Stem cell factor inhibits erythroid differentiation by modulating the activity of G1-cyclin-dependent kinase complexes: A role for p27 in erythroid differentiation coupled G1 arrest

Cell Growth and Differentiation

Volumn 11, Issue 5, 2000, Pages 269-277

  Tamir, Ami ^a,b   Petrocelli, Teresa ^a   Stetler, Kendra ^a   Chu, Wendy ^a   Howard, Jeff ^a,c   St Croix, Brad ^a   Slingerland, Joyce ^a   Ben David, Yaacov ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE; CYCLIN E; ERYTHROPOIETIN; PROTEIN P15; PROTEIN P27; STEM CELL FACTOR;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROBLAST; ERYTHROID CELL; ERYTHROLEUKEMIA CELL; GENE EXPRESSION; GENE TARGETING; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; CDC2-CDC28 KINASES; CDC25 PHOSPHATASE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CYCLIN A; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE 6; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; CYCLINS; DOWN-REGULATION; ERYTHROCYTES; G1 PHASE; LEUKEMIA, ERYTHROBLASTIC, ACUTE; MICE; MICE, INBRED BALB C; MICROTUBULE-ASSOCIATED PROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; S PHASE; STEM CELL FACTOR; TRANSFECTION; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA;

EID: 0034093121     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Orkin, S. H. Transcription factors and hematopoietic development. J. Biol. Chem., 270: 4955-4958, 1995.
2. Marks, P. A., Richon, V. M., Kiyokawa, H., and Rifkind, R. A. Inducing differentiation of transformed cells with hybrid polar compounds: a cell cycle-dependent process. Proc. Natl. Acad. Sci. USA, 91: 10251-10254, 1994.
3. Tamir, A., Howard, J., Higgins, R. R., Li, Y. J., Berger, L., Zacksenhaus, E., Reis, M., and Ben-David, Y. Fli-1, an ets-related transcription factor, regulates erythropoietin-induced erythroid proliferation and differentiation: evidence for direct transcriptional repression of the Rb gene during differentiation. Mol. Cell. Biol., 19: 4452-4464, 1999.
4. Dranoff, G., Crawford, A. D., Sadelain, M., Ream, B., Rashid, A., Bronson, R. T., Dickersin, G. R., Bachurski, C. J., Mark, E. L., and Whitsett, J. A. Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis. Science (Washington DC), 264: 713-716, 1994.
5. Stanley, E., Lieschke, G. J., Grail, D., Metcalf, D., Hodgson, G., Gall, J. A., Maher, D. W., Cebon, J., Sinickas, V., and Dunn, A. R. Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc. Natl. Acad. Sci. USA, 91: 5592-5596, 1994.
6. Nishinakamura, R., Nakayama, N., Hirabayashi, Y., Inoue, T., Aud, D., McNeil, T., Azuma, S., Yoshida, S., Toyoda, Y., and Arai, K. Mice deficient for the IL-3/GM-CSF/IL-5 βc receptor exhibit lung pathology and impaired immune response, while β IL3 receptor-deficient mice are normal. Immunity, 2: 211-222, 1995.
7. Bernstein, A., Forrester, L., Reith, A. D., Dubreuil, P., and Rottapel, R. The murine W/c-kit and Steel loci and the control of hematopoiesis. Semin. Hematol., 28: 138-142, 1991.
8. Wu, H., Liu, X., Jaenisch, R., and Lodish, H. F. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell, 83: 59-87, 1995.
9. Lin, C. S., Lim, S. K., D'Agati, V., and Costantini, F. Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev., 10: 154-164, 1996.
10. Kieran, M. W., Perkins, A. C., Orkin, S. H., and Zon, L. I. Thrombo-poietin rescues in vitro erythroid colony formation from mouse embryos lacking the erythropoietin receptor. Proc. Natl. Acad. Sci. USA, 93: 9126-9131, 1996.
11. Melloni, E., Pontremoli, S., Michetti, M., Sacco, O., Cakiroglu, A. G., Jackson, J. F., Rifkind, R. A., and Marks, P. A. Protein kinase C activity and hexamethylenebisacetamide-induced erythroleukemia cell differentiation. Proc. Natl. Acad. Sci. USA, 84: 5282-5286, 1987.
12. Kiyokawa, H., Richon, V. M., Rifkind, R. A., and Marks, P. A. Suppression of cyclin-dependent kinase 4 during induced differentiation of erythroleukemia cells. Mol. Cell. Biol., 14: 7195-7203, 1994.
