The glucocorticoid receptor is a key regulator of the decision between self-renewal and differentiation in erythroid progenitors

EMBO Journal

Volumn 16, Issue 2, 1997, Pages 267-280

  Wessely, Oliver ^a   Deiner, Eva Maria ^a   Beug, Hartmut ^a   Von Lindern, Marieke ^a,b  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

Author keywords

c myb; Differentiation; Erythropoiesis; Glucocorticoid receptor; Proliferation

Indexed keywords

ESTROGEN RECEPTOR; GLUCOCORTICOID RECEPTOR; HORMONE RECEPTOR; ONCOPROTEIN; PROTEIN TYROSINE KINASE; STEM CELL FACTOR; STEROID HORMONE RECEPTOR BLOCKING AGENT; THYROID HORMONE RECEPTOR;

ANIMAL CELL; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CHICKEN; CONTROLLED STUDY; DEVELOPMENT; ERYTHROID PRECURSOR CELL; MODEL; NONHUMAN; ONCOGENE C ERB; ONCOGENE C MYB; PRIORITY JOURNAL; TISSUE REGENERATION; TRANSACTIVATION;

ANIMALS; BLOTTING, NORTHERN; CELL DIFFERENTIATION; CELL DIVISION; CHICK EMBRYO; CHICKENS; DEXAMETHASONE; DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; ERYTHROID PROGENITOR CELLS; FURYLFURAMIDE; KINETICS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MYB; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ESTROGEN; RECEPTORS, GLUCOCORTICOID; STEM CELL FACTOR; TRANS-ACTIVATORS;

ANIMALIA; GALLUS GALLUS;

EID: 0031032760     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.2.267     Document Type: Article

References (77)

1. Amylon, M.D., Perrine, S.P. and Glader, B.E. (1986) Prednisone stimulation of erythropoiesis in leukemic children during remission. Am. J. Hematol., 23, 179-181.
2. Bartunek, P., Pichlikova, L., Stengl, G., Boehmelt, G., Martin, F.H., Beug, H., Dvorak, M. and Zenke, M. (1996) Avian stem cell factor (SCF): production and characterization of the recombinant his-tagged SCF of chicken and its neutralizing antibody. Cytokine, 8, 14-20.
3. Baxter, J.D. and Forsham, P.H. (1972) Tissue effects of glucocorticoids. Am. J. Med., 53, 573-589.
4. Beato, M., Herrlich, P. and Schütz, G. (1995) Steroid hormone receptors: many actors in search of a plot. Cell, 83, 851-857.
5. Beug, H., Palmieri, S., Freudenstein, C., Zentgraf, H. and Graf, T. (1982) Hormone-dependent terminal differentiation in vitro of chicken erythroleukemia cells transformed by ts mutants of avian erythroblastosis virus. Cell, 28, 907-919.
6. Beug, H., Müllner, E.W. and Hayman, M.J. (1994) Insights into erythroid differentiation obtained from studies on avian erythroblastosis virus. Curr. Opin. Cell Biol. 6, 816-824.
7. Beug, H., Schroeder, C., Wessely, O., Meyer, S., Ischenko, I.D., Deiner, E. and Hayman, M.J. (1995) Transformation of erythroid progenitors by viral and cellular tyrosine kinases. Cell Growth Differ., 6, 999-1008.
8. Billat, C.L., Felix, J.M. and Jacquot, R.L. (1982) In vitro and in vivo regulation of hepatic erythropoiesis by erythropoietin and glucocorticoids in the rat fetus. Exp. Hematol., 10, 133-140.
9. Bonde, B.G., Sharif, M. and Privalsky, M.L. (1991) Ontogeny of the v-erbA oncoprotein from the thyroid hormone receptor: an alteration in the DNA binding domain plays a role crucial for v-erbA function. J. Virol., 65, 2037-2046.
10. Boumpas, D.T., Chrousos, G.P. Wilder, R.L., Cupps, T.R. and Balow, J.E. (1993) Glucocorticoid therapy for immune-mediated diseases, basic and clinical correlates. Ann. Intern. Med., 119, 1198-1208.
11. Briegel, K., Lim, K.C. Plank, C., Beug, H., Engel, J.D. and Zenke, M. (1993) Ectopic expression of a conditional GATA-2/estrogen receptor chimera arrests erythroid differentiation in a hormone-dependent manner. Genes Dev., 7, 1097-1109.
12. Caldenhoven, E., Liden, J., Wissink, S., Van de Stolpe, A., Raaijmakers, J., Koenderman, L., Okret, S., Gustafsson, J.A. and Van der Saag, P.T. (1995) Negative cross-talk between ReIA and the glucocorticoid receptor: a possible mechanism for the antiinflammatory action of glucocorticoids. Mol. Endocrinol., 9, 401-412.
13. Casini, T. and Graf, T. (1995) Bicistronic retroviral vector reveals capacity of v-erbA to induce erythroleukemia and to co-operate with v-myb. Oncogene, 11, 1019-1026.
14. Cavaillès, V. Dauvios, S., L'lllorset, F., Lopez, G., Hoarc, S., Kushner, P.J. and Parker, M.G. (1995) Nuclear factor RIP 140 modulates transcriptional activation by the estrogen receptor. EMBO J., 14, 3741-3751.
15. Chan, H.S., Saunders, E.F. and Freedman, M.H. (1982a) Diamond-Blackfan syndrome. I. Erythropoiesis in prednisone-responsive and resistant disease. Pediatr. Res., 16, 474-476.
16. Chan, H.S., Saunders, E.F. and Freedman, M.H. (1982b) Diamond-Blackfan syndrome. II. In vitro corticosteroid effect on erythropoiesis. Pedriatr. Res., 16, 477-478.
17. Chang, T.J., Scher, B.M., Waxman, S. and Scher, W. (1993) Inhibition of mouse GATA-1 function by the glucocorticoid receptor: possible mechanism of steroid inhibition of erythroleukemia cell differentiation. Mol. Endocrinol., 7, 528-542.
18. Chiba, H., Muramatsu, M., Nomoto, A. and Kato, H. (1994) Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. Nucleic Acids Res., 22, 1815-1820.
19. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
20. Clarke, M.F. Kukowska-Latallo, J.F., Westin, E., Smith, M. and Prochownik, E.V. (1988) Constitutive expression of a c-myb cDNA blocks Friend murine erythroleukemia cell differentiation. Mol. Cell. Biol., 8, 884-892.
21. Cole, P.J. et al. (1995) Targeted disruption of the glucocorticoid receptor C gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev., 9, 1608-1621.
22. Crowe, A.J. and Hayman, M.J. (1991) Altered glycosylation of the envsea oncoprotein inhibits intracellular transport and transformation. J. Virol., 65, 6173-6180.
23. Dainiak, N., Hoffman, R., Ritchey, A.K., Floyd, V. and Callahan, M. (1980) In vitro steroid sensitivity testing: a possible means to predict response to therapy in primary hypoproliferative anemia. Am. J. Hematol., 9, 401-412.
24. Danielian, P.S., White, R., Lees, J.A. and Parker, M.G. (1992) Identification of a conserved region required for hormone dependent transcriptional activation by steroid hormone receptors. EMBO J., 11, 1025-1033.
25. Dewaal, R.R.W. (1994) The anti-inflammatory activity of glucocortocoids. Mol. Biol. Rep., 19, 81-88.
26. Dolznig, H., Bartunek, P. Nasmyth, K., Müllner, E. and Beug, H. (1995) Terminal differentiation of normal chicken erythroid progenitors: shortening of G1 correlates with loss of D cyclin/CDK-4 expression and altered cell size control. Cell Growth Differ., 6, 1341-1352.
27. Espinás, M.L., Roux, J., Pictet, R. and Grange, T. (1995) Glucocorticoids and protein kinase A coordinately modulate transcription factor recruitment at a glucocorticoid-responsive unit. Mol. Cell. Biol., 15, 5346-5354.
28. Fuerstenberg, S., Leitner, I., Schroeder, C. Schwarz, H., Vennström, B. and Beug, H. (1992) Transcriptional repression of band 3 and CAII in v-erbA transformed erythroblasts accounts for an important part of the leukemic phenotype. EMBO J., 11, 3355-3366.
29. Golde, D.W., Bersch, N. and Cline, M.J. (1976) Potentiation of erythropoiesis in vitro by dexamethasone. J. Clin. Invest., 57, 57-62.
30. Gorman, C.M., Moffat, L.F and Howard, B.H. (1982) Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol, 2, 1044-1051.
31. Graf, T. (1973) Two types of target cells for transformation with avian myelocytomatosis virus. Virology. 54, 39-413.
32. Grasser, F.A., Graf, T. and Lipsick, J.S. (1991) Protein truncation is required for the activation of the c-myb protooncogene. Mol. Cell. Biol., 11, 3987-3996.
33. Hayman, M.J. and Beug, H. (1992) Avian erythroblastosis: a model system to study oncogene cooperativity in leukemia. Oncogenes in the Development of Leukemia, Cancer Surveys. Imperial Cancer Research Fund. London, Vol. 15, pp. 53-68.
34. Hayman, M.J., Meyer, S., Martin, F., Steinlein, P. and Beug, H. (1993) Self-renewal and differentiation of normal avian erythroid progenitor cells: regulatory roles of the c-erbB/TGFα receptor and the c-kit/SCF receptor. Cell, 74, 157-169.
35. Heck, S., Kullmann, M., Gast, A., Ponta, H., Rahmsdorf, H.J., Herrlich, P. and Cato, A.C. (1994) A distinct modulating domain in glucocorticoid receptor monomers in the repression of activity of the transcription factor AP-1. EMBO J., 13, 4087-4095.
36. Helmberg, A., Auphan, N., Caelles, C. and Karin, M. (1995) Glucocorticoid-induced apoptosis of human leukemic cells is caused by the repressive function of the glucocorticoid receptor. EMBO J., 14, 452-460.
37. Hu, Y.L., Ramsay, R.G., Kanei-Ishii, C., Ishii, S. and Gonda, T.J. (1991) Transformation by carboxyl-deleted Myb reflects increased transactivating capacity and disruption of a negative regulatory domain. Oncogene, 6, 1549-1553.
38. Introna, M., Luchetti, M., Castellano, M., Arsura, M. and Golay, J. (1994) The myb oncogene family of transcription factors: potent regulators of hematopoietic cell proliferation and differentation. Semin. Cancer Biol., 5, 114-125.
39. Jonat, C., Rahmsdorf, H.J., Park, K.K., Cato, A.C., Gebel, S., Ponta, H. and Herrlich, P. (1990) Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell, 62, 1189-1204.
40. 1 and β-majglobin gene expression. Proc. Natl Acad. Sci. USA, 82, 5020-5024.
41. Keller, G. (1992) Hematopoietic stem cells. Curr. Opin. Immunol., 4, 133-139.
42. Khazaie, K., Dull, T.J., Graf, T., Schlessinger, J., Ullrich, A., Beug, H. and Vennstrom, B. (1988) Truncation of the human EGF receptor leads to differential transforming potentials in primary avian fibroblasts and erythroblasts. EMBO J., 7, 3061-3071.
43. Kowenz, E., Leutz, A., Doderlein, G., Graf, T. and Beug, H. (1987) ts-oncogene-transformed erythroleukemic cells: a novel test system for purifying and characterizing avian erythroid growth factors. In Neth, R., Gallo, R.C., Greaves, M.F. and Kabisch, H. (eds). Modern Trends in Human Leukemia VII. New Results in Clinical and Biological Research Including Pediatric Oncology. Springer Verlag, Heidelberg, Vol. 31, pp. 199-209.
44. Liang, R., Chan, T.K. and Todd, D. (1994) Childhood acute lymphoblastic leukemia and aplastic anemia. Leukemia and Lymphoma, 13, 411-415.
45. Mader, S., Kumar, V., de Verneuil, H. and Chambon, P. (1989) Three amino acids of the oestrogen receptor are essential to its ability to distinguish an oestrogen from a glucocorticoid-response element. Nature, 338, 271-274.
46. Mangelsdorff, D.J. et al. (1995) The nuclear receptor superfamily: the second decade. Cell, 83, 835-839.
47. Metz, T. (1994) Oncogenes and erythroid differentiation. Semin. Cancer Biol., 5, 125-135.
48. Mikulits, W., Chen, D. and Müllner, E.W. (1995) Dexamethasone inducible gene expression optimized by glucocorticoid antagonists. Nucleic Acids Res., 23, 2342-2343.
49. Minie, M., Clark, D., Trainor, C., Evans, T., Reitman, M., Hannon, R., Gould, H. and Felsenfeld, G. (1992) Developmental regulation of globin gene expression. J. Cell Sci. Suppl., 16, 15-20.
50. Mucenski, M.L., McLain, K., Kier, A.B., Swerdlow, S.H., Schreiner, C.M., Miller, T.A., Pietryga, D.W., Scott, W.J.,Jr and Potter, S.S. (1991) A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell, 65, 677-689.
51. Muchardt, C. and Yaniv, M. (1993) A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J., 12, 4279-4290.
52. Müller, M. and Renkawitz, R. (1991) The glucocorticoid receptor. Biochim. Biophys. Acta, 1088, 171-182.
53. Müllner, E.W., Dolznig, H. and Beug, H. (1996) Cell cycle regulation and erythroid differentiation. In Vainio, O. and Imhof, B. (eds). Immunology and Developmental Biology of the Chicken. Current Topics in Microbiology and Immunology. Vol. 212, Springer Verlag. New York, pp. 175-194.
54. Pain, B. et al. (1991) EGF-R as a hemopoietic growth factor receptor: the c-erbB product is present in erythrocytic cells. Cell, 65, 37-46.
55. Patel, V.P. and Lodish, H.F. (1987) A fibronectin matrix is required for differentiation of murine erythroleukemia cells into reticulocytes. J. Cell Biol., 105, 3105-3118.
56. Ray, A. and Prefontaine, K.E. (1994) Physical association and functional antagonism between the p65 subunit of transcription factor NFκB and the glucocorticoid receptor. Proc. Natl Acad. Sci. USA. 91, 752-756.
57. Rolink, A. and Melchers, F. (1991) Molecular and cellular origins of B-lymphocyte diversity. Cell. 66, 1081-1094.
58. Sap, J., Munoz, A., Damm, K., Goldberg, Y. Ghysdael, J., Leutz, A., Beug, H. and Vennstrom, B. (1986) The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature, 324, 635-640.
59. Sawada, K., Krantz, S.B., Dai, C.H., Sato, N., Ieko, M., Sakurama, S., Yasukouchi, T. and Nakagawa, S. (1991) Transitional change of colony stimulating factor requirements for erythroid progenitors. J. Cell. Physiol., 149, 1-8.
60. Sawyers, C.L., Denny, C.T. and Witte, O.N. (1991) Leukemia and the disruption of normal hematopoiesis. Cell, 64, 337-350.
61. Schroeder, C., Gibson, L., Zenke, M. and Beug, H. (1992) Modulation of normal erythroid differentiation by the endogenous thyroid hormone and retinoic acid receptors: a possible target for v-erbA oncogene action. Oncogene, 7, 217-227.
62. Schroeder, C., Gibson, L., Nordström, C. and Beug, H. (1993) The estrogen receptor cooperates with the TGFα receptor (c-erbB) in regulation of chicken erythroid progenitor self-renewal. EMBO J., 12, 951-960.
63. Smarda, J., Sugarman, J., Glass, C. and Lipsick, J. (1995) Retinoic acid receptor alpha suppresses transformation by v-myb. Mol. Cell. Biol., 15, 2474-2481.
64. Smit-McBride, Z. and Privalsky, M.L. (1994) DNA sequence specificity of the v-erb A oncoprotein/thyroid hormone receptor: role of the P-box and its interaction with more N-terminal determinants of DNA recognition. Mol. Endocrinol., 8, 819-828.
65. Steinlein, P., Deiner, E.M., Leutz, A. and Beug, H. (1994) Recombinant murine erythropoietin receptor expressed in avian progenitors mediates terminal erythroid differentiation in vitro. Growth Factors. 10, 1-16.
66. Steinlein, P., Wessely, O., Meyer, S., Deiner, E.M., Hayman, M.J. and Beug, H. (1995) Primary, self-renewing erythroid progenitors develop from BFU-E through activation of both tyrosine kinase and steroid hormone receptors. Curr. Biol., 5, 191-204.
67. Thompson, M.A. and Ramsay, R.G. (1995) Myb: an old oncoprotein with new roles. BioEssays, 17, 341-350.
68. Tsai, M.J. and O'Malley, B.W. (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem., 63, 451-486.
69. Tsiftsoglou, A.S., Housman, D. and Wong, W. (1986) The inhibition of commitment of mouse erythroleukemia cells by steroid involves a glucocorticoid-receptor mediated process(es) acting at the nuclear level. Biochim. Biophys. Acta, 889, 251-261.
70. Udupa, K.B., Crabtree, H.M. and Lipschitz, D.A. (1986) In vitro culture of proerythroblasts: characterization of proliferative response to erythropoietin and steroids. Br. J. Haematol, 62, 705-714.
71. Weber, B.L., Westin, E.H. and Clarke, M.F. (1990) Differentiation of mouse erythroleukemia cells enhanced by alternatively spliced c-myb mRNA. Science, 249, 1291-1293.
72. White, R., Lees, J.A., Needham, M., Ham, J. and Parker, M. (1987) Structural organization and expression of the mouse estrogen receptor. Mol. Endocrinol., 1, 735-744.
73. Yoshinaga, S.K., Peterson, C.L., Herskowitz, I. and Yamamoto, K.R. (1992) Roles of SWI1, SWI2 and SWI3 proteins for transcriptional enhancements by steroid receptors. Science, 258, 1598-1604.
74. Zenke, M., Khazaie, K. and Beug, H. (1990a) V-myc transformed macrophages expressing the normal human EGF receptor are induced to proliferate by EGF via a nonautocrine mechanism. In Sachs, L., Abraham, N.G., Wiedermann, C.J., Levine, A.S. and Konwalinka, G. (eds), Molecular Biology of Hematopoiesis. Intercept, Andover, Hampshire, UK, pp. 453-467.
75. Zenke, M., Munoz, A., Sap, J., Vennstrom, B. and Beug, H. (1990b) v-erbA oncogene activation entails the loss of hormone-dependent regulator activity of c-erbA. Cell, 61, 1035-49.
76. Zitnik, G., Peterson K., Stamatoyannopoulos, G. and Papayannopoulou, T. (1995) Effects of butyrate and glucocorticoids on γ- to β-globin gene switching in somatic cell hybrids. Mol. Cell. Biol., 19, 790-795.
77. Zito, G.E. and Lynch, E.C. (1977) Prednisone-responsive congenital erythroid hypoplasia. J. Am. Med. Assoc., 237, 991-992.