Thrombopoietin-induced polyploidization of bone marrow megakaryocytes is due to a unique regulatory mechanism in late mitosis

Journal of Cell Biology

Volumn 139, Issue 2, 1997, Pages 449-457

  Nagata, Yuka ^a   Muro, Yoshinao ^b   Todokoro, Kazuo ^a  

^a RIKEN TSUKUBA INSTITUTE   (Japan)

^b NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MICROTUBULE PROTEIN; THROMBOPOIETIN;

ANAPHASE; ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CENTROSOME; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; MEGAKARYOCYTE; METAPHASE; MITOSIS; MITOSIS SPINDLE; MOUSE; NONHUMAN; POLYPLOIDY; PRIORITY JOURNAL; PROPHASE; SISTER CHROMATID;

ANAPHASE; ANIMALS; ANTIBODIES, MONOCLONAL; BONE MARROW CELLS; CELL CYCLE; CENTROSOME; DNA REPLICATION; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; INDOLES; MEGAKARYOCYTES; METAPHASE; MICE; MICE, INBRED STRAINS; MITOSIS; MITOTIC SPINDLE APPARATUS; NUCLEAR ENVELOPE; POLYPLOIDY; PROPHASE; RECOMBINANT PROTEINS; THROMBOPOIETIN; TUBULIN;

EID: 0030727534     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.2.449     Document Type: Article

References (45)

