Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1992 Oct;11(10):3681–3694. doi: 10.1002/j.1460-2075.1992.tb05453.x

Cooperation of proto-signals for nuclear accumulation of estrogen and progesterone receptors.

T Ylikomi 1, M T Bocquel 1, M Berry 1, H Gronemeyer 1, P Chambon 1
PMCID: PMC556828  PMID: 1327748

Abstract

Multiple proto-signals (p-NLSs) for nuclear targeting, none of which suffices on its own, cooperate in the estrogen (ER) and progesterone (PR) receptors. In the ER, an estrogen-inducible p-NLS was found in the hormone binding domain (HBD), in addition to three lysine/arginine-rich motifs resembling prototype constitutive nuclear localization signals (NLSs). The inducible and the constitutive ER p-NLSs cooperate in the presence of estrogen and hydroxy-tamoxifen, but not in the presence of ICI 164,384. In the PR, three p-NLSs, two of which are located within and directly adjacent to the second zinc finger, cooperate with each other and a weak hormone-inducible p-NLS in the PR HBD. No 'masking' of p-NLSs by the HBD was observed for ER and PR, while the ligand-free glucocorticoid receptor HBD inhibited the activity of both homologous and heterologous NLSs. Nuclear co-translocation experiments indicated that in vivo the stability of ER and PR dimers is hormonally controlled, but that, in the absence of the cognate ligand, ER dimers are more stable than PR dimers. This is likely to account for the differential hormone requirement of ER and PR DNA binding in vitro.

Full text

PDF
3681

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adam S. A., Lobl T. J., Mitchell M. A., Gerace L. Identification of specific binding proteins for a nuclear location sequence. Nature. 1989 Jan 19;337(6204):276–279. doi: 10.1038/337276a0. [DOI] [PubMed] [Google Scholar]
  2. Antakly T., Thompson E. B., O'Donnell D. Demonstration of the intracellular localization and up-regulation of glucocorticoid receptor by in situ hybridization and immunocytochemistry. Cancer Res. 1989 Apr 15;49(8 Suppl):2230s–2234s. [PubMed] [Google Scholar]
  3. Arriza J. L., Weinberger C., Cerelli G., Glaser T. M., Handelin B. L., Housman D. E., Evans R. M. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science. 1987 Jul 17;237(4812):268–275. doi: 10.1126/science.3037703. [DOI] [PubMed] [Google Scholar]
  4. Baker A. R., McDonnell D. P., Hughes M., Crisp T. M., Mangelsdorf D. J., Haussler M. R., Pike J. W., Shine J., O'Malley B. W. Cloning and expression of full-length cDNA encoding human vitamin D receptor. Proc Natl Acad Sci U S A. 1988 May;85(10):3294–3298. doi: 10.1073/pnas.85.10.3294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beato M. Gene regulation by steroid hormones. Cell. 1989 Feb 10;56(3):335–344. doi: 10.1016/0092-8674(89)90237-7. [DOI] [PubMed] [Google Scholar]
  6. Berry M., Metzger D., Chambon P. Role of the two activating domains of the oestrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti-oestrogen 4-hydroxytamoxifen. EMBO J. 1990 Sep;9(9):2811–2818. doi: 10.1002/j.1460-2075.1990.tb07469.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bocquel M. T., Kumar V., Stricker C., Chambon P., Gronemeyer H. The contribution of the N- and C-terminal regions of steroid receptors to activation of transcription is both receptor and cell-specific. Nucleic Acids Res. 1989 Apr 11;17(7):2581–2595. doi: 10.1093/nar/17.7.2581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chambraud B., Berry M., Redeuilh G., Chambon P., Baulieu E. E. Several regions of human estrogen receptor are involved in the formation of receptor-heat shock protein 90 complexes. J Biol Chem. 1990 Nov 25;265(33):20686–20691. [PubMed] [Google Scholar]
