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. 1997 Jun;17(6):3181–3193. doi: 10.1128/mcb.17.6.3181

Glucocorticoid receptor-mediated cell cycle arrest is achieved through distinct cell-specific transcriptional regulatory mechanisms.

I Rogatsky 1, J M Trowbridge 1, M J Garabedian 1
PMCID: PMC232171  PMID: 9154817

Abstract

Glucocorticoids inhibit proliferation of many cell types, but the events leading from the activated glucocorticoid receptor (GR) to growth arrest are not understood. Ectopic expression and activation of GR in human osteosarcoma cell lines U2OS and SAOS2, which lack endogenous receptors, result in a G1 cell cycle arrest. GR activation in U2OS cells represses expression of the cyclin-dependent kinases (CDKs) CDK4 and CDK6 as well as their regulatory partner, cyclin D3, leading to hypophosphorylation of the retinoblastoma protein (Rb). We also demonstrate a ligand-dependent reduction in the expression of E2F-1 and c-Myc, transcription factors involved in the G1-to-S-phase transition. Mitogen-activated protein kinase, CDK2, cyclin E, and the CDK inhibitors (CDIs) p27 and p21 are unaffected by receptor activation in U2OS cells. The receptor's N-terminal transcriptional activation domain is not required for growth arrest in U2OS cells. In Rb-deficient SAOS2 cells, however, the expression of p27 and p21 is induced upon receptor activation. Remarkably, in SAOS2 cells that express a GR deletion derivative lacking the N-terminal transcriptional activation domain, induction of CDI expression is abolished and the cells fail to undergo ligand-dependent cell cycle arrest. Similarly, murine S49 lymphoma cells, which, like SAOS2 cells, lack Rb, require the N-terminal activation domain for growth arrest and induce CDI expression upon GR activation. These cell-type-specific differences in receptor domains and cellular targets linking GR activation to cell cycle machinery suggest two distinct regulatory mechanisms of GR-mediated cell cycle arrest: one involving transcriptional repression of G1 cyclins and CDKs and the other involving enhanced transcription of CDIs by the activated receptor.

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Selected References

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  1. Alnemri E. S., Fernandes T. F., Haldar S., Croce C. M., Litwack G. Involvement of BCL-2 in glucocorticoid-induced apoptosis of human pre-B-leukemias. Cancer Res. 1992 Jan 15;52(2):491–495. [PubMed] [Google Scholar]
  2. Blake M. C., Azizkhan J. C. Transcription factor E2F is required for efficient expression of the hamster dihydrofolate reductase gene in vitro and in vivo. Mol Cell Biol. 1989 Nov;9(11):4994–5002. doi: 10.1128/mcb.9.11.4994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buse P., Woo P. L., Alexander D. B., Cha H. H., Reza A., Sirota N. D., Firestone G. L. Transforming growth factor-alpha abrogates glucocorticoid-stimulated tight junction formation and growth suppression in rat mammary epithelial tumor cells. J Biol Chem. 1995 Mar 24;270(12):6505–6514. doi: 10.1074/jbc.270.12.6505. [DOI] [PubMed] [Google Scholar]
  4. Carroll R. S., Zhang J., Dashner K., Sar M., Black P. M. Steroid hormone receptors in astrocytic neoplasms. Neurosurgery. 1995 Sep;37(3):496–504. doi: 10.1227/00006123-199509000-00019. [DOI] [PubMed] [Google Scholar]
