Skip to main content
SpringerLink
Log in

Role of protein kinase CK2 in phosphorylation of nucleosomal proteins in relation to transcriptional activity

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Protein kinase CK2 undergoes rapid translocation to nuclear matrix and nucleosomes on androgenic stimulation of growth in prostatic epithelial cells. Further, CK2 appears to be regulated differentially in the transcriptionally active and inactive nucleosomes. We have investigated the role of CK2 in phosphorylation of nucleosome-associated proteins in the transcriptionally active and inactive nucleosomes that were isolated from ventral prostate subjected to different androgenic status in vivo. Proteins associated with these nucleosomes were phosphorylated via the intrinsic protein kinase activity, using [γ-32P]ATP in the absence and presence of GTP. Several proteins appear to be potential substrates for CK2 associated with the nucleosomes. Among them are proteins that are differentially associated with the transcriptionally active and inactive nucleosomes. Phosphorylation of several of these proteins is modulated depending not only on their sites of association (i.e., active vs. inactive nucleosomes) but also on the state of transcriptional activity. Differential phosphorylation of specific proteins by CK2 associated with the active and inactive nucleosomes may be pertinent to the process of transcription regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Pinna LA: Casein kinase 2: An ‘eminence grise’ in cellular regulation? Biochim Biophys Acta 1054: 267–284, 1990

    PubMed  Google Scholar 

  2. Tuazon PT, Traugh JA: Casein kinase I and II-multipotential serine protein kinases: Structure, function, and regulation. In: P. Greengard, G.A. Robison (eds). Advances in Second Messenger and Phosphoprotein Research. Raven Press Ltd, New York, 1991, Vol 23, pp 123–164

    Google Scholar 

  3. Issinger O-G: Casein kinases: Pleiotropic mediators of cellular regulation. Pharmacol Therap 59: 1–30, 1993

    Google Scholar 

  4. Litchfield DW, Lüscher B: Casein kinase II in signal transduction and cell cycle regulation. Mol Cell Biochem 128: 187–199, 1993

    Google Scholar 

  5. Ahmed K: Significance of the casein kinase system in cell growth and proliferation with emphasis on studies of the androgenic regulation of the prostate. Cell Mol Biol Res 40: 1–11, 1994

    PubMed  Google Scholar 

  6. Allende JE, Allende CC: Protein kinase CK2: An enzyme with multiple substrates and a puzzling regulation. FASEB J 9: 313–323, 1995

    PubMed  Google Scholar 

  7. Williams-Ashman HG: Biochemical features of androgen physiology. In: L.J. DeGroot, G.G. Cahill Jr, L. Martini, D.H. Nelson, W.D. Odell, J.T. Potts Jr, E. Steinberger, A.I. Winegard (eds). Endocrinology. Grune and Stratton, New York, 1979, pp 1527–1533

    Google Scholar 

  8. Coffey DS: Androgen action and the sex accessory tissues. In: E. Knobil, J. Neill (eds). The Physiology of Reproduction. Raven Press, New York, 1988, pp 1081–1119

    Google Scholar 

  9. Liao S, Kokontis J, Sai T, Hiipakka RA: Androgen receptors: structures, mutations, antibodies and cellular dynamics. J Steroid Biochem 34: 41–51, 1989

    PubMed  Google Scholar 

  10. Ahmed K, Davis A, Hanten J, Lambert D, McIvor RS, Goueli SA: Cloning of cDNAs encoding the alpha and beta subunits of rat casein kinase 2 (CK-2): Investigation of molecular regulation of CK-2 by androgens in rat ventral prostate. Cell Mol Biol Res 39: 451–462, 1993

    PubMed  Google Scholar 

  11. Ahmed K, Yenice S, Goueli SA: Casein kinases and prostatic cell growth. In: R.J. Wegmann, M.A. Wegmann (eds). Recent Advances in Cellular and Molecular Biology. Vol 4. Peeters Press, Leuven, 1992, pp 7–15

    Google Scholar 

  12. Ahmed K, Yenice S, Davis A, Goueli S: Association of casein kinase 2 with nuclear chromatin in relation to androgenic regulation of rat prostate. Proc Natl Acad Sci USA 90: 4426–4430, 1993

    PubMed  Google Scholar 

  13. Ahmed K, Tawfic S: Mechanism of intracellular regulation of casein kinase 2 (CK-2): Role of stimulus mediated subnuclear association. Cell Mol Biol Res 40: 539–545, 1994

    PubMed  Google Scholar 

  14. Tawfic S, Ahmed K: Association of casein kinase 2 (CK-2) with nuclear matrix: Possible role in nuclear matrix protein phosphorylation. J Biol Chem 269: 7489–7493, 1994

    PubMed  Google Scholar 

  15. Tawfic S, Ahmed K: Growth stimulus-mediated differential translocation of casein kinase 2 to the nuclear matrix: Evidence based on androgen action in the prostate. J Biol Chem 269: 24615–24620, 1994

    PubMed  Google Scholar 

  16. Tawfic S, Olson MOJ, Ahmed K: Role of protein phosphorylation in posttranslational regulation of protein B23 during programmed cell death in the prostate gland. J Biol Chem 270: 21009–21015, 1995

    PubMed  Google Scholar 

  17. Tawfic S, Faust RA, Gapany M, Ahmed K: Nuclear matrix as an anchor for protein kinase CK2 nuclear signalling. J Cell Biochem 61: 165–171, 1996

    Google Scholar 

  18. Tawfic S, Davis AT, Faust RA, Gapany M, Ahmed K: Association of protein kinase CK2 with nuclear matrix: Influence of method of preparation of nuclear matrix. J Cell Biochem 64: 499–504, 1997

    PubMed  Google Scholar 

  19. Zhang P, Davis AT, Ahmed K: Mechanism of protein kinase CK2 association with nuclear matrix: Role of disulfide bond formation. J Cell Biochem 69: 211–220, 1998

    PubMed  Google Scholar 

  20. Getzenberg RH, Pienta KJ, Coffey DS: Nuclear structure and the three dimensional organization of DNA. J Cell Biochem 47: 289–299, 1991

    PubMed  Google Scholar 

  21. Berezney R: The nuclear matrix: A heuristic model for investigating genomic organization and function in the cell nucleus. J Cell Biochem 47: 109–123, 1991

    PubMed  Google Scholar 

  22. Nickerson JA, Penman S: The nuclear matrix: Structure and involvement in gene expression. In: G.S. Stein, J.B. Lian (eds). Molecular and Cellular Approaches to the Control of Proliferation and Differentiation. Academic Press, San Diego, CA, 1992, pp 343–380

    Google Scholar 

  23. Stein GS, Stein JL, van Wijnen AJ, Lian JB: The maturation of a cell. Am Scientist 84: 28–37, 1996

    Google Scholar 

  24. Guo C, Davis A, Ahmed K: Protein kinase CK2 association with nucleosomes in relation to their state of activity. FASEB J 11: A1181, 1997

    Google Scholar 

  25. Guo C, Davis AT, Ahmed K: Dynamics of protein kinase CK2 association with nucleosomes in relation to transcriptional activity. J Biol Chem 273: 13675–13680, 1998

    PubMed  Google Scholar 

  26. Allfrey VG, Chen TA: Nucleosomes of transcriptionally active chromatin: Isolation of template-active nucleosomes by affinity chromatography. Meth Cell Biol 35: 315–335, 1991

    Google Scholar 

  27. Chen TA, Smith MM, Le S, Sternglanz R, Allfrey VG: Nucleosome fractionation by mercury affinity chromatography: Contrasting distribution of transcriptionally active DNA sequences and acetylated histones in nucleosome fractions of wild-type yeast cells and cells expressing a histone H3 gene altered to encode a cysteine 110 residue. J Biol Chem 266: 6489–6498, 1991

    PubMed  Google Scholar 

  28. Filhol O, Baudier J, Delphin C, Loue-Mackenbach P, Chambaz EM, Cochet C: Casein kinase II and the tumor suppressor protein p53 associate in a molecular complex that is negatively regulated upon p53 phosphorylation. J Biol Chem 267: 20577–20583, 1992

    PubMed  Google Scholar 

  29. Wada T, Kakagi T, Yamaguchi Y, Kawase H, Hiramoto M, Ferdous A, Takayama M, Lee YAW, Hurst HC, Handa H: Copurification of casein kinase II with transcription factor ATF/E4TF3. Nucleic Acids Res 24: 876–884, 1996

    PubMed  Google Scholar 

  30. Janosch P, Schellerer M, Seitz T, Reim P, Eulitz M, Brielmeier M, Kölch W, Sedivy JM, Mischak H: Characterization of Iκ B kinases: Iκ B-α is not phosphorylated by Raf-1 or protein kinase C isozymes, but is a casein kinase II substrate. J Biol Chem 271: 13866–13874, 1996

    Google Scholar 

  31. Li D, Dobrowolska G, Krebs EG: The physical association of casein kinase 2 with nucleolin. J Biol Chem 271: 15662–15668, 1996

    PubMed  Google Scholar 

  32. Boldyreff B, Issinger O-G: A-Raf kinase is a new interacting partner of protein kinase CK2β subunit. FEBS Lett 403: 197–199, 1997

    PubMed  Google Scholar 

  33. Li D, Krebs EG: Specific interaction between casein kinase 2 and the nucleolar protein Nopp140. J Biol Chem 272: 3773–3779, 1997

    PubMed  Google Scholar 

  34. Guo B, Odgren PR, van Wijnen AJ, Last TJ, Nickerson J, Penman S, Lian JB, Stein JL, Stein GS: The nuclear matrix protein NMP-1 is the transcription factor YY1. Proc Natl Acad Sci USA 92: 10526–10530, 1995

    PubMed  Google Scholar 

  35. Voit R, Schnapp A, Kuhn A, Rosenbauer H, Hirschmann P, Stunnenberg HG, Grummt I: The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J 11: 2211–2218, 1992

    PubMed  Google Scholar 

  36. Lin R, Beauparlant P, Makris C, Meloche S, Hiscott J: Phosphorylation of the IκB± in the C-terminal PEST domain by casein kinase II affects intrinsic protein stability. Mol Cell Biol 16: 1401–1409, 1996

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cellular and Molecular Biochemistry Research Laboratory (151), Department of Laboratory Medicine and Pathology, University of Minnesota and the Department of Veterans Affairs Medical Center, Minneapolis, Minnesota, USA

    Chuanhai Guo, Alan T. Davis, Shihui Yu, Sherif Tawfic & Khalil Ahmed

Authors
  1. Chuanhai Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan T. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shihui Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sherif Tawfic
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Khalil Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guo, C., Davis, A.T., Yu, S. et al. Role of protein kinase CK2 in phosphorylation of nucleosomal proteins in relation to transcriptional activity. Mol Cell Biochem 191, 135–142 (1999). https://doi.org/10.1023/A:1006881405383

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006881405383

Search

Navigation