Skip to main content
SpringerLink
Log in

The binding of the α subunit of protein kinase CK2 and RAP74 subunit of TFIIF to protein-coding genes in living cells is DRB sensitive

  • Chapter
A Molecular and Cellular View of Protein Kinase CK2

Part of the book series: Developments in Molecular and Cellular Biochemistry ((DMCB,volume 27))

  • 122 Accesses

Abstract

In a previous report, we documented that a major portion of the nuclear protein kinase CK2α (CK2α) subunit does not form heterooligomeric structures with the β subunit, but it binds tightly to nuclear structures in an epithelial Chironomus cell line [1]. We report here that the CK2α, but not β, subunit is co-localized with productively transcribing RNA polymerase II (pol II) on polytene chromosomes of Chironomus salivary gland cells. Likewise, the RAP74 subunit of TFIIF, a potential substrate for CK2, is co-localized with pol II. The occupancies of chromosomes with the CK2α and RAP74 subunits are sensitive to DRB, an inhibitor of pol II-based transcription and the activity of CK2 and pol II carboxyl-terminal kinases. DRB alters the chromosomal distribution of the CK2α and RAP74 subunits: there is a time-dependent clearance from the chromosomes of CK2α and RAP74 subunits, which coincides in time the completion and release of preinitiated transcripts after addition of DRB. The results suggest that both the CK2α and RAP74 subunits travel with the elongating pol II molecules along the DNA template during the entire transcription cycle. No detectable re-association of CK2α and RAP74 with the promoters takes, however, place after the completion of the preinitiated transcripts in the presence of DRB. In contrast, the binding of hypophosporylated pol II and TFIIH to the active gene loci is not abolished by the DRB regimen. Our data are consistent with the possibility that in living Chironomus salivary gland cells, DRB interferes with the recruitment of TFIIF, but not of TFIIH, to the promoter by interference with the activity of the CK2α subunit enzyme and phosphorylation of RAP74 and thereby DRB blocks transcription initiation. (Mol Cell Biochem 191: 149–159, 1999)

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Stigare J, Buddelmeijer N, Pigon A, Egyházi E: A majority of casein kinase II α subunit is tightly bound to the nuclear structure but not to the β subunit. Mol Cell Biochem 129: 77–85, 1993

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  3. Tuazon PT, Traugh JA: Casein kinase I and II-multipotent serine protein kinases: Structure, function, and regulation. Adv Sec Mess Phosphoprot Res 23: 124–154,1991

    Google Scholar 

  4. Cochet C, Chambaz EM: Oligomeric structure and catalytic activity of G type casein kinase. J Biol Chem 258: 1403–1406, 1983

    PubMed  CAS  Google Scholar 

  5. Stigare J, Buddelmeijer N, Pigon A, Egyházi E: Analysi of a novel DNA-binding protein kinase CKIl-like enzyme of Chironomus cells. Cell Mol Biol Res 40: 463–172, 1994

    PubMed  CAS  Google Scholar 

  6. Luscher B, Litchfield DW: Biosynthesis of casein kinase II in lymphoid cell lines. Eur J Biochem 220: 521–526, 1994

    Article  PubMed  CAS  Google Scholar 

  7. Gietz D, Graham KC, Litchfield DW: Interactions between the subunits of casein kinase II. J Biol Chem 270: 13017–13021, 1995

    Article  PubMed  CAS  Google Scholar 

  8. Lin WJ, Tuazon PT, Traugh JA: Characterization of the catalytic subunit of casein kinase II expressed in Escherichia coli and regulation of activity. J Biol Chem 266: 5664–5669, 1991

    PubMed  CAS  Google Scholar 

  9. Hanks SK, Quinn AM, Hunter T: The protein kinase family: Conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52, 1988

    Article  PubMed  CAS  Google Scholar 

  10. Lin WJ, Sheu GT, Traugh JA: The effect of autophosphorylation on activity of casein kinase II: Evidence for mutations on the β subunit. Biochemistry 33; 6998–7004, 1994

