YM155 sensitizes triple-negative breast cancer to membrane-bound TRAIL through p38 MAPK- and CHOP-mediated DR5 upregulation

International Journal of Cancer

Volumn 136, Issue 2, 2015, Pages 299-309

  Pennati, Marzia ^a   Sbarra, Stefania ^a   De Cesare, Michelandrea ^a   Lopergolo, Alessia ^a   Locatelli, Silvia L ^b   Campi, Elisa ^a   Daidone, Maria Grazia ^a   Carlo Stella, Carmelo ^b   Gianni, Alessandro M ^a   Zaffaroni, Nadia ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

death receptors; survivin; TRAIL; triple negative breast cancer; YM155

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN HOMOLOGOUS PROTEIN; DEATH RECEPTOR 5; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P53; SEPANTRONIUM BROMIDE; SURVIVIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; BIRC5 PROTEIN, HUMAN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; IMIDAZOLE DERIVATIVE; INHIBITOR OF APOPTOSIS PROTEIN; NAPHTHOQUINONE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER CELL LINE; CANCER INHIBITION; CD34 SELECTION; CHEMOSENSITIZATION; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; FEMALE; GENE EXPRESSION REGULATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVIN GENE; TRAIL GENE; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MEMBRANE; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; FLOW CYTOMETRY; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL MEMBRANE; CELL PROLIFERATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMIDAZOLES; INHIBITOR OF APOPTOSIS PROTEINS; MICE; MICE, INBRED NOD; MICE, SCID; NAPHTHOQUINONES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSCRIPTION FACTOR CHOP; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84922323069     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28993     Document Type: Article

References (50)

