Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Paper
  • Published:

Ets and retroviruses–transduction and activation of members of the Ets oncogene family in viral oncogenesis

Oncogene volume 19, pages 6472–6481 (2000)Cite this article

Abstract

Studies of retroviral-induced oncogenesis in animal systems led to the initial discovery of viral oncogenes and their cellular homologs, and provided critical insights into their role in the neoplastic process. V-ets, the founding member of the ETS oncogene family, was originally identified as part of the fusion oncogene encoded by the avian acute leukemia virus E26 and subsequent analysis of virus induced leukemias led to the initial isolation of two other members of the ETS gene family. PU.1 was identified as a target of insertional activation in the majority of tumors induced by the murine Spleen Focus Forming virus (SFFV), while fli-1 proved to be the target of Friend murine leukemia virus (F-MuLV) in F-MuLV induced erythroleukemia, as well as that of the 10A1 and Graffi viruses. The common features of the erythroid and myeloid diseases induced by these viruses provided the initial demonstration that these and other members of the ETS family play important roles in hematopoietic development as well as disease. This review provides an overview of the role of ETS genes in retrovirally induced neoplasia, their possible mechanisms of action, and how these viral studies relate to current knowledge of the functions of these genes in hematopoiesis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  • Athanasiou M, Clausen PA, Mavrothalassitis GJ, Zhang XK, Watson DK and Blair DG. . 1996a Cell Growth Differ. 7: 1525–1584.

  • Athanasiou M, Mavrothalassitis GJ, Sun-Hoffman L and Blair DG. . 2000 Leukemia 14: 439–445.

  • Athanasiou M, Mavrothalassitis GJ, Yuan CC and Blair DG. . 1996b Oncogene 12: 337–344.

  • Aurigemma RE, Shen-Ong GL, Athanasiou M, Hanson CA, Yuan CC, Blair DG and Ruscetti SK. . 1994 Molecular Biology of Haematopoiesis, Vol. 3. Nader GA, Shadduck RK, Levine AS and Takaku F (eds). Intercept, Ltd.: Andover, Hampshire, pp. 669–679.

  • Bastian LS, Kwiatkowski BA, Breininger J, Danner S and Roth G. . 1999 Blood 93: 2637–2644.

  • Bear SE, Bellacosa A, Lazo PA, Jenkins NA, Copeland NG, Hanson C, Levan G and Tsichlis PN. . 1989 Proc. Natl. Acad. Sci. USA 86: 7495–7499.

  • Bellacosa A, Datta K, Bear SE, Patriotis C, Lazo PA, Copeland NG, Jenkins NA and Tsichlis PN. . 1994 J. Virol 68: 2320–2330.

  • Bellacosa A, Lazo PA, Bear SE and Tsichlis PN. . 1991 Mol. Cell Biol. 11: 2864–2872.

  • Ben-David Y and Bernstein A. . 1991 Cell 66: 831–834.

  • Ben-David Y, Giddens EB and Bernstein A. . 1990 Proc. Natl. Acad. Sci. USA 87: 1332–1336.

  • Ben-David Y, Giddens EB, Letwin K and Bernstein A. . 1991 Genes Dev. 5: 908–918.

  • Ben-David Y, Prideaux VR, Chow V, Benchimol S and Bernstein A. . 1988 Oncogene 3: 179–185.

  • Bergeron D, Houde J, Poliquin L, Barbeau B and Rassart E. . 1993 Leukemia 7: 954–962.

  • Bergeron D, Poliquin L, Houde J, Barbeau B and Rassart E. . 1992 Virology 191: 661–669.

  • Bergeron D, Poliquin L, Kozak CA and Rassart E. . 1991 J. Virol 65: 7–15.

  • Beug H, Leutz A, Kahn P and Graf T. . 1984 Cell 39: 579–588.

  • Bosselut R, Levin J, Adjadj E and Ghysdael J. . 1993 Nucleic Acids Res. 21: 5184–5191.

  • Boyle WJ, Lampert MA, Lipsick JS and Baluda MA. . 1984 Proc. Natl. Acad. Sci. USA 81: 4265–4269.

  • Clarke AR, Maandag ER, van Roon M, van der Lugt NM, van der Valk M, Hooper ML, Berns A and te Riele H. . 1992 Nature 359: 328–330.

  • Coffin JM, Hughes SH and Varmus HE. . 1997 Retroviruses CSHL Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Kovar H, Joubert I, de Jong P, Rouleau G, Aurias A and Thomas G. . 1992 Nature 359: 162–165.

  • de Launoit Y, Audette M, Pelczar H, Plaza S and Baert JL. . 1998 Oncogene 16: 2065–2073.

  • Delgado MD, Gutierrez P, Richard C, Cuadrado MA, Moreau-Gachelin F and Leon J. . 1998 Biochem. Biophys. Res. Commun. 252: 383–391.

  • Delgado MD, Hallier M, Meneceur P, Tavitian A and Moreau-Gachelin F. . 1994 Oncogene 9: 1723–1727.

  • Denicourt C, Edouard E and Rassart E. . 1999 J. Virol. 73: 4439–4442.

  • de Taisne C, Gegonne A, Stehelin D, Bernheim A and Berger R. . 1984 Nature 310: 581–587.

  • Deveaux S, Filipe A, Lemarchandel V, Ghysdael J, Romeo PH and Mignotte V. . 1996 Blood 87: 4678–4685.

  • Domenget C, Leprince D, Pain B, Peyrol S, Li RP, Stehelin D, Samarut J and Jurdic P. . 1992 Oncogene 7: 2231–2241.

  • Dube A, Akbarali Y, Sato TN, Libermann TA and Oettgen P. . 1999 Circ. Res. 84: 1177–1185.

  • Frampton J, Ramqvist T and Graf T. . 1996 Genes Dev. 10: 2720–2731.

  • Friend C. . 1957 J. of Exper. Med. 105: 307–318.

  • Frykberg L, Metz T, Brady G, Introna M, Beug H, Vennstrom B and Graf T. . 1988 Oncogene Res. 3: 313–322.

  • Gardner MB, Klement V, Henderson BE, Casagrande J, Bryant ML, Doutherty MF and Estes JD. . 1978 Tumors of early life in man and animals. Severi L. (ed.): Monteluce, Italy, pp. 343–356.

  • Gauthier JM, Bourachot B, Doucas V, Yaniv M and Moreau-Gachelin F. . 1993 EMBO J. 12: 5089–5096.

  • Gegonne A, Leprince D, Pognonec P, Dernis D, Raes MB, Stehelin D and Ghysdael J. . 1987 Virology 156: 177–180.

  • Ghysdael J and Boureux A. . 1997 Oncogenes as transcriptional regulators. Vol. 1. Yaniv M and Ghysdael J. (eds). Birkhauser Verlag: Basel, Switzerland pp. 29–88.

  • Goebl MK. . 1990 Cell 61: 1165–1166.

  • Golay J, Introna M and Graf T. . 1988 Cell 55: 1147–1158.

  • Gory S, Dalmon J, Prandini MH, Kortulewski T, de Launoit Y and Huber P. . 1998 J. Biol. Chem. 273: 6750–6755.

  • Graf T, Beug H, Royer-Pokora B and Meyer-Glauner W. . 1978 In: Clarkson B, Marks PA and Till JE (eds). Differentiation of normal and neoplastic hematopoietic cells. Cold Spring Harbor, Cold Spring Harbor Laboratory 625–639.

  • Graf T, McNagny K, Brady G and Frampton J. . 1992 Cell 70: 201–213.

  • Graf T, Oker-Blom N, Todorov TG and Beug H. . 1979 Virology 99: 431–436.

  • Hart A, Melet F, Grossfeld P, Chien K, Jones C, Tunnacliffe A, Favier R and Bernstein A. . 2000 Immunity 13: 167–177.

  • Hu N, Gulley ML, Kung JT and Lee EY. . 1997 Cancer Res. 57: 4123–4129.

  • Ivanov X, Mladenov Z, Nedyalk S and Todorov TG. . 1962 Bugarian Acad. Sci. Bull. Inst. Pathol. Comp. Animaux Domestiques. 9: 5–36.

  • Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA and Weinberg RA. . 1992 Nature 359: 295–300.

  • Jurdic P, Benchaibi M, Gandrillon O and Samarut J. . 1987 J. Virol. 61: 3058–5765.

  • Klemsz MJ, Maki RA, Papayannopoulou T, Moore J and Hromas R. . 1993 J. Biol. Chem. 268: 5769–5773.

  • Klemsz MJ, McKercher SR, Celada A, Van Beveren C and Maki RA. . 1990 Cell. 61: 113–124.

  • Kraut N, Frampton J and Graf T. . 1995 Oncogene 10: 1027–1036.

  • Kwiatkowski BA, Bastian LS, Bauer Jr TR, Tsai S, Zielinska-Kwiatkowska AG and Hickstein DD. . 1998 J. Biol. Chem. 273: 17525–17530.

  • Lautenberger JA and Papas TS. . 1993 J. Virol. 67: 610–612.

  • Lavigueur A and Bernstein A. . 1991 Oncogene 6: 2197–2201.

  • Lee EY, Chang CY, Hu N, Wang YC, Lai CC, Herrup K, Lee WH and Bradley A. . 1992 Nature 359: 288–294.

  • Lemarchandel V, Ghysdael J, Mignotte V, Rahuel C and Romeo PH. . 1993 Mol. Cell. Biol. 13: 668–676.

  • Leprince D, Gegonne A, Coll J, de Taisne C, Schneeberger A, Lagrou C and Stehelin D. . 1983 Nature 306: 395–397.

  • Leprince D, Gesquiere JC and Stehelin D. . 1990 Oncogene Res. 5: 255–265.

  • Lim F, Kraut N, Framptom J and Graf T. . 1992 EMBO J. 11: 643–652.

  • Metz T and Graf T. . 1991a Cell. 66: 95–105.

  • Metz T and Graf T. . 1991b Genes. Dev. 5: 369–380.

  • Moreau-Gachelin F, Ray D, Mattei MG, Tambourin P and Tavitian A. . 1989 Oncogene 4: 1449–1456.

  • Moreau-Gachelin F, Tavitian A and Tambourin P. . 1988 Nature 331: 277–280.

  • Moreau-Gachelin F, Wendling F, Molina T, Denis N, Titeux M, Grimber G, Briand P, Vainchenker W and Tavitian A. . 1996 Mol. Cell. Biol. 16: 2453–2463.

  • Moscovici C, Samarut J, Gazzolo L and Moscovici MG. . 1981 Virology 113: 765–768.

  • Mowat M, Cheng A, Kimura N, Bernstein A and Benchimol S. . 1985 Nature 314: 633–636.

  • Ness SA, Marknell A and Graf T. . 1989 Cell. 59: 1115–1125.

  • Nunn M, Weiher H, Bullock P and Duesberg P. . 1984 Virology 139: 330–339.

  • Nunn MF and Hunter T. . 1989 J. Virol. 63: 398–402.

  • Nunn MF, Seeburg PH, Moscovici C and Duesberg PH. . 1983 Nature 306: 391–395.

  • Ott D, Friedrich R and Rein A. . 1990 J. Virol. 64: 757–766.

  • Ott DE, Keller J and Rein A. . 1994 Virology 205: 563–568.

  • Ott DE, Keller J, Sill K and Rein A. . 1992 J. Virol. 66: 6107–6116.

  • Papas TS, Bhat NK, Spyropoulos DD, Miaatvedt AE, Vournakis J, Seth A and Watson DK. . 1997 Leukemia 11: (Suppl 3) 557–566.

  • Pereira R, Quang CT, Lesault I, Dolznig H, Beug H and Ghysdael J. . 1999 Oncogene 18: 1597–1608.

  • Radke K, Beug H, Kornfeld S and Graf T. . 1982 Cell 31: 643–653.

  • Rascle A, Ferrand N, Gandrillon O and Samarut J. . 1996 Mol. Cell. Biol. 16: 6338–6351.

  • Ravel-Chapuis P, Leprince D, Pain B, Li R, Domenget C, Stehelin D, Samarut J and Jurdic P. . 1991 J. Virol. 65: 3928–3931.

  • Rossi F, McNagny KM, Logie C, Stewart AF and Graf T. . 1996 Curr. Biol. 6: 866–872.

  • Ru M, Shustik C and Rassart E. . 1993 J. Virol. 67: 4722–4731.

  • Ruscetti S, Aurigemma R, Yuan CC, Sawyer S and Blair DG. . 1992 J. Virol. 66: 20–26.

  • Ruscetti SK. . 1999 Int. J. Biochem. Cell. Biol. 31: 1089–1109.

  • Schuetze S, Stenberg PE and Kabat D. . 1993 Mol. Cell. Biol. 13: 5670–5678.

  • Schwachtgen JL, Janel N, Barek L, Duterque-Coquillaud M, Ghysdael J, Meyer D and Kerbiriou-Nabias D. . 1997 Oncogene 15: 3091–3102.

  • Seth A and Papas TS. . 1990 Oncogene 5: 1761–1767.

  • Sieweke MH, Tekotte H, Frampton J and Graf T. . 1996 Cell 85: 49–60.

  • Sieweke MH, Tekotte H, Frampton J and Graf T. . 1997 Leukemia 11: (Suppl 3) 486–488.

  • Silver J and Kozak C. . 1986 J. Virol. 57: 526–583.

  • Sotirov N. . 1981 J. Natl. Cancer Inst. 66: 1143–1149.

  • Spiro C, Gliniak B and Kabat D. . 1988 J. Virol. 62: 4129–4135.

  • Spyropoulos DD, Pharr PN, Lavenburg KR, Jackers P, Papas TS, Ogawa M and Watson DK. . 2000 Mol. Cell. Biol. 20: 5643–5652.

  • Starck J, Doubeikovski A, Sarrazin S, Gonnet C, Rao G, Skoultchi A, Godet J, Dusanter-Fourt I and Morle F. . 1999 Mol. Cell. Biol. 19: 121–135.

  • Tamir A, Howard J, Higgins RR, Li YJ, Berger L, Zacksenhaus E, Reis M and Ben-David Y. . 1999 Mol. Cell. Biol. 19: 4452–4464.

  • Topol LZ, Tatosyan AG, Ascione R, Thompson DM, Blair DG, Kola I and Seth A. . 1992 Cancer Lett. 67: 71–78.

  • Watson DK, Ascione R and Papas TS. . 1990 Crit. Rev. Oncog. 1: 409–486.

  • Watson DK, McWilliams-Smith MJ, Flordellis CS and Papas TS. . 1988 Advances in gene Technology: Molecular biology of the Endocrine System. Puett D, Ahmad F, Black S, Lopez DM, Melner MH, Scott WA and Whelan WJ . (eds). Cambridge University Press: Cambridge, p. 158.

  • Watson DK, McWilliams-Smith MJ, Kozak C, Reeves R, Gearhart J, Nunn MF, Nash W, Fowle JRD, Duesberg P, Papas TS and et al. 1986 Proc. Natl. Acad. Sci. USA 83: 1792–1796.

  • Watson DK, McWilliams-Smith MJ, Nunn MF, Duesberg PH, O'Brien SJ and Papas TS. . 1985 Proc. Natl. Acad. Sci. USA 82: 7294–7298.

  • Yamada T, Kondoh N, Matsumoto M, Yoshida M, Maekawa A and Oikawa T. . 1997 Blood 89: 1383–1393.

  • Yuan CC, Kan N, Dunn KJ, Papas TS and Blair DG. . 1989 J. Virol. 63: 205–215.

  • Zhang L, Eddy A, Teng YT, Fritzler M, Kluppel M, Melet F and Bernstein A. . 1995 Mol. Cell. Biol. 15: 6961–6970.

  • Zhang L, Lemarchandel V, Romeo PH, Ben-David Y, Greer P and Bernstein A. . 1993 Oncogene 8: 1621–1630.

Download references

Acknowledgements

We want to express our gratitude for the opportunity to work with Takis Papas, who first introduced us to the ETS family of oncogenes, and whose enthusiasm, support, encouragement and friendship we were fortunate to experience through our many years of association. The authors also wish to thank Dennis Watson for helpful suggestions and permission to cite unpublished data, and Karen Cannon for help in preparation of the manuscript. This work was supported in part with Federal Funds from the National Cancer Institute, National Institutes of Health, under contract No. N01-CO-56000. The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.

Author information

Authors and Affiliations

  1. Division of Basic Science, National Cancer Institute, Basic Research Laboratory, Oncogene Mechanisms Section, Frederick, MD 21702-1207, Maryland, USA

    Donald G Blair

  2. Intramural Research Support Program, SAIC, Frederick, MD 21702-1207, Maryland, USA

    Meropi Athanasiou

Authors
  1. Donald G Blair
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meropi Athanasiou
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blair, D., Athanasiou, M. Ets and retroviruses–transduction and activation of members of the Ets oncogene family in viral oncogenesis. Oncogene 19, 6472–6481 (2000). https://doi.org/10.1038/sj.onc.1204046

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1204046

Keywords

This article is cited by

Search

Advanced search

Quick links