  9. Chang C. S., Kokontis J., Liao S. T. Structural analysis of complementary DNA and amino acid sequences of human and rat androgen receptors. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7211–7215. doi: 10.1073/pnas.85.19.7211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dang C. V., Lee W. M. Identification of the human c-myc protein nuclear translocation signal. Mol Cell Biol. 1988 Oct;8(10):4048–4054. doi: 10.1128/mcb.8.10.4048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Danielsen M., Hinck L., Ringold G. M. Two amino acids within the knuckle of the first zinc finger specify DNA response element activation by the glucocorticoid receptor. Cell. 1989 Jun 30;57(7):1131–1138. doi: 10.1016/0092-8674(89)90050-0. [DOI] [PubMed] [Google Scholar]
  12. Danielsen M., Northrop J. P., Ringold G. M. The mouse glucocorticoid receptor: mapping of functional domains by cloning, sequencing and expression of wild-type and mutant receptor proteins. EMBO J. 1986 Oct;5(10):2513–2522. doi: 10.1002/j.1460-2075.1986.tb04529.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Davis L. I., Fink G. R. The NUP1 gene encodes an essential component of the yeast nuclear pore complex. Cell. 1990 Jun 15;61(6):965–978. doi: 10.1016/0092-8674(90)90062-j. [DOI] [PubMed] [Google Scholar]
  14. Dingwall C., Laskey R. A. Protein import into the cell nucleus. Annu Rev Cell Biol. 1986;2:367–390. doi: 10.1146/annurev.cb.02.110186.002055. [DOI] [PubMed] [Google Scholar]
  15. Eckhardt S. G., Milich D. R., McLachlan A. Hepatitis B virus core antigen has two nuclear localization sequences in the arginine-rich carboxyl terminus. J Virol. 1991 Feb;65(2):575–582. doi: 10.1128/jvi.65.2.575-582.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eriksson P., Wrange O. Protein-protein contacts in the glucocorticoid receptor homodimer influence its DNA binding properties. J Biol Chem. 1990 Feb 25;265(6):3535–3542. [PubMed] [Google Scholar]
  17. Eul J., Meyer M. E., Tora L., Bocquel M. T., Quirin-Stricker C., Chambon P., Gronemeyer H. Expression of active hormone and DNA-binding domains of the chicken progesterone receptor in E. coli. EMBO J. 1989 Jan;8(1):83–90. doi: 10.1002/j.1460-2075.1989.tb03351.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Evans R. M. The steroid and thyroid hormone receptor superfamily. Science. 1988 May 13;240(4854):889–895. doi: 10.1126/science.3283939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fawell S. E., Lees J. A., White R., Parker M. G. Characterization and colocalization of steroid binding and dimerization activities in the mouse estrogen receptor. Cell. 1990 Mar 23;60(6):953–962. doi: 10.1016/0092-8674(90)90343-d. [DOI] [PubMed] [Google Scholar]
  20. Fawell S. E., White R., Hoare S., Sydenham M., Page M., Parker M. G. Inhibition of estrogen receptor-DNA binding by the "pure" antiestrogen ICI 164,384 appears to be mediated by impaired receptor dimerization. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6883–6887. doi: 10.1073/pnas.87.17.6883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fischer-Fantuzzi L., Vesco C. Cell-dependent efficiency of reiterated nuclear signals in a mutant simian virus 40 oncoprotein targeted to the nucleus. Mol Cell Biol. 1988 Dec;8(12):5495–5503. doi: 10.1128/mcb.8.12.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gasc J. M., Delahaye F., Baulieu E. E. Compared intracellular localization of the glucocorticosteroid and progesterone receptors: an immunocytochemical study. Exp Cell Res. 1989 Apr;181(2):492–504. doi: 10.1016/0014-4827(89)90106-7. [DOI] [PubMed] [Google Scholar]
  23. Gasc J. M., Renoir J. M., Radanyi C., Joab I., Tuohimaa P., Baulieu E. E. Progesterone receptor in the chick oviduct: an immunohistochemical study with antibodies to distinct receptor components. J Cell Biol. 1984 Oct;99(4 Pt 1):1193–1201. doi: 10.1083/jcb.99.4.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Giguere V., Ong E. S., Segui P., Evans R. M. Identification of a receptor for the morphogen retinoic acid. Nature. 1987 Dec 17;330(6149):624–629. doi: 10.1038/330624a0. [DOI] [PubMed] [Google Scholar]