1. Griffiths CL, Olin JL,. Triple negative breast cancer: a brief review of its characteristics and treatment options. J Pharm Pract 2012; 25: 319-23.
2. Elsawaf Z, Sinn HP, Rom J, et al., Biological subtypes of triple-negative breast cancer are associated with distinct morphological changes and clinical behaviour. Breast 2013; 22: 986-92.
3. Salami S, Ramezani F, Aghazadeh T, et al., Impact of triple negative phenotype on prognosis and early onset of breast cancer in Iranian females. Asian Pac J Cancer Prev 2011; 12: 719-24.
4. Steponaviciene L, Lachej-Mikeroviene N, Smailyte G, et al., Triple negative breast cancer: adjuvant chemotherapy effect on survival. Adv Med Sci 2011; 56: 285-90.
5. Crown J, O'Shaughnessy J, Gullo G,. Emerging targeted therapies in triple-negative breast cancer. Ann Oncol 2012; 23 (Suppl 6): vi56-vi65.
6. Hellwig CT, Rehm M,. TRAIL signaling and synergy mechanisms used in TRAIL-based combination therapies. Mol Cancer Ther 2012; 11: 3-13.
7. Altieri DC,. Targeting survivin in cancer. Cancer Lett 2013; 332: 225-28.
8. Carlo-Stella C, Lavazza C, Carbone A, et al., Anticancer cell therapy with TRAIL-armed CD34+ progenitor cells. Adv Exp Med Biol 2008; 610: 100-11.
9. Carlo-Stella C, Lavazza C, Di Nicola M, et al., Antitumor activity of human CD34+ cells expressing membrane-bound tumor necrosis factor-related apoptosis-inducing ligand. Hum Gene Ther 2006; 17: 1225-40.
10. Lavazza C, Carlo-Stella C, Giacomini A, et al., Human CD34+ cells engineered to express membrane-bound tumor necrosis factor-related apoptosis-inducing ligand target both tumor cells and tumor vasculature. Blood 2010; 115: 2231-40.
11. Lee CW, Raskett CM, Prudovsky I, et al., Molecular dependence of estrogen receptor-negative breast cancer on a notch-survivin signaling axis. Cancer Res 2008; 68: 5273-81.
12. Nakahara T, Kita A, Yamanaka K, et al., Broad spectrum and potent antitumor activities of YM155, a novel small-molecule survivin suppressant, in a wide variety of human cancer cell lines and xenograft models. Cancer Sci 2011; 102: 614-21.
13. Aoyama Y, Nishimura T, Sawamoto T, et al., Pharmacokinetics of sepantronium bromide (YM155), a small-molecule suppressor of survivin, in Japanese patients with advanced solid tumors: dose proportionality and influence of renal impairment. Cancer Chemother Pharmacol 2012; 70: 373-80.
14. Cheson BD, Bartlett NL, Vose JM, et al., A phase II study of the survivin suppressant YM155 in patients with refractory diffuse large B-cell lymphoma. Cancer 2012; 118: 3128-34.
15. Kelly RJ, Thomas A, Rajan A, et al., A phase I/II study of sepantronium bromide (YM155, survivin suppressor) with paclitaxel and carboplatin in patients with advanced non-small-cell lung cancer. Ann Oncol 2013; 24: 2601-6.
16. Kim EH, Kim HS, Kim SU, et al., Sodium butyrate sensitizes human glioma cells to TRAIL-mediated apoptosis through inhibition of Cdc2 and the subsequent downregulation of survivin and XIAP. Oncogene 2005; 24: 6877-89.
17. Chen W, Wang X, Zhuang J, et al., Induction of death receptor 5 and suppression of survivin contribute to sensitization of TRAIL-induced cytotoxicity by quercetin in non-small cell lung cancer cells. Carcinogenesis 2007; 28: 2114-21.
18. Zhang HY, Du ZX, Liu BQ, et al., Tunicamycin enhances TRAIL-induced apoptosis by inhibition of cyclin D1 and the subsequent downregulation of survivin. Exp Mol Med 2009; 41: 362-9.
19. Kim JY, Kim EH, Kim SU, et al., Capsaicin sensitizes malignant glioma cells to TRAIL-mediated apoptosis via DR5 upregulation and survivin downregulation. Carcinogenesis 2010; 31: 367-75.
20. Raviv Z, Zilberberg A, Cohen S, et al., Methyl jasmonate down-regulates survivin expression and sensitizes colon carcinoma cells towards TRAIL-induced cytotoxicity. Br J Pharmacol 2011; 164: 1433-44.
21. Kim YS, Jin HO, Seo SK, et al., Sorafenib induces apoptotic cell death in human non-small cell lung cancer cells by down-regulating mammalian target of rapamycin (mTOR)-dependent survivin expression. Biochem Pharmacol 2011; 82: 216-26.
22. Charette N, De Saeger C, Horsmans Y, et al., Salirasib sensitizes hepatocarcinoma cells to TRAIL-induced apoptosis through DR5 and survivin-dependent mechanisms. Cell Death Dis 2013; 4: e471.
23. Chawla-Sarkar M, Bae SI, Reu FJ, et al., Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 2004; 11: 915-23.
24. Naundorf H, Rewasowa EC, Fichtner I, et al., Characterization of two human mammary carcinomas, MT-1 and MT-3, suitable for in vivo testing of ether lipids and their derivatives. Breast Cancer Res Treat 1992; 23: 87-95.
25. Rossini A, Giussani M, Giacomini A, et al., Surveillance of spontaneous breast cancer metastasis by TRAIL-expressing CD34+ cells in a xenograft model. Breast Cancer Res Treat 2012; 136: 457-67.
26. Paduano F, Villa R, Pennati M, et al., Silencing of survivin gene by small interfering RNAs produces supra-additive growth suppression in combination with 17-allylamino-17-demethoxygeldanamycin in human prostate cancer cells. Mol Cancer Ther 2006; 5: 179-86.
