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Article

EWS/FLI-1 Induces Rapid Onset of Myeloid/Erythroid Leukemia in Mice

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Pages 7918-7934 | Received 16 Jan 2007, Accepted 06 Sep 2007, Published online: 27 Mar 2023

REFERENCES

  • Abaan, O. D., A. Levenson, O. Khan, P. A. Furth, A. Uren, and J. A. Toretsky. 2005. PTPL1 is a direct transcriptional target of EWS-FLI1 and modulates Ewing's sarcoma tumorigenesis. Oncogene 24:2715–2722.
  • Akashi, K., D. Traver, T. Miyamoto, and I. L. Weissman. 2000. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404:193–197.
  • Anderson, M. K., G. Hernandez-Hoyos, R. A. Diamond, and E. V. Rothenberg. 1999. Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage. Development 126:3131–3148.
  • Arvand, A., and C. T. Denny. 2001. Biology of EWS/ETS fusions in Ewing's family tumors. Oncogene 20:5747–5754.
  • Asari, S., S. Okada, Y. Ohkubo, A. Sakamoto, M. Arima, M. Hatano, Y. Kuroda, and T. Tokuhisa. 2004. Beta-galactosidase of ROSA26 mice is a useful marker for detecting the definitive erythropoiesis after stem cell transplantation. Transplantation 78:516–523.
  • Bailly, R. A., R. Bosselut, J. Zucman, F. Cormier, O. Delattre, M. Roussel, G. Thomas, and J. Ghysdael. 1994. 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. 14:3230–3241.
  • Baird, K., S. Davis, C. R. Antonescu, U. L. Harper, R. L. Walker, Y. Chen, A. A. Glatfelter, P. H. Duray, and P. S. Meltzer. 2005. Gene expression profiling of human sarcomas: insights into sarcoma biology. Cancer Res. 65:9226–9235.
  • Baldus, C. D., S. Liyanarachchi, K. Mrozek, H. Auer, S. M. Tanner, M. Guimond, A. S. Ruppert, N. Mohamed, R. V. Davuluri, M. A. Caligiuri, C. D. Bloomfield, and A. de la Chapelle. 2004. Acute myeloid leukemia with complex karyotypes and abnormal chromosome 21: amplification discloses overexpression of APP, ETS2, and ERG genes. Proc. Natl. Acad. Sci. USA 101:3915–3920.
  • Ben-David, Y., E. B. Giddens, and A. Bernstein. 1990. Identification and mapping of a common proviral integration site Fli-1 in erythroleukemia cells induced by Friend murine leukemia virus. Proc. Natl. Acad. Sci. USA 87:1332–1336.
  • Bertolotti, A., Y. Lutz, D. J. Heard, P. Chambon, and L. Tora. 1996. hTAF(II)68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J. 15:5022–5031.
  • Bertolotti, A., T. Melot, J. Acker, M. Vigneron, O. Delattre, and L. Tora. 1998. EWS, but not EWS-FLI-1, is associated with both TFIID and RNA polymerase II: interactions between two members of the TET family, EWS and hTAFII68, and subunits of TFIID and RNA polymerase II complexes. Mol. Cell. Biol. 18:1489–1497.
  • Braunreiter, C. L., J. D. Hancock, C. M. Coffin, K. M. Boucher, and S. L. Lessnick. 2006. Expression of EWS-ETS fusions in NIH 3T3 cells reveals significant differences to Ewing's sarcoma. Cell Cycle 5:2753–2759.
  • Castillero-Trejo, Y., S. Eliazer, L. Xiang, J. A. Richardson, and R. L. Ilaria, Jr. 2005. Expression of the EWS/FLI-1 oncogene in murine primary bone-derived cells results in EWS/FLI-1-dependent, ewing sarcoma-like tumors. Cancer Res. 65:8698–8705.
  • Chan, I. T., J. L. Kutok, I. R. Williams, S. Cohen, L. Kelly, H. Shigematsu, L. Johnson, K. Akashi, D. A. Tuveson, T. Jacks, and D. G. Gilliland. 2004. Conditional expression of oncogenic K-ras from its endogenous promoter induces a myeloproliferative disease. J. Clin. Investig. 113:528–538.