13. Sherr, C. J. Cancer cell cycles. Science (Washington DC), 274: 1672-1677, 1996.
14. Morgan, D. O. Principles of CDK regulation. Nature (Lond.), 374: 131-134, 1995.
15. Sherr, C. J., and Roberts, J. M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev., 9: 1149-1163, 1995.
16. Sherr, C. J. Mammalian G1 cyclins. Cell, 73: 1059-1065, 1993.
17. Akiyama, T., Ohuchi, T., Sumida, S., Matsumoto, K., and Toyoshima, K. Phosphorylation of the retinoblastoma protein by cdk2. Proc. Natl. Acad. Sci. USA, 89: 7900-7904, 1992.
18. Taya, Y., Yasuda, H., Kamijo, M., Nakaya, K., Nakamura, Y., Obba, Y., and Nishimura, S. In vitro phosphorylation of the tumor suppressor gene RB protein by mitosis-specific histone H1 kinase. Biochem. Biophys. Res. Commun., 164: 580-586, 1989.
19. Lees, J. A., Buchkovich, K. J., Marshak, D. R., Anderson, C. W., and Harlow, E. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J., 10: 4279-4290, 1991.
20. Lin, B. T., Gruenwald, S., Morla, A. O., Lee, W. H., and Wang, J. Y. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase. EMBO J., 10: 857-864, 1991.
21. Weinberg, R. A. Tumor suppressor genes. Science (Washington DC), 254: 1138-1146, 1991.
22. Buchkovich, K., Duffy, L. A., and Harlow, E. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell, 58: 1097-1105, 1989.
23. Chen, P. L., Scully, P., Shew, J. Y., Wang, J. Y., and Lee, W. H. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell, 58: 1193-1198, 1989.
24. DeCaprio, J. A., Ludlow, J. W., Lynch, D., Furukawa, Y., Griffin, J., Piwnica-Worms, H., Huang, C. M., and Livingston, D. M. The product of the retinoblastoma susceptibility gene has properties of a cell cycle regulatory element. Cell, 58: 1085-1095, 1989.
25. Mihara, K., Cao, X. R., Yen, A., Chandler, S., Driscoll, B., Murphree, A. L., T'Ang, A., and Fung, Y. K. Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product. Science (Washington DC), 246: 1300-1303, 1989.
26. Hiebert, S. W., Chellappan, S. P., Horowitz, J. M., and Nevins, J. R. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev., 6: 177-185, 1992.
27. Weintraub, S. J., Prater, C. A., and Dean, D. C. Retinoblastoma protein switches the E2F site from positive to negative element. Nature (Lond.), 358: 259-261, 1992.
28. McNiece, I. K., Langley, K. E., and Zsebo, K. M. Recombinant human stem cell factor synergises with GM-CSF, G-CSF, IL-3 and epo to stimulate human progenitor cells of the myeloid and erythroid lineages. Exp. Hematol., 19: 226-231, 1991.
29. Migliaccio, G., Migliaccio, A. R., Druzin, M. L., Giardina, P. J., Zsebo, K. M., and Adamson, J. W. Effects of recombinant human stem cell factor (SCF) on the growth of human progenitor cells in vitro. J. Cell. Physiol., 148: 503-509, 1991.
30. Kiyokawa, H., Busquets, X., Powell, C. T., Ngo, L., Rifkind, R. A., and Marks, P. A. Cloning of a D-type cyclin from murine erythroleukemia cells. Proc. Natl. Acad. Sci. USA, 89: 2444-2447, 1992.
31. St. Croix, B., Sheehan, C., Rak, J. W., Florenes, V. A., Slingerland, J. M., and Kerbel, R. S. E-Cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27(KIP1). J. Cell. Biol., 142: 557-571, 1998.
32. Kiyokawa, H., Kineman, R. D., Manova-Todorova, K. O., Soares, V. C., Hoffman, E. S., Ono, M., Khanam, D., Hayday, A. C., Frohman, L. A., and Koff, A. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell, 85: 721-732, 1996.
33. Fero, M. L., Rivkin, M., Tasch, M., Porter, P., Carow, C. E., Firpo, E., Polyak, K., Tsai, L. H., Broudy, V., Perlmutter, R. M., Kaushansky, K., and Roberts, J. M. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell, 85: 733-744, 1996.
34. Nakayama, K., Ishida, N., Shirane, M., Inomata, A., Inoue, T., Shishido, N., Horii, I., and Loh, D. Y. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell, 85: 707-720, 1996.
35. Durand, B., Gao, F. B., and Raff, M. Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J., 16: 306-317, 1997.
36. Solomon, M. J., and Kaldis, P. Regulation of CDKs by phosphorylation. Results Prob. Cell Differ., 22: 79-109, 1998.
37. Jinno, S., Suto, K., Nagata, A., Igarashi, M., Kanaoka, Y., Nojima, H., and Okayama, H. Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J., 13: 1549-1556, 1994.
38. Hoffman, B., and Liebermann, D. A. The proto-oncogene c-myc and apoptosis. Oncogene, 17: 3351-3357, 1998.
39. Galaktionov, K., Chen, X., and Beach, D. Cdc25 cell-cycle phosphatase as a target of c-myc. Nature (Lond.), 332: 511-517, 1996.
40. Weinberg, R. A. The retinoblastoma protein and cell cycle control. Cell, 81: 323-330, 1995.
41. Magnaghi-Jaulin, L., Groisman, R., Naguibneva, I., Robin, P., Lorain, S., Le Villain, J. P., Troalen, F., Trouche, D., and Harel-Bellan, A. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature (Lond.), 391: 601-605, 1998.
42. Brehm, A., Miska, E. A., McCance, D. J., Reid, J. L., Bannister, A. J., and Kouzarides, T. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature (Lond.), 391: 597-601, 1998.
43. Kiess, M., Gill, R. M., and Hamel, P. A. Expression of the positive regulator of cell cycle progression, cyclin D3, is induced during differentiation of myoblasts into quiescent myotubes. Oncogene, 10: 159-166, 1995.
44. LaBaer, J., Garrett, M. D., Stevenson, L. F., Slingerland, J. M., Sandhu, C., Chou, H. S., Fattaey, A., and Harlow, E. New functional activities for the p21 family of CDK inhibitors. Genes Dev., 11: 847-862, 1997.
45. Cheng, M., Olivier, P., Diehl, J. A., Fero, M., Roussel, M. F., Roberts, J. M., and Sherr, C. J. The p21(Cip1) and p27(Kip1) CDK "inhibitors" are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J., 78: 1571-1583, 1999.
46. Koyama, H., Raines, E. W., Bornfeldt, K. E., Roberts, J. M., and Ross, R. Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell, 87: 1069-1078, 1996.
47. Wang, Q. M., Jones, J. B., and 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., 56: 264-267, 1996.
48. Chen, Y., Robles, A. I., Martinez, L A., Liu, F., Gimenez-Conti, I. B., and Conti, C. J. Expression of G1 cyclins, cyclin-dependent kinases, and cyclin-dependent kinase inhibitors in androgen-induced prostate proliferation in castrated rats. Cell Growth Differ., 7: 1571-1578, 1996.
49. Baldassarre, G., Barone, M. V., Belletti, B., Sandomenico, C., Bruni, P., Spiezia, S., Boccia, A., Vento, M. T., Romano, A., Pepe, S., Fusco, A., and Viglietto, G. Key role of the cyclin-dependent kinase inhibitor p27kip1 for embryonal carcinoma cell survival and differentiation. Oncogene, 18: 6241-6251, 1999.
50. Sherr, C. J., and Roberts, J. M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev., 13: 1501-1512, 1999.
51. Serve, H., Yee, N. S., Stella, G., Sepp-Lorenzino, L., Tan, J. C., and Besmer, P. Differential roles of PI3-kinase and Kit tyrosine 821 in Kit receptor-mediated proliferation, survival and cell adhesion in mast cells. EMBO J., 14: 473-483, 1995.
52. Wu, H., Klingmuller, U., Besmer, P., and Lodish, H. F. Interaction of the erythropoietin and stem-cell-factor receptors. Nature (Lond.), 377: 242-243, 1995.
53. Seshasayee, D., Gaines, P., and Wojchowski, D. M. GATA-1 dominantly activates a program of erythroid gene expression in factor-dependent myeloid FDCW2 cells. Mol. Cell. Biol., 78: 3278-3288, 1998.
54. Tsai, S., Bartelmez, S., Sitnicka, E., and Collins, S. Lymphohematopoietic progenitors immortalized by a retroviral vector harboring a dominant-negative retinoic acid receptor can recapitulate lymphoid, myeloid, and erythroid development. Genes Dev., 8: 2831-2841, 1994.
55. Selten, G., Cuypers, H. T., Zijlstra, M., Melief, C., and Berns, A. Involvement of c-myc in MuLV induced T cell lymphomas in mice: frequency and mechanism of activation. EMBO J., 3: 3215-3222, 1984.
56. Dulic, V., Lees, E., and Reed, S. I. Association of human cyclin E with a periodic G1-S phase protein kinase. Science (Washington DC), 257: 1958-1961, 1992.
57. Petrocelli, T., Poon, R., Drucker, D. J., Slingertand, J. M., and Rosen, C. F. UVB radiation induces p21 Cip1/WAF1 and mediates G1 and S phase checkpoints. Oncogene, 12: 1387-1396, 1996.