  5. Chandler V. L., Maler B. A., Yamamoto K. R. DNA sequences bound specifically by glucocorticoid receptor in vitro render a heterologous promoter hormone responsive in vivo. Cell. 1983 Jun;33(2):489–499. doi: 10.1016/0092-8674(83)90430-0. [DOI] [PubMed] [Google Scholar]
  6. Chapman M. S., Askew D. J., Kuscuoglu U., Miesfeld R. L. Transcriptional control of steroid-regulated apoptosis in murine thymoma cells. Mol Endocrinol. 1996 Aug;10(8):967–978. doi: 10.1210/mend.10.8.8843413. [DOI] [PubMed] [Google Scholar]
  7. Chin Y. E., Kitagawa M., Su W. C., You Z. H., Iwamoto Y., Fu X. Y. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science. 1996 May 3;272(5262):719–722. doi: 10.1126/science.272.5262.719. [DOI] [PubMed] [Google Scholar]
  8. Cole T. J., Blendy J. A., Monaghan A. P., Krieglstein K., Schmid W., Aguzzi A., Fantuzzi G., Hummler E., Unsicker K., Schütz G. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 1995 Jul 1;9(13):1608–1621. doi: 10.1101/gad.9.13.1608. [DOI] [PubMed] [Google Scholar]
  9. Coleman R. E. Glucocorticoids in cancer therapy. Biotherapy. 1992;4(1):37–44. doi: 10.1007/BF02171708. [DOI] [PubMed] [Google Scholar]
  10. Cook P. W., Swanson K. T., Edwards C. P., Firestone G. L. Glucocorticoid receptor-dependent inhibition of cellular proliferation in dexamethasone-resistant and hypersensitive rat hepatoma cell variants. Mol Cell Biol. 1988 Apr;8(4):1449–1459. doi: 10.1128/mcb.8.4.1449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Datto M. B., Yu Y., Wang X. F. Functional analysis of the transforming growth factor beta responsive elements in the WAF1/Cip1/p21 promoter. J Biol Chem. 1995 Dec 1;270(48):28623–28628. doi: 10.1074/jbc.270.48.28623. [DOI] [PubMed] [Google Scholar]
  12. DeGregori J., Kowalik T., Nevins J. R. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol Cell Biol. 1995 Aug;15(8):4215–4224. doi: 10.1128/mcb.15.8.4215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Diamond M. I., Miner J. N., Yoshinaga S. K., Yamamoto K. R. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science. 1990 Sep 14;249(4974):1266–1272. doi: 10.1126/science.2119054. [DOI] [PubMed] [Google Scholar]
  14. Dieken E. S., Miesfeld R. L. Transcriptional transactivation functions localized to the glucocorticoid receptor N terminus are necessary for steroid induction of lymphocyte apoptosis. Mol Cell Biol. 1992 Feb;12(2):589–597. doi: 10.1128/mcb.12.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Eastman-Reks S. B., Vedeckis W. V. Glucocorticoid inhibition of c-myc, c-myb, and c-Ki-ras expression in a mouse lymphoma cell line. Cancer Res. 1986 May;46(5):2457–2462. [PubMed] [Google Scholar]
  16. Ewen M. E., Sluss H. K., Sherr C. J., Matsushime H., Kato J., Livingston D. M. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell. 1993 May 7;73(3):487–497. doi: 10.1016/0092-8674(93)90136-e. [DOI] [PubMed] [Google Scholar]
  17. Frost G. H., Rhee K., Ma T., Thompson E. A. Expression of c-Myc in glucocorticoid-treated fibroblastic cells. J Steroid Biochem Mol Biol. 1994 Aug;50(3-4):109–119. doi: 10.1016/0960-0760(94)90017-5. [DOI] [PubMed] [Google Scholar]
  18. Gametchu B., Harrison R. W. Characterization of a monoclonal antibody to the rat liver glucocorticoid receptor. Endocrinology. 1984 Jan;114(1):274–279. doi: 10.1210/endo-114-1-274. [DOI] [PubMed] [Google Scholar]
  19. Gaynon P. S., Lustig R. H. The use of glucocorticoids in acute lymphoblastic leukemia of childhood. Molecular, cellular, and clinical considerations. J Pediatr Hematol Oncol. 1995 Feb;17(1):1–12. doi: 10.1097/00043426-199502000-00001. [DOI] [PubMed] [Google Scholar]
