Home LiteratureArticle Details
PMID: 9571237 Published · ppublish English Journal Article

Coiled bodies and U2 snRNA genes adjacent to coiled bodies are enriched in factors required for snRNA transcription.

Molecular biology of the cell ·Vol. 9 ·No. 5 ·1998-05-00 ·Pages 1025-36

Schul W, van Driel R, de Jong L

Abstract

A significant percentage of the gene clusters that contain the human genes for U1 small nuclear RNA (snRNA) or for U2 snRNA have been found associated with small nuclear domains, known as coiled bodies. We show here, by immunofluorescent labeling of human cells, that coiled bodies are enriched in factors required for the transcription of these snRNA genes. The 45-kDa gamma-subunit of the transcription factor, proximal element sequence-binding transcription factor (PTF), which is specific for the snRNA genes, was found in high concentrations in coiled bodies, along with the general transcription factor TATA-box binding protein and a subset of RNA polymerase II. We show that the transcription factors and RNA polymerase II are concentrated in irregularly shaped domains that not only overlap with coiled bodies but also extend to their immediate surroundings. Fluorescent in situ hybridization showed that these domains can overlap with U2 snRNA genes adjacent to coiled bodies. In addition, we found the domains to contain newly synthesized RNA, visualized by 5-bromo-uridine triphosphate labeling. Our data suggest that coiled bodies are involved in the expression of snRNA genes, which leads us to propose the model that coiled bodies are associated with snRNA genes to facilitate and regulate their transcription. These findings point to a general principle of higher order organization of gene expression in the nucleus.

