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PMID: 2780290 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Protein kinase NII and the regulation of rDNA transcription in mammalian cells.

Nucleic acids research ·Vol. 17 ·No. 16 ·1989-08-25 ·Pages 6625-36

Belenguer P, Baldin V, Mathieu C, Prats H, Bensaid M, Bouche G, Amalric F

Abstract

Transcription of ribosomal RNA genes is generally accepted to correlate with cell growth. Using primary cultures of adult bovine aortic endothelial (ABAE) cells, we have shown that transcription of rDNA in confluent cells falls to 5% of the transcription level in growing cells. Protein kinase NII appears to be a limiting factor to promote rDNA transcription in isolated nuclei of confluent cells. Protein kinase NII was detected by immunocytochemistry in the cytoplasm, nuclei and nucleoli of growing cells while it was no longer present in nucleoli of confluent cells. The kinase activity, in isolated nuclei, was estimated by endogenous phosphorylation of a specific substrate, nucleolin. A 10% residual activity was present in confluent cell nuclei compared to growing cell nuclei. Concomitantly, the transcription 'in vitro' of rDNA in the corresponding nuclei was also highly reduced (by 85%). Addition of exogenous protein kinase NII to confluent cell nuclei induced a strong increase in the phosphorylation of specific proteins including nucleolin. In parallel, the transcription of rDNA was increased by a factor of 5, to nearly the level observed in nuclei prepared from growing cells. These data suggest that, in confluent cells, factors necessary for rDNA transcription machinery are present but inactive in the nucleolus and that the phosphorylation of one or several of these factors (nucleolin, topoisomerase I,...) by protein kinase NII is a key event in the regulation of rDNA transcription.

MeSH Terms
Alkaline Phosphatase/metabolism Animals Cattle Cell Division Cells, Cultured DNA, Ribosomal/genetics Endothelium, Vascular/cytology,enzymology,metabolism Genes, Regulator Kinetics Nuclear Proteins/metabolism Phosphoproteins/metabolism Phosphorylation Protein Kinases/metabolism RNA-Binding Proteins Transcription, Genetic
Chemicals
DNA, Ribosomal Nuclear Proteins Phosphoproteins RNA-Binding Proteins nucleolin Protein Kinases protein kinase NII Alkaline Phosphatase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Belenguer P
Centre de Recherche de Biochimie et de Génétique Cellulaires du CNRS, Toulouse, France.
Baldin V
Mathieu C
Prats H
Bensaid M
Bouche G
Amalric F
References (34)
34 references, click to expand
  1. Adenosine 5'-triphosphate synthesis in Escherichia coli submitted to a microsecond electric pulse.
    Biochemistry. 1986 Jan 28;25(2):368-73 PMID: 3082356
  2. Transcription of cloned eukaryotic ribosomal RNA genes.
    Annu Rev Biochem. 1986;55:801-30 PMID: 3527052
  3. Isolation and sequencing of cDNA clones encoding alpha and beta subunits of Drosophila melanogaster casein kinase II.
    Mol Cell Biol. 1987 Oct;7(10):3409-17 PMID: 3119988
  4. A major nucleolar protein, nucleolin, induces chromatin decondensation by binding to histone H1.
    Eur J Biochem. 1988 Aug 15;175(3):525-30 PMID: 3409881
  5. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  6. Fractionation and reconstitution of factors required for accurate transcription of mammalian ribosomal RNA genes: identification of a species-dependent initiation factor.
    Nucleic Acids Res. 1982 Nov 11;10(21):6659-70 PMID: 7177852
  7. Role of phosphorylation on the maturation pathways of a 100 kDa nucleolar protein.
    FEBS Lett. 1983 May 8;155(2):218-22 PMID: 6852233
  8. A transcription terminator located upstream of the mouse rDNA initiation site affects rRNA synthesis.
    Cell. 1986 Dec 26;47(6):901-11 PMID: 3779845
  9. Structure and organization of mouse U3B RNA functional genes.
    J Biol Chem. 1988 Dec 25;263(36):19461-7 PMID: 3198636
  10. Activated sludge biodegradation of 12 commercial phthalate esters.
    Appl Environ Microbiol. 1985 Feb;49(2):443-5 PMID: 16346734
  11. Basic fibroblast growth factor enters the nucleolus and stimulates the transcription of ribosomal genes in ABAE cells undergoing G0----G1 transition.
    Proc Natl Acad Sci U S A. 1987 Oct;84(19):6770-4 PMID: 3477808
  12. Phosphoprotein phosphatase activity of Novikoff hepatoma nucleoli.
    Biochem Biophys Res Commun. 1976 Jun 7;70(3):717-22 PMID: 180995
  13. Effects of androgen and polyamines on the phosphorylation of nucleolar proteins from rat ventral prostates with particular reference to 110-kDa phosphoprotein.
    J Biol Chem. 1985 Jul 5;260(13):8050-5 PMID: 4008489
  14. Post-transcriptional regulation of glyceraldehyde-3-phosphate-dehydrogenase gene expression in rat tissues.
    Nucleic Acids Res. 1984 Sep 25;12(18):6951-63 PMID: 6548307
  15. Possible role of protein phosphorylation in the mitogenic effect of high density lipoproteins on cultured vascular endothelial cells.
    J Biol Chem. 1986 Jun 15;261(17):8002-8 PMID: 3486870
  16. Topoisomerase I phosphorylation in vitro and in rapidly growing Novikoff hepatoma cells.
    EMBO J. 1985 Nov;4(11):2921-6 PMID: 2998765
  17. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene.
    Nature. 1984 Oct 4-10;311(5985):433-8 PMID: 6090941
  18. A comparative study of "soluble" RNA polymerase activity of Zajdela hepatoma ascites cells and calf thymus.
    FEBS Lett. 1972 Apr 15;22(1):67-72 PMID: 11946563
  19. Protein serine/threonine kinases.
    Annu Rev Biochem. 1987;56:567-613 PMID: 2956925
  20. Transcriptional regulation of two serum-induced RNAs in mouse fibroblasts: equivalence of one species to B2 repetitive elements.
    Mol Cell Biol. 1985 Nov;5(11):3280-8 PMID: 3837843
  21. Polyamine-mediated phosphorylation of a nucleolar protein from Physarum polycephalum that stimulates rRNA synthesis.
    Proc Natl Acad Sci U S A. 1979 Jun;76(6):2541-5 PMID: 288043
  22. Hormonal regulation of transcription of rDNA. Inhibition of transcription during glucocorticoid-mediated inhibition of proliferation of lymphosarcoma P1798 cells in culture.
    J Biol Chem. 1983 Aug 25;258(16):9768-73 PMID: 6688417
  23. Control of nucleolar RNA synthesis by the intracellular pool sizes of ATP and GTP.
    Cell. 1976 Mar;7(3):447-53 PMID: 947552
  24. Clonal growth of bovine vascular endothelial cells: fibroblast growth factor as a survival agent.
    Proc Natl Acad Sci U S A. 1976 Nov;73(11):4120-4 PMID: 1069301
  25. c-myc gene is transcribed at high rate in G0-arrested fibroblasts and is post-transcriptionally regulated in response to growth factors.
    Nature. 1985 Oct 3-9;317(6036):443-5 PMID: 3900742
  26. Interrelations between the maturation of a 100 kDa nucleolar protein and pre rRNA synthesis in CHO cells.
    Nucleic Acids Res. 1984 Apr 11;12(7):3025-35 PMID: 6562463
  27. Casein kinase II accumulation in the nucleolus and its role in nucleolar phosphorylation.
    Biochim Biophys Acta. 1988 Apr 2;969(1):100-9 PMID: 3280036
  28. Amino acid starvation affects the initiation frequency of nucleolar RNA polymerase.
    Cell. 1976 Mar;7(3):439-45 PMID: 947551
  29. Two promoters of different strengths control the transcription of the mouse alpha-amylase gene Amy-1a in the parotid gland and the liver.
    Cell. 1983 Jun;33(2):501-8 PMID: 6190572
  30. Phosphorylation of nucleolin by a nucleolar type NII protein kinase.
    Biochemistry. 1987 Dec 1;26(24):7876-83 PMID: 3427111
  31. Growth in size and cell DNA replication.
    Exp Cell Res. 1984 Mar;151(1):1-5 PMID: 6321212
  32. Detection and localization of a class of proteins immunologically related to a 100-kDa nucleolar protein.
    Eur J Biochem. 1982 Nov 15;128(2-3):475-80 PMID: 7151790
  33. Specific dephosphorylation by phosphatases 1 and 2A of a nuclear protein structurally and immunologically related to nucleolin. Possible influence on the regulation of rRNA synthesis.
    Eur J Biochem. 1989 Mar 15;180(2):449-55 PMID: 2538332
  34. Polyamine-activated protein kinase reaction from nuclei and nucleoli of Physarum polycephalum which phosphorylates a unique Mr 70 000 nonhistone protein.
    Biochemistry. 1981 Apr 28;20(9):2525-32 PMID: 7236618
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
0305-1048
Published
1989-08-25
Pages
6625-36
Language
English
Region
England
NLM ID
0411011
PMCID
PMC318355
Subset
IM
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