Abstract
The E26 and avian erythroblastosis virus (AEV) avian retroviruses induce acute leukemia in chickens. E26 can block both erythroid and myeloid differentiation at an early multipotent stage. Moreover, E26 can block erythroid differentiation at the erythroid burst-forming unit/erythroid CFU (BFU-E/CFU-E) stage, which also corresponds to the differentiation stage blocked by AEV. AEV carries two oncogenes, v-erbA and v-erbB, whereas E26 encodes a single 135-kDa Gag-Myb-Ets fusion oncoprotein. v-ErbA is responsible for the erythroid differentiation arrest through negative interferences with both the retinoic acid receptor (RAR) and the thyroid hormone receptor (T3R/c-ErbA). We investigated whether Myb-Ets could block erythroid differentiation in a manner similar to v-ErbA. We show here that Myb-Ets inhibits both RAR and c-ErbA activities on specific hormone response elements in transient-expression assays. Moreover, Myb-Ets abrogates the inactivation of transcription factor AP-1 by RAR and T3R, another feature shared with v-ErbA. Myb-Ets also antagonizes the biological response of erythrocytic progenitor cells to retinoic acid and T3. Analysis of a series of mutants of Myb-Ets reveals that the domains of the oncoprotein involved in these inhibitory activities are the same as those involved in oncogenic transformation of hematopoietic cells. These data demonstrate that the Myb-Ets oncoprotein shares properties with the v-ErbA oncoprotein and that inhibition of ligand-dependent RAR and c-ErbA functions by Myb-Ets is responsible for blocking the differentiation of hematopoietic progenitors.
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- Altabef M., Garcia M., Lavau C., Bae S. C., Dejean A., Samarut J. A retrovirus carrying the promyelocyte-retinoic acid receptor PML-RARalpha fusion gene transforms haematopoietic progenitors in vitro and induces acute leukaemias. EMBO J. 1996 Jun 3;15(11):2707–2716. [PMC free article] [PubMed] [Google Scholar]
- Amouyel P., Laudet V., Martin P., Li R. P., Quatannens B., Stéhelin D., Saule S. Two nuclear oncogenic proteins, P135gag-myb-ets and p61/63myc, cooperate to induce transformation of chicken neuroretina cells. J Virol. 1989 Aug;63(8):3382–3388. doi: 10.1128/jvi.63.8.3382-3388.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Angel P., Baumann I., Stein B., Delius H., Rahmsdorf H. J., Herrlich P. 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5'-flanking region. Mol Cell Biol. 1987 Jun;7(6):2256–2266. doi: 10.1128/mcb.7.6.2256. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barettino D., Bugge T. H., Bartunek P., Vivanco Ruiz M. D., Sonntag-Buck V., Beug H., Zenke M., Stunnenberg H. G. Unliganded T3R, but not its oncogenic variant, v-erbA, suppresses RAR-dependent transactivation by titrating out RXR. EMBO J. 1993 Apr;12(4):1343–1354. doi: 10.1002/j.1460-2075.1993.tb05779.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benchaibi M., Mallet F., Thoraval P., Savatier P., Xiao J. H., Verdier G., Samarut J., Nigon V. Avian retroviral vectors derived from avian defective leukemia virus: role of the translational context of the inserted gene on efficiency of the vectors. Virology. 1989 Mar;169(1):15–26. doi: 10.1016/0042-6822(89)90036-6. [DOI] [PubMed] [Google Scholar]