    Article  PubMed  CAS  Google Scholar 

  11. Meggio F, Boldyreff B, Marin O, Issinger O-G, Pinna L: Phosphorylation and activation of protein kinase CK2 by p34cdc2 are independent events. Eur J Biochem 230: 1025–1031, 1995

    Article  PubMed  CAS  Google Scholar 

  12. Marshak DR, Russo GL: Regulation of casein kinase CK2 during the cell cycle. Cell Mol Biol Res 40: 513–517, 1994

    PubMed  CAS  Google Scholar 

  13. Pepperkok R, Lorenz P, Pyerin W: Casein kinase II is required for transition of G0/G1, early Gl and Gl/S phase of the cell cycle. J Biol Chem 269: 6986–6991, 1994

    PubMed  CAS  Google Scholar 

  14. Hanna DE, Rethinaswamy A, Glover CVC: Casein kinase II is required for cell cycle progression during Gl and G2/M in Saccharomyces cerevisiae. J Biol Chem 270: 25904–25914, 1995

    Google Scholar 

  15. Litchfield DW, Dobrowolska G, Krebs EG: Regulation of casein kinase II by growth factors: A réévaluation. Cell Mol Biol Res 40: 373–381, 1994

    PubMed  CAS  Google Scholar 

  16. Seldin DC, Leder P: Casein kinase Ha transgene-induced murine Lymphoma: Relation toTheileriosis in cattle. Science 267: 894–896,1995

    Article  PubMed  CAS  Google Scholar 

  17. Janknecht R, Hipskind RA, Houthaeve T, Stunnenbern HG: Identification of multiple SRF N-terminal phosphorylation sites affecting DNA binding properties. EMBOJ 11: 1045–1054, 1992

    CAS  Google Scholar 

  18. Bousset K, Oelgeschläger MHH, Henriksson M, Schreek S, Bukhardt H, Litchfield DW, Luscher-Firzlaff JM, Luscher B: Regulation of transcriprion factors c-Myc, Max, and c-Myb by casein kinase II. Cell Mol Biol Res 40: 501–511, 1994

    PubMed  CAS  Google Scholar 

  19. Meek DW, Simon S, Kikkawa U, Eckhardt W: The p53 tumour suppressor protein is phosphorylated at serine 389 by casein kinase II. EMBOJ 9: 3253–3260, 1990

    CAS  Google Scholar 

  20. Filhol O, Baudiers J, Delphin C, Loue-Mackenbach P, Chambaz EM, Cochet C: Casein kinase II and the tumor repressor protein p52 associate in a molecular complex that is negatively regulated upon p53 phosphorylation. J Biol Chem 267: 20577–20583, 1992

    PubMed  CAS  Google Scholar 

  21. Dahmus M: Phosphorylation of eukaryotic DNA-dependent RNA polymerase. J Biol Chem 256: 3332–3339, 1981

    PubMed  CAS  Google Scholar 

  22. Duceman BW, Rose KM, Jacob ST: Activation of purified hepatoma RNA polymerase I by homologues protein kinase NO. J Biol Chem 256: 10755–10758, 1981

    PubMed  CAS  Google Scholar 

  23. Stetler DA, Rose KM: Phosphorylation of deoxyribonucleic acid dependent RNA polymerase II nuclear protein kinase Nil: mechanism of enhanced ribonucleic acid synthesis. Biochemistry 21: 3721–3728, 1982

    Article  PubMed  CAS  Google Scholar 

  24. Durban E, Goodenough M, Mills J, Busch H: Topoisomerase phosphorylation in vitro and in rapidly growing Novikoff hepatoma cells. EMBO J 4: 2921–2926, 1985

    PubMed  CAS  Google Scholar 

  25. Cardenas M, Dang Q, Glover CVC, Gasser SM: Casein kinase II phos-phorylates the eukaryot-specific C-terminal domain of topoisomerase II in vivo. EMBO J 11: 1785–1796, 1992

