Abstract
Retinoic acid (RA) treatment of human embryonal carcinoma (EC) NTera-2 (NT2) cells induces expression of major histocompatibility complex (MHC) class I and beta-2 microglobulin surface molecules. We found that this induction was accompanied by increased levels of MHC class I mRNA, which was attributable to the activation of the two conserved upstream enhancers, region I (NF-kappa B like) and region II. This activation coincided with the induction of nuclear factor binding activities specific for the two enhancers. Region I binding activity was not present in undifferentiated NT2 cells, but binding of an NF-kappa B heterodimer, p50-p65, was induced following RA treatment. The p50-p65 heterodimer was produced as a result of de novo induction of p50 and p65 mRNAs. Region II binding activity was present in undifferentiated cells at low levels but was greatly augmented by RA treatment because of activation of a nuclear hormone receptor heterodimer composed of the retinoid X receptor (RXR beta) and the RA receptor (RAR beta). The RXR beta-RAR beta heterodimer also bound RA responsive elements present in other genes which are likely to be involved in RA triggering of EC cell differentiation. Furthermore, transfection of p50 and p65 into undifferentiated NT2 cells synergistically activated region I-dependent MHC class I reporter activity. A similar increase in MHC class I reporter activity was demonstrated by cotransfection of RXR beta and RAR beta. These data show that following RA treatment, heterodimers of two transcription factor families are induced to bind to the MHC enhancers, which at least partly accounts for RA induction of MHC class I expression in NT2 EC cells.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Andrews P. W. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol. 1984 Jun;103(2):285–293. doi: 10.1016/0012-1606(84)90316-6. [DOI] [PubMed] [Google Scholar]
- Andrews P. W., Trinchieri G., Perussia B., Baglioni C. Induction of class I major histocompatibility complex antigens in human teratocarcinoma cells by interferon without induction of differentiation, growth inhibition, or resistance to viral infection. Cancer Res. 1987 Feb 1;47(3):740–746. [PubMed] [Google Scholar]
- Arcari P., Martinelli R., Salvatore F. The complete sequence of a full length cDNA for human liver glyceraldehyde-3-phosphate dehydrogenase: evidence for multiple mRNA species. Nucleic Acids Res. 1984 Dec 11;12(23):9179–9189. doi: 10.1093/nar/12.23.9179. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Artzt K., Jacob F. Letter: Absence of serologically detectable H-2 on primitive teratocarcinoma cells in culture. Transplantation. 1974 Jun;17(6):632–634. doi: 10.1097/00007890-197406000-00015. [DOI] [PubMed] [Google Scholar]
- Baeuerle P. A., Baltimore D. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-kappa B transcription factor. Cell. 1988 Apr 22;53(2):211–217. doi: 10.1016/0092-8674(88)90382-0. [DOI] [PubMed] [Google Scholar]
- Baeuerle P. A. The inducible transcription activator NF-kappa B: regulation by distinct protein subunits. Biochim Biophys Acta. 1991 Apr 16;1072(1):63–80. doi: 10.1016/0304-419x(91)90007-8. [DOI] [PubMed] [Google Scholar]
- Baldwin A. S., Jr, Sharp P. A. Binding of a nuclear factor to a regulatory sequence in the promoter of the mouse H-2Kb class I major histocompatibility gene. Mol Cell Biol. 1987 Jan;7(1):305–313. doi: 10.1128/mcb.7.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barnstable C. J., Bodmer W. F., Brown G., Galfre G., Milstein C., Williams A. F., Ziegler A. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell. 1978 May;14(1):9–20. doi: 10.1016/0092-8674(78)90296-9. [DOI] [PubMed] [Google Scholar]