  25. Govindan M. V., Devic M., Green S., Gronemeyer H., Chambon P. Cloning of the human glucocorticoid receptor cDNA. Nucleic Acids Res. 1985 Dec 9;13(23):8293–8304. doi: 10.1093/nar/13.23.8293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Green S., Chambon P. Nuclear receptors enhance our understanding of transcription regulation. Trends Genet. 1988 Nov;4(11):309–314. doi: 10.1016/0168-9525(88)90108-4. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Green S., Kumar V., Theulaz I., Wahli W., Chambon P. The N-terminal DNA-binding 'zinc finger' of the oestrogen and glucocorticoid receptors determines target gene specificity. EMBO J. 1988 Oct;7(10):3037–3044. doi: 10.1002/j.1460-2075.1988.tb03168.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Green S., Walter P., Kumar V., Krust A., Bornert J. M., Argos P., Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature. 1986 Mar 13;320(6058):134–139. doi: 10.1038/320134a0. [DOI] [PubMed] [Google Scholar]
  30. Greene G. L., Nolan C., Engler J. P., Jensen E. V. Monoclonal antibodies to human estrogen receptor. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5115–5119. doi: 10.1073/pnas.77.9.5115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gronemeyer H. Transcription activation by estrogen and progesterone receptors. Annu Rev Genet. 1991;25:89–123. doi: 10.1146/annurev.ge.25.120191.000513. [DOI] [PubMed] [Google Scholar]
  32. Gronemeyer H., Turcotte B., Quirin-Stricker C., Bocquel M. T., Meyer M. E., Krozowski Z., Jeltsch J. M., Lerouge T., Garnier J. M., Chambon P. The chicken progesterone receptor: sequence, expression and functional analysis. EMBO J. 1987 Dec 20;6(13):3985–3994. doi: 10.1002/j.1460-2075.1987.tb02741.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Guiochon-Mantel A., Lescop P., Christin-Maitre S., Loosfelt H., Perrot-Applanat M., Milgrom E. Nucleocytoplasmic shuttling of the progesterone receptor. EMBO J. 1991 Dec;10(12):3851–3859. doi: 10.1002/j.1460-2075.1991.tb04954.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Guiochon-Mantel A., Loosfelt H., Lescop P., Sar S., Atger M., Perrot-Applanat M., Milgrom E. Mechanisms of nuclear localization of the progesterone receptor: evidence for interaction between monomers. Cell. 1989 Jun 30;57(7):1147–1154. doi: 10.1016/0092-8674(89)90052-4. [DOI] [PubMed] [Google Scholar]
  35. Hollenberg S. M., Weinberger C., Ong E. S., Cerelli G., Oro A., Lebo R., Thompson E. B., Rosenfeld M. G., Evans R. M. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature. 1985 Dec 19;318(6047):635–641. doi: 10.1038/318635a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kastner P., Krust A., Turcotte B., Stropp U., Tora L., Gronemeyer H., Chambon P. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J. 1990 May;9(5):1603–1614. doi: 10.1002/j.1460-2075.1990.tb08280.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. King W. J., Greene G. L. Monoclonal antibodies localize oestrogen receptor in the nuclei of target cells. Nature. 1984 Feb 23;307(5953):745–747. doi: 10.1038/307745a0. [DOI] [PubMed] [Google Scholar]
  38. Koike S., Sakai M., Muramatsu M. Molecular cloning and characterization of rat estrogen receptor cDNA. Nucleic Acids Res. 1987 Mar 25;15(6):2499–2513. doi: 10.1093/nar/15.6.2499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. doi: 10.1016/0092-8674(86)90762-2. [DOI] [PubMed] [Google Scholar]
  40. Krust A., Green S., Argos P., Kumar V., Walter P., Bornert J. M., Chambon P. The chicken oestrogen receptor sequence: homology with v-erbA and the human oestrogen and glucocorticoid receptors. EMBO J. 1986 May;5(5):891–897. doi: 10.1002/j.1460-2075.1986.tb04300.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Krust A., Kastner P., Petkovich M., Zelent A., Chambon P. A third human retinoic acid receptor, hRAR-gamma. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5310–5314. doi: 10.1073/pnas.86.14.5310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kumar V., Chambon P. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell. 1988 Oct 7;55(1):145–156. doi: 10.1016/0092-8674(88)90017-7. [DOI] [PubMed] [Google Scholar]
  43. Kumar V., Green S., Stack G., Berry M., Jin J. R., Chambon P. Functional domains of the human estrogen receptor. Cell. 1987 Dec 24;51(6):941–951. doi: 10.1016/0092-8674(87)90581-2. [DOI] [PubMed] [Google Scholar]
  44. Kumar V., Green S., Staub A., Chambon P. Localisation of the oestradiol-binding and putative DNA-binding domains of the human oestrogen receptor. EMBO J. 1986 Sep;5(9):2231–2236. doi: 10.1002/j.1460-2075.1986.tb04489.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Lanford R. E., Butel J. S. Construction and characterization of an SV40 mutant defective in nuclear transport of T antigen. Cell. 1984 Jul;37(3):801–813. doi: 10.1016/0092-8674(84)90415-x. [DOI] [PubMed] [Google Scholar]
  46. Lang I., Scholz M., Peters R. Molecular mobility and nucleocytoplasmic flux in hepatoma cells. J Cell Biol. 1986 Apr;102(4):1183–1190. doi: 10.1083/jcb.102.4.1183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  49. Loosfelt H., Atger M., Misrahi M., Guiochon-Mantel A., Meriel C., Logeat F., Benarous R., Milgrom E. Cloning and sequence analysis of rabbit progesterone-receptor complementary DNA. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9045–9049. doi: 10.1073/pnas.83.23.9045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Mader S., Kumar V., de Verneuil H., Chambon P. Three amino acids of the oestrogen receptor are essential to its ability to distinguish an oestrogen from a glucocorticoid-responsive element. Nature. 1989 Mar 16;338(6212):271–274. doi: 10.1038/338271a0. [DOI] [PubMed] [Google Scholar]
  51. Mangelsdorf D. J., Ong E. S., Dyck J. A., Evans R. M. Nuclear receptor that identifies a novel retinoic acid response pathway. Nature. 1990 May 17;345(6272):224–229. doi: 10.1038/345224a0. [DOI] [PubMed] [Google Scholar]
  52. Maxwell B. L., McDonnell D. P., Conneely O. M., Schulz T. Z., Greene G. L., O'Malley B. W. Structural organization and regulation of the chicken estrogen receptor. Mol Endocrinol. 1987 Jan;1(1):25–35. doi: 10.1210/mend-1-1-25. [DOI] [PubMed] [Google Scholar]
  53. Meyer M. E., Pornon A., Ji J. W., Bocquel M. T., Chambon P., Gronemeyer H. Agonistic and antagonistic activities of RU486 on the functions of the human progesterone receptor. EMBO J. 1990 Dec;9(12):3923–3932. doi: 10.1002/j.1460-2075.1990.tb07613.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Misrahi M., Atger M., d'Auriol L., Loosfelt H., Meriel C., Fridlansky F., Guiochon-Mantel A., Galibert F., Milgrom E. Complete amino acid sequence of the human progesterone receptor deduced from cloned cDNA. Biochem Biophys Res Commun. 1987 Mar 13;143(2):740–748. doi: 10.1016/0006-291x(87)91416-1. [DOI] [PubMed] [Google Scholar]
  55. Morin N., Delsert C., Klessig D. F. Nuclear localization of the adenovirus DNA-binding protein: requirement for two signals and complementation during viral infection. Mol Cell Biol. 1989 Oct;9(10):4372–4380. doi: 10.1128/mcb.9.10.4372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Nehrbass U., Kern H., Mutvei A., Horstmann H., Marshallsay B., Hurt E. C. NSP1: a yeast nuclear envelope protein localized at the nuclear pores exerts its essential function by its carboxy-terminal domain. Cell. 1990 Jun 15;61(6):979–989. doi: 10.1016/0092-8674(90)90063-k. [DOI] [PubMed] [Google Scholar]
  57. Newmeyer D. D., Forbes D. J. Nuclear import can be separated into distinct steps in vitro: nuclear pore binding and translocation. Cell. 1988 Mar 11;52(5):641–653. doi: 10.1016/0092-8674(88)90402-3. [DOI] [PubMed] [Google Scholar]
