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PMID: 10588665 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Assembly of the nuclear transcription and processing machinery: Cajal bodies (coiled bodies) and transcriptosomes.

Molecular biology of the cell ·Vol. 10 ·No. 12 ·1999-12-00 ·Pages 4385-402

Gall JG, Bellini M, Wu Z, Murphy C

Abstract

We have examined the distribution of RNA transcription and processing factors in the amphibian oocyte nucleus or germinal vesicle. RNA polymerase I (pol I), pol II, and pol III occur in the Cajal bodies (coiled bodies) along with various components required for transcription and processing of the three classes of nuclear transcripts: mRNA, rRNA, and pol III transcripts. Among these components are transcription factor IIF (TFIIF), TFIIS, splicing factors, the U7 small nuclear ribonucleoprotein particle, the stem-loop binding protein, SR proteins, cleavage and polyadenylation factors, small nucleolar RNAs, nucleolar proteins that are probably involved in pre-rRNA processing, and TFIIIA. Earlier studies and data presented here show that several of these components are first targeted to Cajal bodies when injected into the oocyte and only subsequently appear in the chromosomes or nucleoli, where transcription itself occurs. We suggest that pol I, pol II, and pol III transcription and processing components are preassembled in Cajal bodies before transport to the chromosomes and nucleoli. Most components of the pol II transcription and processing pathway that occur in Cajal bodies are also found in the many hundreds of B-snurposomes in the germinal vesicle. Electron microscopic images show that B-snurposomes consist primarily, if not exclusively, of 20- to 30-nm particles, which closely resemble the interchromatin granules described from sections of somatic nuclei. We suggest the name pol II transcriptosome for these particles to emphasize their content of factors involved in synthesis and processing of mRNA transcripts. We present a model in which pol I, pol II, and pol III transcriptosomes are assembled in the Cajal bodies before export to the nucleolus (pol I), to the B-snurposomes and eventually to the chromosomes (pol II), and directly to the chromosomes (pol III). The key feature of this model is the preassembly of the transcription and processing machinery into unitary particles. An analogy can be made between ribosomes and transcriptosomes, ribosomes being unitary particles involved in translation and transcriptosomes being unitary particles for transcription and processing of RNA.

