TGF-β cooperates with TGF-α to induce the self-renewal of normal erythrocytic progenitors: Evidence for an autocrine mechanism

EMBO Journal

Volumn 18, Issue 10, 1999, Pages 2764-2781

  Gandrillon, Olivier ^a   Schmidt, Uwe ^b   Beug, Hartmut ^b   Samarut, Jacques ^a  

^a UNIVERSITÉ DE LYON   (France)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

Erythropoiesis; Progenitors; Self renewal; Transforming growth factors

Indexed keywords

ANTIBODY; INSULIN; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; BONE MARROW; CELL PROLIFERATION; CHICKEN; ERYTHROCYTE; NONHUMAN; PRIORITY JOURNAL; SERUM; STEM CELL;

ANIMALS; ANTIGENS, SURFACE; BONE MARROW CELLS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL DIFFERENTIATION; CELL DIVISION; CELL SIZE; CHICK EMBRYO; CHICKENS; ERYTHROCYTES; ERYTHROID PROGENITOR CELLS; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; GROWTH SUBSTANCES; INSULIN; MAP KINASE KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; AVES; GALLUS GALLUS;

EID: 0033577694     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.10.2764     Document Type: Article

References (83)

1. Altabef, M., Garcia, M., Lavau, C., Bae, S.-C., Dejean, A. and Samarut, J. (1996) A retrovirus carrying the promyelocyte-retinoic acid receptor PML-RARα fusion gene transforms haematopoietic progenitors in vitro and induces acme leukemia. EMBO J., 15, 2707-2716.
2. Altabef, M., Garcia, M., Varior-Krishnan, G. and Samarut, J. (1997) A truncated RARα co-operates with the v-erbB oncogene to transform early haematopoietic progenitors in vitro and in vivo. Oncogene, 14, 1471-1479.
3. Bagnis, C., Cosset, F.L., Samarut, J., Moscovici, G. and Moscovici, C. (1993) Leukemogenicity of v-myb-transformed monoblasts cells can be modulated by normal bone marrow environment. Oncogene, 8, 737-743.
4. Barnett, J.V., Moustakas, A., Lin, W., Wang, X.F., Lin, H.Y., Galper, J.B. and Maas, R.L. (1994) Cloning and developmental expression of the chick type II and type III TGF β receptors. Dev. Dyn., 199, 12-27.
5. Bauer, A., Mikulits, W., Lagger, G., Stengl, G., Brosch, G. and Beug, H. (1998) The thyroid hormone receptor functions as a ligand-operated developmental switch between proliferation and differentiation of erythroid progenitors. EMBO J., 17, 4291-4303.
6. Beug, H., Doederlein, G., Freudenstein, C. and Graf, T. (1982) Erythroblast cell lines transformed by a temperature-sensitive mutant of avian erythroblastosis virus: a model system to study erythroid differentiation in vitro. J. Cell. Physiol., Suppl. 1. 195-207.
7. Beug, H., Bauer, A., Dolznig, H., Von Lindern, M., Lobmayer, L., Mellitzer, G., Steinlein, P., Wessely, O. and Müllner, E. (1996) Avian erythropoiesis and erythroleukemia: Towards understanding the role of the biomolecules involved. Biochim, Biophys. Acta Rev. Cancer, 1288, M35-M47.
8. Burt, D.W. and Paton, I.R. (1992) Evolutionary origins of the transforming growth factor-β gene family. DNA Cell Biol., 11, 497-510.
9. 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.
10. Chomienne, C., Fenaux, P. and Degos, L. (1996) Retinoid differentiation therapy in promyelocytic leukemia. FASEB J., 10, 1025-1030.
11. Corbel, C., Cormier, F., Pourquie, O. and Bluestein, H.G. (1992) BEN, a novel surface molecule of the immunoglobulin superfamily on avian hemopoietic progenitor cells shared with neural cells. Exp. Cell Res., 203, 91-99.
12. Crawford, S.E., Stellmach, V., Murphy-Ullrich, J.E., Ribeiro, S.M., Lawler, J., Hynes, R.O., Boivin, G.P. and Bouck, N. (1998) Thrombospondin-1 is a major activator of TGF-β1 in vivo. Cell, 93, 1159-1170.
13. Dawson, T. and Wynford-Thomas, D. (1995) Does autocrine growth factor secretion form part of a mechanism which paradoxically protects against tumour development? Br. J. Cancer, 71, 1136-1141.
14. De Larco, J.E. and Todaro, G.J. (1978) Growth factors from murine sarcoma virus-transformed cells. Proc. Natl Acad. Sci. USA, 75, 4001-4005.
15. Dickson, M.C., Martin, J.S., Cousins, F.M. Kulkarni, A.B., Karlsson, S. and Akhurst, R.J. (1995) Defective haematopoiesis and vasculogenesis in transforming growth factor-β1 knock out mice. Development, 121, 1845-1854.
16. 1 correlates with loss of D-cyclin/cdk4 expression and altered cell size control. Cell Growth Differ., 6, 1341-1352.
17. Dudley, D.T., Pang, L., Decker, S.J., Bridges, A.J. and Saltiel, A.R. (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl Acad. Sci. USA, 92, 7686-7689.
18. Dybedal, I. and Jacobsen, S.E. (1995) Transforming growth factor β (TGF-β), a potent inhibitor of erythropoiesis: neutralizing TGF-β antibodies show erythropoietin as a potent stimulator of murine burst-forming unit erythroid colony formation in the absence of a burst-promoting activity. Blood, 86, 949-957.
19. Falk, L.A., De Benedetti, F., Lohrey, N., Birchenall-Roberts, M.C., Ellingsworth, L.W., Faltynek, C.R. and Ruscetti, F.W. (1991) Induction of transforming growth factor-β 1 (TGF-β 1), receptor expression and TGF-β 1 protein production in retinoic acid-treated HL-60 cells: possible TGF-β 1-mediated autocrine inhibition. Blood, 77, 1248-1255.
20. Fiorelli, G. et al. (1994) Role for autocrine TGF-β 1 in regulating differentiation of a human leukemic cell line toward osteoclast-like cells. J. Cell Physiol., 160, 482-490.
21. Fisher, R.C. and Scott, E.W. (1998) Role of PU.1 in hematopoiesis. Stem Cells, 16, 25-37.
22. Flamme, I. and Risau, W. (1992) Induction of vasculogenesis and hematopoiesis in vitro. Development, 116, 435-439.
23. Frampton, J., McNagny, K., Sieweke, M., Philip, A., Smith, G. and Graf, T. (1995) v-Myb DNA binding is required to block thrombocytic differentiation of Myb-Ets-transformed multipotent haematopoietic progenitors. EMBO J., 14, 2866-2875.
24. Freeman, W.M., Walker, S.J. and Vrana, K.E. (1999) Quantitative RT-PCR: pitfalls and potential. Biotechniques, 26, 112-125.
25. Fry, D.W., Kraker, A.J., McMichael, A., Ambroso, L.A., Nelson, J.E., Leopold, W.R., Connors, R.W. and Bridges, A.J. (1994) A specific inhibitor of the epidermal growth factor receptor tyrosine kinase. Science, 265, 1093-1095.
26. Gandrillon, O. and Samarut, J. (1998) Role of the different RAR isoforms in controlling the erythrocytic differentiation sequence. Interference with the v-erbA and p135gap-myb-ets nuclear oncogenes. Oncogene. 16, 563-574.
27. Gandrillon, O., Jurdic, P., Benchaibi, M., Xiao, J.-H., Ghysdael, J. and Samarut, J. (1987) Expression of the v-erb A oncogene in chicken embryo fibroblasts stimulates their proliferation in vitro and enhances tumor growth in vivo. Cell, 49, 687-697.
28. Gandrillon, O., Jurdic, P., Pain, B., Desbois, C., Madjar, J.-J., Moscovici, M.G., Moscovici, C. and Samarut, J. (1989) Expression of the v-erbA product, an altered nuclear hormone receptor, is sufficient to transform erythrocytic cells in vitro but not to induce acute erythroleukemia in vivo, Cell, 58, 115-121.
29. Gandrillon, O., Ferrand, N., Michaille, J.-J., Roze, L., Zile, M.H. and Samarut, J. (1994) c-erbAα/T3R and RARs control commitment of hematopoietic self-renewing progenitor cells to apoptosis or differentiation and are antagonized by the v-erbA oncogene. Oncogene, 9, 749-758.
30. Graf, T., McNagny, K., Brady, G. and Frampton, J. (1992) Chicken 'erythroid' cells transformed by the Gag-Myb-Ets-encoding E26 leukemia virus are multipotent. Cell, 70, 201-213.
31. 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 TGFα/c-erbB and SCF/c-kit receptors. Cell, 74, 157-169.
32. Heldin, C.-H., Miyazono, K. and Dijke, P.T. (1997) TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature, 390, 465-471.
33. Huang, E., Nocka, K., Beier, D.R., Chu, T.Y., Buck, J., Lahm, H.W., Wellner, D., Leder, P. and Besmer, P. (1990) The hematopoietic growth factor KL is encoded by the S1 locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell, 63, 225-233.
34. Keller, J.R., Jacobsen, S.E., Dubois, C.M., Hestdal, K. and Ruscetti, F.W. (1992) Transforming growth factor-beta: a bidirectional regulator of hematopoietic cell growth. Int. J. Cell Cloning, 10, 2-11.
35. Kim, S.J., Angel, P., Lafyatis, R., Hattori, K., Kim, K.Y., Sporn, M.B., Karin, M. and Roberts, A.B. (1990) Autoinduction of transforming growth factor β 1 is mediated by the AP-1 complex. Mol. Cell. Biol., 10, 1492-1497.
36. Kingsley, D.M. (1994) The TGF-β superfamily: new members, new receptors and new genetic tests of function in different organisms. Genes Dev., 8, 133-146.
37. Kohl, N.E. et al. (1994) Protein farnesyltransferase inhibitors block the growth of ras-dependent tumors in nude mice. Proc. Natl Acad. Sci. USA, 91, 9141-9145.
38. Kornfeld, S., Beug, H., Doederlein, G. and Graf, T. (1983) Detection of avian hematopoietic cell surface antigens with monoclonal antibodies to myeloid cells. Their distribution on normal and leukemic cells of various lineages. Exp. Cell Res., 143, 383-394.
39. Kretzschmar, M. and Massagué, J. (1998) SMADs: mediators and regulators of TGF-β signaling. Curr. Opin. Genet. Dev., 8, 103-111.
40. Kretzschmar, M., Doody, J. and Massagué, J. (1997) Opposing BMP and EGF signalling pathways converge on the TGF-β family mediator Smad1. Nature, 389, 618-622.
41. Krystal, G. et al. (1994) Transforming growth factor β 1 is an inducer of erythroid differentiation. J. Exp. Med., 180, 851-860.
42. Lawler, J., Duquette, M., and Ferro, P. (1991) Cloning and sequencing of chicken thrombospondin. J. Biol. Chem., 266, 8039-8043.
43. Leutz, A., Beug, H. and Graf, T. (1984) Purification and characterization of cMGF, a novel chicken myelomonocytic growth factor. EMBO J., 3, 3191-3197.
44. Linnekin, D., Mou, S., Deberry, C.S., Weller, S.R., Keller, J.R., Ruscetti, F.W. and Longo, D.L. (1997) Stem cell factor, the JAK-STAT pathway and signal transduction. Leuk. Lymphoma, 27, 439-444.
45. Majack, R.A., Cook, S.C. and Bornstein, P. (1986) Control of smooth muscle cell growth by components of the extracellular matrix: autocrine role for thrombospondin. Proc. Natl Acad. Sci. USA, 83, 9050-9054.
46. Massagué, J. (1992) Receptors for the TGF-β family. Cell, 69,1067-1070.
47. Massagué, J., Hata, A. and Liu, F. (1997) TGF-β signalling through the Smad pathway. Trends Cell Biol., 7, 187-192.
48. McNagny, K.M., Lim, F., Grieser, S. and Graf, T. (1992) Cell surface proteins of chicken hematopoietic progenitors, thrombocytes and eosinophils detected by novel monoclonal antibodies. Leukemia, 6, 975-984.
49. Mellitzer, G., Wessely, O., Decker, T., Meinke, A., Hayman, M.J. and Beug, H. ( 1996) Activation of Stat 5b in erythroid progenitors correlates with the ability of ErbB to induce sustained cell proliferation. Proc. Natl Acad. Sci. USA, 93, 9600-9605.
50. Metz, T. and Graf, T. (1991a) Fusion of the nuclear oncoproteins v-myb and v-ets is required for the leukemogenicity of E26 virus. Cell, 66, 95-105.
51. Metz, T. and Graf, T. (1991b) v-myb and v-ets transform chicken erythroid cells and cooperate both in trans and in cis to induce distinct differentiation phenotypes. Genes Dev., 5, 369-380.
52. Mizuguchi, T., Kosaka, M. and Saito, S. (1993) Activin A suppresses proliferation of interleukin-3-responsive granulocyte-macrophage colony-forming progenitors and stimulates proliferation and differentiation of interleukin-3-responsive erythroid burst-forming progenitors in the peripheral blood. Blood, 81, 2891-2897.
53. Mullner, E.W., Dolznig, H. and Beug, H. (1996) Cell cycle regulation and erythroid differentiation. Curr. Top. Microbiol. Immunol., 212, 175-194.
54. Muta, K., Krantz, S.B., Bondurant, M.C. and Dai, C.H. (1995) Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood, 86, 572-580.
55. Nohno, T. Sumitomo, S., Ishikawa, T. Ando, C., Nishida, S., Noji, S. and Saito, T. (1993) Nucleotide sequence of a cDNA encoding the chicken receptor protein kinase of the TGF-β receptor family. DNA Seq., 3, 393-396.
56. Oft, M., Peli, J., Rudaz, C., Schwarz, H., Beug, H. and Reichmann, E. (1996) TGFß1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev., 10, 2462-2477.
57. Pain, B. et al. (1991) EGF-R as a hemopoietic growth factor receptor: The c-erbB product is present in normal chicken erythrocytic progenitor cells and controls their self-renewal, Cell, 65, 37-46.
58. Pratsinis, H., Kletsas, D. and Stathakos, D. (1997) Autocrine growth regulation in fetal and adult human fibroblasts. Biochem. Biophys Res. Commun., 237, 348-353.
59. Rascle, A., Gandrillon, O., Cabello, G. and Samarut, J. (1997) The v-erbA oncogene. In Ghysdael, J. and Yaniv, M. (eds), Oncogenes as Transcriplional Regulators. Birkhäuser Publishing Ltd, Basel, Switzerland, pp. 119-165.
60. Reichardt, H.M. et al. (1998) DNA binding of the glucocorticoid receptor is not essential for survival. Cell, 93, 531-541.
61. Roberts, A.B., Lamb, L.C., Newton, D.L., Sporn, M.B., De Larco, J.E. and Todaro, G.J. (1980) Transforming growth factors: isolation of polypeptides from virally and chemically transformed cells by acid/ethanol extraction. Proc. Natl Acad. Sci. USA, 77, 3494-3498.
62. 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.
63. Schmidt, J.A., Marshall, J., Hayman, M.J., Doderlein, G. and Beug, H. (1986a) Monoclonal antibodies to novel erythroid differentiation antigens reveal specific effects of oncogenes on the leukaemic cell phenotype. Leak. Res., 10, 257-272.
64. Schmidt, J.A., Marshall, J., Hayman, J., Ponka, P. and Beug, H. (1986b) Control of erythroid differentiation: possible role of the transferrin cycle. Cell, 46, 41-51.
65. Schroeder, C., Raynoschek, C., Fuhrmann, U., Damm, K., Vennstrom, B. and Beug, H. (1990) The v-erbA oncogene causes repression of erythrocyte-specific genes and an immature, aberrant differentiation phenotype in normal erythroid progenitors. Oncogene, 5, 1445-1453.
66. Schroeder, C., Gibson, L., Nordstrom, C. and Beug, H. (1993) The estrogen receptor cooperates with the TGFa receptor (c-erbB) in regulation of chicken erythroid progenitor self-renewal. EMBO J., 12, 951-960.
67. Solari, F. (1996). Etude de la différenciation ostéoclastique aviaire. PhD thesis, Lyon.
68. Steinlein, P., Wessely, O., Meyer, S., Deine, E.-M., Hayman, M.J. and Beug, H. (1995) Primary, self-renewing erythroid progenitors develop through activation of both tyrosine kinase and steroid hormone receptors. Curr. Biol, 5, 191-204.
69. Stoecklin, E., Wissler, M., Gouilleux, F. and Groner, B. (1996) Functional interactions between Stat5 and the glucocorticoid receptor. Nature, 383, 726-728.
70. Stoecklin, E., Wissler, M., Moriggl, R. and Groner, B. (1997) Specific DNA binding of Stat5, but not of glucocorticoid receptor, is required for their functional cooperation in the regulation of gene transcription. Mol. Cell. Biol, 17, 6708-6716.
71. Tsuji, T., Murata, M., Onomichi, K., Eto, Y. and Shibai, H. (1988) Structural and biological identity of recombinant EDF (erythroid differentiation factor) with natural EDF. Agric. Biol. Chem., 52, 2143-2148.
72. Ulrich, E., Boehmelt, G., Bird, A. and Beug, H. (1992) Immortalization of conditionally transformed chicken cells: loss of normal p53 expression is an early step that is independent of cell transformation. Genes Dev., 6, 876-887.
73. von Lindern, M., Zauner, W., Steinlein, P., Mellitzer, G., Fritsch, G., Huber, K., Löwenberg, B. and Beug, H. (1999) Human erythropoiesis: The glucocorticoid receptor cooperates with the Epo-receptor and c-Kil to induce long-term proliferation of erythroid progenitors. Blood, in press.
74. Wakeling, A.E. (1989) The potential for a novel pure anti-oestrogen. Horm. Res., 1, 257-259.
75. Wang, C.Q., Udupa, K.B. and Lipschitz, D.A. (1992) The role of macrophages in the regulation of erythroid colony growth in vitro. Blood, 80, 1702-1709.
76. Wessely, O., Deiner, E.M., Beug, H. and von Lindern, M. (1997a) The glucocorticoid receptor is a key regulator of the decision between self-renewal and differentiation in erythroid progenitors. EMBO J., 16, 267-280.
77. Wessely, O., von Lindern, M., Levitzki, A., Gazit, A., Ischenko, I., Mellitzer, G., Hayman, M.J. and Beug, H. (1997b) Distinct regulatory roles of the receptor tyrosine kinases c-ErbB and c-Kit in erythroid differentiation and proliferation. Cell Growth Differ., 8, 481-93.
78. Wessely, O., Deiner, E.M., Lim, K.C. Mellitzer, G., Steinlein, P. and Beug, H. (1998) Mammalian granulocyte-macrophage colony-stimulating factor receptor expressed in primary avian hematopoietic progenitors: lineage-specific regulation of proliferation and differentiation. J. Cell Biol. 141, 1041-1051.
79. Wessely, O., Bauer, A., Tran Quang, C., Deiner, E.M., von Lindern, M., Mellitzer, G., Steinlein, P., Ghysdael, J. and Beug, H. (1999) A novel way to induce erythroid progenitor self renewal: cooperation of c-Kit with the erythropoietin receptor. Biol. Chem. (Hoppe Seyler), 380, 187-202.
80. Wrana, J.L., Attisano, L., Carcamo, J., Zentella, A., Doody, J., Laiho, M., Wang, X.F. and Massague, J. (1992) TGFβ signals through a heteromeric protein kinase receptor complex. Cell, 71, 1003-1014.
81. Wu, H., Liu, X., Jaenisch, R. and Lodish, H.F. (1995) Generation of committed erythroid BFU-E and CFU-E progenitors does not require erylhropoietin or the erythropoietin receptor. Cell, 83, 59-67.
82. Zeng, G., McCue, H.M., Mastrangelo, L. and Millis, A.J. (1996) Endogenous TGF-beta activity is modified during cellular aging: effects on metalloproteinase and TIMP-1 expression. Exp. Cell Res., 228, 271-276.
83. Zhang, Y., Feng, X.-H. and Derynck, R. (1998) Smad3 and Smad4 cooperate with c-jun/c-fos to mediate TGF-β-induced transcription. Nature, 394, 909-913.