Synthetic siRNA targeting the breakpoint of EWS/Fli-1 inhibits growth of Ewing sarcoma xenografts in a mouse model

International Journal of Cancer

Volumn 128, Issue 1, 2011, Pages 216-226

  Takigami, Iori ^a   Ohno, Takatoshi ^a   Kitade, Yukio ^a   Hara, Akira ^a   Nagano, Akihito ^a   Kawai, Gou ^a   Saitou, Mitsuru ^a   Matsuhashi, Aya ^a   Yamada, Kazunari ^a   Shimizu, Katsuji ^a  

^a GIFU UNIVERSITY   (Japan)

Author keywords

Aromatic compound; Atelocollagen; Sarcoma; SiRNA; Xenograft

Indexed keywords

AROMATIC COMPOUND; ATELOCOLLAGEN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FLI 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EWING SARCOMA; GENE EXPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO CULTURE; MALE; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; RNA INTERFERENCE; RNA PROCESSING; SARCOMA CELL; TUMOR CELL; TUMOR GROWTH; TUMOR XENOGRAFT;

ANIMALS; APOPTOSIS; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMOSOME BREAKPOINTS; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MOLECULAR STRUCTURE; ONCOGENE PROTEINS, FUSION; PROTO-ONCOGENE PROTEIN C-FLI-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; SARCOMA, EWING'S; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 78349258515     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25564     Document Type: Article

References (47)

1. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Kovar H, Joubert I, de Jong P, Rouleau G, et al. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 1992; 359: 162 5.
2. May WA, Gishizky ML, Lessnick SL, Lunsford LB, Lewis BC, Delattre O, Zucman J, Thomas G, Denny CT,. Ewing sarcoma 11;22 translocation produces a chimeric transcription factor that requires the DNA-binding domain encoded by FLI1 for transformation. Proc Natl Acad Sci U S A 1993; 90: 5752 6.
3. Zucman J, Melot T, Desmaze C, Ghysdael J, Plougastel B, Peter M, Zucker JM, Triche TJ, Sheer D, Turc-Carel C, et al. Combinatorial generation of variable fusion proteins in the Ewing family of tumours. EMBO J 1993; 12: 4481 7.
4. Ohno T, Rao VN, Reddy ES,. EWS/Fli-1 chimeric protein is a transcriptional activator. Cancer Res 1993; 53: 5859 63.
5. Ohno T, Ouchida M, Lee L, Gatalica Z, Rao VN, Reddy ES,. The EWS gene, involved in Ewing family of tumors, malignant melanoma of soft parts and desmoplastic small round cell tumors, codes for an RNA binding protein with novel regulatory domains. Oncogene 1994; 9: 3087 97.
6. Rao VN, Ohno T, Prasad DD, Bhattacharya G, Reddy ES,. Analysis of the DNA-binding and transcriptional activation functions of human Fli-1 protein. Oncogene 1993; 8: 2167 73.
7. Yamamoto T, Ohno T, Wakahara K, Nagano A, Kawai G, Saitou M, Takigami I, Matsuhashi A, Yamada K, Shimizu K,. Simultaneous inhibition of mitogen-activated protein kinase and phosphatidylinositol 3-kinase pathways augment the sensitivity to actinomycin D in Ewing sarcoma. J Cancer Res Clin Oncol 2009; 135: 1125 36.
8. Ouchida M, Ohno T, Fujimura Y, Rao VN, Reddy ES,. Loss of tumorigenicity of Ewing's sarcoma cells expressing antisense RNA to EWS-fusion transcripts. Oncogene 1995; 11: 1049 54.
9. Dohjima T, Ohno T, Banno Y, Nozawa Y, Wen-yi Y, Shimizu K,. Preferential down-regulation of phospholipase C-beta in Ewing's sarcoma cells transfected with antisense EWS-Fli-1. Br J Cancer 2000; 82: 16 9.
10. Dohjima T, Lee NS, Li H, Ohno T, Rossi JJ,. Small interfering RNAs expressed from a Pol III promoter suppress the EWS/Fli-1 transcript in an Ewing sarcoma cell line. Mol Ther 2003; 7: 811 6.
11. Takahashi A, Higashino F, Aoyagi M, Yoshida K, Itoh M, Kyo S, Ohno T, Taira T, Ariga H, Nakajima K, Hatta M, Kobayashi M, et al. EWS/ETS fusions activate telomerase in Ewing's tumors. Cancer Res 2003; 63: 8338 44.
12. Nozawa S, Ohno T, Banno Y, Dohjima T, Wakahara K, Fan DG, Shimizu K,. Inhibition of platelet-derived growth factor-induced cell growth signaling by a short interfering RNA for EWS-Fli1 via down-regulation of phospholipase D2 in Ewing sarcoma cells. J Biol Chem 2005; 280: 27544 51.
13. Wakahara K, Ohno T, Kimura M, Masuda T, Nozawa S, Dohjima T, Yamamoto T, Nagano A, Kawai G, Matsuhashi A, Saitoh M, Takigami I, et al. EWS-Fli1 up-regulates expression of the Aurora A and Aurora B kinases. Mol Cancer Res 2008; 6: 1937 45.
14. Nagano A, Ohno T, Shimizu K, Hara A, Yamamoto T, Kawai G, Saitou M, Takigami I, Matsuhashi A, Yamada K, Takei Y,. EWS/Fli-1 chimeric fusion gene upregulates vascular endothelial growth factor-A. Int J Cancer 2010; 126: 2790 8.
15. Elbashir SM, Lendeckel W, Tuschl T,. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 2001; 15: 188 200.
16. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T,. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001; 411: 494 8.
17. Ueno Y, Inoue T, Yoshida M, Yoshikawa K, Shibata A, Kitamura Y, Kitade Y,. Synthesis of nuclease-resistant siRNAs possessing benzene-phosphate backbones in their 3′-overhang regions. Bioorg Med Chem Lett 2008; 18: 5194 6.
18. Ueno Y, Watanabe Y, Shibata A, Yoshikawa K, Takano T, Kohara M, Kitade Y,. Synthesis of nuclease-resistant siRNAs possessing universal overhangs. Bioorg Med Chem 2009; 17: 1974 81.
19. Bailly RA, Bosselut R, Zucman J, Cormier F, Delattre O, Roussel M, Thomas G, Ghysdael J,. DNA-binding and transcriptional activation properties of the EWS-FLI-1 fusion protein resulting from the t(11;22) translocation in Ewing sarcoma. Mol Cell Biol 1994; 14: 3230 41.
20. Boulares AH, Yakovlev AG, Ivanova V, Stoica BA, Wang G, Iyer S, Smulson M,. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 1999; 274: 22932 40.
21. Simbulan-Rosenthal CM, Rosenthal DS, Iyer S, Boulares AH, Smulson ME,. Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. J Biol Chem 1998; 273: 13703 12.
22. Kontny U,. Regulation of apoptosis and proliferation in Ewing's sarcoma opportunities for targeted therapy. Hematol Oncol 2006; 24: 14 21.
23. Rodriguez-Galindo C, Spunt SL, Pappo AS,. Treatment of Ewing sarcoma family of tumors: current status and outlook for the future. Med Pediatr Oncol 2003; 40: 276 87.
24. Matsumoto Y, Tanaka K, Nakatani F, Matsunobu T, Matsuda S, Iwamoto Y,. Downregulation and forced expression of EWS-Fli1 fusion gene results in changes in the expression of G(1)regulatory genes. Br J Cancer 2001; 84: 768 75.
25. Mateo-Lozano S, Gokhale PC, Soldatenkov VA, Dritschilo A, Tirado OM, Notario V,. Combined transcriptional and translational targeting of EWS/FLI-1 in Ewing's sarcoma. Clin Cancer Res 2006; 12: 6781 90.
26. Lambert G, Bertrand JR, Fattal E, Subra F, Pinto-Alphandary H, Malvy C, Auclair C, Couvreur P,. EWS fli-1 antisense nanocapsules inhibits ewing sarcoma-related tumor in mice. Biochem Biophys Res Commun 2000; 279: 401 6.
27. Toub N, Bertrand JR, Tamaddon A, Elhamess H, Hillaireau H, Maksimenko A, Maccario J, Malvy C, Fattal E, Couvreur P,. Efficacy of siRNA nanocapsules targeted against the EWS-Fli1 oncogene in Ewing sarcoma. Pharm Res 2006; 23: 892 900.
28. Matsunobu T, Tanaka K, Nakamura T, Nakatani F, Sakimura R, Hanada M, Li X, Okada T, Oda Y, Tsuneyoshi M, Iwamoto Y,. The possible role of EWS-Fli1 in evasion of senescence in Ewing family tumors. Cancer Res 2006; 66: 803 11.
29. Chansky HA, Barahmand-Pour F, Mei Q, Kahn-Farooqi W, Zielinska- Kwiatkowska A, Blackburn M, Chansky K, Conrad EU, 3rd, Bruckner JD, Greenlee TK, Yang L,. Targeting of EWS/FLI-1 by RNA interference attenuates the tumor phenotype of Ewing's sarcoma cells in vitro. J Orthop Res 2004; 22: 910 7.
30. Braasch DA, Jensen S, Liu Y, Kaur K, Arar K, White MA, Corey DR,. RNA interference in mammalian cells by chemically-modified RNA. Biochemistry 2003; 42: 7967 75.
31. Czauderna F, Fechtner M, Dames S, Aygun H, Klippel A, Pronk GJ, Giese K, Kaufmann J,. Structural variations and stabilising modifications of synthetic siRNAs in mammalian cells. Nucleic Acids Res 2003; 31: 2705 16.
32. Amarzguioui M, Holen T, Babaie E, Prydz H,. Tolerance for mutations and chemical modifications in a siRNA. Nucleic Acids Res 2003; 31: 589 95.
33. Elmen J, Thonberg H, Ljungberg K, Frieden M, Westergaard M, Xu Y, Wahren B, Liang Z, Orum H, Koch T, Wahlestedt C,. Locked nucleic acid (LNA) mediated improvements in siRNA stability and functionality. Nucleic Acids Res 2005; 33: 439 47.
34. Minakuchi Y, Takeshita F, Kosaka N, Sasaki H, Yamamoto Y, Kouno M, Honma K, Nagahara S, Hanai K, Sano A, Kato T, Terada M, et al. Atelocollagen-mediated synthetic small interfering RNA delivery for effective gene silencing in vitro and in vivo. Nucleic Acids Res 2004; 32: e109.
35. Takei Y, Kadomatsu K, Yuzawa Y, Matsuo S, Muramatsu T,. A small interfering RNA targeting vascular endothelial growth factor as cancer therapeutics. Cancer Res 2004; 64: 3365 70.
36. Takei Y, Kadomatsu K, Goto T, Muramatsu T,. Combinational antitumor effect of siRNA against midkine and paclitaxel on growth of human prostate cancer xenografts. Cancer 2006; 107: 864 73.
37. Ochiya T, Nagahara S, Sano A, Itoh H, Terada M,. Biomaterials for gene delivery: atelocollagen-mediated controlled release of molecular medicines. Curr Gene Ther 2001; 1: 31 52.
38. Ochiya T, Takahama Y, Nagahara S, Sumita Y, Hisada A, Itoh H, Nagai Y, Terada M,. New delivery system for plasmid DNA in vivo using atelocollagen as a carrier material: the Minipellet. Nat Med 1999; 5: 707 10.
39. Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ,. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 2001; 293: 1146 50.
40. Martinez J, Patkaniowska A, Urlaub H, Luhrmann R, Tuschl T,. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 2002; 110: 563 74.
41. Lingel A, Simon B, Izaurralde E, Sattler M,. Structure and nucleic-acid binding of the Drosophila argonaute 2 PAZ domain. Nature 2003; 426: 465 9.
42. Yan KS, Yan S, Farooq A, Han A, Zeng L, Zhou MM,. Structure and conserved RNA binding of the PAZ domain. Nature 2003; 426: 468 74.
43. Ma JB, Ye K, Patel DJ,. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 2004; 429: 318 22.
44. Pelengaris S, Khan M, Evan G,. c-MYC: more than just a matter of life and death. Nat Rev Cancer 2002; 2: 764 76.
45. Wang YH, Liu S, Zhang G, Zhou CQ, Zhu HX, Zhou XB, Quan LP, Bai JF, Xu NZ,. Knockdown of c-Myc expression by RNAi inhibits MCF-7 breast tumor cells growth in vitro and in vivo. Breast Cancer Res 2005; 7: R220 8.
46. Zhang X, Ge YL, Tian RH,. The knockdown of c-myc expression by RNAi inhibits cell proliferation in human colon cancer HT-29 cells in vitro and in vivo. Cell Mol Biol Lett 2009; 14: 305 18.
47. Dauphinot L, De Oliveira C, Melot T, Sevenet N, Thomas V, Weissman BE, Delattre O,. Analysis of the expression of cell cycle regulators in Ewing cell lines: EWS-FLI-1 modulates p57KIP2and c-Myc expression. Oncogene 2001; 20: 3258 65.