MeSH Terms
Caco-2 Cells Cell Nucleus/metabolism DNA-Binding Proteins/metabolism HeLa Cells Humans RNA Polymerase II/metabolism RNA, Small Nuclear/genetics Ribonucleoprotein, U2 Small Nuclear/genetics TATA-Box Binding Protein Transcription Factor TFIIH Transcription Factors/metabolism Transcription Factors, TFII Tumor Cells, Cultured
Chemicals
DNA-Binding Proteins RNA, Small Nuclear Ribonucleoprotein, U2 Small Nuclear SNAPC protein complex, human TATA-Box Binding Protein Transcription Factors Transcription Factors, TFII Transcription Factor TFIIH RNA Polymerase II transcription factor TFIIF
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Schul W
E.C. Slater Instituut, University of Amsterdam, BioCentrum Amsterdam, 1018 TV Amsterdam, The Netherlands.
van Driel R
de Jong L
References (64)
64 references, click to expand
  1. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I.
    J Mol Biol. 1977 Jun 15;113(1):237-51 PMID: 881736
  2. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains.
    J Cell Biol. 1995 Apr;129(2):287-98 PMID: 7536746
  3. Retention and 5' cap trimethylation of U3 snRNA in the nucleus.
    Science. 1994 May 13;264(5161):959-61 PMID: 8178154
  4. The RNA 3' cleavage factors CstF 64 kDa and CPSF 100 kDa are concentrated in nuclear domains closely associated with coiled bodies and newly synthesized RNA.
    EMBO J. 1996 Jun 3;15(11):2883-92 PMID: 8654386
  5. Analysis of the autoantibody response to fibrillarin in human disease and murine models of autoimmunity.
    J Immunol. 1995 Jan 15;154(2):961-71 PMID: 7529293
  6. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  7. hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs.
    Nucleic Acids Res. 1992 Jul 25;20(14):3671-8 PMID: 1641332
  8. Regional and temporal specialization in the nucleus: a transcriptionally-active nuclear domain rich in PTF, Oct1 and PIKA antigens associates with specific chromosomes early in the cell cycle.
    EMBO J. 1998 Mar 16;17(6):1768-78 PMID: 9501098
  9. Nucleoplasmic organization of small nuclear ribonucleoproteins in cultured human cells.
    J Cell Biol. 1993 May;121(4):715-27 PMID: 8491767
  10. Human genes for U2 small nuclear RNA are tandemly repeated.
    Mol Cell Biol. 1984 Mar;4(3):492-9 PMID: 6201719
  11. U2 and U1 snRNA gene loci associate with coiled bodies.
    J Cell Biochem. 1995 Dec;59(4):473-85 PMID: 8749717
  12. Domain structure of a human general transcription initiation factor, TFIIF.
    Nucleic Acids Res. 1993 Jan 25;21(2):273-9 PMID: 8441635
  13. Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing.
    Cell. 1995 May 5;81(3):391-401 PMID: 7736591
  14. Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II.
    J Biol Chem. 1989 Jul 5;264(19):11511-20 PMID: 2472398
  15. Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis.
    Mol Biol Cell. 1994 Sep;5(9):955-66 PMID: 7841523
  16. Is the coiled body involved in nucleolar functions?
    Exp Cell Res. 1994 Apr;211(2):415-9 PMID: 8143790
  17. A multisubunit factor, CstF, is required for polyadenylation of mammalian pre-mRNAs.
    Genes Dev. 1990 Dec;4(12A):2112-20 PMID: 1980119
  18. Mutational analysis of p80 coilin indicates a functional interaction between coiled bodies and the nucleolus.
    J Cell Biol. 1995 Nov;131(4):817-31 PMID: 7490287
  19. The cdk7-cyclin H-MAT1 complex associated with TFIIH is localized in coiled bodies.
    Mol Biol Cell. 1997 Jul;8(7):1207-17 PMID: 9243502
  20. Targeting TBP to a non-TATA box cis-regulatory element: a TBP-containing complex activates transcription from snRNA promoters through the PSE.
    Genes Dev. 1993 Aug;7(8):1535-48 PMID: 8339931
  21. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition.
    J Cell Biol. 1996 Aug;134(4):815-26 PMID: 8769408
  22. Nuclear distribution of transcription factors in relation to sites of transcription and RNA polymerase II.
    J Cell Sci. 1997 Aug;110 ( Pt 15):1781-91 PMID: 9264465
  23. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  24. Mammalian nuclei contain foci which are highly enriched in components of the pre-mRNA splicing machinery.
    EMBO J. 1991 Jan;10(1):195-206 PMID: 1824936
  25. RNA polymerase II transcription initiation: a structural view.
    Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):15-22 PMID: 8990153
  26. Immunocytochemistry of the cell nucleus.
    Electron Microsc Rev. 1990;3(2):301-53 PMID: 2103346
  27. Nuclear ultrastructures associated with the RNA synthesis and processing.
    J Cell Biochem. 1995 Sep;59(1):11-26 PMID: 8530530
  28. Phosphorylation of RNA polymerase IIA occurs subsequent to interaction with the promoter and before the initiation of transcription.
    J Biol Chem. 1990 Aug 5;265(22):13165-73 PMID: 2376591
  29. Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies.
    J Cell Biol. 1992 Apr;117(1):1-14 PMID: 1532583
  30. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy.
    J Cell Sci. 1992 Nov;103 ( Pt 3):857-62 PMID: 1478975
  31. Cloning and characterization of SNAP50, a subunit of the snRNA-activating protein complex SNAPc.
    EMBO J. 1996 Dec 16;15(24):7129-36 PMID: 9003788
  32. Oct-1 and Oct-2 potentiate functional interactions of a transcription factor with the proximal sequence element of small nuclear RNA genes.
    Mol Cell Biol. 1992 Jul;12(7):3247-61 PMID: 1535687
