ahead of print 16 December 2011.
93. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008; 133: 693-703. (Pubitemid 351636305)
94. Laukens B, Jennewein C, Schenk B, Vanlangenakker N, Schier A, Cristofanon S et al. 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.
95. Vanlangenakker N, Vanden Berghe T, Bogaert P, Laukens B, Zobel K, Deshayes K et al. 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.
96. He S, Wang L, Miao L, Wang T, Du F, Zhao L et al. Receptor interacting protein kinase-3. determines cellular necrotic response to TNF-alpha. Cell 2009; 137: 1100-1111.
97. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011; 471: 363-367.
98. Zhang H, Zhou X, McQuade T, Li J, Chan FK, Zhang J. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 2011; 471: 373-376.
99. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011; 471: 368-372.
100. Servida F, Lecis D, Scavullo C, Drago C, Seneci P, Carlo-Stella C et al. 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.
101. Guo F, Nimmanapalli R, Paranawithana S, Wittman S, Griffin D, Bali P et al. Ectopic overexpression of second mitochondria-derived activator of caspases (Smac/DIABLO) or cotreatment with N-terminus of Smac/DIABLO peptide potentiates epothilone B derivative-(BMS 247550) and Apo-2L/TRAIL-induced apoptosis. Blood 2002; 99: 3419-3426. (Pubitemid 34525325)
102. Loeder S, Zenz T, Schnaiter A, Mertens D, Winkler D, Dohner H et al. A novel paradigm to trigger apoptosis in chronic lymphocytic leukemia. Cancer Res 2009; 69: 8977-8986.
103. Zenz T, Mertens D, Dohner H, Stilgenbauer S. Importance of genetics in chronic lymphocytic leukemia. Blood Rev 2011; 25: 131-137.
104. Kater AP, Dicker F, Mangiola M, Welsh K, Houghten R, Ostresh J et al. Inhibitors of XIAP sensitize CD40-activated chronic lymphocytic leukemia cells to CD95-mediated apoptosis. Blood 2005; 106: 1742-1748. (Pubitemid 41208589)
105. Chauhan D, Neri P, Velankar M, Podar K, Hideshima T, Fulciniti M et al. Targeting mitochondrial factor Smac/DIABLO as therapy for multiple myeloma (MM). Blood 2007; 109: 1220-1227. (Pubitemid 46220671)
106. Kashkar H, Seeger JM, Hombach A, Deggerich A, Yazdanpanah B, Utermohlen O et al. XIAP targeting sensitizes Hodgkin lymphoma cells for cytolytic T-cell attack. Blood 2006; 108: 3434-3440.
107. Schimmer AD, Estey EH, Borthakur G, Carter BZ, Schiller GJ, Tallmann MS et al. PhaseI/II trial of AEG35156 X-linked inhibitor of apoptosis protein antisense oligonucleotide combined with idarubicin and cytarabine in patients with relapsed or primary refractory acute myeloid leukemia. J Clin Oncol 2009; 27: 4741-4746.
108. Carter BZ, Mak DH, Morris SJ, Borthakur G, Estey E, Byrd AL et al. XIAP antisense oligonucleotide (AEG35156) achieves target knockdown and induces apoptosis preferentially in CD34+38-cells in a phase 1/2 study of patients with relapsed/refractory AML. Apoptosis 2011; 16: 67-74.
109. Schimmer AD, Herr W, Hanel M, Borthakur G, Frankel A, Horst HA et al. Addition of AEG35156 XIAP antisense oligonucleotide in reinduction chemotherapy does not improve remission rates in patients with primary refractory acute myeloid leukemia in a randomized Phase II study. Clin Lymph Myeloma Leukemia 2011; 11: 433-438.
110. Infante JR, Dees EC, Burris HA, Zawel L, Sager JA, Stevenson C et al. A phase I study of LCL-161, an oral inhibitor, in patients with advanced cancer. The Annual Meeting of the American Association for Cancer Research (Washington, DC, USA, 2010). 2010.
111. Amaravadi RK, Schilder RJ, Dy GK, Ma WW, Fetterly GJ, Weng DE et al. Phase I study of the Smac mimetic TL32711 in adult subjects with advanced solid tumors & lymphoma to evaluate safety, pharmocokinetics, pharmocodynamics and anti-tumor activity. 2011 Annual AACR Conference (Orlando, FL, 2011). 2011.
112. Sikic BI, Eckhardt SG, Gallant G, Burris HA, Camidge DR, Covelas AD et al. Safety, pharmocokinetics (PK), and pharmacodynamics (PD) of HGS1029, an inhibitor of apoptosis protein (IAP), in patients (Pts.) with advanced solid tumors: results of a phase I study. 2011 Annual ASCO Meeting (Chicago, IL, 2011). 2011.
113. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, Jovanovic M et al. Targeting XIAP bypasses Bcl-2-mediated resistance to TRAIL and cooperates with TRAIL to suppress pancreatic cancer growth in vitro and in vivo. Cancer Res 2008; 68: 7956-7965.
114. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, Jovanovic M et al. Small molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma. Cancer Res 2009; 69: 2425-2434.
115. Genentech I. A study evaluating the safety, tolerability and pharmacokinetics of GDC-0917 administered to patients with refractory solid tumors or lymphoma. ClinicalTrials.gov, 2010.
116. Cai Q, Sun H, Peng Y, Lu J, Nikolovska-Coleska Z, McEachern D et al. A potent and orally active antagonist (SM-406/AT-406) of multiple inhibitor of apoptosis proteins (IAPs) in clinical development for cancer treatment. J Med Chem 2011; 54: 2714-2726.