  20. Godowski P. J., Picard D., Yamamoto K. R. Signal transduction and transcriptional regulation by glucocorticoid receptor-LexA fusion proteins. Science. 1988 Aug 12;241(4867):812–816. doi: 10.1126/science.3043662. [DOI] [PubMed] [Google Scholar]
  21. Goya L., Maiyar A. C., Ge Y., Firestone G. L. Glucocorticoids induce a G1/G0 cell cycle arrest of Con8 rat mammary tumor cells that is synchronously reversed by steroid withdrawal or addition of transforming growth factor-alpha. Mol Endocrinol. 1993 Sep;7(9):1121–1132. doi: 10.1210/mend.7.9.8247014. [DOI] [PubMed] [Google Scholar]
  22. Helmberg A., Auphan N., Caelles C., Karin M. Glucocorticoid-induced apoptosis of human leukemic cells is caused by the repressive function of the glucocorticoid receptor. EMBO J. 1995 Feb 1;14(3):452–460. doi: 10.1002/j.1460-2075.1995.tb07021.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Herrera R. E., Chen F., Weinberg R. A. Increased histone H1 phosphorylation and relaxed chromatin structure in Rb-deficient fibroblasts. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11510–11515. doi: 10.1073/pnas.93.21.11510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hiebert S. W., Blake M., Azizkhan J., Nevins J. R. Role of E2F transcription factor in E1A-mediated trans activation of cellular genes. J Virol. 1991 Jul;65(7):3547–3552. doi: 10.1128/jvi.65.7.3547-3552.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hiebert S. W., Lipp M., Nevins J. R. E1A-dependent trans-activation of the human MYC promoter is mediated by the E2F factor. Proc Natl Acad Sci U S A. 1989 May;86(10):3594–3598. doi: 10.1073/pnas.86.10.3594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hsu S. C., Qi M., DeFranco D. B. Cell cycle regulation of glucocorticoid receptor function. EMBO J. 1992 Sep;11(9):3457–3468. doi: 10.1002/j.1460-2075.1992.tb05425.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jacks T., Fazeli A., Schmitt E. M., Bronson R. T., Goodell M. A., Weinberg R. A. Effects of an Rb mutation in the mouse. Nature. 1992 Sep 24;359(6393):295–300. doi: 10.1038/359295a0. [DOI] [PubMed] [Google Scholar]
  28. Jiang H., Lin J., Su Z. Z., Collart F. R., Huberman E., Fisher P. B. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene. 1994 Nov;9(11):3397–3406. [PubMed] [Google Scholar]
  29. Karin M., Haslinger A., Holtgreve H., Richards R. I., Krauter P., Westphal H. M., Beato M. Characterization of DNA sequences through which cadmium and glucocorticoid hormones induce human metallothionein-IIA gene. Nature. 1984 Apr 5;308(5959):513–519. doi: 10.1038/308513a0. [DOI] [PubMed] [Google Scholar]
  30. Kaspers G. J., Veerman A. J., Popp-Snijders C., Lomecky M., Van Zantwijk C. H., Swinkels L. M., Van Wering E. R., Pieters R. Comparison of the antileukemic activity in vitro of dexamethasone and prednisolone in childhood acute lymphoblastic leukemia. Med Pediatr Oncol. 1996 Aug;27(2):114–121. doi: 10.1002/(SICI)1096-911X(199608)27:2<114::AID-MPO8>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar]
  31. Lees E. Cyclin dependent kinase regulation. Curr Opin Cell Biol. 1995 Dec;7(6):773–780. doi: 10.1016/0955-0674(95)80060-3. [DOI] [PubMed] [Google Scholar]
