Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1996 Jul 1;317(Pt 1):321–327. doi: 10.1042/bj3170321

Decreased accumulation and dephosphorylation of the mitosis-specific form of nucleophosmin/B23 in staurosporine-induced chromosome decondensation.

Y Y Lu 1, C Y Lam 1, B Y Yung 1
PMCID: PMC1217481  PMID: 8694782

Abstract

Nucleophosmin/B23 is highly phosphorylated by cdc2 kinase during mitosis, and this phosphorylation most probably has a role in initiating and controlling the entry of cells into mitosis [Peter, Nakagawa, Doree, Labbe and Nigg (1990) Cell 60, 791-801]. In the present study, the protein kinase inhibitor staurosporine has been used to examine possible changes in nucleophosmin/B23 at mitosis in HeLa cells. Addition of staurosporine to HeLa cells already arrested at mitosis by nocodazole causes: (i) decreased accumulation of the mitosis-specific form of nucleophosmin/B23, (ii) dephosphorylation of nucleophosmin/ B23, (iii) redistribution of nucleophosmin/B23 to the cytosol, and (iv) concomitant decondensation of chromosomes. These results suggest that the mitosis-specific phosphorylated form of nucleophosmin/B23 may play a role in maintaining mitotic chromosomes in their condensed state.

Full Text

The Full Text of this article is available as a PDF (364.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adachi Y., Copeland T. D., Hatanaka M., Oroszlan S. Nucleolar targeting signal of Rex protein of human T-cell leukemia virus type I specifically binds to nucleolar shuttle protein B-23. J Biol Chem. 1993 Jul 5;268(19):13930–13934. [PubMed] [Google Scholar]
  2. Borer R. A., Lehner C. F., Eppenberger H. M., Nigg E. A. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 1989 Feb 10;56(3):379–390. doi: 10.1016/0092-8674(89)90241-9. [DOI] [PubMed] [Google Scholar]
  3. Chan P. K., Aldrich M., Cook R. G., Busch H. Amino acid sequence of protein B23 phosphorylation site. J Biol Chem. 1986 Feb 5;261(4):1868–1872. [PubMed] [Google Scholar]
  4. Chan P. K., Chan W. Y., Yung B. Y., Cook R. G., Aldrich M. B., Ku D., Goldknopf I. L., Busch H. Amino acid sequence of a specific antigenic peptide of protein B23. J Biol Chem. 1986 Oct 25;261(30):14335–14341. [PubMed] [Google Scholar]
  5. Chan P. K. Cross-linkage of nucleophosmin in tumor cells by nitrogen mustard. Cancer Res. 1989 Jun 15;49(12):3271–3275. [PubMed] [Google Scholar]
  6. Chan P. K., Liu Q. R., Durban E. The major phosphorylation site of nucleophosmin (B23) is phosphorylated by a nuclear kinase II. Biochem J. 1990 Sep 1;270(2):549–552. doi: 10.1042/bj2700549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chan W. Y., Liu Q. R., Borjigin J., Busch H., Rennert O. M., Tease L. A., Chan P. K. Characterization of the cDNA encoding human nucleophosmin and studies of its role in normal and abnormal growth. Biochemistry. 1989 Feb 7;28(3):1033–1039. doi: 10.1021/bi00429a017. [DOI] [PubMed] [Google Scholar]
  8. Chang J. H., Dumbar T. S., Olson M. O. cDNA and deduced primary structure of rat protein B23, a nucleolar protein containing highly conserved sequences. J Biol Chem. 1988 Sep 15;263(26):12824–12827. [PubMed] [Google Scholar]
  9. Crissman H. A., Gadbois D. M., Tobey R. A., Bradbury E. M. Transformed mammalian cells are deficient in kinase-mediated control of progression through the G1 phase of the cell cycle. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7580–7584. doi: 10.1073/pnas.88.17.7580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dumbar T. S., Gentry G. A., Olson M. O. Interaction of nucleolar phosphoprotein B23 with nucleic acids. Biochemistry. 1989 Nov 28;28(24):9495–9501. doi: 10.1021/bi00450a037. [DOI] [PubMed] [Google Scholar]