  • Codrington, R., R. Pannell, A. Forster, L. F. Drynan, A. Daser, N. Lobato, M. Metzler, and T. H. Rabbitts. 2005. The Ews-ERG fusion protein can initiate neoplasia from lineage-committed haematopoietic cells. PLoS Biol. 3:e242.
  • Crispino, J. D. 2005. GATA1 in normal and malignant hematopoiesis. Semin. Cell Dev. Biol. 16:137–147.
  • Deneen, B., and C. T. Denny. 2001. Loss of p16 pathways stabilizes EWS/FLI1 expression and complements EWS/FLI1 mediated transformation. Oncogene 20:6731–6741.
  • Deneen, B., H. Hamidi, and C. T. Denny. 2003. Functional analysis of the EWS/ETS target gene uridine phosphorylase. Cancer Res. 63:4268–4274.
  • Deneen, B., S. M. Welford, T. Ho, F. Hernandez, I. Kurland, and C. T. Denny. 2003. PIM3 proto-oncogene kinase is a common transcriptional target of divergent EWS/ETS oncoproteins. Mol. Cell. Biol. 23:3897–3908.
  • Dominici, M., C. Pritchard, J. E. Garlits, T. J. Hofmann, D. A. Persons, and E. M. Horwitz. 2004. Hematopoietic cells and osteoblasts are derived from a common marrow progenitor after bone marrow transplantation. Proc. Natl. Acad. Sci. USA 101:11761–11766.
  • Ekert, H., E. L. Sievers, A. Tan, D. I. Martin, F. O. Smith, D. Barnard, and I. D. Bernstein. 1994. GATA-1 is expressed in acute erythroblastic leukaemia. Br. J. Haematol. 86:410–412.
  • Florin, L., H. Alter, H. J. Grone, A. Szabowski, G. Schutz, and P. Angel. 2004. Cre recombinase-mediated gene targeting of mesenchymal cells. Genesis 38:139–144.
  • Fraser, M. M., X. Zhu, C. H. Kwon, E. J. Uhlmann, D. H. Gutmann, and S. J. Baker. 2004. Pten loss causes hypertrophy and increased proliferation of astrocytes in vivo. Cancer Res. 64:7773–7779.
  • Fukuma, M., H. Okita, J. Hata, and A. Umezawa. 2003. Upregulation of Id2, an oncogenic helix-loop-helix protein, is mediated by the chimeric EWS/ets protein in Ewing sarcoma. Oncogene 22:1–9.
  • Gregory, T., C. Yu, A. Ma, S. H. Orkin, G. A. Blobel, and M. J. Weiss. 1999. GATA-1 and erythropoietin cooperate to promote erythroid cell survival by regulating bcl-xL expression. Blood 94:87–96.
  • Guerra, C., N. Mijimolle, A. Dhawahir, P. Dubus, M. Barradas, M. Serrano, V. Campuzano, and M. Barbacid. 2003. Tumor induction by an endogenous K-ras oncogene is highly dependent on cellular context. Cancer Cell 4:111–120.
  • Heilman, S. A., Y. H. Kuo, C. S. Goudswaard, P. J. Valk, and L. H. Castilla. 2006. Cbfβ reduces Cbfβ-SMMHC-associated acute myeloid leukemia in mice. Cancer Res. 66:11214–11218.
  • Higuchi, M., D. O'Brien, P. Kumaravelu, N. Lenny, E. J. Yeoh, and J. R. Downing. 2002. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell 1:63–74.
  • Howard, J. C., S. Yousefi, G. Cheong, A. Bernstein, and Y. Ben-David. 1993. Temporal order and functional analysis of mutations within the Fli-1 and p53 genes during the erythroleukemias induced by F-MuLV. Oncogene 8:2721–2729.
  • Ichikawa, H., K. Shimizu, Y. Hayashi, and M. Ohki. 1994. An RNA-binding protein gene, TLS/FUS, is fused to ERG in human myeloid leukemia with t(16;21) chromosomal translocation. Cancer Res. 54:2865–2868.
  • Janknecht, R. 2005. EWS-ETS oncoproteins: the linchpins of Ewing tumors. Gene 363:1–14.
  • Kanazawa, T., C. Ogawa, T. Taketani, T. Taki, Y. Hayashi, and A. Morikawa. 2005. TLS/FUS-ERG fusion gene in acute lymphoblastic leukemia with t(16;21)(p11;q22) and monitoring of minimal residual disease. Leuk. Lymphoma 46:1833–1835.
  • Kim, S., C. T. Denny, and R. Wisdom. 2006. Cooperative DNA binding with AP-1 proteins is required for transformation by EWS-Ets fusion proteins. Mol. Cell. Biol. 26:2467–2478.
  • Knoop, L. L., and S. J. Baker. 2000. The splicing factor U1C represses EWS/FLI-mediated transactivation. J. Biol. Chem. 275:24865–24871.
  • Kogan, S. C., J. M. Ward, M. R. Anver, J. J. Berman, C. Brayton, R. D. Cardiff, J. S. Carter, S. de Coronado, J. R. Downing, T. N. Fredrickson, D. C. Haines, A. W. Harris, N. L. Harris, H. Hiai, E. S. Jaffe, I. C. MacLennan, P. P. Pandolfi, P. K. Pattengale, A. S. Perkins, R. M. Simpson, M. S. Tuttle, J. F. Wong, and H. C. Morse III. 2002. Bethesda proposals for classification of nonlymphoid hematopoietic neoplasms in mice. Blood 100:238–245.
  • Komatsu, N., K. Kirito, T. Izumi, M. Eguchi, and Y. Miura. 1998. GATA-1 and erythropoietin receptor genes are highly expressed in erythroleukemia. Exp. Hematol. 26:1148–1154.
  • Kondo, M., A. J. Wagers, M. G. Manz, S. S. Prohaska, D. C. Scherer, G. F. Beilhack, J. A. Shizuru, and I. L. Weissman. 2003. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu. Rev. Immunol. 21:759–806.
  • Kondo, M., I. L. Weissman, and K. Akashi. 1997. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91:661–672.
  • Kuhn, R., F. Schwenk, M. Aguet, and K. Rajewsky. 1995. Inducible gene targeting in mice. Science 269:1427–1429.
  • Laird, P. W., A. Zijderveld, K. Linders, M. A. Rudnicki, R. Jaenisch, and A. Berns. 1991. Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19:4293.
  • Le, D. T., N. Kong, Y. Zhu, J. O. Lauchle, A. Aiyigari, B. S. Braun, E. Wang, S. C. Kogan, M. M. Le Beau, L. Parada, and K. M. Shannon. 2004. Somatic inactivation of Nf1 in hematopoietic cells results in a progressive myeloproliferative disorder. Blood 103:4243–4250.
  • Lee, C. R., D. Cervi, A. H. Truong, Y. J. Li, A. Sarkar, and Y. Ben-David. 2003. Friend virus-induced erythroleukemias: a unique and well-defined mouse model for the development of leukemia. Anticancer Res. 23:2159–2166.
  • Lessnick, S. L., C. S. Dacwag, and T. R. Golub. 2002. The Ewing's sarcoma oncoprotein EWS/FLI induces a p53-dependent growth arrest in primary human fibroblasts. Cancer Cell 1:393–401.
  • Lowry, J. A., and J. P. Mackay. 2006. GATA-1: one protein, many partners. Int. J. Biochem. Cell Biol. 38:6–11.
  • May, W. A., S. L. Lessnick, B. S. Braun, M. Klemsz, B. C. Lewis, L. B. Lunsford, R. Hromas, and C. T. Denny. 1993. The Ewing's sarcoma EWS/FLI-1 fusion gene encodes a more potent transcriptional activator and is a more powerful transforming gene than FLI-1. Mol. Cell. Biol. 13:7393–7398.
  • Melet, F., B. Motro, D. J. Rossi, L. Zhang, and A. Bernstein. 1996. Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced erythroleukemia. Mol. Cell. Biol. 16:2708–2718.
  • Mercer, K., S. Giblett, S. Green, D. Lloyd, S. DaRocha Dias, M. Plumb, R. Marais, and C. Pritchard. 2005. Expression of endogenous oncogenic V600EB-raf induces proliferation and developmental defects in mice and transformation of primary fibroblasts. Cancer Res. 65:11493–11500.
  • Miettinen, M., and J. Lasota. 2005. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl. Immunohistochem. Mol. Morphol. 13:205–220.
  • Munugalavadla, V., and R. Kapur. 2005. Role of c-Kit and erythropoietin receptor in erythropoiesis. Crit. Rev. Oncol. Hematol. 54:63–75.
  • Ned, R. M., W. Swat, and N. C. Andrews. 2003. Transferrin receptor 1 is differentially required in lymphocyte development. Blood 102:3711–3718.
  • Nishimori, H., Y. Sasaki, K. Yoshida, H. Irifune, H. Zembutsu, T. Tanaka, T. Aoyama, T. Hosaka, S. Kawaguchi, T. Wada, J. Hata, J. Toguchida, Y. Nakamura, and T. Tokino. 2002. The Id2 gene is a novel target of transcriptional activation by EWS-ETS fusion proteins in Ewing family tumors. Oncogene 21:8302–8309.
  • Oikawa, T., and T. Yamada. 2003. Molecular biology of the Ets family of transcription factors. Gene 303:11–34.
  • Olmsted-Davis, E. A., Z. Gugala, F. Camargo, F. H. Gannon, K. Jackson, K. A. Kienstra, H. D. Shine, R. W. Lindsey, K. K. Hirschi, M. A. Goodell, M. K. Brenner, and A. R. Davis. 2003. Primitive adult hematopoietic stem cells can function as osteoblast precursors. Proc. Natl. Acad. Sci. USA 100:15877–15882.
  • Ott, D. E., J. Keller, and A. Rein. 1994. 10A1 MuLV induces a murine leukemia that expresses hematopoietic stem cell markers by a mechanism that includes fli-1 integration. Virology 205:563–568.
  • Panagopoulos, I., P. Aman, T. Fioretos, M. Hoglund, B. Johansson, N. Mandahl, S. Heim, M. Behrendtz, and F. Mitelman. 1994. Fusion of the FUS gene with ERG in acute myeloid leukemia with t(16;21)(p11;q22). Genes Chromosomes Cancer 11:256–262.
  • Peister, A., J. A. Mellad, B. L. Larson, B. M. Hall, L. F. Gibson, and D. J. Prockop. 2004. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103:1662–1668.
  • Pimanda, J. E., L. Silberstein, M. Dominici, B. Dekel, M. Bowen, S. Oldham, A. Kallianpur, S. J. Brandt, D. Tannahill, B. Gottgens, and A. R. Green. 2006. Transcriptional link between blood and bone: the stem cell leukemia gene and its +19 stem cell enhancer are active in bone cells. Mol. Cell. Biol. 26:2615–2625.
  • Prieur, A., F. Tirode, P. Cohen, and O. Delattre. 2004. EWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol. Cell. Biol. 24:7275–7283.
  • Rangarajan, A., and R. A. Weinberg. 2003. Opinion: comparative biology of mouse versus human cells: modelling human cancer in mice. Nat. Rev. Cancer 3:952–959.
  • Riggi, N., L. Cironi, P. Provero, M. L. Suva, K. Kaloulis, C. Garcia-Echeverria, F. Hoffmann, A. Trumpp, and I. Stamenkovic. 2005. Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res. 65:11459–11468.
  • Rodriguez, P., E. Bonte, J. Krijgsveld, K. E. Kolodziej, B. Guyot, A. J. Heck, P. Vyas, E. de Boer, F. Grosveld, and J. Strouboulis. 2005. GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J. 24:2354–2366.
  • Ross, M. E., R. Mahfouz, M. Onciu, H. C. Liu, X. Zhou, G. Song, S. A. Shurtleff, S. Pounds, C. Cheng, J. Ma, R. C. Ribeiro, J. E. Rubnitz, K. Girtman, W. K. Williams, S. C. Raimondi, D. C. Liang, L. Y. Shih, C. H. Pui, and J. R. Downing. 2004. Gene expression profiling of pediatric acute myelogenous leukemia. Blood 104:3679–3687.
  • Shimamoto, T., J. H. Ohyashiki, K. Ohyashiki, K. Kawakubo, N. Kimura, S. Nakazawa, and K. Toyama. 1994. GATA-1, GATA-2, and stem cell leukemia gene expression in acute myeloid leukemia. Leukemia 8:1176–1180.
  • Shing, D. C., D. J. McMullan, P. Roberts, K. Smith, S. F. Chin, J. Nicholson, R. M. Tillman, P. Ramani, C. Cullinane, and N. Coleman. 2003. FUS/ERG gene fusions in Ewing's tumors. Cancer Res. 63:4568–4576.
  • Smith, R., L. A. Owen, D. J. Trem, J. S. Wong, J. S. Whangbo, T. R. Golub, and S. L. Lessnick. 2006. Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 9:405–416.
  • Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:70–71.
  • Sposi, N. M., L. Cianetti, E. Tritarelli, E. Pelosi, S. Militi, T. Barberi, M. Gabbianelli, E. Saulle, L. Kuhn, C. Peschle, and U. Testa. 2000. Mechanisms of differential transferrin receptor expression in normal hematopoiesis. Eur. J. Biochem. 267:6762–6774.
  • Stachura, D. L., S. T. Chou, and M. J. Weiss. 2006. Early block to erythromegakaryocytic development conferred by loss of transcription factor GATA-1. Blood 107:87–97.
  • Thompson, A. D., B. S. Braun, A. Arvand, S. D. Stewart, W. A. May, E. Chen, J. Korenberg, and C. Denny. 1996. EAT-2 is a novel SH2 domain containing protein that is up regulated by Ewing's sarcoma EWS/FLI1 fusion gene. Oncogene 13:2649–2658.
  • Tirode, F., K. Laud-Duval, A. Prieur, B. Delorme, P. Charbord, and O. Delattre. 2007. Mesenchymal stem cell features of Ewing tumors. Cancer Cell 11:421–429.
  • Torchia, E. C., S. Jaishankar, and S. J. Baker. 2003. Ewing tumor fusion proteins block the differentiation of pluripotent marrow stromal cells. Cancer Res. 63:3464–3468.
  • Tuveson, D. A., A. T. Shaw, N. A. Willis, D. P. Silver, E. L. Jackson, S. Chang, K. L. Mercer, R. Grochow, H. Hock, D. Crowley, S. R. Hingorani, T. Zaks, C. King, M. A. Jacobetz, L. Wang, R. T. Bronson, S. H. Orkin, R. A. DePinho, and T. Jacks. 2004. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5:375–387.
  • Vodyanik, M. A., J. A. Thomson, and I. I. Slukvin. 2006. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood 108:2095–2105.
  • Watanabe, G., H. Nishimori, H. Irifune, Y. Sasaki, S. Ishida, H. Zembutsu, T. Tanaka, S. Kawaguchi, T. Wada, J. Hata, M. Kusakabe, K. Yoshida, Y. Nakamura, and T. Tokino. 2003. Induction of tenascin-C by tumor-specific EWS-ETS fusion genes. Genes Chromosomes Cancer 36:224–232.
  • Welch, J. J., J. A. Watts, C. R. Vakoc, Y. Yao, H. Wang, R. C. Hardison, G. A. Blobel, L. A. Chodosh, and M. J. Weiss. 2004. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood 104:3136–3147.
  • Xia, S. J., and F. G. Barr. 2004. Analysis of the transforming and growth suppressive activities of the PAX3-FKHR oncoprotein. Oncogene 23:6864–6871.
  • Yang, L., H. A. Chansky, and D. D. Hickstein. 2000. EWS.Fli-1 fusion protein interacts with hyperphosphorylated RNA polymerase II and interferes with serine-arginine protein-mediated RNA splicing. J. Biol. Chem. 275:37612–37618.
  • Yu, K., J. Xu, Z. Liu, D. Sosic, J. Shao, E. N. Olson, D. A. Towler, and D. M. Ornitz. 2003. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130:3063–3074.
  • Zambrowicz, B. P., A. Imamoto, S. Fiering, L. A. Herzenberg, W. G. Kerr, and P. Soriano. 1997. Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc. Natl. Acad. Sci. USA 94:3789–3794.
  • Zhang, L., A. Eddy, Y. T. Teng, M. Fritzler, M. Kluppel, F. Melet, and A. Bernstein. 1995. An immunological renal disease in transgenic mice that overexpress Fli-1, a member of the ets family of transcription factor genes. Mol. Cell. Biol. 15:6961–6970.
  • Zou, J., H. Ichikawa, M. L. Blackburn, H. M. Hu, A. Zielinska-Kwiatkowska, Q. Mei, G. J. Roth, H. A. Chansky, and L. Yang. 2005. The oncogenic TLS-ERG fusion protein exerts different effects in hematopoietic cells and fibroblasts. Mol. Cell. Biol. 25:6235–6246.

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