27. Kern DH, Morgan CR, Hildebrand-Zanki SU,. In vitro pharmacodynamics of 1-β-d-arabinofuranosylcytosine: synergy of antitumor activity with cis-diamminedichloroplatinum (II). Cancer Res 1988; 48: 117-21.
28. Nakahara T, Kita A, Yamanaka K, et al., YM155, a novel small-molecule survivin suppressant, induces regression of established human hormone-refractory prostate tumor xenografts. Cancer Res 2007; 67: 8014-21.
29. Mühlenbeck F, Schneider P, Bodmer JL, et al., The tumor necrosis factor-related apoptosis-inducing ligand receptors TRAIL-R1 and TRAIL-R2 have distinct cross-linking requirements for initiation of apoptosis and are non-redundant in JNK activation. J Biol Chem 2000; 275: 32208-13.
30. Matsui TA, Sowa Y, Yoshida T, et al., Sulforaphane enhances TRAIL-induced apoptosis through the induction of DR5 expression in human osteosarcoma cells. Carcinogenesis 2006; 27: 1768-77.
31. Kouhara J, Yoshida T, Nakata S, et al., Fenretinide up-regulates DR5/TRAIL-R2 expression via the induction of the transcription factor CHOP and combined treatment with fenretinide and TRAIL induces synergistic apoptosis in colon cancer cell lines. Int J Oncol 2007; 30: 679-87.
32. Sung B, Ravindran J, Prasad S, et al., Gossypol induces death receptor-5 through activation of the ROS-ERK-CHOP pathway and sensitizes colon cancer cells to TRAIL. J Biol Chem 2010; 285: 35418-27.
33. Gupta SC, Reuter S, Phromnoi K, et al., Nimbolide sensitizes human colon cancer cells to TRAIL through reactive oxygen species- and ERK-dependent up-regulation of death receptors, p53, and Bax. J Biol Chem 2011; 286: 1134-46.
34. Inoue H, Waiwut P, Saiki I, et al., Gomisin N enhances TRAIL-induced apoptosis via reactive oxygen species-mediated up-regulation of death receptors 4 and 5. Int J Oncol 2012; 40: 1058-65.
35. Kim EY, Ryu JH, Kim AK,. CAPE promotes TRAIL-induced apoptosis through the upregulation of TRAIL receptors via activation of p38 and suppression of JNK in SK-Hep1 hepatocellular carcinoma cells. Int J Oncol 2013; 43: 1291-300.
36. Park EJ, Choi KS, Yoo YH, et al., Nutlin-3, a small-molecule MDM2 inhibitor, sensitizes Caki cells to TRAIL-induced apoptosis through p53-mediated PUMA upregulation and ROS-mediated DR5 upregulation. Anticancer Drugs 2013; 24: 260-9.
37. Woo JS, Kim SM, Jeong CH, et al., Lipoxygenase inhibitor MK886 potentiates TRAIL-induced apoptosis through CHOP- and p38 MAPK-mediated up-regulation of death receptor 5 in malignant glioma. Biochem Biophys Res Commun 2013; 431: 354-9.
38. Yoon MJ, Kang YJ, Kim IY, et al., Monensin, a polyether ionophore antibiotic, overcomes TRAIL resistance in glioma cells via endoplasmic reticulum stress, DR5 upregulation and c-FLIP downregulation. Carcinogenesis 2013; 34: 1918-28.
39. Wu GS, Burns TF, McDonald ER, III, et al., KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet 1997; 17: 141-3.
40. Barancík M, Bohácová V, Kvackajová J, et al., SB203580, a specific inhibitor of p38-MAPK pathway, is a new reversal agent of P-glycoprotein mediated multidrug resistance. Eur J Pharm Sci 2001; 14: 29-36.
41. Yamanaka K, Nakata M, Kaneko N, et al., YM155, a selective survivin suppressant, inhibits tumor spread and prolongs survival in a spontaneous metastatic model of human triple negative breast cancer. Int J Oncol 2011; 39: 569-75.
42. Jin Z, McDonald ER, III, Dicker DT, et al., Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 2004; 279: 35829-39.
43. Chen JJ1, Shen HC, Rivera Rosado LA, et al., Mislocalization of death receptors correlates with cellular resistance to their cognate ligands in human breast cancer cells. Oncotarget 2012; 3: 833-42.
44. Austin CD, Lawrence DA, Peden AA, et al., Death-receptor activation halts clathrin-dependent endocytosis. Proc Natl Acad Sci USA 2006; 103: 10283-8.
45. Zhang Y, Zhang B,. TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol Cancer Res 2008; 6: 1861-71.
46. Lim SC, Duong HQ, Choi JE, et al., Lipid raft-dependent death receptor 5 (DR5) expression and activation are critical for ursodeoxycholic acid-induced apoptosis in gastric cancer cells. Carcinogenesis 2011; 32: 723-31.
47. Yamaguchi H, Wang HG,. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem 2004; 279: 45495-502.
48. Kim YH, Park JW, Lee JY, et al., Sodium butyrate sensitizes TRAIL-mediated apoptosis by induction of transcription from the DR5 gene promoter through Sp1 sites in colon cancer cells. Carcinogenesis 2004; 25: 1813-20.
49. Shetty S1, Graham BA, Brown JG, et al., Transcription factor NF-kappaB differentially regulates death receptor 5 expression involving histone deacetylase 1. Mol Cell Biol 2005; 25: 5404-16.
50. Mahajan S1, Dammai V, Hsu T, et al., Hypoxia-inducible factor-2alpha regulates the expression of TRAIL receptor DR5 in renal cancer cells. Carcinogenesis 2008; 29: 1734-41.