    PubMed  CAS  Google Scholar 

  26. Voit R, Schnapp A, Kuhn A: The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tale which is essential for transactivation. EMBO J 6: 2211–2218, 1992

    Google Scholar 

  27. Caizergues-Ferrer M, Belenguer P, Lapeyre B, Amalric F, Wallace MO, Olson MJ: Phosphorylation of nucleolin by nuclear type Nll protein kinase. Biochemistry 26: 7876–7883, 1987

    Article  PubMed  CAS  Google Scholar 

  28. Karlin S: Unusual charge configurations in transcriptions factors of the basic RNA polymerase II initiation complex. Proc Natl Acad Sci USA 90: 5593–5597, 1993

    Article  PubMed  CAS  Google Scholar 

  29. Hockman DJ, Schultz MC: Casein kinase II is requires for efficient transcription by RNA pol III. Mol Cell Biol 16: 892–898, 1996

    PubMed  CAS  Google Scholar 

  30. Zandomeni R, Weinmann R: Inhibitory effect of 5,6-dichloro-1-β-Dribofuranosylbenzimidazole on a protein kinase. J Biol Chem 259: 14804–14811, 1984

    PubMed  CAS  Google Scholar 

  31. Egyházi E, Daneholt B, Edström J, Lambert B, Ringborg U: Differential inhibitory effect of a substituted benzimidazole on RNA labeling in polytene chromosomes. J Cell Biol 47: 516–520, 1970

    Google Scholar 

  32. Tamm I, Hand R, Caliguiri LA: Action of benzimidazole riboside on RNA synthesis in L-929 and HeLa cells. J Cell Biol 69: 229–240, 1976

    Article  PubMed  CAS  Google Scholar 

  33. Egyházi E, Pigon A: Selective repression of RNA polymerase II by micro-injected phosvitin. Chromosoma 94: 329–336, 1986

    Article  PubMed  Google Scholar 

  34. Zandomeni R, Zandomeni MC, Shugar D, Weinmann R: Casein kinase type II is involved in the inhibition by 5,6-dichloro-1-β-Dribofuranosylbenzimidazole of specific RNA polymerase II transcription. J Biol Chem 261: 3414–3419, 1986

    PubMed  CAS  Google Scholar 

  35. Beermann W: Chromomerenkostanz und spezifische Modifikation der Kromosomenstruktur in der Entwicklung und Organdifferenzierung von Chironomus tentans. Chromosoma 5: 139–198, 1952

    Article  Google Scholar 

  36. Lambert B, Daneholt B: Microanalysis of RNA from defined cellular components. Meth Cell Biol 10: 17–47, 1975

    Article  CAS  Google Scholar 

  37. Wyss C: Chironomus tentans epithelial cell lines sensitive to ecdysteroids, juvenile hormone, insulin and heat shock. Exp Cell Res 139: 309–319, 1982

    Article  PubMed  CAS  Google Scholar 

  38. Filhol O, Cochet C, Wedegaertner P, Gill GN, Chambaz EM: Coexpression of both α and β subunits is required for assembly of regulated casein kinase II. Biochemistry 30: 11133–11140, 1991

    Article  PubMed  CAS  Google Scholar 

  39. Harlow E, Lane DP: Cold Spring Harbor Laboratory. Cold Spring Harbor, New York, 1988, pp 313–315

    Google Scholar 

  40. Sass H: Features of in vitro puffing and RNA synthesis in polytene chromosomes of Chironomus. Chromosoma 78: 33–78, 1980

    Article  PubMed  CAS  Google Scholar 

  41. Egyházi E, Pigon A, Ossoinak A, Holst M, Tayip U: Phosphorylation of some chromosomal nonhistone proteins in active genes is blocked by the transcription inhibitor 5,6-dichloro-l-β-D-ribofuranosylbenzimidazole (DRB). J Cell Biol 98: 954–962, 1984

    Article  PubMed  Google Scholar 

  42. Egyház i E, Ossoinak A, Pigon A, Lee JM, Greenleaf, AL: Phos-phorylation-dependence of initiating productive transcription of Balbiani ring 2 genes in living cells. Chromosoma 104: 422–433, 1996

    Article  PubMed  Google Scholar 

  43. Edstrüm JE: Microextraction and microelectrophoresis for detemination and analysis of nucleic acids in isolated cellular units. In: D. Prescott (ed). Methods in Cell Physiology. Academic Press, New York Vol. 1, 1964, pp 417–447

    Google Scholar 

  44. Pelting C: Ribonukleinsäure-Synthese der Riesenchromosomen Autoradiographische Untersuchungen an Chironomus tentans. Chromosoma 15: 71–122, 1964

    Article  Google Scholar 

  45. Weeks JR, Hardin SE, Shen J, Lee JM, Greenleaf AL: Locus-specific Variation in phosphorylation state of RNA polymerase II in vivo: Correlations with gene activity and transcript processing. Genes Dev 7: 2329–2344, 1993

    Article  PubMed  CAS  Google Scholar 

  46. Egyházi E: Initiation inhibition and reinitiation of the synthesis of heterogeneous nuclear RNA in living cells. Nature 262:319–321,1976

    Article  PubMed  Google Scholar 

  47. Egyház i E, Pigon A, Rydlander L: 5,6-Dichlororibofuranosylbenzimidazole inhibits the rate of transcription initiation in intact Chironomus cells. Eur J Biochem 122: 445–451, 1982

    Article  PubMed  Google Scholar 

  48. Trigon S, Morange M: Different Carboxyl-terminal domain kinase activities are induced by heat shock and arsenite. J Biol Chem 270: 13091–13098, 1995

    Article  PubMed  CAS  Google Scholar 

  49. Dubois MF, Vincent M, Vigneron M, Adamczewski J, Egly JM, Bensaude O: Heat-shock inactivation of the TFIIH-associated kinase and change in the phosphorylation sites on the C-terminal domain of pol II. Nucleic Acid Res 25: 694–700, 1997

    Article  PubMed  CAS  Google Scholar 

  50. Egház i E, Ossoinak A, Lee JM, Greenleaf AL, Mäk elä TP, Pigon A: Heat shock specific phosphorylation and transcriptional activity of RNA polymerase II. Exp Cell Res (in press)

    Google Scholar 

  51. Tan S, Conaway RC, Conaway JW: Dissection of transcription factor TFIIF functional domains required for initiation and elongation. Proc Natl Acad Sci USA 92: 6042–6046, 1995

    Article  PubMed  CAS  Google Scholar 

  52. Chang C, Kostrub CV, Burton ZF: RAP30/74 (transcription factor IIF) is required for promoter escape by RNA polymerase II. J Biol Chem 268:20482–20489, 1993

    PubMed  CAS  Google Scholar 

  53. Zawel L, Kumar KP, Reinberg D: Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev 9: 1479–1490, 1995

    Article  PubMed  CAS  Google Scholar 

  54. Kitajima S, Chibazakura T, Yonaha M, Yasukochi Y: Regulation of human transcription initiation factor TFIIF by phosphorylation. 269: 29970–29977, 1994

    CAS  Google Scholar 

  55. Quadroni, James P, Carafoli EJ: Isolation of phosphorylated calmodulin from rat liver and identification of the in vivo phosphorylation sites. Biol Chem 269: 16116–16122, 1994

    CAS  Google Scholar 

  56. Hupp TR, Meek DW, Midgley CA, Lane DP: Regulation of specific DNA binding function of p53. Cell 71: 875–886, 1992

    Article  PubMed  CAS  Google Scholar 

  57. Hupp T, Sparks A, Lane DP: Small peptides activate the latent sequence-specific DNA binding function of p53. Cell 83:237–245,1995

    Article  PubMed  CAS  Google Scholar 

  58. Yankulov K, Yamashita K, Roy R, Egly J-M, Bentley DL: The transcriptional elongation inhibitor 5,6-dichloro-1-β-D-ribofuranosylbenzimidazole inhibits transcription factor IIH-associated protein kinase. J Biol Chem 270: 23922–23925, 1995

    Article  PubMed  CAS  Google Scholar 

  59. Marshall NF, Peng J, Xie Z, Price DH: Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J Biol Chem 271: 27176–27183, 1996

    Article  PubMed  CAS  Google Scholar 

  60. Serizawa H, Conaway JW, Conaway RC: Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature 363: 371–374, 1993

    Article  PubMed  CAS  Google Scholar 

  61. Payne JM, Laybourn PJ, Dahmus ME: The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit lla. J Biol Chem 264: 19621–19629, 1989

    PubMed  CAS  Google Scholar 

  62. Zandomani R, Bunick D, Ackerman S, Mittleman B, Weinmann R: Machanism of action of DRB. Effect on specific in vitro initiation of transcription. J Mol Biol 167: 561–574, 1983

    Article  Google Scholar 

  63. Mukherjee R, Molloy GR: 5,6-Dichloro-l-β-D-ribofuranosylbenzimidazole inhibits transcription of the β-hemoglobin gene in vivo at initiation. J Biol Chem 262: 13697–13706, 1987

    PubMed  CAS  Google Scholar 

  64. Fraser NW, Sehgal PB, Darnell JE: DRB-induced premature termination of late adenovirus transcription. Nature 272: 590–593, 1978

    Article  PubMed  CAS  Google Scholar 

  65. Laub O, Jakobovits EB, Aloni Y: 5,6-Dichloro-l-β-D-ribofuranosylbenzimidazole enhances premature termination of late transcription of simian virus 40 DNA. Proc Natl Acad Sci USA 77: 3297–3301, 1980

    Article  PubMed  CAS  Google Scholar 

  66. Kephart DD, Marshall NF, Price DH: Stability of Drosophila RNA polymerase II elongation complexes in vitro. Mol Cell Biol 12: 2067–2077, 1992

    PubMed  CAS  Google Scholar 

  67. Nikolov DB, Burley SK: RNA polymerase II transcription initiation: A structural view. Proc Natl Acad Sci USA 94: 15–22, 1997

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell and Molecular Biology, Laboratory of Medical Cell Biology, Karolinska Institutet, Stockholm, Sweden

    E. Egyházi, A. Ossoinak & A. Pigon

  2. Biochimie de Régulations Cellulaires et Endocrines, Centre d’Études Nucleairés,, Institut National de la Santé et de la Recherche Médicale Unité 244, Grenoble Cedex, France

    O. Filhol-Cochet & C. Cochet

Authors
  1. E. Egyházi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Ossoinak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. Filhol-Cochet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Cochet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Pigon
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Cellular and Molecular Biochemistry, Research Laboratory (151) V.A. Medical Centre, One Veterans Drive, Minneapolis, MN, 55417, USA

    Khalil Ahmed

  2. Biokemisk Institut, Odense Universitet, Campusvej 55, DK-5230, Odense M, Denmark

    O. G. Issinger

  3. Laboratoire de Biochemie des Regulations Cellulaires Endocrines, INSERM U244 DBMS, CEA Grenoble, 17 rue des Martyrs, F-38054, Grenoble Cedex 9, France

    E. Chambaz

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Egyházi, E., Ossoinak, A., Filhol-Cochet, O., Cochet, C., Pigon, A. (1999). The binding of the α subunit of protein kinase CK2 and RAP74 subunit of TFIIF to protein-coding genes in living cells is DRB sensitive. In: Ahmed, K., Issinger, O.G., Chambaz, E. (eds) A Molecular and Cellular View of Protein Kinase CK2. Developments in Molecular and Cellular Biochemistry, vol 27. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-8624-5_19

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-8624-5_19

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-4648-7

  • Online ISBN: 978-1-4419-8624-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation