The sensitivity of the Ewing's sarcoma family of tumours to fenretinide-induced cell death is increased by EWS-Fli1-dependent modulation of p38MAPK activity

Oncogene

Volumn 27, Issue 7, 2008, Pages 985-996

  Myatt, S S ^a,b   Burchill, S A ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; ESFT; EWS Fli1; Fenretinide; p38MAPK; ROS

Indexed keywords

CASPASE; CYTOCHROME C; FENRETINIDE; GLYCOSYLTRANSFERASE; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; RNA BINDING PROTEIN EWS; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FLI 1;

ARTICLE; CELL DEATH; CELL LINE; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIVITY; ENZYME ACTIVITY; EWING SARCOMA; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CASPASES; CELL PROLIFERATION; CYTOCHROMES C; DOWN-REGULATION; ELECTROPORATION; FENRETINIDE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MEMBRANE POTENTIALS; MITOCHONDRIA; ONCOGENE PROTEINS, FUSION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEIN C-FLI-1; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SARCOMA, EWING'S; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 38949174605     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/sj.onc.1210705     Document Type: Article

References (41)

1. Asumendi A, Morales MC, Alvarez A, Arechaga J, Perez-Yarza G. (2002). Implication of mitochondria-derived ROS and cardiolipin peroxidation in N-(4-hydroxyphenyl)retinamide-induced apoptosis. Br J Cancer 86: 1951-1956.
2. Benhar M, Dalyot I, Engelberg D, Levitzki A. (2001). Enhanced ROS production in oncogenically transformed cells potentiatesc-Jun N-terminal kinase and p38 mitogen-activated protein kinase activation and sensitization to genotoxic stress. Mol Cell Biol 21: 6913-6926.
3. Boya P, Morales MC, Gonzalez-Polo RA, Andreau K, Gourdier I, Perfettini JL et al. (2003). The chemopreventive agent N-(4-hydroxyphenyl)retinamide induces apoptosis through a mitochondrial pathway regulated by proteins from the Bcl-2 family. Oncogene 22: 6220-6230.
4. Burchill SA, Bradbury FM, Smith B, Lewis IJ, Selby P. (1994). Neuroblastoma cell detection by reverse transcriptasepolymerase chain reaction (RT-PCR) for tyrosine hydroxylase mRNA. Int J Cancer 57: 671-675.
5. Burchill SA. (2003). Ewing's sarcoma: diagnostic, prognostic, and therapeutic implications of molecular abnormalities. J Clin Pathol 56: 96-102.
6. Castillero-Trejo Y, Eliazer S, Xiang L, Richardson JA, Ilaria Jr RL. (2005). Expression of the EWS/FLI-1 oncogene in murine primary bone-derived cellsres ultsin EWS/FLI-1-dependent, Ewing sarcoma-like tumors. Cancer Res 65: 8698-8705.
7. Chansky HA, Barahmand-Pour F, Mei Q, Kahn-Farooqi W, Zielinska- Kwiatkowska A, Blackburn M et al. (2004). Targeting of EWS/FLI-1 by RNA interference attenuates the tumor phenotype of Ewing's sarcoma cells in vitro. J Orthop Res 22: 910-917.
8. Chiesa F, Tradati N, Grigolato R, Boracchi P, Biganzoli E, Crose N et al. (2005). Randomized trial of fenretinide (4-HPR) to prevent recurrences, new localizations and carcinomas in patients operated on for oral leukoplakia: long-term results. Int J Cancer 115: 625-629.
9. Corazzari M, Lovat PE, Oliverio S, Di Sano F, Donnorso RP, Redfern CP et al. (2005). Analysis of mitochondria during cell death. Biochem Biophys Res Commun 331: 810-815.
10. Delattre O, Zucman J, Melot T, Garau XS, Zucker JM, Lenoir GM et al. (1994). The Ewing family of tumors-a subgroup of small-round-cell tumors defined by specific chimeric transcripts. N Engl J Med 331: 294-299.
11. Dohjima T, Lee NS, Li H, Ohno T, Rossi JJ. (2003). Small interfering RNAs expressed from a Pol III promoter suppress the EWS/Fli-1 transcript in a Ewing sarcoma cell line. Mol Ther 7: 811-816.
12. Formelli F, Clerici M, Campa T, Di Mauro MG, Magni A, Mascotti G et al. (1993). Synthetic retinoid fenretinide is effective against a human ovarian carcinoma xenograft and potentiates cisplatin activity. J Clin Oncol 11: 2036-2042.
13. Garaventa A, Luksch R, Lo Piccolo MS, Cavadini E, Montaldo PG, Pizzitola MR et al. (2003). Phase I trial and pharmacokinetics of fenretinide in children with neuroblastoma. Clin Cancer Res 9: 2032-2039.
14. Horbinski C, Chu CT. (2005). Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic Biol Med 38: 2-11.
15. Huang S, Shu L, Easton J, Harwood FC, Germain GS, Ichijo H et al. (2004). Inhibition of mammalian target of rapamycin activates apoptosis signal-regulating kinase 1 signaling by suppressing protein phosphatase 5 activity. J Biol Chem 279: 36490-36496.
16. Hu-Lieskovan S, Heidel JD, Bartlett DW, Davis ME, Triche TJ. (2005b). Sequence-specific knock-down of EWS-FLI1 by targeted, nonviral delivery of small interfering RNA inhibits tumor growth in a murine model of metastatic Ewing's sarcoma. Cancer Res 65: 8984-8992.
17. Hu-Lieskovan S, Zhang J, Wu L, Shimada H, Schofield DE, Triche TJ. (2005a). EWS-FLI1 fusion protein up-regulates critical genes in neural crest development and is responsible for the observed phenotype of Ewing's family of tumors. Cancer Res 65: 4633-4644.
18. Johnson GL, Lapadat R. (2002). Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298: 1911-1912.
19. Kim HJ, Chakravarti N, Oridate N, Choe C, Claret FX, Lotan R. (2006). N-(4-Hydroxyphenyl) retinamide-induced apoptosis triggered by reactive oxygen species is mediated by activation of MAPKs in head and neck squamous carcinoma cells. Oncogene 25: 2785-2794.
20. Malone W, Perloff M, Crowell J, Sigman C, Higley H. (2003). Fenretinide: a prototype cancer prevention drug. Expert Opin Investig Drugs 12: 1829-1842.
21. Matsunobu T, Tanaka K, Nakamura T, Nakatani F, Sakimura R, Hanada M et al. (2006). The possible role of EWS-Fli1 in evasion of senescence in Ewing family tumors. Cancer Res 66: 803-811.
22. May WA, Gishizky ML, Lessnick SL, Lunsford LB, Lewis BC, Delattre O et al. (1993). Ewing sarcoma 11;22 translocation produces a chimeric transcription factor that requiresthe DNA-binding domain encoded by FLI1 for transformation. Proc Natl Acad Sci USA 90: 5752-5756.
23. Mittal V. (2004). Improving the efficiency of RNA interference in mammals. Nat Rev Genet 5: 355-365.
24. Myatt SS, Redfern CP, Burchill SA. (2005). p38MAPK-Dependent sensitivity of Ewing's sarcoma family of tumors to fenretinide-induced cell death. Clin Cancer Res 11: 3136-3148.
25. O'Donnell PH, Guo WX, Reynolds CP, Maurer BJ. (2002). N-(4-hydroxyphenyl)retinamide increases ceramide and is cytotoxic to acute lymphoblastic leukemia cell lines, but not to non-malignant lymphocytes. Leukemia 16: 902-910.
26. Osone S, Hosoi H, Kuwahara Y, Matsumot Y, Lehara T, Sugimoto T. (2004). Fenretinide induces sustained-activation of JNK/p38 MAPK and apoptosis in a reactive oxygen species-dependent manner in neuroblastoma cells. Int J Cancer 112: 219-224.
27. Pienta KJ, Esper PS, Zwas F, Krzeminski R, Flaherty LE. (1997). Phase II chemoprevention trial of oral fenretinide in patients at risk for adenocarcinoma of the prostate. Am J Clin Oncol 20: 36-39.
28. Prieur A, Tirode F, Cohen P, Delattre O. (2004). EWS/FLI-1 silencing and gene profiling of Ewing cells reveal down-stream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol Cell Biol 24: 7275-7283.
29. Simeone AM, Deng CX, Kelloff GJ, Steele VE, Johnson MM, Tari AM. (2005). N-(4-Hydroxyphenyl)retinamide is more potent than other phenylretinamides in inhibiting the growth of BRCA1-mutated breast cancer cells. Carcinogenesis 26: 1000-1007.
30. Smith R, Owen LA, Trem DJ, Wong JS, Whangbo JS, Golub TR et al. (2006). Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 9: 405-416.
31. Takeda K, Matsuzawa A, Nishitoh H, Ichijo H. (2003). Roles of MAPKKK ASK1 in stress-induced cell death. Cell Struct Funct 28: 23-29.
32. Thompson AD, Teitell MA, Arvand A, Denny CT. (1999). Divergent Ewing's sarcoma EWS/ETS fusions confer a common tumorigenic phenotype on NIH3T3 cells. Oncogene 18: 5506-5513.
33. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K et al. (2001). ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2: 222-228.
34. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, Yodoi J. (2002). Redox control of cell death. Antioxid Redox Signal 4: 405-414.
35. Villablanca JG, Krailo MD, Ames MM, Reid JM, Reaman GH, Reynolds CP. (2006). Phase I trial of oral fenretinide in children with high-risk solid tumors: a report from the Children's Oncology Group (CCG 09709). J Clin Oncol 24: 3423-3430.
36. Westerhout EM, Ooms M, Vink M, Das AT, Berkhout B. (2005). HIV-1 can escape from RNA interference by evolving an alternative structure in its RNA genome. Nucleic Acids Res 33: 796-804.
37. Williamson AJ, Dibling BC, Boyne JR, Selby P, Burchill SA. (2004). Basic fibroblast growth factor-induced cell death is effected through sustained activation of p38MAPK and up-regulation of the death receptor p75NTR. J Biol Chem 279: 47912-47928.
38. Won JS, Singh I. (2006). Sphingolipid signaling and redox regulation. Free Radic Biol Med 40: 1875-1888.
39. Wu JM, DiPietrantonio AM, Hsieh TC. (2001). Mechanism of fenretinide (4-HPR)-induced cell death. Apoptosis 6: 377-388.
40. Yi H, Fujimura Y, Ouchida M, Prasad DD, Rao VN, Reddy ES. (1997). Inhibition of apoptosis by normal and aberrant Fli-1 and erg proteins involved in human solid tumors and leukemias. Oncogene 14: 1259-1268.
41. Zanardi S, Serrano D, Argusti A, Barile M, Puntoni M, Decensi A. (2006). Clinical trials with retinoids for breast cancer chemoprevention. Endocr Relat Cancer 13: 51-68.