- Bours V., Burd P. R., Brown K., Villalobos J., Park S., Ryseck R. P., Bravo R., Kelly K., Siebenlist U. A novel mitogen-inducible gene product related to p50/p105-NF-kappa B participates in transactivation through a kappa B site. Mol Cell Biol. 1992 Feb;12(2):685–695. doi: 10.1128/mcb.12.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bours V., Villalobos J., Burd P. R., Kelly K., Siebenlist U. Cloning of a mitogen-inducible gene encoding a kappa B DNA-binding protein with homology to the rel oncogene and to cell-cycle motifs. Nature. 1990 Nov 1;348(6296):76–80. doi: 10.1038/348076a0. [DOI] [PubMed] [Google Scholar]
- Brodsky F. M., Bodmer W. F., Parham P. Characterization of a monoclonal anti-beta 2-microglobulin antibody and its use in the genetic and biochemical analysis of major histocompatibility antigens. Eur J Immunol. 1979 Jul;9(7):536–545. doi: 10.1002/eji.1830090709. [DOI] [PubMed] [Google Scholar]
- Bugge T. H., Pohl J., Lonnoy O., Stunnenberg H. G. RXR alpha, a promiscuous partner of retinoic acid and thyroid hormone receptors. EMBO J. 1992 Apr;11(4):1409–1418. doi: 10.1002/j.1460-2075.1992.tb05186.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burke P. A., Hirschfeld S., Shirayoshi Y., Kasik J. W., Hamada K., Appella E., Ozato K. Developmental and tissue-specific expression of nuclear proteins that bind the regulatory element of the major histocompatibility complex class I gene. J Exp Med. 1989 Apr 1;169(4):1309–1321. doi: 10.1084/jem.169.4.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chamberlain J. W., Vasavada H. A., Ganguly S., Weissman S. M. Identification of cis sequences controlling efficient position-independent tissue-specific expression of human major histocompatibility complex class I genes in transgenic mice. Mol Cell Biol. 1991 Jul;11(7):3564–3572. doi: 10.1128/mcb.11.7.3564. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Croce C. M., Linnenbach A., Huebner K., Parnes J. R., Margulies D. H., Appella E., Seidman J. G. Control of expression of histocompatibility antigens (H-2) and beta 2-microglobulin in F9 teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5754–5758. doi: 10.1073/pnas.78.9.5754. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daniel F., Morello D., Le Bail O., Chambon P., Cayre Y., Kourilsky P. Structure and expression of the mouse beta 2-microglobulin gene isolated from somatic and non-expressing teratocarcinoma cells. EMBO J. 1983;2(7):1061–1065. doi: 10.1002/j.1460-2075.1983.tb01546.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Darrow A. L., Rickles R. J., Pecorino L. T., Strickland S. Transcription factor Sp1 is important for retinoic acid-induced expression of the tissue plasminogen activator gene during F9 teratocarcinoma cell differentiation. Mol Cell Biol. 1990 Nov;10(11):5883–5893. doi: 10.1128/mcb.10.11.5883. [DOI] [PMC free article] [PubMed] [Google Scholar]
- David-Watine B., Israël A., Kourilsky P. The regulation and expression of MHC class I genes. Immunol Today. 1990 Aug;11(8):286–292. doi: 10.1016/0167-5699(90)90114-o. [DOI] [PubMed] [Google Scholar]
- Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drew P. D., Lonergan M., Goldstein M. E., Lampson L. A., Ozato K., McFarlin D. E. Regulation of MHC class I and beta 2-microglobulin gene expression in human neuronal cells. Factor binding to conserved cis-acting regulatory sequences correlates with expression of the genes. J Immunol. 1993 Apr 15;150(8 Pt 1):3300–3310. [PubMed] [Google Scholar]