  33. A TBP-TAF complex required for transcription of human snRNA genes by RNA polymerase II and III.
    Nature. 1995 Apr 13;374(6523):653-6 PMID: 7715707
  34. The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit IIa.
    J Biol Chem. 1989 Nov 25;264(33):19621-9 PMID: 2584185
  35. The N-terminal domain of the human TATA-binding protein plays a role in transcription from TATA-containing RNA polymerase II and III promoters.
    EMBO J. 1994 Mar 1;13(5):1166-75 PMID: 7510635
  36. Both Oct-1 and Oct-2A contain domains which can activate the ubiquitously expressed U2 snRNA genes.
    EMBO J. 1991 Aug;10(8):2291-6 PMID: 1829677
  37. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10004-8 PMID: 1946417
  38. The ERCC2/DNA repair protein is associated with the class II BTF2/TFIIH transcription factor.
    EMBO J. 1994 May 15;13(10):2388-92 PMID: 8194528
  39. True genes for human U1 small nuclear RNA. Copy number, polymorphism, and methylation.
    J Biol Chem. 1984 Feb 10;259(3):2013-21 PMID: 6198328
  40. U7 small nuclear RNA in C snurposomes of the Xenopus germinal vesicle.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6257-9 PMID: 8327506
  41. Distinct factors with Sp1 and NF-A specificities bind to adjacent functional elements of the human U2 snRNA gene enhancer.
    Genes Dev. 1987 Oct;1(8):808-17 PMID: 3428599
  42. Is the sphere organelle/coiled body a universal nuclear component?
    Dev Genet. 1995;16(1):25-35 PMID: 7758244
  43. Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding.
    Cell. 1986 Sep 12;46(6):905-11 PMID: 2944599
  44. 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
  45. Enzymatic synthesis of biotin-labeled polynucleotides: novel nucleic acid affinity probes.
    Proc Natl Acad Sci U S A. 1981 Nov;78(11):6633-7 PMID: 6273878
  46. A novel heterogeneous nuclear RNP protein with a unique distribution on nascent transcripts.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2575-87 PMID: 2687284
  47. Association of the neuron-specific RNA binding domain-containing protein ELAV with the coiled body in Drosophila neurons.
    Chromosoma. 1997 Apr;105(6):332-41 PMID: 9087375
  48. Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells.
    Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5915-9 PMID: 7597053
  49. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies.
    Exp Cell Res. 1991 Jul;195(1):27-37 PMID: 2055273
  50. The coiled body.
    Trends Cell Biol. 1993 Jun;3(6):198-204 PMID: 14731494
  51. Proximal sequence element-binding transcription factor (PTF) is a multisubunit complex required for transcription of both RNA polymerase II- and RNA polymerase III-dependent small nuclear RNA genes.
    Mol Cell Biol. 1995 Apr;15(4):2019-27 PMID: 7891697
  52. The SNAP45 subunit of the small nuclear RNA (snRNA) activating protein complex is required for RNA polymerase II and III snRNA gene transcription and interacts with the TATA box binding protein.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4289-93 PMID: 8633057
  53. Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity.
    EMBO J. 1997 Mar 17;16(6):1401-12 PMID: 9135155
  54. Nopp140 shuttles on tracks between nucleolus and cytoplasm.
    Cell. 1992 Jul 10;70(1):127-38 PMID: 1623516
  55. The interaction of RNA polymerase II with the adenovirus-2 major late promoter is precluded by phosphorylation of the C-terminal domain of subunit IIa.
    J Biol Chem. 1992 May 25;267(15):10500-6 PMID: 1316903
  56. Promoter-selective activation domains in Oct-1 and Oct-2 direct differential activation of an snRNA and mRNA promoter.
    Cell. 1992 Feb 21;68(4):755-67 PMID: 1739980
  57. Cooperative interactions between transcription factors Sp1 and OTF-1.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4732-6 PMID: 2191301
  58. Cloning of two proximal sequence element-binding transcription factor subunits (gamma and delta) that are required for transcription of small nuclear RNA genes by RNA polymerases II and III and interact with the TATA-binding protein.
    Mol Cell Biol. 1996 Jan;16(1):1-9 PMID: 8524284
  59. Newly synthesized small nuclear RNAs appear transiently in the cytoplasm.
    J Mol Biol. 1988 Jan 20;199(2):259-67 PMID: 3351925
  60. Identification of transcription factors required for the expression of mammalian U6 genes in vitro.
    EMBO J. 1991 Sep;10(9):2595-603 PMID: 1868835
  61. Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin.
    J Exp Med. 1991 Jun 1;173(6):1407-19 PMID: 2033369
  62. Cloning and characterization of the beta subunit of human proximal sequence element-binding transcription factor and its involvement in transcription of small nuclear RNA genes by RNA polymerases II and III.
    Mol Cell Biol. 1996 Oct;16(10):5419-26 PMID: 8816454
  63. Visualization of focal sites of transcription within human nuclei.
    EMBO J. 1993 Mar;12(3):1059-65 PMID: 8458323
  64. Molecular analysis of the coiled body.
    J Cell Sci Suppl. 1995;19:107-13 PMID: 8655641
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
DOI
10.1091/mbc.9.5.1025
Published
1998-05-00
Pages
1025-36
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC25327
Subset
IM
External Links
PubMed source DOI: 10.1091/mbc.9.5.1025 PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2