  32. Liu M., Lee M. H., Cohen M., Bommakanti M., Freedman L. P. Transcriptional activation of the Cdk inhibitor p21 by vitamin D3 leads to the induced differentiation of the myelomonocytic cell line U937. Genes Dev. 1996 Jan 15;10(2):142–153. doi: 10.1101/gad.10.2.142. [DOI] [PubMed] [Google Scholar]
  33. Macleod K. F., Sherry N., Hannon G., Beach D., Tokino T., Kinzler K., Vogelstein B., Jacks T. p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 1995 Apr 15;9(8):935–944. doi: 10.1101/gad.9.8.935. [DOI] [PubMed] [Google Scholar]
  34. Miesfeld R., Okret S., Wikström A. C., Wrange O., Gustafsson J. A., Yamamoto K. R. Characterization of a steroid hormone receptor gene and mRNA in wild-type and mutant cells. Nature. 1984 Dec 20;312(5996):779–781. doi: 10.1038/312779a0. [DOI] [PubMed] [Google Scholar]
  35. Miner J. N., Diamond M. I., Yamamoto K. R. Joints in the regulatory lattice: composite regulation by steroid receptor-AP1 complexes. Cell Growth Differ. 1991 Oct;2(10):525–530. [PubMed] [Google Scholar]
  36. Moberg K. H., Logan T. J., Tyndall W. A., Hall D. J. Three distinct elements within the murine c-myc promoter are required for transcription. Oncogene. 1992 Mar;7(3):411–421. [PubMed] [Google Scholar]
  37. Muchardt C., Yaniv M. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J. 1993 Nov;12(11):4279–4290. doi: 10.1002/j.1460-2075.1993.tb06112.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mudrak I., Ogris E., Rotheneder H., Wintersberger E. Coordinated trans activation of DNA synthesis- and precursor-producing enzymes by polyomavirus large T antigen through interaction with the retinoblastoma protein. Mol Cell Biol. 1994 Mar;14(3):1886–1892. doi: 10.1128/mcb.14.3.1886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Müller R. Transcriptional regulation during the mammalian cell cycle. Trends Genet. 1995 May;11(5):173–178. doi: 10.1016/S0168-9525(00)89039-3. [DOI] [PubMed] [Google Scholar]
  40. Nazareth L. V., Harbour D. V., Thompson E. B. Mapping the human glucocorticoid receptor for leukemic cell death. J Biol Chem. 1991 Jul 15;266(20):12976–12980. [PubMed] [Google Scholar]
  41. Neuman E., Flemington E. K., Sellers W. R., Kaelin W. G., Jr Transcription of the E2F-1 gene is rendered cell cycle dependent by E2F DNA-binding sites within its promoter. Mol Cell Biol. 1994 Oct;14(10):6607–6615. doi: 10.1128/mcb.14.10.6607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ogris E., Rotheneder H., Mudrak I., Pichler A., Wintersberger E. A binding site for transcription factor E2F is a target for trans activation of murine thymidine kinase by polyomavirus large T antigen and plays an important role in growth regulation of the gene. J Virol. 1993 Apr;67(4):1765–1771. doi: 10.1128/jvi.67.4.1765-1771.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Oswald F., Lovec H., Möröy T., Lipp M. E2F-dependent regulation of human MYC: trans-activation by cyclins D1 and A overrides tumour suppressor protein functions. Oncogene. 1994 Jul;9(7):2029–2036. [PubMed] [Google Scholar]
  44. Pockwinse S. M., Stein J. L., Lian J. B., Stein G. S. Developmental stage-specific cellular responses to vitamin D and glucocorticoids during differentiation of the osteoblast phenotype: interrelationship of morphology and gene expression by in situ hybridization. Exp Cell Res. 1995 Jan;216(1):244–260. doi: 10.1006/excr.1995.1031. [DOI] [PubMed] [Google Scholar]