  58. Notides A. C., Lerner N., Hamilton D. E. Positive cooperativity of the estrogen receptor. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4926–4930. doi: 10.1073/pnas.78.8.4926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Paine P. L., Moore L. C., Horowitz S. B. Nuclear envelope permeability. Nature. 1975 Mar 13;254(5496):109–114. doi: 10.1038/254109a0. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Picard D., Kumar V., Chambon P., Yamamoto K. R. Signal transduction by steroid hormones: nuclear localization is differentially regulated in estrogen and glucocorticoid receptors. Cell Regul. 1990 Feb;1(3):291–299. doi: 10.1091/mbc.1.3.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Picard D., Yamamoto K. R. Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J. 1987 Nov;6(11):3333–3340. doi: 10.1002/j.1460-2075.1987.tb02654.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Ponglikitmongkol M., White J. H., Chambon P. Synergistic activation of transcription by the human estrogen receptor bound to tandem responsive elements. EMBO J. 1990 Jul;9(7):2221–2231. doi: 10.1002/j.1460-2075.1990.tb07392.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Pratt W. B., Jolly D. J., Pratt D. V., Hollenberg S. M., Giguere V., Cadepond F. M., Schweizer-Groyer G., Catelli M. G., Evans R. M., Baulieu E. E. A region in the steroid binding domain determines formation of the non-DNA-binding, 9 S glucocorticoid receptor complex. J Biol Chem. 1988 Jan 5;263(1):267–273. [PubMed] [Google Scholar]
  65. Richardson W. D., Mills A. D., Dilworth S. M., Laskey R. A., Dingwall C. Nuclear protein migration involves two steps: rapid binding at the nuclear envelope followed by slower translocation through nuclear pores. Cell. 1988 Mar 11;52(5):655–664. doi: 10.1016/0092-8674(88)90403-5. [DOI] [PubMed] [Google Scholar]
  66. Robbins J., Dilworth S. M., Laskey R. A., Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell. 1991 Feb 8;64(3):615–623. doi: 10.1016/0092-8674(91)90245-t. [DOI] [PubMed] [Google Scholar]
  67. Roberts B. L., Richardson W. D., Smith A. E. The effect of protein context on nuclear location signal function. Cell. 1987 Jul 31;50(3):465–475. doi: 10.1016/0092-8674(87)90500-9. [DOI] [PubMed] [Google Scholar]
  68. Roberts B. Nuclear location signal-mediated protein transport. Biochim Biophys Acta. 1989 Aug 14;1008(3):263–280. doi: 10.1016/0167-4781(89)90016-x. [DOI] [PubMed] [Google Scholar]
  69. Rusconi S., Yamamoto K. R. Functional dissection of the hormone and DNA binding activities of the glucocorticoid receptor. EMBO J. 1987 May;6(5):1309–1315. doi: 10.1002/j.1460-2075.1987.tb02369.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Sabbah M., Gouilleux F., Sola B., Redeuilh G., Baulieu E. E. Structural differences between the hormone and antihormone estrogen receptor complexes bound to the hormone response element. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):390–394. doi: 10.1073/pnas.88.2.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Sabbah M., Redeuilh G., Baulieu E. E. Subunit composition of the estrogen receptor. Involvement of the hormone-binding domain in the dimeric state. J Biol Chem. 1989 Feb 15;264(5):2397–2400. [PubMed] [Google Scholar]
  72. Sanchez E. R., Hirst M., Scherrer L. C., Tang H. Y., Welsh M. J., Harmon J. M., Simons S. S., Jr, Ringold G. M., Pratt W. B. Hormone-free mouse glucocorticoid receptors overexpressed in Chinese hamster ovary cells are localized to the nucleus and are associated with both hsp70 and hsp90. J Biol Chem. 1990 Nov 25;265(33):20123–20130. [PubMed] [Google Scholar]
  73. Schneider J., Schindewolf C., van Zee K., Fanning E. A mutant SV40 large T antigen interferes with nuclear localization of a heterologous protein. Cell. 1988 Jul 1;54(1):117–125. doi: 10.1016/0092-8674(88)90185-7. [DOI] [PubMed] [Google Scholar]
  74. Skafar D. F. Differential DNA binding by calf uterine estrogen and progesterone receptors results from differences in oligomeric states. Biochemistry. 1991 Jun 25;30(25):6148–6154. doi: 10.1021/bi00239a010. [DOI] [PubMed] [Google Scholar]
  75. Tasset D., Tora L., Fromental C., Scheer E., Chambon P. Distinct classes of transcriptional activating domains function by different mechanisms. Cell. 1990 Sep 21;62(6):1177–1187. doi: 10.1016/0092-8674(90)90394-t. [DOI] [PubMed] [Google Scholar]
  76. Tora L., Mullick A., Metzger D., Ponglikitmongkol M., Park I., Chambon P. The cloned human oestrogen receptor contains a mutation which alters its hormone binding properties. EMBO J. 1989 Jul;8(7):1981–1986. doi: 10.1002/j.1460-2075.1989.tb03604.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Tratner I., Verma I. M. Identification of a nuclear targeting sequence in the Fos protein. Oncogene. 1991 Nov;6(11):2049–2053. [PubMed] [Google Scholar]
  78. Tsai S. Y., Carlstedt-Duke J., Weigel N. L., Dahlman K., Gustafsson J. A., Tsai M. J., O'Malley B. W. Molecular interactions of steroid hormone receptor with its enhancer element: evidence for receptor dimer formation. Cell. 1988 Oct 21;55(2):361–369. doi: 10.1016/0092-8674(88)90059-1. [DOI] [PubMed] [Google Scholar]
  79. Tuohimaa P., Renoir J. M., Radanyi C., Mester J., Joab I., Buchou T., Baulieu E. E. Antibodies against highly purified B-subunit of the chick oviduct progesterone receptor. Biochem Biophys Res Commun. 1984 Mar 15;119(2):433–439. doi: 10.1016/s0006-291x(84)80267-3. [DOI] [PubMed] [Google Scholar]
  80. Turcotte B., Meyer M. E., Bocquel M. T., Bélanger L., Chambon P. Repression of the alpha-fetoprotein gene promoter by progesterone and chimeric receptors in the presence of hormones and antihormones. Mol Cell Biol. 1990 Sep;10(9):5002–5006. doi: 10.1128/mcb.10.9.5002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Umesono K., Evans R. M. Determinants of target gene specificity for steroid/thyroid hormone receptors. Cell. 1989 Jun 30;57(7):1139–1146. doi: 10.1016/0092-8674(89)90051-2. [DOI] [PubMed] [Google Scholar]
  82. Weiler I. J., Lew D., Shapiro D. J. The Xenopus laevis estrogen receptor: sequence homology with human and avian receptors and identification of multiple estrogen receptor messenger ribonucleic acids. Mol Endocrinol. 1987 May;1(5):355–362. doi: 10.1210/mend-1-5-355. [DOI] [PubMed] [Google Scholar]
  83. 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]
  84. Welshons W. V., Lieberman M. E., Gorski J. Nuclear localization of unoccupied oestrogen receptors. Nature. 1984 Feb 23;307(5953):747–749. doi: 10.1038/307747a0. [DOI] [PubMed] [Google Scholar]
  85. White R., Lees J. A., Needham M., Ham J., Parker M. Structural organization and expression of the mouse estrogen receptor. Mol Endocrinol. 1987 Oct;1(10):735–744. doi: 10.1210/mend-1-10-735. [DOI] [PubMed] [Google Scholar]
  86. Wikström A. C., Bakke O., Okret S., Brönnegård M., Gustafsson J. A. Intracellular localization of the glucocorticoid receptor: evidence for cytoplasmic and nuclear localization. Endocrinology. 1987 Apr;120(4):1232–1242. doi: 10.1210/endo-120-4-1232. [DOI] [PubMed] [Google Scholar]
  87. Wrenn C. K., Katzenellenbogen B. S. Cross-linking of estrogen receptor to chromatin in intact MCF-7 human breast cancer cells: optimization and effect of ligand. Mol Endocrinol. 1990 Nov;4(11):1647–1654. doi: 10.1210/mend-4-11-1647. [DOI] [PubMed] [Google Scholar]
  88. Yamasaki L., Kanda P., Lanford R. E. Identification of four nuclear transport signal-binding proteins that interact with diverse transport signals. Mol Cell Biol. 1989 Jul;9(7):3028–3036. doi: 10.1128/mcb.9.7.3028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Ylikomi T., Gasc J. M., Isola J., Baulieu E. E., Tuohimaa P. Progesterone receptor in the chick bursa of fabricius: characterization and immunohistochemical localization. Endocrinology. 1985 Jul;117(1):155–160. doi: 10.1210/endo-117-1-155. [DOI] [PubMed] [Google Scholar]
  90. 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]
  91. de Thé H., Marchio A., Tiollais P., Dejean A. A novel steroid thyroid hormone receptor-related gene inappropriately expressed in human hepatocellular carcinoma. Nature. 1987 Dec 17;330(6149):667–670. doi: 10.1038/330667a0. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES