Targeting the XIAP/caspase-7 complex selectively kills caspase-3-deficient malignancies

Journal of Clinical Investigation

Volumn 123, Issue 9, 2013, Pages 3861-3875

  Lin, Yuan Feng ^a   Lai, Tsung Ching ^b   Chang, Chih Kang ^a   Chen, Chi Long ^c   Huang, Ming Shyan ^d   Yang, Chih Jen ^d   Liu, Hon Ge ^a   Dong, Jhih Jhong ^e   Chou, Yi An ^e   Teng, Kuo Hsun ^a   Chen, Shih Hsun ^f   Tian, Wei Ting ^e   Jan, Yi Hua ^b   Hsiao, Michael ^b   Liang, Po Huang ^a,e  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^b GENOMICS RESEARCH CENTER   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 7; CYSTEINE DERIVATIVE; MICRORNA; MULTIPROTEIN COMPLEX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN P19; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; X LINKED INHIBITOR OF APOPTOSIS CASPASE 7 COMPLEX; ANTINEOPLASTIC AGENT; CASP3 PROTEIN, HUMAN; CASP7 PROTEIN, HUMAN; LYSINE; XIAP PROTEIN, HUMAN;

ALKYLATION; ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER PROGNOSIS; CANCER RESISTANCE; CELL KILLING; CELL STRAIN MCF 7; CONTROLLED STUDY; CYTOTOXICITY; DISEASE FREE SURVIVAL; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG TARGETING; ENZYME ACTIVITY; ENZYME DEFICIENCY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; BREAST TUMOR; COLON TUMOR; DEFICIENCY; DRUG RESISTANCE; DRUG SCREENING; ENZYME ACTIVATION; ENZYMOLOGY; FEMALE; GENETICS; KAPLAN MEIER METHOD; LUNG TUMOR; MCF 7 CELL LINE; METABOLISM; MORTALITY; MOUSE; NONOBESE DIABETIC MOUSE; SCID MOUSE;

ALKYLATION; AMINO ACID SEQUENCE; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CASPASE 3; CASPASE 7; COLONIC NEOPLASMS; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; LYSINE; MCF-7 CELLS; MICE; MICE, INBRED NOD; MICE, SCID; PROTEIN INTERACTION MAPS; SIGNAL TRANSDUCTION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84883547208     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI67951     Document Type: Article

References (55)

1. Devarajan E, et al. Down-regulation of caspase 3 in breast cancer: a possible mechanism for chemoresistance. Oncogene. 2002;21(57):8843-8851. (Pubitemid 36132404)
2. Sun Y, et al. Differential caspase-3 expression in noncancerous, premalignant and cancer tissues of stomach and its clinical implication. Cancer Detect Prev. 2006;30(2):168-173. (Pubitemid 43766227)
3. Winter RN, Kramer A, Borkowski A, Kyprianou N. Loss of caspase-1 and caspase-3 protein expression in human prostate cancer. Cancer Res. 2001;61(3):1227-1232. (Pubitemid 32174447)
4. Volm M, Koomagi R. Prognostic relevance of c-Myc and caspase-3 for patients with non-small cell lung cancer. Oncol Rep. 2000;7(1):95-98.
5. Oudejans JJ, et al. Absence of caspase 3 activation in neoplastic cells of nasopharyngeal carcinoma biopsies predicts rapid fatal outcome. Mod Pathol. 2005;18(7):877-885. (Pubitemid 41059946)
6. Andressakis D, Lazaris AC, Tsiambas E, Kavantzas N, Rapidis A, Patsouris E. Evaluation of caspase-3 and caspase-8 deregulation in tongue squamous cell carcinoma, based on immunohistochemistry and computerised image analysis. J Laryngol Otol. 2008;122(11):1213-1218.
7. Zygouris P, et al. Evaluation of combined h-TERT, bcl-2, and caspases 3 and 8 expression in cutaneous malignant melanoma based on tissue microarrays and computerized image analysis. J BUON. 2007;12(4):513-519.
8. Huang H, et al. Expression and prognostic significance of osteopontin and caspase-3 in hepatocellular carcinoma patients after curative resection. Cancer Sci. 2010;101(5):1314-1319.
9. Iolascon A, et al. Caspase 3 and 8 deficiency in human neuroblastoma. Cancer Genet Cytogenet. 2003;146(1):41-47. (Pubitemid 37117433)
10. de Heer P, et al. Caspase-3 activity predicts local recurrence in rectal cancer. Clin Cancer Res. 2007;13(19):5810-5815.
11. de Oca J, et al. Caspase-3 activity, response to chemotherapy and clinical outcome in patients with colon cancer. Int J Colorectal Dis. 2008;23(1):21-27. (Pubitemid 350142356)
12. Gronda M, et al. Assessment of the downstream portion of the mitochondrial pathway of caspase activation in patients with acute myeloid leukemia. Apoptosis. 2005;10(6):1285-1294. (Pubitemid 43117676)
13. Blanc C, et al. Caspase-3 is essential for procaspase-9 processing and cisplatin-induced apoptosis of MCF-7 breast cancer cells. Cancer Res. 2000;60(16):4386-4390. (Pubitemid 32103616)
14. Hui KK, Kanungo AK, Elia AJ, Henderson JT. Caspase-3 deficiency reveals a physiologic role for Smac/DIABLO in regulating programmed cell death. Cell Death Differ. 2011;18(11):1780-1790.
15. Paulsen M, et al. Interaction with XIAP prevents full caspase-3/-7 activation in proliferating human T lymphocytes. Eur J Immunol. 2008;38(7):1979-1987.
16. Szymczyk KH, Freeman TA, Adams CS, Srinivas V, Steinbeck MJ. Active caspase-3 is required for osteoclast differentiation. J Cell Physiol. 2006;209(3):836-844. (Pubitemid 44665705)
17. Acarin L, Villapol S, Faiz M, Rohn TT, Castellano B, González B. Caspase-3 activation in astrocytes following postnatal excitotoxic damage correlates with cytoskeletal remodeling but not with cell death or proliferation. Glia. 2007;55(9):954-965. (Pubitemid 46903996)
18. Walsh JG, Cullen SP, Sheridan C, Lüthi AU, Gerner C, Martin SJ. Executioner caspase-3 and caspase-7 are functionally distinct proteases. Proc Natl Acad Sci U S A. 2008;105(35):12815-12819.
19. Kuida K, et al. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature. 1996;384(6607):368-372.
20. Gafni J, Cong X, Chen SF, Gibson BW, Ellerby LM. Calpain-1 cleaves and activates caspase-7. J Biol Chem. 2009;284(37):25441-25449.
21. Lakhani SA, et al. Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science. 2006;311(5762):847-851. (Pubitemid 43228848)
22. Lee AT, Azimahtol HL, Tan AN. Styrylpyrone Derivative (SPD) induces apoptosis in a caspase-7-dependent manner in the human breast cancer cell line MCF-7. Cancer Cell Int. 2003;3(1):16.
23. Houde C, et al. Caspase-7 expanded function and intrinsic expression level underlies strain-specific brain phenotype of caspase-3-null mice. J Neurosci. 2004;24(44):9977-9984. (Pubitemid 39463579)
24. Zheng TS, et al. Deficiency in caspase-9 or caspase-3 induces compensatory caspase activation. Nat Med. 2000;6(11):1241-1247.
25. Twiddy D, Cohen GM, Macfarlane M, Cain K. Caspase-7 is directly activated by the approximately 700-kDa apoptosome complex and is released as a stable XIAP-caspase-7 approximately 200-kDa complex. J Biol Chem. 2006;281(7):3876- 3888. (Pubitemid 43847811)
26. Suzuki Y, Nakabayashi Y, Nakata K, Reed JC, Takahashi R. X-linked inhibitor of apoptosis protein (XIAP) inhibits caspase-3 and -7 in distinct modes. J Biol Chem. 2001;276(29):27058-27063.
27. Yang PM, Tseng HH, Peng CW, Chen WS, Chiu SJ. Dietary flavonoid fisetin targets caspase-3-deficient human breast cancer MCF-7 cells by induction of caspase-7-associated apoptosis and inhibition of autophagy. Int J Oncol. 2012;40(2):469-478.
28. Yamasaki-Miyamoto Y, Yamasaki M, Tachibana H, Yamada K. Fucoidan induces apoptosis through activation of caspase-8 on human breast cancer MCF-7 cells. J Agric Food Chem. 2009;57(18):8677-8682.
29. Chou CC, Wu YC, Wang YF, Chou MJ, Kuo SJ, Chen DR. Capsaicin-induced apoptosis in human breast cancer MCF-7 cells through caspase-independent pathway. Oncol Rep. 2009;21(3):665-671.
30. Lin YF, Tsai WP, Liu HG, Liang PH. Intracellular β-tubulin/ chaperonin containing TCP1-β complex serves as a novel chemotherapeutic target against drug-resistant tumors. Cancer Res. 2009;69(17):6879-6888.
31. Lin YF, Lee YF, Liang PH. Targeting β-tubulin: CCT-β complexes incurs Hsp90- and VCP-related protein degradation and induces ER stress-associated apoptosis by triggering capacitative Ca(2+) entry, mitochondrial perturbation and caspase overactivation. Cell Death Dis. 2012;3:e434.
32. Germain M, Affar EB, D'Amours D, Dixit VM, Salvesen GS, Poirier GG. Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J Biol Chem. 1999;274(40):28379-28384.
33. Xue LY, Chiu SM, Oleinick NL. Staurosporine-induced death of MCF-7 human breast cancer cells: a distinction between caspase-3-dependent steps of apoptosis and the critical lethal lesions. Exp Cell Res. 2003;283(2):135-145. (Pubitemid 36269020)
34. Lee D, et al. Potent and selective nonpeptide inhibitors of caspases 3 and 7. J Med Chem. 2001;44(12):2015-2026. (Pubitemid 32884524)
35. Scott FL, Denault JB, Riedl SJ, Shin H, Renatus M, Salvesen GS. XIAP inhibits caspase-3 and -7 using two binding sites: evolutionarily conserved mechanism of IAPs. EMBO J. 2005;24(3):645-655. (Pubitemid 40343265)
36. Lee SJ, et al. Metronomic activity of CD44-targeted hyaluronic acid-paclitaxel in ovarian carcinoma. Clin Cancer Res. 2012;18(15):4114-4121.
37. Tabchy A, et al. Evaluation of a 30-gene paclitaxel, fluorouracil, doxorubicin, and cyclophosphamide chemotherapy response predictor in a multicenter randomized trial in breast cancer. Clin Cancer Res. 2010;16(21):5351-5361.
38. Tsang WP, Kwok TT. Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis. 2008;13(10):1215-1222.
39. Yang X, et al. Granzyme B mimics apical caspases. Description of a unified pathway for trans-activation of executioner caspase-3 and -7. J Biol Chem. 1998;273(51):34278-34283. (Pubitemid 29008904)
40. Ross-Innes CS, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. 2012;481(7381):389- 393.
41. Friedrich K, et al. Overexpression of caspase-3 restores sensitivity for drug-induced apoptosis in breast cancer cell lines with acquired drug resistance. Oncogene. 2001;20(22):2749-2760. (Pubitemid 32549832)
42. Denault JB, Salvesen GS. Human caspase-7 activity and regulation by its N-terminal peptide. J Biol Chem. 2003;278(36):34042-34050. (Pubitemid 37553241)
43. Wu TY, Wagner KW, Bursulaya B, Schultz PG, Deveraux QL. Development and characterization of nonpeptidic small molecule inhibitors of the XIAP/caspase-3 interaction. Chem Biol. 2003;10(8):759-767. (Pubitemid 37089851)
44. Oost TK, et al. Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer. J Med Chem. 2004;47(18):4417-4426. (Pubitemid 39096830)
45. Schimmer AD, Dalili S, Batey RA, Riedl SJ. Targeting XIAP for the treatment of malignancy. Cell Death Differ. 2006;13(2):179-188. (Pubitemid 43102202)
46. Gao Z, et al. A dimeric Smac/diablo peptide directly relieves caspase-3 inhibition by XIAP. Dynamic and cooperative regulation of XIAP by Smac/Diablo. J Biol Chem. 2007;282(42):30718-30727. (Pubitemid 350035215)
47. Lu J, et al. 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. 2008;68(22):9384-9393.
48. Dineen SP, et al. Smac mimetic increases chemotherapy response and improves survival in mice with pancreatic cancer. Cancer Res. 2010;70(7):2852-2861.
49. Schimmer AD, et al. Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell. 2004;5(1):25-35. (Pubitemid 38121594)
50. Balko JM, et al. Profiling of residual breast cancers after neoadjuvant chemotherapy identifies DUSP4 deficiency as a mechanism of drug resistance. Nat Med. 2012;18(7):1052-1059.
51. Ikeda H, et al. Combination treatment with fulvestrant and various cytotoxic agents (doxorubicin, paclitaxel, docetaxel, vinorelbine, and 5-fluorouracil) has a synergistic effect in estrogen receptor-positive breast cancer. Cancer Sci. 2011;102(11):2038-2042.
52. Jost PJ, et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature. 2009;460(7258):1035-1039.
53. Wang HM, et al. Parallel gene cloning and protein production in multiple expression systems. Biotechnol Prog. 2009;25(6):1582-1586.
54. Stennicke HR, Salvesen GS. Caspases: preparation and characterization. Methods. 1999;17(4):313-319. (Pubitemid 29440606)
55. Yang JM, Chen CC. GEMDOCK: a generic evolutionary method for molecular docking. Proteins. 2004;55(2):288-304.