  45. Qin X. Q., Livingston D. M., Ewen M., Sellers W. R., Arany Z., Kaelin W. G., Jr The transcription factor E2F-1 is a downstream target of RB action. Mol Cell Biol. 1995 Feb;15(2):742–755. doi: 10.1128/mcb.15.2.742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Rhee K., Bresnahan W., Hirai A., Hirai M., Thompson E. A. c-Myc and cyclin D3 (CcnD3) genes are independent targets for glucocorticoid inhibition of lymphoid cell proliferation. Cancer Res. 1995 Sep 15;55(18):4188–4195. [PubMed] [Google Scholar]
  47. Rhee K., Reisman D., Bresnahan W., Thompson E. A. Glucocorticoid regulation of G1 cyclin-dependent kinase genes in lymphoid cells. Cell Growth Differ. 1995 Jun;6(6):691–698. [PubMed] [Google Scholar]
  48. Sala A., Nicolaides N. C., Engelhard A., Bellon T., Lawe D. C., Arnold A., Graña X., Giordano A., Calabretta B. Correlation between E2F-1 requirement in the S phase and E2F-1 transactivation of cell cycle-related genes in human cells. Cancer Res. 1994 Mar 15;54(6):1402–1406. [PubMed] [Google Scholar]
  49. Schüle R., Rangarajan P., Kliewer S., Ransone L. J., Bolado J., Yang N., Verma I. M., Evans R. M. Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor. Cell. 1990 Sep 21;62(6):1217–1226. doi: 10.1016/0092-8674(90)90397-w. [DOI] [PubMed] [Google Scholar]
  50. Shalhoub V., Conlon D., Tassinari M., Quinn C., Partridge N., Stein G. S., Lian J. B. Glucocorticoids promote development of the osteoblast phenotype by selectively modulating expression of cell growth and differentiation associated genes. J Cell Biochem. 1992 Dec;50(4):425–440. doi: 10.1002/jcb.240500411. [DOI] [PubMed] [Google Scholar]
  51. Sherr C. J. D-type cyclins. Trends Biochem Sci. 1995 May;20(5):187–190. doi: 10.1016/s0968-0004(00)89005-2. [DOI] [PubMed] [Google Scholar]
  52. Sherr C. J. Mammalian G1 cyclins. Cell. 1993 Jun 18;73(6):1059–1065. doi: 10.1016/0092-8674(93)90636-5. [DOI] [PubMed] [Google Scholar]
  53. Sherr C. J. The ins and outs of RB: coupling gene expression to the cell cycle clock. Trends Cell Biol. 1994 Jan;4(1):15–18. doi: 10.1016/0962-8924(94)90033-7. [DOI] [PubMed] [Google Scholar]
  54. Sibley C. H., Yamamoto K. R. Mouse lymphoma cells: mechanisms of resistance to glucocorticoids. Monogr Endocrinol. 1979;12:357–376. doi: 10.1007/978-3-642-81265-1_20. [DOI] [PubMed] [Google Scholar]
  55. Singh P., Coe J., Hong W. A role for retinoblastoma protein in potentiating transcriptional activation by the glucocorticoid receptor. Nature. 1995 Apr 6;374(6522):562–565. doi: 10.1038/374562a0. [DOI] [PubMed] [Google Scholar]
  56. Steinman R. A., Hoffman B., Iro A., Guillouf C., Liebermann D. A., el-Houseini M. E. Induction of p21 (WAF-1/CIP1) during differentiation. Oncogene. 1994 Nov;9(11):3389–3396. [PubMed] [Google Scholar]
  57. Sánchez I., Goya L., Vallerga A. K., Firestone G. L. Glucocorticoids reversibly arrest rat hepatoma cell growth by inducing an early G1 block in cell cycle progression. Cell Growth Differ. 1993 Mar;4(3):215–225. [PubMed] [Google Scholar]
  58. Sørensen S., Helweg-Larsen S., Mouridsen H., Hansen H. H. Effect of high-dose dexamethasone in carcinomatous metastatic spinal cord compression treated with radiotherapy: a randomised trial. Eur J Cancer. 1994;30A(1):22–27. doi: 10.1016/s0959-8049(05)80011-5. [DOI] [PubMed] [Google Scholar]
  59. Thompson E. B., Nazareth L. V., Thulasi R., Ashraf J., Harbour D., Johnson B. H. Glucocorticoids in malignant lymphoid cells: gene regulation and the minimum receptor fragment for lysis. J Steroid Biochem Mol Biol. 1992 Mar;41(3-8):273–282. doi: 10.1016/0960-0760(92)90352-j. [DOI] [PubMed] [Google Scholar]
