Novel SMAC-mimetics synergistically stimulate melanoma cell death in combination with TRAIL and Bortezomib

British Journal of Cancer

Volumn 102, Issue 12, 2010, Pages 1707-1716

  Lecis, D ^a   Drago, C ^b   Manzoni, L ^b,c   Seneci, P ^b   Scolastico, C ^b   Mastrangelo, E ^b,d   Bolognesi, M ^b,d   Anichini, A ^a   Kashkar, H ^e   Walczak, H ^f   Delia, D ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c CNR Consiglio Nazionale delle Ricerche   (Italy)

^d CNR Consiglio Nazionale delle Ricerche   (Italy)

^e UNIVERSITY OF COLOGNE   (Germany)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; Melanoma; SMAC mimetics; TRAIL

Indexed keywords

ANTINEOPLASTIC AGENT; AZABICYCLO DERIVATIVE; BORTEZOMIB; CASPASE 8; HOMODIMER; LIVIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE MIMETIC; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ARTICLE; BINDING AFFINITY; BIOACCUMULATION; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CELL DEATH; CELL STIMULATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BINDING; DRUG POTENTIATION; ENZYME DEGRADATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MELANOMA CELL; PRIORITY JOURNAL; TUMOR RESISTANCE; WESTERN BLOTTING;

BORONIC ACIDS; CASPASE 8; CELL DEATH; CELL LINE, TUMOR; DOWN-REGULATION; DRUG INTERACTIONS; DRUG SYNERGISM; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MELANOMA; MITOCHONDRIAL PROTEINS; PYRAZINES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 77953292557     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605687     Document Type: Article

References (50)

1. Ashkenazi A, Herbst RS (2008) To kill a tumor cell: the potential of proapoptotic receptor agonists. J Clin Invest 118: 1979-1990
2. Bertrand MJM, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, Barker PA (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 30: 689
3. Boccadoro M, Morgan G, Cavenagh J (2005) Preclinical evaluation of the proteasome inhibitor bortezomib in cancer therapy. Cancer Cell Int 5: 18
4. Chauhan D, Neri P, Velankar M, Podar K, Hideshima T, Fulciniti M, Tassone P, Raje N, Mitsiades C, Mitsiades N, Richardson P, Zawel L, Tran M, Munshi N, Anderson KC (2007) Targeting mitochondrial factor Smac/DIABLO as therapy for multiple myeloma (MM). Blood 109: 1220-1227 (Pubitemid 46220671)
5. Chen LH, Jiang CC, Kiejda KA, Wang YF, Thorne RF, Zhang XD, Hersey P (2007) Thapsigargin sensitizes human melanoma cells to TRAIL-induced apoptosis by up-regulation of TRAIL-R2 through the unfolded protein response. Carcinogenesis 28: 2328-2336
6. Chen LH, Jiang CC, Watts R, Thorne RF, Kiejda KA, Zhang XD, Hersey P (2008) Inhibition of endoplasmic reticulum stress-induced apoptosis of melanoma cells by the ARC protein. Cancer Res 68: 834-842
7. Cossu F, Mastrangelo E, Milani M, Sorrentino G, Lecis D, Delia D, Manzoni L, Seneci P, Scolastico C, Bolognesi M (2009a) Designing Smac-mimetics as antagonists of XIAP, cIAP1, and cIAP2. Biochem Biophys Res Commun 378: 162
8. Cossu F, Milani M, Mastrangelo E, Vachette P, Servida F, Lecis D, Canevari G, Delia D, Drago C, Rizzo V, Manzoni L, Seneci P, Scolastico C, Bolognesi M (2009b) Structural bases for bivalent Smac-mimetics recognition in the IAP protein family. J Mol Biol 392: 630-644
9. Cummins JM, Kohli M, Rago C, Kinzler KW, Vogelstein B, Bunz F (2004) X-linked inhibitor of apoptosis protein (XIAP) is a nonredundant modulator of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis in human cancer cells. Cancer Res 64: 3006
10. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 17: 2215-2223
11. Deveraux QL, Takahashi R, Salvesen GS, Reed JC (1997) X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388: 300-304
12. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42
13. Eckelman BP, Salvesen GS (2006) The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J Biol Chem 281: 3254
14. Gaither A, Porter D, Yao Y, Borawski J, Yang G, Donovan J, Sage D, Slisz J, Tran M, Straub C, Ramsey T, Iourgenko V, Huang A, Chen Y, Schlegel R, Labow M, Fawell S, Sellers WR, Zawel L (2007) A Smac mimetic rescue screen reveals roles for inhibitor of apoptosis proteins in t. Cancer Res 67: 11493
15. Galbán S, Hwang C, Rumble JM, Oetjen KA, Wright CW, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, Duckett CS (2009) Cytoprotective effects of IAPs revealed by a small molecule antagonist. Biochem J 417: 765-771
16. Ganten TM, Haas TL, Sykora J, Stahl H, Sprick MR, Fas SC, Krueger A, Weigand MA, Grosse-Wilde A, Stremmel W, Krammer PH, Walczak H (2004) Enhanced caspase-8 recruitment to and activation at the DISC is critical for sensitisation of human hepatocellular carcinoma cells to TRAIL-induced apoptosis by chemotherapeutic drugs. Cell Death Differ 11: S86-S96
17. Ganten TM, Koschny R, Sykora J, Schulze-Bergkamen H, Buchler P, Haas TL, Schader MB, Untergasser A, Stremmel W, Walczak H (2006) Preclinical differentiation between apparently safe and potentially hepatotoxic applications of TRAIL either alone or in combination with chemotherapeutic drugs. Clin Cancer Res 12: 2640
18. Hayakawa A, Kawamoto Y, Nakajima H, Sakai J, Takasawa R, Nakashima I, Magae J, Tanuma S (2008) Bid truncation mediated by caspases-3 and-9 in vinorelbine-induced apoptosis. Apoptosis 13: 523-530
19. Jiang CC, Chen LH, Gillespie S, Kiejda KA, Mhaidat N, Wang YF, Thorne R, Zhang XD, Hersey P (2007) Tunicamycin sensitizes human melanoma cells to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by up-regulation of TRAIL-R2 via the unfolded protein response. Cancer Res 67: 5880
20. Kashkar H, Deggerich A, Seeger J, Yazdanpanah B, Wiegmann K, Haubert D, Pongratz C, Kronke M (2007) NF-\{kappa\}B-independent down-regulation of XIAP by bortezomib sensitizes HL B cells against cytotoxic drugs. Blood 109: 3982-3988
21. Kempkensteffen C, Hinz S, Christoph F, Köllermann J, Krause H, Schrader M, Schostak M, Miller K, Weikert S (2007) Expression parameters of the inhibitors of apoptosis cIAP1 and cIAP2 in renal cell carcinomas and their prognostic relevance. Int J Cancer 120: 1081-1086
22. Koschny R, Holland H, Sykora J, Haas TL, Sprick MR, Ganten TM, Krupp W, Bauer M, Ahnert P, Meixensberger J, Walczak H (2007) Bortezomib sensitizes primary human astrocytoma cells of WHO grades I to IV for tumor necrosis factor-related apoptosis-inducing ligand-induced apop-tosis. Clin Cancer Res 13: 3403-3412
23. Kurbanov BM, Fecker LF, Geilen CC, Sterry W, Eberle J (2006) Resistance of melanoma cells to TRAIL does not result from upregulation of antiapoptotic proteins by NF-[kappa]B but is related to downregulation of initiator caspases and DR4. Oncogene 26: 3364-3377
24. Kurbanov BM, Geilen CC, Fecker LF, Orfanos CE, Eberle J (2005) Efficient TRAIL-R1//DR4-mediated apoptosis in melanoma cells by tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J Investig Dermatol 125: 1010-1019
25. Lee SH, Kim YK, Kim CS, Seol SK, Kim J, Cho S, Song YL, Bartenschlager R, Jang SK (2005) E2 of hepatitis C virus inhibits apoptosis. J Immunol 175: 8226-8235
26. Lejeune FJ, Rüegg C, Liénard D (1998) Clinical applications of TNF-a in cancer. Curr Opin Immunol 10: 573
27. Li L, Thomas RM, Suzuki H, De Brabander JK, Wang X, Harran PG (2004) A small molecule Smac mimic potentiates TRAIL-and TNF{alpha}-mediated cell death. Science 305: 1471-1474
28. Liu Z, Sun C, Olejniczak ET, Meadows RP, Betz SF, Oost T, Herrmann J, Wu JC, Fesik SW (2000) Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature 408: 1004-1008
29. Lu J, Bai L, Sun H, Nikolovska-Coleska Z, McEachern D, Qiu S, Miller RS, Yi H, Shangary S, Sun Y, Meagher JL, Stuckey JA, Wang S (2008) SM-164: a novel, bivalent Smac mimetic that induces apoptosis and tumor regression by concurrent removal of the blockade of cIAP-1/2 and XIAP. Cancer Res 68: 9384
30. Mastrangelo E, Cossu F, Milani M, Sorrentino G, Lecis D, Delia D, Manzoni L, Drago C, Seneci P, Scolastico C, Rizzo V, Bolognesi M (2008) Targeting the X-linked inhibitor of apoptosis protein through 4-substituted azabicyclo [5.3.0]alkane Smac mimetics. Structure, activity, and recognition principles. J Mol Biol 384: 673
31. Newsom-Davis T, Prieske S, Walczak H (2009) Is TRAIL the holy grail of cancer therapy? Apoptosis 14: 607-623
32. Nikolovska-Coleska Z, Meagher JL, Jiang S, Kawamoto SA, Gao W, Yi H, Qin D, Roller PP, Stuckey JA, Wang S (2008) Design and characterization of bivalent Smac-based peptides as antagonists of XIAP and development and validation of a fluorescence polarization assay for XIAP containing both BIR2 and BIR3 domains. Anal Biochem 374: 87
33. Nikolovska-Coleska Z, Wang R, Fang X, Pan H, Tomita Y, Li P, Roller PP, Krajewski K, Saito NG, Stuckey JA, Wang S (2004) Development and optimization of a binding assay for the XIAP BIR3 domain using fluorescence polarization. Anal Biochem 332: 261
34. Oost TK, Sun C, Armstrong RC, Al-Assaad A, Betz SF, Deckwerth TL, Ding H, Elmore SW, Meadows RP, Olejniczak ET, Oleksijew A, Oltersdorf T, Rosenberg SH, Shoemaker AR, Tomaselli KJ, Zou H, Fesik SW (2004) Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer. J Med Chem 47: 4417-4426
35. Petersen SL, Wang L, Yalcin-Chin A, Li L, Peyton M, Minna J, Harran P, Wang X (2007) Cancer Cell 12: 445
36. Rozanov DV, Savinov AY, Golubkov VS, Rozanova OL, Postnova TI, Sergienko EA, Vasile S, Aleshin AE, Rega MF, Pellecchia M, Strongin AY (2009) Engineering a leucine zipper-TRAIL homotrimer with improved cytotoxicity in tumor cells. Mol Cancer Ther 8: 1515
37. Seneci P, Bianchi A, Battaglia C, Belvisi L, Bolognesi M, Caprini A, Cossu F, Franco ED, Matteo M de, Delia D, Drago C, Khaled A, Lecis D, Manzoni L, Marizzoni M, Mastrangelo E, Milani M, Motto I, Moroni E, Potenza D, Rizzo V, Servida F, Turlizzi E, Varrone M, Vasile F, Scolastico C (2009) Rational design, synthesis and characterization of potent, non-peptidic Smac mimics/XIAP inhibitors as proapoptotic agents for cancer therapy. Bioorg Med Chem 17: 5834
38. Sun H, Nikolovska-Coleska Z, Lu J, Qiu S, Yang C, Gao W, Meagher J, Stuckey J, Wang S (2006) Design, synthesis, and evaluation of a potent, cell-permeable, conformationally constrained second mitochondria derived activator of caspase (Smac) mimetic. J Med Chem 49: 7916-7920
39. Takahashi R, Deveraux Q, Tamm I, Welsh K, Assa-Munt N, Salvesen GS, Reed JC (1998) A single BIR domain of XIAP sufficient for inhibiting caspases. J Biol Chem 273: 7787
40. Todaro M, Lombardo Y, Francipane MG, Alea MP, Cammareri P, Iovino F, Di Stefano, Di Bernardo C, Agrusa A, Condorelli G, Walczak H, Stassi G (2008) Apoptosis resistance in epithelial tumors is mediated by tumor-cell-derived interleukin-4. Cell Death Differ 15: 762-772
41. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, Zobel K, Dynek JN, Elliott LO, Wallweber HJA, Flygare JA, Fairbrother WJ, Deshayes K, Dixit VM, Vucic D (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-kB activation, and TNFa-dependent apoptosis. Cell 131: 669
42. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA, Chunduru SK, Condon SM, McKinlay M, Brink R, Leverkus M, Tergaonkar V, Schneider P, Callus BA, Koentgen F, Vaux DL, Silke J (2007) Cell 131: 682
43. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, Jovanovic M, Bhanot U, Hasel C, Moller P, Gschwend JE, Simmet T, Debatin K, Fulda S (2009) Small molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma. Cancer Res 69: 2425-2434
44. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, Jovanovic M, Gschwend JE, Simmet T, Debatin K, Fulda S (2008) 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 68: 7956-7965
45. Walczak H, Degli-Esposti MA, Johnson RS, Smolak PJ, Waugh JY, Boiani N, Timour MS, Gerhart MJ, Schooley KA, Smith CA, Goodwin RG, Rauch CT (1997) TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL. EMBO J 16: 5386-5397
46. 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 JCL, Lynch DH (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163 (Pubitemid 29068521)
47. Wang L, Du F, Wang X (2008) Cell 133: 693
48. Wieder T, Essmann F, Prokop A, Schmelz K, Schulze-Osthoff K, Beyaert R, Dorken B, Daniel PT (2001) Activation of caspase-8 in drug-induced apoptosis of B-lymphoid cells is independent of CD95/Fas receptor-ligand interaction and occurs downstream of caspase-3. Blood 97: 1378-1387
49. Wu G, Chai J, Suber TL, Wu J, Du C, Wang X, Shi Y (2000) Structural basis of IAP recognition by Smac/DIABLO. Nature 408: 1008-1012
50. Zhang XD, Zhang XY, Gray CP, Nguyen T, Hersey P (2001) Tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis of human melanoma is regulated by Smac/DIABLO release from mitochondria. Cancer Res 61: 7339-7348