- Driggers P. H., Elenbaas B. A., An J. B., Lee I. J., Ozato K. Two upstream elements activate transcription of a major histocompatibility complex class I gene in vitro. Nucleic Acids Res. 1992 May 25;20(10):2533–2540. doi: 10.1093/nar/20.10.2533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fan C. M., Maniatis T. A DNA-binding protein containing two widely separated zinc finger motifs that recognize the same DNA sequence. Genes Dev. 1990 Jan;4(1):29–42. doi: 10.1101/gad.4.1.29. [DOI] [PubMed] [Google Scholar]
- Flanagan J. R., Murata M., Burke P. A., Shirayoshi Y., Appella E., Sharp P. A., Ozato K. Negative regulation of the major histocompatibility complex class I promoter in embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3145–3149. doi: 10.1073/pnas.88.8.3145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Franzoso G., Bours V., Park S., Tomita-Yamaguchi M., Kelly K., Siebenlist U. The candidate oncoprotein Bcl-3 is an antagonist of p50/NF-kappa B-mediated inhibition. Nature. 1992 Sep 24;359(6393):339–342. doi: 10.1038/359339a0. [DOI] [PubMed] [Google Scholar]
- Ghosh S., Gifford A. M., Riviere L. R., Tempst P., Nolan G. P., Baltimore D. Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal. Cell. 1990 Sep 7;62(5):1019–1029. doi: 10.1016/0092-8674(90)90276-k. [DOI] [PubMed] [Google Scholar]
- Giguère V., Yang N., Segui P., Evans R. M. Identification of a new class of steroid hormone receptors. Nature. 1988 Jan 7;331(6151):91–94. doi: 10.1038/331091a0. [DOI] [PubMed] [Google Scholar]
- Hamada K., Gleason S. L., Levi B. Z., Hirschfeld S., Appella E., Ozato K. H-2RIIBP, a member of the nuclear hormone receptor superfamily that binds to both the regulatory element of major histocompatibility class I genes and the estrogen response element. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8289–8293. doi: 10.1073/pnas.86.21.8289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harada H., Willison K., Sakakibara J., Miyamoto M., Fujita T., Taniguchi T. Absence of the type I IFN system in EC cells: transcriptional activator (IRF-1) and repressor (IRF-2) genes are developmentally regulated. Cell. 1990 Oct 19;63(2):303–312. doi: 10.1016/0092-8674(90)90163-9. [DOI] [PubMed] [Google Scholar]
- Hedley M. L., Drake B. L., Head J. R., Tucker P. W., Forman J. Differential expression of the class I MHC genes in the embryo and placenta during midgestational development in the mouse. J Immunol. 1989 Jun 1;142(11):4046–4053. [PubMed] [Google Scholar]
- Henseling U., Schmidt W., Schöler H. R., Gruss P., Hatzopoulos A. K. A transcription factor interacting with the class I gene enhancer is inactive in tumorigenic cell lines which suppress major histocompatibility complex class I genes. Mol Cell Biol. 1990 Aug;10(8):4100–4109. doi: 10.1128/mcb.10.8.4100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heyman R. A., Mangelsdorf D. J., Dyck J. A., Stein R. B., Eichele G., Evans R. M., Thaller C. 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell. 1992 Jan 24;68(2):397–406. doi: 10.1016/0092-8674(92)90479-v. [DOI] [PubMed] [Google Scholar]
- Hogan B. L., Taylor A., Adamson E. Cell interactions modulate embryonal carcinoma cell differentiation into parietal or visceral endoderm. Nature. 1981 May 21;291(5812):235–237. doi: 10.1038/291235a0. [DOI] [PubMed] [Google Scholar]
- Jaffe L., Jeannotte L., Bikoff E. K., Robertson E. J. Analysis of beta 2-microglobulin gene expression in the developing mouse embryo and placenta. J Immunol. 1990 Nov 15;145(10):3474–3482. [PubMed] [Google Scholar]
- Kidd S. Characterization of the Drosophila cactus locus and analysis of interactions between cactus and dorsal proteins. Cell. 1992 Nov 13;71(4):623–635. doi: 10.1016/0092-8674(92)90596-5. [DOI] [PubMed] [Google Scholar]
- Kieran M., Blank V., Logeat F., Vandekerckhove J., Lottspeich F., Le Bail O., Urban M. B., Kourilsky P., Baeuerle P. A., Israël A. The DNA binding subunit of NF-kappa B is identical to factor KBF1 and homologous to the rel oncogene product. Cell. 1990 Sep 7;62(5):1007–1018. doi: 10.1016/0092-8674(90)90275-j. [DOI] [PubMed] [Google Scholar]
- Kimura A., Israël A., Le Bail O., Kourilsky P. Detailed analysis of the mouse H-2Kb promoter: enhancer-like sequences and their role in the regulation of class I gene expression. Cell. 1986 Jan 31;44(2):261–272. doi: 10.1016/0092-8674(86)90760-9. [DOI] [PubMed] [Google Scholar]
- Kliewer S. A., Umesono K., Mangelsdorf D. J., Evans R. M. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature. 1992 Jan 30;355(6359):446–449. doi: 10.1038/355446a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LaRosa G. J., Gudas L. J. Early retinoic acid-induced F9 teratocarcinoma stem cell gene ERA-1: alternate splicing creates transcripts for a homeobox-containing protein and one lacking the homeobox. Mol Cell Biol. 1988 Sep;8(9):3906–3917. doi: 10.1128/mcb.8.9.3906. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leid M., Kastner P., Lyons R., Nakshatri H., Saunders M., Zacharewski T., Chen J. Y., Staub A., Garnier J. M., Mader S. Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell. 1992 Jan 24;68(2):377–395. doi: 10.1016/0092-8674(92)90478-u. [DOI] [PubMed] [Google Scholar]
- Lenardo M. J., Baltimore D. NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell. 1989 Jul 28;58(2):227–229. doi: 10.1016/0092-8674(89)90833-7. [DOI] [PubMed] [Google Scholar]
- Levin A. A., Sturzenbecker L. J., Kazmer S., Bosakowski T., Huselton C., Allenby G., Speck J., Kratzeisen C., Rosenberger M., Lovey A. 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature. 1992 Jan 23;355(6358):359–361. doi: 10.1038/355359a0. [DOI] [PubMed] [Google Scholar]
- Linney E. Retinoic acid receptors: transcription factors modulating gene regulation, development, and differentiation. Curr Top Dev Biol. 1992;27:309–350. doi: 10.1016/s0070-2153(08)60538-4. [DOI] [PubMed] [Google Scholar]
- Logeat F., Israël N., Ten R., Blank V., Le Bail O., Kourilsky P., Israël A. Inhibition of transcription factors belonging to the rel/NF-kappa B family by a transdominant negative mutant. EMBO J. 1991 Jul;10(7):1827–1832. doi: 10.1002/j.1460-2075.1991.tb07708.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lüscher B., Mitchell P. J., Williams T., Tjian R. Regulation of transcription factor AP-2 by the morphogen retinoic acid and by second messengers. Genes Dev. 1989 Oct;3(10):1507–1517. doi: 10.1101/gad.3.10.1507. [DOI] [PubMed] [Google Scholar]
- Mangelsdorf D. J., Borgmeyer U., Heyman R. A., Zhou J. Y., Ong E. S., Oro A. E., Kakizuka A., Evans R. M. Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev. 1992 Mar;6(3):329–344. doi: 10.1101/gad.6.3.329. [DOI] [PubMed] [Google Scholar]
- Marks M. S., Hallenbeck P. L., Nagata T., Segars J. H., Appella E., Nikodem V. M., Ozato K. H-2RIIBP (RXR beta) heterodimerization provides a mechanism for combinatorial diversity in the regulation of retinoic acid and thyroid hormone responsive genes. EMBO J. 1992 Apr;11(4):1419–1435. doi: 10.1002/j.1460-2075.1992.tb05187.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marks M. S., Levi B. Z., Segars J. H., Driggers P. H., Hirschfeld S., Nagata T., Appella E., Ozato K. H-2RIIBP expressed from a baculovirus vector binds to multiple hormone response elements. Mol Endocrinol. 1992 Feb;6(2):219–230. doi: 10.1210/mend.6.2.1569965. [DOI] [PubMed] [Google Scholar]
- Marotti K. R., Brown G. D., Strickland S. Two-stage hormonal control of type IV collagen mRNA levels during differentiation of F9 teratocarcinoma cells. Dev Biol. 1985 Mar;108(1):26–31. doi: 10.1016/0012-1606(85)90005-3. [DOI] [PubMed] [Google Scholar]
- Massa P. T., Hirschfeld S., Levi B. Z., Quigley L. A., Ozato K., McFarlin D. E. Expression of major histocompatibility complex (MHC) class I genes in astrocytes correlates with the presence of nuclear factors that bind to constitutive and inducible enhancers. J Neuroimmunol. 1992 Nov;41(1):35–42. doi: 10.1016/0165-5728(92)90193-O. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Molitor J. A., Walker W. H., Doerre S., Ballard D. W., Greene W. C. NF-kappa B: a family of inducible and differentially expressed enhancer-binding proteins in human T cells. Proc Natl Acad Sci U S A. 1990 Dec;87(24):10028–10032. doi: 10.1073/pnas.87.24.10028. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morello D., Daniel F., Baldacci P., Cayre Y., Gachelin G., Kourilsky P. Absence of significant H-2 and beta 2-microglobulin mRNA expression by mouse embryonal carcinoma cells. Nature. 1982 Mar 18;296(5854):260–262. doi: 10.1038/296260a0. [DOI] [PubMed] [Google Scholar]
- Murphy S. P., Garbern J., Odenwald W. F., Lazzarini R. A., Linney E. Differential expression of the homeobox gene Hox-1.3 in F9 embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5587–5591. doi: 10.1073/pnas.85.15.5587. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nagata T., Segars J. H., Levi B. Z., Ozato K. Retinoic acid-dependent transactivation of major histocompatibility complex class I promoters by the nuclear hormone receptor H-2RIIBP in undifferentiated embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):937–941. doi: 10.1073/pnas.89.3.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okazawa H., Okamoto K., Ishino F., Ishino-Kaneko T., Takeda S., Toyoda Y., Muramatsu M., Hamada H. The oct3 gene, a gene for an embryonic transcription factor, is controlled by a retinoic acid repressible enhancer. EMBO J. 1991 Oct;10(10):2997–3005. doi: 10.1002/j.1460-2075.1991.tb07850.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oshima R. G., Abrams L., Kulesh D. Activation of an intron enhancer within the keratin 18 gene by expression of c-fos and c-jun in undifferentiated F9 embryonal carcinoma cells. Genes Dev. 1990 May;4(5):835–848. doi: 10.1101/gad.4.5.835. [DOI] [PubMed] [Google Scholar]
- Ozato K., Wan Y. J., Orrison B. M. Mouse major histocompatibility class I gene expression begins at midsomite stage and is inducible in earlier-stage embryos by interferon. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2427–2431. doi: 10.1073/pnas.82.8.2427. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paterson B. M., Eldridge J. D. alpha-Cardiac actin is the major sarcomeric isoform expressed in embryonic avian skeletal muscle. Science. 1984 Jun 29;224(4656):1436–1438. doi: 10.1126/science.6729461. [DOI] [PubMed] [Google Scholar]
- Petkovich M., Brand N. J., Krust A., Chambon P. A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature. 1987 Dec 3;330(6147):444–450. doi: 10.1038/330444a0. [DOI] [PubMed] [Google Scholar]
- Robertson M. Retinoic acid receptor. Towards a biochemistry of morphogenesis. Nature. 1987 Dec 3;330(6147):420–421. doi: 10.1038/330420a0. [DOI] [PubMed] [Google Scholar]
- Rosner M. H., Vigano M. A., Ozato K., Timmons P. M., Poirier F., Rigby P. W., Staudt L. M. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature. 1990 Jun 21;345(6277):686–692. doi: 10.1038/345686a0. [DOI] [PubMed] [Google Scholar]
- Ryseck R. P., Bull P., Takamiya M., Bours V., Siebenlist U., Dobrzanski P., Bravo R. RelB, a new Rel family transcription activator that can interact with p50-NF-kappa B. Mol Cell Biol. 1992 Feb;12(2):674–684. doi: 10.1128/mcb.12.2.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmid R. M., Perkins N. D., Duckett C. S., Andrews P. C., Nabel G. J. Cloning of an NF-kappa B subunit which stimulates HIV transcription in synergy with p65. Nature. 1991 Aug 22;352(6337):733–736. doi: 10.1038/352733a0. [DOI] [PubMed] [Google Scholar]
- Sen R., Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell. 1986 Dec 26;47(6):921–928. doi: 10.1016/0092-8674(86)90807-x. [DOI] [PubMed] [Google Scholar]
- Shirayoshi Y., Miyazaki J., Burke P. A., Hamada K., Appella E., Ozato K. Binding of multiple nuclear factors to the 5' upstream regulatory element of the murine major histocompatibility class I gene. Mol Cell Biol. 1987 Dec;7(12):4542–4548. doi: 10.1128/mcb.7.12.4542. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silverman T., Rein A., Orrison B., Langloss J., Bratthauer G., Miyazaki J., Ozato K. Establishment of cell lines from somite stage mouse embryos and expression of major histocompatibility class I genes in these cells. J Immunol. 1988 Jun 15;140(12):4378–4387. [PubMed] [Google Scholar]
- Simeone A., Acampora D., Arcioni L., Andrews P. W., Boncinelli E., Mavilio F. Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature. 1990 Aug 23;346(6286):763–766. doi: 10.1038/346763a0. [DOI] [PubMed] [Google Scholar]
- Stornaiuolo A., Acampora D., Pannese M., D'Esposito M., Morelli F., Migliaccio E., Rambaldi M., Faiella A., Nigro V., Simeone A. Human HOX genes are differentially activated by retinoic acid in embryonal carcinoma cells according to their position within the four loci. Cell Differ Dev. 1990 Aug;31(2):119–127. doi: 10.1016/0922-3371(90)90015-o. [DOI] [PubMed] [Google Scholar]
- Strickland S., Mahdavi V. The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell. 1978 Oct;15(2):393–403. doi: 10.1016/0092-8674(78)90008-9. [DOI] [PubMed] [Google Scholar]
- Tsukiyama T., Ueda H., Hirose S., Niwa O. Embryonal long terminal repeat-binding protein is a murine homolog of FTZ-F1, a member of the steroid receptor superfamily. Mol Cell Biol. 1992 Mar;12(3):1286–1291. doi: 10.1128/mcb.12.3.1286. [DOI] [PMC free article] [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]
- Yang-Yen H. F., Chiu R., Karin M. Elevation of AP1 activity during F9 cell differentiation is due to increased c-jun transcription. New Biol. 1990 Apr;2(4):351–361. [PubMed] [Google Scholar]
- Yano O., Kanellopoulos J., Kieran M., Le Bail O., Israël A., Kourilsky P. Purification of KBF1, a common factor binding to both H-2 and beta 2-microglobulin enhancers. EMBO J. 1987 Nov;6(11):3317–3324. doi: 10.1002/j.1460-2075.1987.tb02652.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yu V. C., Delsert C., Andersen B., Holloway J. M., Devary O. V., När A. M., Kim S. Y., Boutin J. M., Glass C. K., Rosenfeld M. G. RXR beta: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell. 1991 Dec 20;67(6):1251–1266. doi: 10.1016/0092-8674(91)90301-e. [DOI] [PubMed] [Google Scholar]
- Zelent A., Krust A., Petkovich M., Kastner P., Chambon P. Cloning of murine alpha and beta retinoic acid receptors and a novel receptor gamma predominantly expressed in skin. Nature. 1989 Jun 29;339(6227):714–717. doi: 10.1038/339714a0. [DOI] [PubMed] [Google Scholar]
- de Thé H., Vivanco-Ruiz M. M., Tiollais P., Stunnenberg H., Dejean A. Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature. 1990 Jan 11;343(6254):177–180. doi: 10.1038/343177a0. [DOI] [PubMed] [Google Scholar]
- de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]