  60. Thompson E. B., Thulasi R., Saeed M. F., Johnson B. H. Glucocorticoid antagonist RU 486 reverses agonist-induced apoptosis and c-myc repression in human leukemic CEM-C7 cells. Ann N Y Acad Sci. 1995 Jun 12;761:261–275. doi: 10.1111/j.1749-6632.1995.tb31383.x. [DOI] [PubMed] [Google Scholar]
  61. Vanderbilt J. N., Miesfeld R., Maler B. A., Yamamoto K. R. Intracellular receptor concentration limits glucocorticoid-dependent enhancer activity. Mol Endocrinol. 1987 Jan;1(1):68–74. doi: 10.1210/mend-1-1-68. [DOI] [PubMed] [Google Scholar]
  62. Wade M., Kowalik T. F., Mudryj M., Huang E. S., Azizkhan J. C. E2F mediates dihydrofolate reductase promoter activation and multiprotein complex formation in human cytomegalovirus infection. Mol Cell Biol. 1992 Oct;12(10):4364–4374. doi: 10.1128/mcb.12.10.4364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Wang J., Walsh K. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science. 1996 Jul 19;273(5273):359–361. doi: 10.1126/science.273.5273.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Wang Q. M., Jones J. B., Studzinski G. P. Cyclin-dependent kinase inhibitor p27 as a mediator of the G1-S phase block induced by 1,25-dihydroxyvitamin D3 in HL60 cells. Cancer Res. 1996 Jan 15;56(2):264–267. [PubMed] [Google Scholar]
  65. Webster M. K., Guthrie J., Firestone G. L. Glucocorticoid growth suppression response in 13762NF adenocarcinoma-derived Con8 rat mammary tumor cells is mediated by dominant trans-acting factors. Cancer Res. 1991 Nov 15;51(22):6031–6038. [PubMed] [Google Scholar]
  66. Weinberg R. A. The retinoblastoma protein and cell cycle control. Cell. 1995 May 5;81(3):323–330. doi: 10.1016/0092-8674(95)90385-2. [DOI] [PubMed] [Google Scholar]
  67. Weintraub S. J., Prater C. A., Dean D. C. Retinoblastoma protein switches the E2F site from positive to negative element. Nature. 1992 Jul 16;358(6383):259–261. doi: 10.1038/358259a0. [DOI] [PubMed] [Google Scholar]
  68. Yamamoto K. R., Stampfer M. R., Tomkins G. M. Receptors from glucocorticoid-sensitive lymphoma cells and two clases of insensitive clones: physical and DNA-binding properties. Proc Natl Acad Sci U S A. 1974 Oct;71(10):3901–3905. doi: 10.1073/pnas.71.10.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Yamamoto K. R. Steroid receptor regulated transcription of specific genes and gene networks. Annu Rev Genet. 1985;19:209–252. doi: 10.1146/annurev.ge.19.120185.001233. [DOI] [PubMed] [Google Scholar]
  70. Yang-Yen H. F., Chambard J. C., Sun Y. L., Smeal T., Schmidt T. J., Drouin J., Karin M. Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell. 1990 Sep 21;62(6):1205–1215. doi: 10.1016/0092-8674(90)90396-v. [DOI] [PubMed] [Google Scholar]
  71. Yoshinaga S. K., Peterson C. L., Herskowitz I., Yamamoto K. R. Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors. Science. 1992 Dec 4;258(5088):1598–1604. doi: 10.1126/science.1360703. [DOI] [PubMed] [Google Scholar]
  72. Zeng Y. X., el-Deiry W. S. Regulation of p21WAF1/CIP1 expression by p53-independent pathways. Oncogene. 1996 Apr 4;12(7):1557–1564. [PubMed] [Google Scholar]
  73. Zhang X. K., Dong J. M., Chiu J. F. Regulation of alpha-fetoprotein gene expression by antagonism between AP-1 and the glucocorticoid receptor at their overlapping binding site. J Biol Chem. 1991 May 5;266(13):8248–8254. [PubMed] [Google Scholar]

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