  11. Fallon R. J. Staurosporine inhibits a tyrosine protein kinase in human hepatoma cell membranes. Biochem Biophys Res Commun. 1990 Aug 16;170(3):1191–1196. doi: 10.1016/0006-291x(90)90519-s. [DOI] [PubMed] [Google Scholar]
  12. Fankhauser C., Izaurralde E., Adachi Y., Wingfield P., Laemmli U. K. Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the Rev response element. Mol Cell Biol. 1991 May;11(5):2567–2575. doi: 10.1128/mcb.11.5.2567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Feuerstein N., Spiegel S., Mond J. J. The nuclear matrix protein, numatrin (B23), is associated with growth factor-induced mitogenesis in Swiss 3T3 fibroblasts and with T lymphocyte proliferation stimulated by lectins and anti-T cell antigen receptor antibody. J Cell Biol. 1988 Nov;107(5):1629–1642. doi: 10.1083/jcb.107.5.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gadbois D. M., Hamaguchi J. R., Swank R. A., Bradbury E. M. Staurosporine is a potent inhibitor of p34cdc2 and p34cdc2-like kinases. Biochem Biophys Res Commun. 1992 Apr 15;184(1):80–85. doi: 10.1016/0006-291x(92)91160-r. [DOI] [PubMed] [Google Scholar]
  15. Gautier T., Masson C., Quintana C., Arnoult J., Hernandez-Verdun D. The ultrastructure of the chromosome periphery in human cell lines. An in situ study using cryomethods in electron microscopy. Chromosoma. 1992 Jun;101(8):502–510. doi: 10.1007/BF00352473. [DOI] [PubMed] [Google Scholar]
  16. Goessens G. Nucleolar structure. Int Rev Cytol. 1984;87:107–158. doi: 10.1016/s0074-7696(08)62441-9. [DOI] [PubMed] [Google Scholar]
  17. Herbert J. M., Seban E., Maffrand J. P. Characterization of specific binding sites for [3H]-staurosporine on various protein kinases. Biochem Biophys Res Commun. 1990 Aug 31;171(1):189–195. doi: 10.1016/0006-291x(90)91375-3. [DOI] [PubMed] [Google Scholar]
  18. Hernandez-Verdun D., Gautier T. The chromosome periphery during mitosis. Bioessays. 1994 Mar;16(3):179–185. doi: 10.1002/bies.950160308. [DOI] [PubMed] [Google Scholar]
  19. Hügle B., Hazan R., Scheer U., Franke W. W. Localization of ribosomal protein S1 in the granular component of the interphase nucleolus and its distribution during mitosis. J Cell Biol. 1985 Mar;100(3):873–886. doi: 10.1083/jcb.100.3.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Inouye C. J., Seto E. Relief of YY1-induced transcriptional repression by protein-protein interaction with the nucleolar phosphoprotein B23. J Biol Chem. 1994 Mar 4;269(9):6506–6510. [PubMed] [Google Scholar]
  21. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  22. Ochs R., Lischwe M., O'Leary P., Busch H. Localization of nucleolar phosphoproteins B23 and C23 during mitosis. Exp Cell Res. 1983 Jun;146(1):139–149. doi: 10.1016/0014-4827(83)90332-4. [DOI] [PubMed] [Google Scholar]
  23. Peculis B. A., Gall J. G. Localization of the nucleolar protein NO38 in amphibian oocytes. J Cell Biol. 1992 Jan;116(1):1–14. doi: 10.1083/jcb.116.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Peter M., Nakagawa J., Dorée M., Labbé J. C., Nigg E. A. Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase. Cell. 1990 Mar 9;60(5):791–801. doi: 10.1016/0092-8674(90)90093-t. [DOI] [PubMed] [Google Scholar]