1. Adachi, M., R. Ryo, T. Sato, and N. Yamaguchi. 1991. Platelet factor 4 gene expression in a human megakaryocytic leukemia cell line (CMK) and its differentiated subclone (CMK11-5). Exp. Hematol. 19:923-927.
2. Angchaisuksiri, P., P.L. Carlson, and E.N. Dessypris. 1996. Effects of recombinant human thrombopoietin on megakaryocyte colony formation and megakaryocyte ploidy by human CD34+ cells in a serum-free system. Br. J. Haematol. 93:13-17.
3. Bartley, T.D., J. Bogenberger, P. Hunt, Y.S, Li, H.S. Lu. F. Martin, M.S. Chang, B Samal, J.L. Nichol, S. Swift, et al. 1994. Identification and cloning of a megakaryocyte growth and development factor that is a ligand for the cytokine receptor Mp1. Cell. 77:1117-1124.
4. Broudy, V.C., N.L. Lin, and K. Kaushansky. 1995. Thrombopoietin (c-mpl ligand) acts synergistically with erythropoietin, stem cell factor, and interleu-kin-11 to enhance murine megakaryocyte colony growth and increases megakaryocyte ploidy in vitro. Blood. 85:1719-1726.
5. Datta, N.S., J.L. Williams, J. Caldwell, A.M. Curry, E.K. Ashcraft, and M.W. Long. 1996. Novel alterations in CDK1/cyclin B1 kinase complex formation occur during the acquisition of a polyploid DNA content. Mol. Biol Cell. 1: 209-223
6. Debili, N., F. Wendling, A. Katz, J. Guichard, J. Breton-Gorius, P. Hunt, and W. Vainchenker. 1995. The Mpl-ligand or thrombopoietin or megakaryocyte growth and differentiative factor has both direct proliferative and differentiative activities on human megakaryocyte progenitors. Blood. 86:2516-2525.
7. de Sauvase, F.J., P.E. Hass, S.D. Spencer, B.E. Malloy, A.L. Gurney, S.A. Spencer, W.C. Darbonne, W.J. Henzel, S.C. Wong, W.J. Kuang, et al. 1994. Stimulation of megakaryocytopoiesis and thrombopoiesis by the c-Mp1 ligand. Nature (Lond). 369:533-538.
8. Draetta, 0., F. Luca, J. Westendorf, L. Brizuela, J. Ruderman, and D. Beach. 1989. Cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF. Cell. 56:829-838.
9. Ebbe, S. 1976. Biology of megakaryocytes. Prog. Hemostasis Thromb. 3:211-229.
10. Greenberg, S.M., D.S. Rosenthal, T.A. Greeley, R. Tantravahi, and R.I. Handin. 1988. Characterization of a new megakaryocytic cell line: the Dami cell, Blood. 72:1968-1977.
11. Gn, X.F., A. Allain, L. Li, E.M. Cramer, D. Tenza, J.P. Caen, and Z.C. Han. 1993. Expression of cyclin B in megakaryocytes and cells of other hematopoietic lineages. C. R. Acad. Sci. III. 316:1438-1445.
12. Hennessy, K.M., C.D. Clark, and D. Botstein. 1990. Subcellular localization of yeast CDC46 varies with the cell cycle. Genes Dev. 4:2252-2263.
13. Hennessy, K.M., A. Lee, E. Chen, and D. Botstein. 1991. A group of interacting yeast DNA replication genes. Genes Dev. 5:958-969.
14. Hudson, K.M., N.C. Denko, E. Schwab, E. Oswald, A. Weiss, and M.A. Lieberman. 1996. Megakaryocytic cell line-specific hyperploidy by cytotoxic necrotizing factor bacterial toxins. Blood. 88:3465-3473.
15. Hunt, T., F.C. Luca, and J.V. Ruderman. 1992. The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo. J. Cell Biol. 116: 707-724.
16. Joshi, H.C. 1994. Microtubule organizing centers and γ-tubulin. Curr. Opin. Cell Biol. 6:54-62.
17. Kaushansky, K., S. Lok, R.D. Holly, V.C. Broudy, N. Lin, M.C. Baily, J.W. Forstorm, M.M. Buddle, P.J. Oort, F.S. Hagen, et al. 1994. Promotion of megakaryocyte progenitor expansion and differentiation by the c-Mpl ligand thrombopoietin. Nature (Land.). 369:568-571.
18. Kikuchi, J., Y. Furukawa, S. Iwase, Y. Terui, M. Nakamura, S. Kitagawa, M. Kitagawa, N. Komatsu, and Y. Miura. 1997. Polyploidization and functional maturation are two distinct processes during megakaryocytic differentiation: involvement of cyclin-dependent kinase inhibitor p21 in polyploidization. Blood. 89:3980-3987.
19. Kimura, H., N. Nozaki, and K. Sugimoto. 1994. DNA polymerase a associated protein P1, a murine homology of yeast MCM3. changes its intranuclear distribution during the DNA synthetic period. EMBO (Eur. Mol. Biol. Organ.) J. 13:4311-4320.
20. Kubota, Y. S. Mimura, S. Nishimoto, H. Takisawa, and H. Nojima. 1994. Identification of the yeast MCM3-related protein as a component of Xenopus DNA replication licensing factor. Cell. 81:601-609.
21. Kuter, D.J., D.L. Beeler, and R.D. Rosenberg, 1994. The purification of megapoietin: a physiological regulator of megakaryocyte growth and platelet production. Prot: Natl. Acad. Sci. USA. 91:11104-11108.
22. Laskey, R.A., M.P. Fairman, and J.J. Blow. 1989. S phase of the cell cycle. Science (Wash. DC). 246:609-614.
23. Long, M.W., N. Williams, and S. Ebbe. 1982a. Immature megakaryocytes in the mouse: physical characteristics, cell cycle status, and in vitro responsiveness to thrombopoietic stimulatory factor. Blood. 59:569-575.
24. Long, M.W., N. Williams, and T.P. McDonald. 19826. Immature megakaryo-cytes in the mouse: in vitro relationship to megakaryocyte progenitor cells and mature megakaryocytes. J. Cell Physiol. 112:339-344.
25. Moore, J.D., and S.A. Endow. 1996. Kinesin proteins: a phylum of motors for microtubule-based motility. Bio Essays. 18:207-218.
26. Muro, Y., K. Sugimoto, T. Okazaki, and M. Ohashi. 1990. The heterogeneity of anticentromere antibodies in immunoblotting analysis. J. Rheumatol. 17: 1042-1047.
27. Nagahisa, H., Y. Nagata, T. Ohnuki, M. Osada, T. Nagasawa, T. Abe, and K. Todokoro. 1996. Bone marrow stromal cells produce thrombopoietin and stimulate megakaryocyte growth and maturation but suppress proplatelet formation. Blood. 87:1309-1316.
28. Nagata, Y., H. Nagahisa, Y. Aida, K. Okutomi, T. Nagasawa, and K. Todokoro. 1995. Thrombopoietin induces megakaryocyte differentiation in hematopoietic progenitor FDC-P2 cells. J. Biol. Chem. 270:19673-19675.
29. Nislow, C., V.A. Lombillo, R. Kuriyama, and J.R. McIntosh. 1992. A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature (Lond.). 359:543-547.
30. Odell, T.T., C.W. Jackson, and T.J. Friday. 1970. Megakaryocytopoiesis in rats with special reference to polyploidy. Blood. 35:775-782.
31. Ogura, M., Y. Morishima, R. Ohno, Y. Kato, N. Hirabayashi, H. Nagura, and H. Saito. 1985. Establishment of a novel human megakaryoblastic leukemia cell line, MEG-01, with positive Philadelphia chromosome. Blood. 66:1384-1392.
32. Ravid, K., D.J. Kuter, D.L. Beeler, T. Doi, and R.D. Rosenberg. 1993. Selection of an HEL-derived cell line expressing high levels of platelet factor 4. Blood 81:2885-2890.
33. Sledge, G.W., M. Glant, J. Jansen, N.A. Heerema, B.J. Roth, M. Goheen, and R. Huffman. 1986. Establishment in long term culture of megakaryocytic leukemia cells (EST-IU) from the marrow of a patient with leukemia and a mediastinal germ cell neoplasm. Cancer Res. 46:2155-2159.
34. Solomon, M.J., M. Glotzer, T.H. Lee, M. Philippe, and M.W. Kirschner. 1990. Cyclin activation of p34cdc2. Cell. 63:1013-1024.
35. Tabilio, A., P.G. Pelicci, G. Vinci, P. Mannoni, C.I. Civin, W. Vainchenker, U. Testa, M. Lipinski, H. Rochart, and J. Breton-Gorius. 1983. Myeloid and megakaryocytic properties of K-562 cell lines. Cancer Res. 43:4569-4573.
36. Takada, M., N. Morii, S. Kumagai, and R. Ryo. 1996. The involvement of the rho gen product, a small molecular weight GTP-binding protein, in polyploidization of a human megakaryocytic cell line. CMK. Exp. Hematol. 24: 524-530.
37. Therman, E., O.E. Sarto, and P.A. Stubblefield. 1983. Endomitosis: a reappraisal. Hum. Genet. 63:13-18.
38. Walczak, C.E., and T.J. Mitchison, 1996. Kinesin-related proteins at mitotic spindle poles: function and regulation. Cell. 85:943-946.
39. Wang, Z., Y. Zhang, D, Kamen, E. Lee, and K. Ravid. 1995. Cyclin D3 is essential for megakaryocytopoiesis. Blood. 86:3783-3788.
40. Wendung, F., E. Maraskovsky, N. Debili, F. Christina, M. Teepe, M. Titeux, N. Methia, J. Breton-Gorius, D. Cosman, and W. Vainchenker. 1994. cMp1 ligand is a humoral regulator of megakaryocytopoiesis. Nature (Lond.). 369: 571-574.
41. Williams, N., and H. Jackson. 1982. Kinetic analysis of megakaryocyte numbers and ploidy levels in developing colonies from mouse bone marrow cells. Cell Tiss. Kinet. 15:483-494.
42. Yan, H., A.M. Merchant, and B.K. Tye. 1993. Cell cycle-regulated nuclear localization of MCM2 and MCM3, which are required for the initiation of DNA synthesis at chromosomal replication origins in yeast. Genes Dev. 7: 2149-2160.
43. Yokoyama, N., N. Hayashi, T. Seki, N. Pante, T. Ohba, K. Nishii, K. Kuma, T. Hayashida, T. Miyata, U. Aebi, et al. 1995. A giant nucleopore protein that binds Ran/TC4. Nature (Lond.). 376:184-188.
44. Zhang, Y., Z. Wang, and K. Ravid. 1996. The cell cycle in polyploid megakaryocytes is associated with reduced activity of cyclin B1-dependent Cdc2 ki-nase. J. Biol. Chem. 271:4266-4272.
45. Zheng, Y., M.K. Jung, and B.R. Oakley. 1991. γ-Tubulin is present in Drosophila melanogoster and Homo sapiens and is associated with the centrosome. Cell. 65:817-823.