Home LiteratureArticle Details
PMID: 8609158 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs.

The Journal of cell biology ·Vol. 133 ·No. 2 ·1996-04-00 ·Pages 235-46

Roussel P, André C, Comai L, Hernandez-Verdun D

Abstract

In cycling cells, the rDNAs are expressed from telophase to the end of G2 phase. The early resumption of rDNA transcription at telophase raises the question of the fate of the rDNA transcription machinery during mitosis. At the beginning of mitosis, rDNA transcription is arrested, and the rDNAs are clustered in specific chromosomal sites, the nucleolar organizer regions (NOR). In human cells, we demonstrate that the rDNA transcription machinery, as defined in vitro, is colocalized in some NORs and absent from others whatever the mitotic phase: RNA polymerase I and the RNA polymerase I transcription factors, upstream binding factor and promoter selectivity factor (as verified for TATA-binding protein and TATA-binding protein-associated factor for RNA polymerase I [110]), were colocalized in the same NORs. The RNA polymerase I complex was localized using two different antibodies recognizing the two largest subunits or only the third largest subunit, respectively. These two antibodies immunoprecipitated the RNA polymerase I complex in interphase cells as well as in mitotic cells. These results clearly indicated that the RNA polymerase I complex remained assembled during mitosis. In addition, RNA polymerase I and the transcription factors varied in the same proportions in the positive NORs, suggesting stoichiometric association of these components. The fact that the rDNA transcription machinery is not equally distributed among NORs most likely reflects the implication of the different NORs during the subsequent interphase. Indeed, we demonstrate that only positive NORs exhibit transcription activity at telophase and that the level of transcription activity is related to the amount of rDNA transcription machinery present in the NOR. We propose that assembly of rDNA transcription machinery preceding mitosis determines expression of the rDNAs at the beginning of the next cell cycle. Consequently, the association of rDNAs with the rDNA transcription machinery defines the "active" NORs and the level of activity at the transition telophase/interphase.

MeSH Terms
Cell Nucleolus/chemistry DNA, Ribosomal/genetics DNA-Binding Proteins/analysis Drosophila Proteins HeLa Cells Humans Immune Sera Interphase Mitosis/genetics Nucleolus Organizer Region/chemistry,genetics Pol1 Transcription Initiation Complex Proteins RNA Polymerase I/analysis,metabolism TATA-Binding Protein Associated Factors TATA-Box Binding Protein Trans-Activators/analysis Transcription Factor TFIID Transcription Factors/analysis Transcription, Genetic/physiology
Chemicals
DNA, Ribosomal DNA-Binding Proteins Drosophila Proteins Immune Sera Pol1 Transcription Initiation Complex Proteins TAF1C protein, human TATA-Binding Protein Associated Factors TATA-Box Binding Protein Trans-Activators Transcription Factor TFIID Transcription Factors transcription factor UBF RNA Polymerase I
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Roussel P
Institut Jacques Monod, Paris, France.
André C
Comai L
Hernandez-Verdun D
References (50)
50 references, click to expand
  1. Molecular mechanisms governing species-specific transcription of ribosomal RNA.
    Cell. 1989 Nov 3;59(3):489-97 PMID: 2805069
  2. Nucleolar transcription factor hUBF contains a DNA-binding motif with homology to HMG proteins.
    Nature. 1990 Apr 26;344(6269):830-6 PMID: 2330041
  3. The nucleolus and ribosome formation.
    Curr Opin Cell Biol. 1990 Jun;2(3):521-7 PMID: 2198902
  4. A growth-dependent transcription initiation factor (TIF-IA) interacting with RNA polymerase I regulates mouse ribosomal RNA synthesis.
    EMBO J. 1990 Sep;9(9):2857-63 PMID: 2390974
  5. Quantitative determination of rDNA transcription units in vertebrate cells.
    Exp Cell Res. 1991 Mar;193(1):78-86 PMID: 1995304
  6. Human autoantibody to RNA polymerase I transcription factor hUBF. Molecular identity of nucleolus organizer region autoantigen NOR-90 and ribosomal RNA transcription upstream binding factor.
    J Exp Med. 1991 Nov 1;174(5):1239-44 PMID: 1940801
  7. Inheritance of ribosomal gene activity and level of DNA methylation of individual gene clusters in a three generation family.
    Hum Genet. 1991 Dec;88(2):146-52 PMID: 1721893
  8. The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1.
    Cell. 1992 Mar 6;68(5):965-76 PMID: 1547496
  9. Characterization and immunolocalization of a nucleolar antigen with anti-NOR serum in HeLa cells.
    Exp Cell Res. 1992 Jun;200(2):393-403 PMID: 1572405
  10. Nucleolin is an Ag-NOR protein; this property is determined by its amino-terminal domain independently of its phosphorylation state.
    Exp Cell Res. 1992 Nov;203(1):259-69 PMID: 1385190
  11. Localization of the RNA polymerase I transcription factor hUBF during the cell cycle.
    J Cell Sci. 1993 Feb;104 ( Pt 2):327-37 PMID: 8505363
  12. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus.
    J Cell Biol. 1993 Jul;122(2):283-93 PMID: 8320255
  13. TBP, a universal eukaryotic transcription factor?
    Genes Dev. 1993 Jul;7(7B):1291-308 PMID: 8330735
  14. Function of the growth-regulated transcription initiation factor TIF-IA in initiation complex formation at the murine ribosomal gene promoter.
    Mol Cell Biol. 1993 Nov;13(11):6723-32 PMID: 8413268
  15. A TBP-containing multiprotein complex (TIF-IB) mediates transcription specificity of murine RNA polymerase I.
    Nucleic Acids Res. 1993 Sep 11;21(18):4180-6 PMID: 8414971
  16. The RNA polymerase I-specific transcription initiation factor UBF is associated with transcriptionally active and inactive ribosomal genes.
    Chromosoma. 1993 Nov;102(9):599-611 PMID: 8306821
  17. The HMG box-containing nucleolar transcription factor UBF interacts with a specific subunit of RNA polymerase I.
    EMBO J. 1994 Jan 1;13(1):190-9 PMID: 8306961
  18. TBP-associated factors interact with DNA and govern species specificity of RNA polymerase I transcription.
    EMBO J. 1994 Jun 1;13(11):2611-6 PMID: 8013460
  19. Immunocytochemical characterization of human NOR-90 (upstream binding factor) and associated antigens reactive with autoimmune sera. Two MR forms of NOR-90/hUBF autoantigens.
    Mol Biol Rep. 1994 Mar;19(2):115-24 PMID: 8072492
  20. TIF-IC, a factor involved in both transcription initiation and elongation of RNA polymerase I.
    EMBO J. 1994 Sep 1;13(17):4028-35 PMID: 8076598
  21. Identification of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity.
    Exp Cell Res. 1994 Oct;214(2):465-72 PMID: 7523152
  22. High conservation of subunit composition of RNA polymerase I(A) between yeast and mouse and the molecular cloning of mouse RNA polymerase I 40-kDa subunit RPA40.
    J Biol Chem. 1994 Oct 28;269(43):26976-81 PMID: 7929437
  23. Reconstitution of transcription factor SL1: exclusive binding of TBP by SL1 or TFIID subunits.
    Science. 1994 Dec 23;266(5193):1966-72 PMID: 7801123
  24. Assembly of transcriptionally active RNA polymerase I initiation factor SL1 from recombinant subunits.
    Science. 1994 Dec 23;266(5193):2015-8 PMID: 7801130
  25. Amplified ribosomal RNA genes in a rat hepatoma cell line are enriched in 5-methylcytosine.
    Proc Natl Acad Sci U S A. 1981 Jan;78(1):489-93 PMID: 6165993
  26. Human nucleolus organizers on nonhomologous chromosomes can share the same ribosomal gene variants.
    Proc Natl Acad Sci U S A. 1981 Sep;78(9):5744-8 PMID: 6272316
  27. High-resolution analysis of human peripheral lymphocyte chromosomes by flow cytometry.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7727-31 PMID: 6950411
  28. Localization of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry.
    Proc Natl Acad Sci U S A. 1984 Mar;81(5):1431-5 PMID: 6369327
  29. Cytologic demonstration of differential activity of rRNA gene clusters in different human tissues.
    Hum Genet. 1985;69(3):212-7 PMID: 2579890
  30. Eukaryotic RNA polymerases.
    CRC Crit Rev Biochem. 1985;18(1):31-90 PMID: 3893883
  31. Structural and functional aspects of nucleolar organizer regions (NORs) of human chromosomes.
    Int Rev Cytol. 1985;94:151-76 PMID: 2410391
  32. Scl 70 autoantibodies from scleroderma patients recognize a 95 kDa protein identified as DNA topoisomerase I.
    Chromosoma. 1986;94(2):132-8 PMID: 2428564
  33. Inhibition of nucleolar reformation after microinjection of antibodies to RNA polymerase I into mitotic cells.
    J Cell Biol. 1987 Oct;105(4):1483-91 PMID: 3312231
  34. Functional cooperativity between transcription factors UBF1 and SL1 mediates human ribosomal RNA synthesis.
    Science. 1988 Sep 2;241(4870):1192-7 PMID: 3413483
  35. Identification and definition of nucleolus-related fibrillar bodies in micronucleated cells.
    Exp Cell Res. 1988 Oct;178(2):518-23 PMID: 3049124
  36. Immunocytogenetics: localization of transcriptionally active rRNA genes in nucleoli and nucleolus organizer regions by use of human autoantibodies to RNA polymerase I.
    Cytogenet Cell Genet. 1988;48(1):35-42 PMID: 3053054
  37. Three-dimensional organization of micronuclei induced by colchicine in PtK1 cells.
    Exp Cell Res. 1989 Mar;181(1):27-39 PMID: 2917606
  38. Nucleologenesis: use of non-isotopic in situ hybridization and immunocytochemistry to compare the localization of rDNA and nucleolar proteins during mitosis.
    Biol Cell. 1989;65(3):239-46 PMID: 2752212
  39. A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis.
    J Cell Biol. 1995 May;129(3):561-75 PMID: 7730396
  40. Three-dimensional co-location of RNA polymerase I and DNA during interphase and mitosis by confocal microscopy.
    J Cell Sci. 1995 Jan;108 ( Pt 1):115-25 PMID: 7738089
  41. Cellular sites of RNA synthesis.
    Prog Nucleic Acid Res Mol Biol. 1964;3:33-57 PMID: 5318918
  42. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  43. Location of ribosomal DNA in the human chromosome complement.
    Proc Natl Acad Sci U S A. 1972 Nov;69(11):3394-8 PMID: 4508329
  44. Localization of DNA-dependent RNA polymerase activities in fixed human fibroblasts by autoradiography.
    Exp Cell Res. 1973 Jan;76(1):223-8 PMID: 4682648
  45. Visualization of nucleolar organizer regions im mammalian chromosomes using silver staining.
    Chromosoma. 1975 Nov 20;53(1):37-50 PMID: 53131
  46. Suppression of human nucleolus organizer activity in mouse-human somatic hybrid cells.
    Exp Cell Res. 1976 Sep;101(2):235-43 PMID: 61125
  47. Detection of nucleolus organizer regions in chromosomes of human, chimpanzee, gorilla, orangutan and gibbon.
    Chromosoma. 1976 Jun 30;56(1):15-27 PMID: 61844
  48. Expression of human and suppression of mouse nucleolus organizer activity in mouse-human somatic cell hybrids.
    Proc Natl Acad Sci U S A. 1976 Dec;73(12):4531-5 PMID: 1070003
  49. Quantitative conservation of chromatin-bound RNA polymerases I and II in mitosis. Implications for chromosome structure.
    J Cell Biol. 1979 Feb;80(2):451-64 PMID: 457752
  50. Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method.
    Experientia. 1980 Aug 15;36(8):1014-5 PMID: 6160049
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1996-04-00
Pages
235-46
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120807
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]