Salinomycin potentiates the cytotoxic effects of TRAIL on glioblastoma cell lines

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Calzolari, Alessia ^a   Saulle, Ernestina ^a   De Angelis, Maria Laura ^a   Pasquini, Luca ^a   Boe, Alessandra ^a   Pelacchi, Federica ^a   Ricci Vitiani, Lucia ^a   Baiocchi, Marta ^a   Testa, Ugo ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DEATH RECEPTOR 4; DEATH RECEPTOR 5; RH SUPERKILLER TRAIL; SALINOMYCIN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; CYTOTOXIN; PYRAN DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL GROWTH; CELL MEMBRANE DEPOLARIZATION; CELL SURFACE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG POTENTIATION; ENZYME ACTIVATION; FEMALE; GLIOBLASTOMA; GROWTH INHIBITION; HUMAN; HUMAN CELL; LOW DRUG DOSE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR GROWTH; UPREGULATION; ANIMAL; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; NUDE MOUSE; TUMOR CELL LINE;

ANIMALS; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOTOXINS; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GLIOBLASTOMA; HUMANS; MICE, NUDE; PYRANS; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84899743360     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094438     Document Type: Article

References (46)

1. Stupp R, Hegi ME, vandenBent MJ, Mason WP, Weller M, et al. (2006) Changing paradigms - un update on multidisciplinary management of malignant glioma. Oncologist 11: 165-180. (Pubitemid 43261763)
2. Kuijlen JMA, Bremert E, Mooij JJA, den Dunnen WFA, Helfrich W (2010) Review: on TRAIL for malignant glioma therapy?. Neuropathol App Neurobiol 36: 168-182.
3. Roth W, Isenmann S, Naumann U, Kü gler S, Bähr M, et al. (1999) Locoregional Apo2L/TRAIL eradicates intracranial human malignant glioma xenografts in athymic mice in the absence of neurotoxicity. Biophys Res Commun 265: 479-483.
4. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, et al. (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163. (Pubitemid 29068521)
5. Yamamoto K, Makino M, Watanapokasin R, Tashiro E, Imoto M (2012) Inostamycin enhanced TRAIL-induced apoptosis through DR5 upregulation on the cell surface. J Antibiot, in press.
6. Miyazaki Y, Shibuya M, Sugawara H, Kawaguchi O, Hirsoe C (1974) Salinomycin, a new polyether antibiotic. J Antibiot 27: 814-821.
7. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, et al. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
8. Huczynski A (2012) Salinomycin: A new cancer drug candidate. Chem Biol Drug Des, in press.
9. Bardsley MR, Horvath VJ, Asuzu D, Lorincz A, Redelman D, et al. (2010) Kitlow stem cells cause resistance to Kit/Platelet-derived growth factor alpha inhibitors in murine gastrointestinal stromal tumors. Gastroenterology 139: 942- 952.
10. Wang Y (2011) Effects of salinomycin on cancer stem cell in human lung adenocarcinoma. Med Chem 7: 106-111.
11. Basu D, Montone KT, Wang LP, Gimotty PA, Hammond R, et al. (2011) Detecting and targeting mesenchymal-like subpopulations within squamous cell carcinomas. Cell Cycle 10: 2008-2016.
12. Fuchs D, Heinold A, Opelz G, Daniel V, Naujokat C (2009) Salinomycin induces apoptosis and overcomes apoptosis resistance in human cancer cells. Biochem Biophys Res Commun 390: 743-749.
13. Riccioni R, Dupuis ML, Bernabei M, Petrucci E, Pasquini L, et al. (2010) The cancer stem cell selective inhibitor salinomycin is a p-glycoprotein inhibitor. Blood Cells Mol Dis 45: 86-92.
14. Fuchs D, Daniel V, Sadeghi M, Opelz G, Naujokat C (2010) Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun 394: 1098-1104.
15. Kim JH, Chae M, Kim WK, Kang HS, Kim HS, et al. (2011) Salinomycin sensitizes cancer cells to the effects of doxorubicin and etoposide treatment by increasing DNA damage and reducing p21 protein. Brit J Parmacol 162: 773- 784.
16. Lu D, Choi MY, Castro JE, Kipps TJ, Carson DA (2011) Salinomycin inhibits Wnt signalling and selectively induces apoptosis in chronic lymphocytic leukemia cells. Proc Natl Acad Sci USA 108: 13253-13257.
17. Tang QL, Zhao ZQ, Li JC, Liang Y, Yin JQ, et al. (2011) Salinomycin inhibits osteosarcoma by targeting its tumor stem cells. Cancer Lett 311: 113-121.
18. Delwar ZM, Avramidis D, Siden A, Cruz M, Yakisich S (2011) Depletion of drug-surviving glioma cells by a second phase treatment with low concentration of salinomycin. Drug Therapy Studies 10: 40-45.
19. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, et al. (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182: 367- 377.
20. Yan K, Yang K, Rich JN (2013) The evolving landscape of glioblastoma stem cells. Curr Opin Neurol 26: 701-707.
21. Pallini R, Ricci-Vitiani L, Banna GL, Signore M, Lombardi D, et al. (2008) Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Cancer Res 14: 8205-8212.
22. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, et al. (2010) Tumor vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 468: 824-828.
23. Ashley DM, Riffkin CD, Lovric MM, Mikeska T, Dobrovic A, et al. (2008) In vitro sensitivity testing of minimally passaged and uncultured gliomas with TRAIL and/or chemotherapy drugs. Br J Cancer 99: 294-304.
24. Panner A, Crane CA, Weng C, Feletti A, Parsa AT, et al. (2009) A novel PTENdependent link to ubiquitination controls FLIPs stability and TRAIL sensitivity in glioblastoma multiforme. Cancer Res 69: 7911-7916.
25. Qi L, Bellail AC, Rossi MR, Zhang Z, Pang H, et al. (2011) Heterogeneity of primary glioblastoma cells in the expression of caspase-8 and the response to TRAIL-induced apoptosis. Apoptosis 16: 1150-1164.
26. Verbrugge I, Johnstone RW (2012) Regulating the TRAIL of destruction: how A20 protects glioblastomas from TRAIL-mediated death. Cancer Discover 2: 112-114.
27. Quintavalle C, Donnarumma E, Iaboni M, Roscigno G, Garofalo M, et al. (2013) Effect of miR-21 and miR-30 b/c on TRAIL-induced apoptosis in glioma cells. Oncogene 32: 4001-4008.
28. Murphy AC, Weyhenmeyer B, Noonan J, Kilbride SM, Shimansky S, et al. (2013) Modulation of Mcl-1 sensitizes glioblastoma to TRAIL-induced apoptosis. Apoptosis 2013; In press.
29. Bellail AC, Tse MC, Song JH, Phuphanich S, Olson JJ, et al. (2010) DR5- mediated DISC controls caspase-8 cleavage and initiation of apoptosis in human glioblastomas. J Cell Mol Med 14: 1303-1317.
30. Ding L, Yuan C, Wei F, Wang G, Zhang J, et al. (2011) Cisplatin restores TRAIL apoptotic pathway in glioblastoma-derived stem cells through upregulation of DR5 and down-regulation of c-FLIP. Cancer Invest 29:511-520.
31. Badr CE, Wurdinger T, Nilsson J, Niers TM, Whalen M, et al. (2011) Lanatoside C sensitizes glioblastoma cells to tumor necrosis factor-related apoptosis-inducing ligand and induces an alternative cell death pathway. Neur Oncol 13: 1213-1224.
32. Tian X, Ye J, Alonso-Basanta M, Hahn SM, Koumenis C, et al. (2011) Modulation of CCAAT/enhancer binding protein homologous protein (CHOP)-dependent DR5 expression by nelfinavir sensitizes glioblastoma multiforme cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J Biol Chem 286: 29408-29416.
33. Roth P, Kissel M, Hermann C, Eisele G, Leban J, et al. (2009) SC68896, a novel small molecule proteasome inhibitor, exerts antiglioma activity in vitro and in vivo. Clin Cancer Res 2009; 15: 6609-6618.
34. Kuijlen JM, Mooij JJ, Platteel I, Hoving EW, van der Graaf WT, et al. (2006) TRAIL-receptor expression is an independent prognostic factor for survival in patients with a primary glioblastoma multiforme. J Neur Oncol 78: 161-171. (Pubitemid 44339684)
35. Joon MJ, Kang YJ, Kim IY, Kim EH, Lee JA, et al. (2013) Monensin, a polyether ionophore antibiotic overcomes TRAIL resistance in glioma cells via endoplasmic reticulum stress, DR5 upregulation and c-FLIP downregulation. Carcinogenesis; In press.
36. Parajuli B, Shin SJ, Kwan SH, Cha SD, Chung R, et al. (2013) Salinomycin induces apoptosis via death receptor-5-up-regulation in cisplatin-resistant ovarian cancer cells. Anticancer Res 2013; 33: 1457-1462.
37. AlDhaheri Y, Attoub S, Arafat K, Abuqamars S, Eid A, et al. (2013) Salinomycin induces apoptosis and senescence in breast cancer: upregulation of p21, downregulation of surviving and histone H3 and H4 hyperactivation. Biochim Biophys Acta 1830: 312-315.
38. Kao KH, Kim H, Bae YK, Kim K, Park BK, et al. (2013) Salinomycin induces cell death via inactivation of Stat3 and downregulation of Skp2. Cell Death Dis 4: e693.
39. Kim KY, Yu SN, Lee SY, Chun SS, Choi YL, et al. (2011) Salinomycin-induced apoptosis of human prostate cancer cells due to accumulated reactive oxygen species and mitochondrial depolarization. Biochem Biophys Res Commun 413: 80-86.
40. Badr CE, Wurdinger T, Nilsson J, Niers J, Whalen M, et al. (2011) Lanatoside C sensitizes glioblastoma cells to tumor necrosis factor-related apoptosis-inducing ligand and induces an alternative cell death pathway. Neuro Oncol. 13: 1213- 1224.
41. Story P, Doube A (2004) A case of human poisoning by salinomycin, an agricultural antibiotic. NZ Med J 117: U799.
42. Boehmerle W, Endres M (2011) Salinomycin induces calpain and cytochrome-c mediated neuronal cell death. Cell Death Disease 2: e168.
43. Booth L, Roberts JL, Conley A, Crickshanks N, Ridder T, et al. (2014) HDAC inhibitors enhance the lethality of low dose salinomycin in parental and stem-like GBM cells. Cancer Biol Ther. In press.
44. DeStasio G, Casalbore P, Pallini R, Gilbert B, Sanita F, et al. (2001) Gadolinium in human glioblastoma cells for gadolinium neutron capture therapy. Cancer Res 2001; 61: 4272-4277. (Pubitemid 32720999)
45. Georgakis GV, Li Y, Humphreys R, Andreef M, O'Brien S, et al. (2005) Activity of selective fully human agonistic antibodies to the TRAIL death receptors TRAIL-R1 and TRAIL-R2 in primary and cultured lymphoma cells: induction of apoptosis and enhancement of doxorubicin- And bortezomib-induced cell death. Br J Haematol 130:501-510. (Pubitemid 43899752)
46. Pukac L, Kanakaraj P, Humphreys R, Alderson R, Bloom M, et al. (2005) HGSETR1, a fully human TRAIL-receptor 1 monoclonal antibody, induces cell death in multiple tumor types in vitro and in vivo. Br J Cancer 92:1430-1441. (Pubitemid 40705010)