  25. Prestayko A. W., Klomp G. R., Schmoll D. J., Busch H. Comparison of proteins of ribosomal subunits and nucleolar preribosomal particles from Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis. Biochemistry. 1974 Apr 23;13(9):1945–1951. doi: 10.1021/bi00706a026. [DOI] [PubMed] [Google Scholar]
  26. Schmidt-Zachmann M. S., Hügle-Dörr B., Franke W. W. A constitutive nucleolar protein identified as a member of the nucleoplasmin family. EMBO J. 1987 Jul;6(7):1881–1890. doi: 10.1002/j.1460-2075.1987.tb02447.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Spector D. L., Ochs R. L., Busch H. Silver staining, immunofluorescence, and immunoelectron microscopic localization of nucleolar phosphoproteins B23 and C23. Chromosoma. 1984;90(2):139–148. doi: 10.1007/BF00292451. [DOI] [PubMed] [Google Scholar]
  28. Takemura M., Ohta N., Furuichi Y., Takahashi T., Yoshida S., Olson M. O., Umekawa H. Stimulation of calf thymus DNA polymerase alpha activity by nucleolar protein B23. Biochem Biophys Res Commun. 1994 Feb 28;199(1):46–51. doi: 10.1006/bbrc.1994.1191. [DOI] [PubMed] [Google Scholar]
  29. Tamaoki T., Nomoto H., Takahashi I., Kato Y., Morimoto M., Tomita F. Staurosporine, a potent inhibitor of phospholipid/Ca++dependent protein kinase. Biochem Biophys Res Commun. 1986 Mar 13;135(2):397–402. doi: 10.1016/0006-291x(86)90008-2. [DOI] [PubMed] [Google Scholar]
  30. Th'ng J. P., Guo X. W., Swank R. A., Crissman H. A., Bradbury E. M. Inhibition of histone phosphorylation by staurosporine leads to chromosome decondensation. J Biol Chem. 1994 Apr 1;269(13):9568–9573. [PubMed] [Google Scholar]
  31. Valdez B. C., Perlaky L., Henning D., Saijo Y., Chan P. K., Busch H. Identification of the nuclear and nucleolar localization signals of the protein p120. Interaction with translocation protein B23. J Biol Chem. 1994 Sep 23;269(38):23776–23783. [PubMed] [Google Scholar]
  32. Yasuda Y., Maul G. G. A nucleolar auto-antigen is part of a major chromosomal surface component. Chromosoma. 1990 Apr;99(2):152–160. doi: 10.1007/BF01735332. [DOI] [PubMed] [Google Scholar]
  33. Yung B. Y., Bor A. M., Chan P. K. Short exposure to actinomycin D induces "reversible" translocation of protein B23 as well as "reversible" inhibition of cell growth and RNA synthesis in HeLa cells. Cancer Res. 1990 Sep 15;50(18):5987–5991. [PubMed] [Google Scholar]
  34. Yung B. Y., Bor A. M., Yang Y. H. Immunolocalization of phosphoprotein B23 in proliferating and non-proliferating HeLa cells. Int J Cancer. 1990 Aug 15;46(2):272–275. doi: 10.1002/ijc.2910460222. [DOI] [PubMed] [Google Scholar]
  35. Yung B. Y., Busch H., Chan P. K. Effects of luzopeptins on protein B23 translocation and ribosomal RNA synthesis in HeLa cells. Cancer Res. 1986 Feb;46(2):922–925. [PubMed] [Google Scholar]
  36. Yung B. Y., Busch H., Chan P. K. Translocation of nucleolar phosphoprotein B23 (37 kDa/pI 5.1) induced by selective inhibitors of ribosome synthesis. Biochim Biophys Acta. 1985 Dec 18;826(4):167–173. doi: 10.1016/0167-4781(85)90002-8. [DOI] [PubMed] [Google Scholar]
  37. Yung B. Y., Chan P. K. Identification and characterization of a hexameric form of nucleolar phosphoprotein B23. Biochim Biophys Acta. 1987 Jul 16;925(1):74–82. doi: 10.1016/0304-4165(87)90149-8. [DOI] [PubMed] [Google Scholar]
  38. Yung B. Y., Chang F. J., Bor A. M., Lee E. S. Schedule-dependent effects of two consecutive, divided, low doses of actinomycin D on translocation of protein B23, inhibition of cell growth and RNA synthesis in HeLa cells. Int J Cancer. 1992 Sep 9;52(2):317–322. doi: 10.1002/ijc.2910520227. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES