Distinct roles of the receptor tyrosine kinases c-ErbB and c-Kit in regulating the balance between erythroid cell proliferation and differentiation

Cell Growth and Differentiation

Volumn 8, Issue 5, 1997, Pages 481-493

  Wessely, Oliver ^a   Mellitzer, Georg ^a   Von Lindern, Marieke ^a   Levitzki, Alexander ^b   Gazit, Aviv ^b   Ischenko, Irene ^c   Hayman, Michael J ^c   Beug, Hartmut ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; ONCOPROTEIN; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; EMBRYO; ENZYME ACTIVITY; ERYTHROPOIESIS; GROWTH REGULATION; HEMATOPOIETIC STEM CELL; NONHUMAN; ONCOGENE C KIT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CHICK EMBRYO; ERYTHROBLASTS; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION;

ANIMALIA; AVES; UNIDENTIFIED RETROVIRUS;

EID: 0030967303     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Till, J. E., and McCulloch, E. A. Hematopoietic stem cell differentiation. Biochim. Biophys. Acta, 605: 431-459, 1980.
2. Keller, G. Hematopoietic stem cells. Curr. Opin. Immunol., 4: 133-139, 1992.
3. Boulay, J. L., and Paul, W. E. Hematopoietin subfamily classification based on size, gene organization and sequence homology. Curr. Biol., 3: 573-581, 1993.
4. Sawyers, C. L., Denny, C. T., and Witte, O. N. Leukemia and the disruption of normal hematopoiesis. Cell, 64: 337-350, 1991.
5. Downward, J., Yarden, Y., Mayes, E., Scrace, G., Totty, N., Stockwell, P., Ullrich, A., Schlessinger, J., and Waterfield, M. D. Close similarity of epidermal growth factor receptor and v-erbB oncogene protein sequences. Nature (Lond.), 307: 521-527, 1984.
6. Sap, J., Munoz, A., Damm, K., Goldberg, Y., Ghysdael, J., Leutz, A., Beug, H., and Vennström, B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature (Lond.), 324: 635-640, 1986.
7. Beug, H., Müllner, E. W., and Hayman, M. J. Insights into erythroid differentiation obtained from studies on avian erythroblastosis virus. Curr. Opin. Cell Biol., 6: 816-824, 1994.
8. Steinlein, P., Wessely, O., Meyer, S., Deiner, E. M., Hayman, M. J., and Beug, H. Primary, self-renewing erythroid progenitors develop from BFU-E through activation of both tyrosine kinase and steroid hormone receptors. Curr. Biol., 5: 191-204, 1995.
9. Wessely, O., Deiner, E. M., Beug, H., and von Lindern, M. The glucocorticoid receptor is a key regulator of the decision between self renewal and differentiation in erythroid progenitors. EMBO J., in press, 1997.
10. Beug, H., Kahn, P., Doederlein, G., Hayman, M. J., and Graf, T., Characterization of hematopoietic cells transformed in vitro by AEV-H, a v-erbB-containing avian erythroblastosis virus. In: R. Neth, R. Gallo, M. Greaves, and K. Janka (eds.), Modern Trends in Human Leukaemia VI, Haematol. Blood Transfusion, Vol. 29, pp. 284-289. Berlin: Springer Verlag, 1985.
11. Knight, J., Zenke, M., Disela, C., Kowenz, E., Vogt, P., Engel, J. D., Hayman, M. J., and Beug, H. Temperature-sensitive v-sea transformed erythroblasts: a model system to study gene expression during erythroid differentiation. Genes Dev., 2: 247-258, 1988.
12. Hayman, M. J., Meyer, S., Martin, F., Steinlein, P., and Beug, H. 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, 1993.
13. Schroeder, C., Gibson, L., Nordström, C., and Beug, H. The estrogen receptor cooperates with the TGFα receptor (c-erbB) in regulation of chicken erythroid progenitor self renewal. EMBO J., 12: 951-960, 1993.
14. Hayman, M. J., Meyer, S., Martin, F., Steinlein, P., and Beug, H. Self-renewal and differentiation of normal avian erythroid progenitor cells: regulatory roles of the TGF α/c-ErbB and SCF/c-kit receptors. Cell, 74: 157-169, 1993.
15. Dolznig, H., Bartunek, P., Nasmyth, K., Müllner, E., and Beug, H. 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, 1995.
16. Beug, H., Doederlein, G., and Zenke, M., Transformation by v-erbA and v-erbB oncogenes: independent modulation of differentiation and proliferation in erythroid progenitors. In: P. A. Sharp (ed.), Nuclear Processes and Oncogenes, Bristol-Myers Squibb Cancer Symposia, 14, pp. 53-84. San Diego: Harcourt Brace Jovanovich, 1992.
17. McNiece, I. K., Langley, K. E., and Zsebo, K. M. Recombinant human stem cell factor synergizes with MG-CSF, G-CSF, II-3 and Epo to stimulate human progenitor cells of the myeloid and erythroid lineages. Exp. Hematol., 79: 226-231, 1991.
18. Broxmeyer, H. E., Cooper, S., Lu, I., Hancog, G., Anderson, D., and Cosman, H. Effect of murine mast cell growth factor (c-Kit protooncogene ligand) on colony formation by human marrow hematopoietic progenitor cells. Blood, 77: 2142-2149, 1991.
19. Muta, K., Krantz, S. B., Bondurant, M. C., and Dai, C. H. Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood, 86: 572-580, 1995.
20. Broxmeyer, H. E., Maze, R., Miyazawa, K., Carow, C., Hendrie, P. C., Cooper, S., Hangoc, G., Vadhan, R. S., and Lu, L. The kit receptor and its ligand, steel factor, as regulators of hemopoiesis. Cancer Cells, 3: 480-487, 1991.
21. Lin, C. S., Lim, S. K., D'Agati, V., and Costatini, F. Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev., 10: 154-164, 1996.
22. Dikic, I., Schlessinger, J., and Lax, I. PC12 cells overexpressing the insulin receptor undergo insulin-dependent neuronal differentiation. Curr. Biol., 4: 702-708, 1994.
23. Traverse, S., Seedorf, K., Paterson, H., Marshall, C. J., Cohen, P., and Ullrich, A. EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Curr. Biol., 4: 694-701, 1994.
24. Meyer, S., LaBudda, K., McGlade, I., and Hayman, M. J. Analysis of the role of the SHC and Grb-2 proteins in signal transduction by the v-erbB protein. Mol. Cell. Biol., 14: 3253-3262, 1994.
25. Mellitzer, G., Wessely, O., Decker, T., Eilers, A., Hayman, M. J., and Beug, H. 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, 1996.
26. Beug, H., Palmieri, S., Freudenstein, C., Zentgraf, H., and Graf, T. Hormone-dependent terminal differentiation in vitro of chicken erythroleukemia cells transformed by ts mutants of avian erythroblastosis virus. Cell, 28: 907-919, 1982.
27. Testa, U., Pelosi, E., Gabbianelli, M., Fossati, C., Campisi, S., Isacchi, G., and Peschle, C. Cascade transactivation of growth factor receptors in early human hematopoiesis. Blood, 81: 1442-1456, 1993.
28. Beug, H., Schroeder, C., Wessely, O., Meyer, S., Ischenko, I. D., Deiner, E., and Hayman, M. J. Tyrosine kinase oncogenes transform erythroid progenitors by functionally replacing endogenous receptor kinase function. Cell Growth & Differ., 6: 999-1008, 1995.
29. Pain, B., Melet, F., Saez, J., Flickinger, T., Raines, M., Peyrol, S., Moscovici, C., Moscovici, M. G., Kung, H-J., Jurdic, P., Lazarides, F., and Samarut, J. EGF-R as a hemopoietic growth factor receptor: the c-erbB product is present in erythrocytic cells. Cell, 65: 37-46, 1991.
30. Gazit, A., Osherov, N., Posner, I., Bar, S. A., Gilon, C., and Levitzki, A. Tyrphostins 3. Structure-activity relationship studies of α-substituted benzylidenemalononitrile 5-S-aryltyrphostins. J. Med. Chem., 36: 3556-3364, 1993.
31. Osherov, N., Gazit, A., Gilon, C., and Levitzki, A. Selective inhibition of the epidermal growth factor and HER2/neu receptors by tyrphostins. J. Biol. Chem., 268: 11134-11142, 1993.
32. Posner, I., Engel, M., Gazit, A., and Levitzki, A. Kinetics of inhibition by tyrphostins of the tyrosine kinase activity of the epidermal growth factor receptor and analysis by a new computer program. Mol. Pharmacol., 45: 673-683, 1994.
33. Anafi, M., Gazit, A., Zehavi, A., Ben, N. Y., and Levitzki, A. Tyrphostin-induced inhibition of p210bcr-abl tyrosine kinase activity induces K562 to differentiate. Blood, 82: 3524-3529, 1993.
34. Gazit, A., Osherov, N., Posner, I., Yaish, R., Poradosu, E., Gilon, C., and Levitzki, A. Tyrphostins 2. Heterocyclic and α-substituted benzonemaloronitrile tyrphostins as potent inhibitors of EGF-receptor and ErbB2/ neu tyrosine kinases. J. Med. Chem., 34: 1897-1907, 1991.
35. Schmidt, J. A., Marshall, J., Hayman, M. J., Ponka, P., and Beug, H. Control of erythroid differentiation: possible role of the transferrin cycle. Cell, 46: 41-51, 1986.
36. Ihle, J. N., and Kerr, I. M. Jaks, and Stats in signaling by the cytokine receptor superfamily. Trends Genet., 11: 69-74, 1995.
37. Crowe, A. J., McGlade, J., Pawson, T., and Hayman, M. J. Phosphorylation of the SHC proteins on tyrosine correlates with the transformation of fibroblasts and erythroblasts by the v-sea tyrosine kinase. J. Virol., 68: 1837-1842, 1994.
38. Dai, C. H., Krantz, S. B., and Zsebo, K. M. Human burst-forming units-erythroid need direct interaction with stem cell factor for further development. Blood, 78: 2493-2497, 1991.
39. Sawada, K., Krantz, S. B., Kans, J. S., Dessypris, E. N., Sawyer, S. T., Glick, A. D., and Civin, C. I. Purification of human erythroid colony forming units and demonstration of specific binding of erythropoietin. J. Clin. Invest., 80: 357-366, 1987.
40. Brannan, C. I., Lyman, S. D., Williams, D. E., Eisenman, J., Anderson, D. M., Cosman, D., Bedell, M. A., Jenkins, N. A., and Copeland, N. G. Steel-Dickie mutation encodes a c-kit ligand lacking transmembrane and cytoplasmic domains. Proc. Natl. Acad. Sci. USA, 88: 4671-4674, 1991.
41. Flanagan, J. G., Chan, D. C., and Leder, P. Transmembrane form of the kit ligand growth factor is determined by alternative splicing and is missing in the Sld mutant. Cell, 64: 1025-1035, 1991.
42. Dolci, S., Williams, D. E., Ernst, M. K., Resnick, J. L., Brannan, C. I., Lock, L. F., Lyman, S. D., Boswell, H. S., and Donovan, P. J. Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature (Lond.), 352: 809-811, 1991.
43. Murphy, M., Reid, K., Williams, D. E., Lyman, S. D., and Bartlett, P. F. Steel factor is required for maintenance, but not differentiation, of melanocyte precursors in the neural crest. Dev. Biol., 153: 396-401, 1992.
44. Broudy, V. C., Morgan, D. A., Lin, N., Zsebo, K. M., Jacobsen, F. W., and Papayannopoulou, T. Stem cell factor influences the proliferation and erythroid differentiation of the MB-02 human erythroleukemia cell line by binding to a high-affinity c-kit receptor. Blood, 82: 436-444, 1993.
45. Chao, M. V. Growth factor signaling: where is the specificity? Cell, 68: 995-997, 1992.
46. Rabin, S. J., Cleghon, V., and Kaplan, D. R. SNT, a differentiation-specific target of neurotrophic factor-induced tyrosine kinase activity in neurons and PC12 cells. Mol. Cell. Biol., 13: 2203-2213, 1993.
47. Traverse, S., Gomez, N., Paterson, H., Marshall, C., and Cohen, P. Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J., 288: 351-355, 1992.
48. Yaish, P., Gazit, A., Gilon, C., and Levitzki, A. Blocking of EGF-dependent cell proliferation by EGF receptor kinase inhibitors. Science (Washington DC), 242: 933-935, 1988.
49. Levitzki, A., and Gazit, A. Tyrosine kinase inhibition: an approach to drug development. Science (Washington DC), 267: 1782-1788, 1995.
50. Kovalenko, M., Gazit, A., Bohmer, A., Rorsman, C., Ronnstrand, L., Heldin, C. H., Waltenberger, J., Bohmer, F. D., and Levitzki, A. Selective platelet-derived growth factor receptor kinase blockers reverse sis-transformation. Cancer Res., 54: 6106-6114, 1994.
51. Osherov, N., and Levitzki, A. Epidermal growth factor-dependent activation of the src-family kinases. Eur. J. Biochem., 225: 1047-1053, 1994.
52. Groner, B., and Gouilleux, F. Prolactin-mediated gene activation in mammary epithelial cells. Curr. Opin. Gen. Dev., 5: 587-594, 1995.
53. Mui, A. L., Wakao, H., O'Farrell, A. M., Harada, N., and Miyajima, A. Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two STATS homologs. EMBO J., 14: 1166-1175, 1995.
54. Wakao, H., Harada, N., Kitamura, T., Mui, A. L., and Miyajima, A. Interleukin 2 and erythropoietin activate STAT5/MGF via distinct pathways. EMBO J., 14: 2527-2535, 1995.
55. Steinlein, P., Deiner, E. M., Leutz, A., and Beug, H. Recombinant murine erythropoietin receptor expressed in avian progenitors mediates terminal erythroid differentiation in vitro. Growth Factors, 10: 1-16, 1994.
56. Beug, H., Bartunek, P., Steinlein, P., and Hayman, M. J. Avian hematopoietic cell culture: in vitro model systems to study the oncogenic transformation of hematopoietic cells. In: P. K. Vogt and I. M. Verma (eds.), Oncogene Techniques, Methods in Enzymology, Vol. 235, pp. 41-76. New York: Academic Press, Inc., 1995.
57. Ulrich, E., Boehmelt, G., Bird, A., and Beug, H. 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, 1992.
58. Fuerstenberg, S., Leitner, I., Schroeder, C., Schwarz, H., Vennström, B., and Beug, H. 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, 1992.
59. Zenke, M., Munoz, A., Sap, J., Vennström, B., and Beug, H. v-erbA oncogene activation entails the loss of hormone-dependent regulator activity of c-erbA. Cell, 61: 1035-1049, 1990.
60. Leutz, A., Beug, H., and Graf, T. Purification and characterization of cMGF, a novel chicken myelomonocytic growth factor. EMBO J., 3: 3191-3197, 1984.
61. Kowenz, E., Leutz, A., Doederlein, G., Graf, T., and Beug, H., ts-oncogene-transformed erythroleukemic cells: a novel test system for purifying and characterizing avian erythroid growth factors. In: R. Neth, R. C. Gallo, M. F. Greaves, and H. Kabisch (eds.), Modern Trends in Human Leukemia VII, Haematol. Blood Transfusion, Vol. 31, pp. 199-209. Heidelberg: Springer Verlag, 1987.
62. Crowe, A. J., and Hayman, M. J. Altered glycosylation of the env-sea oncoprotein inhibits intracellular transport and transformation. J. Virol., 65: 6173-6180, 1991.
63. Schroeder, C., Gibson, L., Zenke, M., and Beug, H. 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, 1992.
64. Gale, N. W., Kaplan, S., Lowenstzein, E. J., J., S., and Bar-Sagi, D. Grb-2 mediates the EGF-dependent activation of guanine-nucleotide exchange on Ras. Nature (Lond.), 363: 88-92, 1993.
65. Wu, H., Klingmüller, V., Besmer, P., and Lodish, H. F. Interaction of the erythropoietin and stem cell factor receptors. Nature (Lond.), 377: 242-246, 1995.