- Beug H., Palmieri S., Freudenstein C., Zentgraf H., Graf T. Hormone-dependent terminal differentiation in vitro of chicken erythroleukemia cells transformed by ts mutants of avian erythroblastosis virus. Cell. 1982 Apr;28(4):907–919. doi: 10.1016/0092-8674(82)90070-8. [DOI] [PubMed] [Google Scholar]
- Boulukos K. E., Pognonec P., Rabault B., Begue A., Ghysdael J. Definition of an Ets1 protein domain required for nuclear localization in cells and DNA-binding activity in vitro. Mol Cell Biol. 1989 Dec;9(12):5718–5721. doi: 10.1128/mcb.9.12.5718. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burris T. P., Nawaz Z., Tsai M. J., O'Malley B. W. A nuclear hormone receptor-associated protein that inhibits transactivation by the thyroid hormone and retinoic acid receptors. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9525–9529. doi: 10.1073/pnas.92.21.9525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Casini T., Graf T. Bicistronic retroviral vector reveals capacity of v-erbA to induce erythroleukemia and to co-operate with v-myb. Oncogene. 1995 Sep 21;11(6):1019–1026. [PubMed] [Google Scholar]
- Cavaillès V., Dauvois S., L'Horset F., Lopez G., Hoare S., Kushner P. J., Parker M. G. Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J. 1995 Aug 1;14(15):3741–3751. doi: 10.1002/j.1460-2075.1995.tb00044.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen H. W., Privalsky M. L. The erbA oncogene represses the actions of both retinoid X and retinoid A receptors but does so by distinct mechanisms. Mol Cell Biol. 1993 Oct;13(10):5970–5980. doi: 10.1128/mcb.13.10.5970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen J. D., Evans R. M. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature. 1995 Oct 5;377(6548):454–457. doi: 10.1038/377454a0. [DOI] [PubMed] [Google Scholar]
- Cole M. D. The myb and myc nuclear oncogenes as transcriptional activators. Curr Opin Cell Biol. 1990 Jun;2(3):502–508. doi: 10.1016/0955-0674(90)90134-z. [DOI] [PubMed] [Google Scholar]
- Damm K., Thompson C. C., Evans R. M. Protein encoded by v-erbA functions as a thyroid-hormone receptor antagonist. Nature. 1989 Jun 22;339(6226):593–597. doi: 10.1038/339593a0. [DOI] [PubMed] [Google Scholar]
- Delattre O., Zucman J., Plougastel B., Desmaze C., Melot T., Peter M., Kovar H., Joubert I., de Jong P., Rouleau G. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature. 1992 Sep 10;359(6391):162–165. doi: 10.1038/359162a0. [DOI] [PubMed] [Google Scholar]
- Desbois C., Aubert D., Legrand C., Pain B., Samarut J. A novel mechanism of action for v-ErbA: abrogation of the inactivation of transcription factor AP-1 by retinoic acid and thyroid hormone receptors. Cell. 1991 Nov 15;67(4):731–740. doi: 10.1016/0092-8674(91)90068-a. [DOI] [PubMed] [Google Scholar]
- Disela C., Glineur C., Bugge T., Sap J., Stengl G., Dodgson J., Stunnenberg H., Beug H., Zenke M. v-erbA overexpression is required to extinguish c-erbA function in erythroid cell differentiation and regulation of the erbA target gene CAII. Genes Dev. 1991 Nov;5(11):2033–2047. doi: 10.1101/gad.5.11.2033. [DOI] [PubMed] [Google Scholar]
- Domenget C., Leprince D., Pain B., Peyrol S., Li R. P., Stehelin D., Samarut J., Jurdic P. The various domains of v-myb and v-ets oncogenes of E26 retrovirus contribute differently, but cooperatively, in transformation of hematopoietic lineages. Oncogene. 1992 Nov;7(11):2231–2241. [PubMed] [Google Scholar]
- Feavers I. M., Jiricny J., Moncharmont B., Saluz H. P., Jost J. P. Interaction of two nonhistone proteins with the estradiol response element of the avian vitellogenin gene modulates the binding of estradiol-receptor complex. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7453–7457. doi: 10.1073/pnas.84.21.7453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frykberg L., Metz T., Brady G., Introna M., Beug H., Vennström B., Graf T. A point mutation in the DNA binding domain of the v-myb oncogene of E26 virus confers temperature sensitivity for transformation of myelomonocytic cells. Oncogene Res. 1988;3(4):313–322. [PubMed] [Google Scholar]
- Gandrillon O., Ferrand N., Michaille J. J., Roze L., Zile M. H., Samarut J. c-erbA alpha/T3R and RARs control commitment of hematopoietic self-renewing progenitor cells to apoptosis or differentiation and are antagonized by the v-erbA oncogene. Oncogene. 1994 Mar;9(3):749–758. [PubMed] [Google Scholar]
- Gandrillon O., Jurdic P., Pain B., Desbois C., Madjar J. J., Moscovici M. G., Moscovici C., Samarut J. Expression of the v-erbA product, an altered nuclear hormone receptor, is sufficient to transform erythrocytic cells in vitro. Cell. 1989 Jul 14;58(1):115–121. doi: 10.1016/0092-8674(89)90408-x. [DOI] [PubMed] [Google Scholar]
- Garrels J. I. Quantitative two-dimensional gel electrophoresis of proteins. Methods Enzymol. 1983;100:411–423. doi: 10.1016/0076-6879(83)00070-1. [DOI] [PubMed] [Google Scholar]
- Gauthier J. M., Bourachot B., Doucas V., Yaniv M., Moreau-Gachelin F. Functional interference between the Spi-1/PU.1 oncoprotein and steroid hormone or vitamin receptors. EMBO J. 1993 Dec 15;12(13):5089–5096. doi: 10.1002/j.1460-2075.1993.tb06203.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glass C. K., Holloway J. M., Devary O. V., Rosenfeld M. G. The thyroid hormone receptor binds with opposite transcriptional effects to a common sequence motif in thyroid hormone and estrogen response elements. Cell. 1988 Jul 29;54(3):313–323. doi: 10.1016/0092-8674(88)90194-8. [DOI] [PubMed] [Google Scholar]
- Golay J., Introna M., Graf T. A single point mutation in the v-ets oncogene affects both erythroid and myelomonocytic cell differentiation. Cell. 1988 Dec 23;55(6):1147–1158. doi: 10.1016/0092-8674(88)90259-0. [DOI] [PubMed] [Google Scholar]
- Goldberg Y., Treier M., Ghysdael J., Bohmann D. Repression of AP-1-stimulated transcription by c-Ets-1. J Biol Chem. 1994 Jun 17;269(24):16566–16573. [PubMed] [Google Scholar]
- Golub T. R., Barker G. F., Lovett M., Gilliland D. G. Fusion of PDGF receptor beta to a novel ets-like gene, tel, in chronic myelomonocytic leukemia with t(5;12) chromosomal translocation. Cell. 1994 Apr 22;77(2):307–316. doi: 10.1016/0092-8674(94)90322-0. [DOI] [PubMed] [Google Scholar]
- Graf T., Beug H. Avian leukemia viruses: interaction with their target cells in vivo and in vitro. Biochim Biophys Acta. 1978 Nov 17;516(3):269–299. doi: 10.1016/0304-419x(78)90011-2. [DOI] [PubMed] [Google Scholar]
- Graf T., McNagny K., Brady G., Frampton J. Chicken "erythroid" cells transformed by the Gag-Myb-Ets-encoding E26 leukemia virus are multipotent. Cell. 1992 Jul 24;70(2):201–213. doi: 10.1016/0092-8674(92)90096-u. [DOI] [PubMed] [Google Scholar]
- Green S., Issemann I., Sheer E. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 1988 Jan 11;16(1):369–369. doi: 10.1093/nar/16.1.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gutman A., Wasylyk B. The collagenase gene promoter contains a TPA and oncogene-responsive unit encompassing the PEA3 and AP-1 binding sites. EMBO J. 1990 Jul;9(7):2241–2246. doi: 10.1002/j.1460-2075.1990.tb07394.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halachmi S., Marden E., Martin G., MacKay H., Abbondanza C., Brown M. Estrogen receptor-associated proteins: possible mediators of hormone-induced transcription. Science. 1994 Jun 3;264(5164):1455–1458. doi: 10.1126/science.8197458. [DOI] [PubMed] [Google Scholar]
- Hermann T., Hoffmann B., Piedrafita F. J., Zhang X. K., Pfahl M. V-erbA requires auxiliary proteins for dominant negative activity. Oncogene. 1993 Jan;8(1):55–65. [PubMed] [Google Scholar]
- Hörlein A. J., När A. M., Heinzel T., Torchia J., Gloss B., Kurokawa R., Ryan A., Kamei Y., Söderström M., Glass C. K. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature. 1995 Oct 5;377(6548):397–404. doi: 10.1038/377397a0. [DOI] [PubMed] [Google Scholar]
- Jurdic P., Benchaibi M., Gandrillon O., Samarut J. Transforming and mitogenic effects of avian leukemia virus E26 on chicken hematopoietic cells and fibroblasts, respectively, correlate with level of expression of the provirus. J Virol. 1987 Oct;61(10):3058–3065. doi: 10.1128/jvi.61.10.3058-3065.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kerner S. A., Scott R. A., Pike J. W. Sequence elements in the human osteocalcin gene confer basal activation and inducible response to hormonal vitamin D3. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4455–4459. doi: 10.1073/pnas.86.12.4455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klempnauer K. H., Symonds G., Evan G. I., Bishop J. M. Subcellular localization of proteins encoded by oncogenes of avian myeloblastosis virus and avian leukemia virus E26 and by chicken c-myb gene. Cell. 1984 Jun;37(2):537–547. doi: 10.1016/0092-8674(84)90384-2. [DOI] [PubMed] [Google Scholar]
- Kraut N., Frampton J., Graf T. Rem-1, a putative direct target gene of the Myb-Ets fusion oncoprotein in haematopoietic progenitors, is a member of the recoverin family. Oncogene. 1995 Mar 16;10(6):1027–1036. [PubMed] [Google Scholar]
- Kraut N., Frampton J., McNagny K. M., Graf T. A functional Ets DNA-binding domain is required to maintain multipotency of hematopoietic progenitors transformed by Myb-Ets. Genes Dev. 1994 Jan;8(1):33–44. doi: 10.1101/gad.8.1.33. [DOI] [PubMed] [Google Scholar]
- Kurokawa R., Söderström M., Hörlein A., Halachmi S., Brown M., Rosenfeld M. G., Glass C. K. Polarity-specific activities of retinoic acid receptors determined by a co-repressor. Nature. 1995 Oct 5;377(6548):451–454. doi: 10.1038/377451a0. [DOI] [PubMed] [Google Scholar]
- Lee J. W., Ryan F., Swaffield J. C., Johnston S. A., Moore D. D. Interaction of thyroid-hormone receptor with a conserved transcriptional mediator. Nature. 1995 Mar 2;374(6517):91–94. doi: 10.1038/374091a0. [DOI] [PubMed] [Google Scholar]
- Leprince D., Duterque-Coquillaud M., Li R. P., Henry C., Flourens A., Debuire B., Stehelin D. Alternative splicing within the chicken c-ets-1 locus: implications for transduction within the E26 retrovirus of the c-ets proto-oncogene. J Virol. 1988 Sep;62(9):3233–3241. doi: 10.1128/jvi.62.9.3233-3241.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leprince D., Gegonne A., Coll J., de Taisne C., Schneeberger A., Lagrou C., Stehelin D. A putative second cell-derived oncogene of the avian leukaemia retrovirus E26. Nature. 1983 Nov 24;306(5941):395–397. doi: 10.1038/306395a0. [DOI] [PubMed] [Google Scholar]
- Lim F., Kraut N., Framptom J., Graf T. DNA binding by c-Ets-1, but not v-Ets, is repressed by an intramolecular mechanism. EMBO J. 1992 Feb;11(2):643–652. doi: 10.1002/j.1460-2075.1992.tb05096.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Macleod K., Leprince D., Stehelin D. The ets gene family. Trends Biochem Sci. 1992 Jul;17(7):251–256. doi: 10.1016/0968-0004(92)90404-w. [DOI] [PubMed] [Google Scholar]
- Metz T., Graf T. Fusion of the nuclear oncoproteins v-Myb and v-Ets is required for the leukemogenicity of E26 virus. Cell. 1991 Jul 12;66(1):95–105. doi: 10.1016/0092-8674(91)90142-l. [DOI] [PubMed] [Google Scholar]
- Metz T., Graf T. v-myb and v-ets transform chicken erythroid cells and cooperate both in trans and in cis to induce distinct differentiation phenotypes. Genes Dev. 1991 Mar;5(3):369–380. doi: 10.1101/gad.5.3.369. [DOI] [PubMed] [Google Scholar]
- Moreau-Gachelin F., Ray D., Mattei M. G., Tambourin P., Tavitian A. The putative oncogene Spi-1: murine chromosomal localization and transcriptional activation in murine acute erythroleukemias. Oncogene. 1989 Dec;4(12):1449–1456. [PubMed] [Google Scholar]
- Morrison N. A., Shine J., Fragonas J. C., Verkest V., McMenemy M. L., Eisman J. A. 1,25-dihydroxyvitamin D-responsive element and glucocorticoid repression in the osteocalcin gene. Science. 1989 Dec 1;246(4934):1158–1161. doi: 10.1126/science.2588000. [DOI] [PubMed] [Google Scholar]
- Moscovici C., Samarut J., Gazzolo L., Moscovici M. G. Myeloid and erythroid neoplastic responses to avian defective leukemia viruses in chickens and in quail. Virology. 1981 Sep;113(2):765–768. doi: 10.1016/0042-6822(81)90205-1. [DOI] [PubMed] [Google Scholar]
- Moscovici M. G., Jurdic P., Samarut J., Gazzolo L., Mura C. V., Moscovici C. Characterization of the hemopoietic target cells for the avian leukemia virus E26. Virology. 1983 Aug;129(1):65–78. doi: 10.1016/0042-6822(83)90396-3. [DOI] [PubMed] [Google Scholar]
- Ness S. A., Marknell A., Graf T. The v-myb oncogene product binds to and activates the promyelocyte-specific mim-1 gene. Cell. 1989 Dec 22;59(6):1115–1125. doi: 10.1016/0092-8674(89)90767-8. [DOI] [PubMed] [Google Scholar]
- Nunn M. F., Seeburg P. H., Moscovici C., Duesberg P. H. Tripartite structure of the avian erythroblastosis virus E26 transforming gene. Nature. 1983 Nov 24;306(5941):391–395. doi: 10.1038/306391a0. [DOI] [PubMed] [Google Scholar]
- Pain B., Melet F., Jurdic P., Samarut J. The carbonic anhydrase II gene, a gene regulated by thyroid hormone and erythropoietin, is repressed by the v-erbA oncogene in erythrocytic cells. New Biol. 1990 Mar;2(3):284–294. [PubMed] [Google Scholar]
- Pain B., Woods C. M., Saez J., Flickinger T., Raines M., Peyrol S., Moscovici C., Moscovici M. G., Kung H. J., Jurdic P. EGF-R as a hemopoietic growth factor receptor: the c-erbB product is present in chicken erythrocytic progenitors and controls their self-renewal. Cell. 1991 Apr 5;65(1):37–46. doi: 10.1016/0092-8674(91)90405-n. [DOI] [PubMed] [Google Scholar]
- Radke K., Beug H., Kornfeld S., Graf T. Transformation of both erythroid and myeloid cells by E26, an avian leukemia virus that contains the myb gene. Cell. 1982 Dec;31(3 Pt 2):643–653. doi: 10.1016/0092-8674(82)90320-8. [DOI] [PubMed] [Google Scholar]
- Rascle A., Ghysdael J., Samarut J. c-ErbA, but not v-ErbA, competes with a putative erythroid repressor for binding to the carbonic anhydrase II promoter. Oncogene. 1994 Oct;9(10):2853–2867. [PubMed] [Google Scholar]
- Ravel-Chapuis P., Leprince D., Pain B., Li R., Domenget C., Stehelin D., Samarut J., Jurdic P. v-myb and v-ets cooperate for the mitogenic stimulation of primary fibroblasts by avian E26 retrovirus. J Virol. 1991 Jul;65(7):3928–3931. doi: 10.1128/jvi.65.7.3928-3931.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sakura H., Kanei-Ishii C., Nagase T., Nakagoshi H., Gonda T. J., Ishii S. Delineation of three functional domains of the transcriptional activator encoded by the c-myb protooncogene. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5758–5762. doi: 10.1073/pnas.86.15.5758. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samarut J., Gazzolo L. Target cells infected by avian erythroblastosis virus differentiate and become transformed. Cell. 1982 Apr;28(4):921–929. doi: 10.1016/0092-8674(82)90071-x. [DOI] [PubMed] [Google Scholar]
- Sande S., Sharif M., Chen H., Privalsky M. v-erbA acts on retinoic acid receptors in immature avian erythroid cells. J Virol. 1993 Feb;67(2):1067–1074. doi: 10.1128/jvi.67.2.1067-1074.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sap J., Muñoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., Beug H., Vennström B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature. 1986 Dec 18;324(6098):635–640. doi: 10.1038/324635a0. [DOI] [PubMed] [Google Scholar]
- Sap J., Muñoz A., Schmitt J., Stunnenberg H., Vennström B. Repression of transcription mediated at a thyroid hormone response element by the v-erb-A oncogene product. Nature. 1989 Jul 20;340(6230):242–244. doi: 10.1038/340242a0. [DOI] [PubMed] [Google Scholar]
- Schroeder C., Gibson L., Nordström C., Beug H. The estrogen receptor cooperates with the TGF alpha receptor (c-erbB) in regulation of chicken erythroid progenitor self-renewal. EMBO J. 1993 Mar;12(3):951–960. doi: 10.1002/j.1460-2075.1993.tb05736.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schroeder C., Gibson L., Zenke M., Beug H. Modulation of normal erythroid differentiation by the endogenous thyroid hormone and retinoic acid receptors: a possible target for v-erbA oncogene action. Oncogene. 1992 Feb;7(2):217–227. [PubMed] [Google Scholar]
- Schuetze S., Stenberg P. E., Kabat D. The Ets-related transcription factor PU.1 immortalizes erythroblasts. Mol Cell Biol. 1993 Sep;13(9):5670–5678. doi: 10.1128/mcb.13.9.5670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharif M., Privalsky M. L. v-erbA oncogene function in neoplasia correlates with its ability to repress retinoic acid receptor action. Cell. 1991 Sep 6;66(5):885–893. doi: 10.1016/0092-8674(91)90435-2. [DOI] [PubMed] [Google Scholar]
- Smarda J., Sugarman J., Glass C., Lipsick J. Retinoic acid receptor alpha suppresses transformation by v-myb. Mol Cell Biol. 1995 May;15(5):2474–2481. doi: 10.1128/mcb.15.5.2474. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sucov H. M., Murakami K. K., Evans R. M. Characterization of an autoregulated response element in the mouse retinoic acid receptor type beta gene. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5392–5396. doi: 10.1073/pnas.87.14.5392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trainor C. D., Evans T., Felsenfeld G. Negative regulation of chicken GATA-1 promoter activity mediated by a hormone response element. Mol Endocrinol. 1995 Sep;9(9):1135–1146. doi: 10.1210/mend.9.9.7491106. [DOI] [PubMed] [Google Scholar]
- Tsai S., Bartelmez S., Sitnicka E., Collins S. Lymphohematopoietic progenitors immortalized by a retroviral vector harboring a dominant-negative retinoic acid receptor can recapitulate lymphoid, myeloid, and erythroid development. Genes Dev. 1994 Dec 1;8(23):2831–2841. doi: 10.1101/gad.8.23.2831. [DOI] [PubMed] [Google Scholar]
- Umesono K., Giguere V., Glass C. K., Rosenfeld M. G., Evans R. M. Retinoic acid and thyroid hormone induce gene expression through a common responsive element. Nature. 1988 Nov 17;336(6196):262–265. doi: 10.1038/336262a0. [DOI] [PubMed] [Google Scholar]
- Wasylyk B., Wasylyk C., Flores P., Begue A., Leprince D., Stehelin D. The c-ets proto-oncogenes encode transcription factors that cooperate with c-Fos and c-Jun for transcriptional activation. Nature. 1990 Jul 12;346(6280):191–193. doi: 10.1038/346191a0. [DOI] [PubMed] [Google Scholar]
- Watson D. K., McWilliams M. J., Papas T. S. Molecular organization of the chicken ets locus. Virology. 1988 May;164(1):99–105. doi: 10.1016/0042-6822(88)90624-1. [DOI] [PubMed] [Google Scholar]
- Weinberger C., Thompson C. C., Ong E. S., Lebo R., Gruol D. J., Evans R. M. The c-erb-A gene encodes a thyroid hormone receptor. Nature. 1986 Dec 18;324(6098):641–646. doi: 10.1038/324641a0. [DOI] [PubMed] [Google Scholar]
- Woods D. B., Ghysdael J., Owen M. J. Identification of nucleotide preferences in DNA sequences recognised specifically by c-Ets-1 protein. Nucleic Acids Res. 1992 Feb 25;20(4):699–704. doi: 10.1093/nar/20.4.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang-Yen H. F., Zhang X. K., Graupner G., Tzukerman M., Sakamoto B., Karin M., Pfahl M. Antagonism between retinoic acid receptors and AP-1: implications for tumor promotion and inflammation. New Biol. 1991 Dec;3(12):1206–1219. [PubMed] [Google Scholar]
- Yen P. M., Ikeda M., Brubaker J. H., Forgione M., Sugawara A., Chin W. W. Roles of v-erbA homodimers and heterodimers in mediating dominant negative activity by v-erbA. J Biol Chem. 1994 Jan 14;269(2):903–909. [PubMed] [Google Scholar]
- Yuan C. C., Kan N., Dunn K. J., Papas T. S., Blair D. G. Properties of a murine retroviral recombinant of avian acute leukemia virus E26: a murine fibroblast assay for v-ets function. J Virol. 1989 Jan;63(1):205–215. doi: 10.1128/jvi.63.1.205-215.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang X. K., Wills K. N., Husmann M., Hermann T., Pfahl M. Novel pathway for thyroid hormone receptor action through interaction with jun and fos oncogene activities. Mol Cell Biol. 1991 Dec;11(12):6016–6025. doi: 10.1128/mcb.11.12.6016. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zucman J., Melot T., Desmaze C., Ghysdael J., Plougastel B., Peter M., Zucker J. M., Triche T. J., Sheer D., Turc-Carel C. Combinatorial generation of variable fusion proteins in the Ewing family of tumours. EMBO J. 1993 Dec;12(12):4481–4487. doi: 10.1002/j.1460-2075.1993.tb06137.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- al Moustafa A. E., Gautier R., Saule S., Dieterlen-Lièvre F., Cormier F. Avian myeloblastic cell lines transformed by two nuclear oncoproteins, P135gag-myb-ets and p61/63myc: a model of retinoic acid-induced differentiation not abrogated by v-erbA. Cell Growth Differ. 1994 Aug;5(8):863–871. [PubMed] [Google Scholar]