MeSH Terms
Animals Cell Nucleolus/metabolism,ultrastructure Cell Nucleus/metabolism,ultrastructure DNA-Directed RNA Polymerases/metabolism Female Fluorescent Antibody Technique In Situ Hybridization Microscopy, Electron Notophthalmus viridescens Oocytes/cytology,metabolism,ultrastructure RNA Polymerase I/metabolism RNA Polymerase II/metabolism RNA Polymerase III/metabolism Ribonucleoproteins, Small Nuclear/metabolism Transcription Factors/metabolism Transcription, Genetic/physiology Xenopus laevis
Chemicals
Ribonucleoproteins, Small Nuclear Transcription Factors RNA Polymerase II DNA-Directed RNA Polymerases RNA Polymerase I RNA Polymerase III
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Gall J G
Department of Embryology, Carnegie Institution, Baltimore, Maryland 21210, USA. gall@mail1.ciwemb.edu
Bellini M
Wu Z
Murphy C
References (101)
101 references, click to expand
  1. Nuclear domains enriched in RNA 3'-processing factors associate with coiled bodies and histone genes in a cell cycle-dependent manner.
    Mol Biol Cell. 1999 Nov;10(11):3815-24 PMID: 10564273
  2. Structure and composition of peripheral nucleoli of salamander oocytes.
    Natl Cancer Inst Monogr. 1966 Dec;23:53-66 PMID: 6007154
  3. Specific gene amplification in oocytes. Oocyte nuclei contain extrachromosomal replicas of the genes for ribosomal RNA.
    Science. 1968 Apr 19;160(3825):272-80 PMID: 4867987
  4. [Structure and function of oocyte chromosomes nucleoli and as well as the extra DNA during oogenesis in panoistic and meroistic insects].
    Chromosoma. 1967;23(2):214-54 PMID: 4875166
  5. Differential synthesis of the genes for ribosomal RNA during amphibian oögenesis.
    Proc Natl Acad Sci U S A. 1968 Jun;60(2):553-60 PMID: 5248812
  6. Fine structural organization of the interphase nucleus in some mammalian cells.
    J Ultrastruct Res. 1969 May;27(3):266-88 PMID: 5813971
  7. Pattern of incorporation of (3H)uridine into RNA of amphibian oocyte nucleoli.
    J Cell Sci. 1967 Jun;2(2):145-50 PMID: 4104121
  8. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals.
    J Morphol. 1972 Feb;136(2):153-79 PMID: 4109871
  9. Visualization of RNA synthesis on chromosomes.
    Int Rev Cytol. 1972;33:1-25 PMID: 4562602
  10. Protein incorporation by isolated amphibian oocytes. 3. Optimum incubation conditions.
    J Exp Zool. 1973 Jun;184(3):321-33 PMID: 4708138
  11. The nucleolus and its genes in amphibian oogenesis.
    Biol Rev Camb Philos Soc. 1972 May;47(2):177-210 PMID: 4587818
  12. Incorporation of tritiated uridine in nuclei of Triturus oocytes treated with alpha-amanitin.
    Exp Cell Res. 1971 Dec;69(2):462-5 PMID: 4950441
  13. Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes.
    Cell. 1980 Mar;19(3):717-28 PMID: 6153931
  14. The ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution.
    Int Rev Cytol. 1980;65:255-99 PMID: 6156137
  15. A specific transcription factor that can bind either the 5S RNA gene or 5S RNA.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):4170-4 PMID: 7001457
  16. In vitro RNA synthesis in oocyte nuclei of the newt Notophthalmus.
    Chromosoma. 1981;82(2):171-87 PMID: 6164523
  17. 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
  18. 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
  19. Identification and characterization of a sphere organelle protein.
    J Cell Biol. 1993 Aug;122(4):767-73 PMID: 8349728
  20. Requirements for nuclear translocation and nucleolar accumulation of nucleolin of Xenopus laevis.
    Eur J Cell Biol. 1993 Aug;61(2):369-82 PMID: 8223724
  21. Macromolecular domains within the cell nucleus.
    Annu Rev Cell Biol. 1993;9:265-315 PMID: 8280462
  22. Structure and function in the nucleus.
    Science. 1998 Apr 24;280(5363):547-53 PMID: 9554838
  23. Coiled bodies and U2 snRNA genes adjacent to coiled bodies are enriched in factors required for snRNA transcription.
    Mol Biol Cell. 1998 May;9(5):1025-36 PMID: 9571237
  24. Conserved boxes C and D are essential nucleolar localization elements of U14 and U8 snoRNAs.
    EMBO J. 1998 Jun 1;17(11):3176-87 PMID: 9606199
  25. Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease.
    Proc Natl Acad Sci U S A. 1981 May;78(5):2737-41 PMID: 6789322
  26. Identification and localization of a novel nucleolar protein of high molecular weight by a monoclonal antibody.
    Exp Cell Res. 1984 Aug;153(2):327-46 PMID: 6539710
  27. Monoclonal antibodies to lampbrush chromosome antigens of Pleurodeles waltlii.
    Chromosoma. 1985;92(1):69-80 PMID: 3891248
  28. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product.
    Mol Cell Biol. 1985 Dec;5(12):3610-6 PMID: 3915782
  29. Lampbrush chromosomes.
    Mol Biol Biochem Biophys. 1986;36:1-252 PMID: 3531807
  30. The lampbrush chromosomes of Xenopus laevis: preparation, identification, and distribution of 5S DNA sequences.
    Chromosoma. 1987;95(4):236-50 PMID: 3622079
  31. A constitutive nucleolar protein identified as a member of the nucleoplasmin family.
    EMBO J. 1987 Jul;6(7):1881-90 PMID: 3308448
  32. Monoclonal antibodies that recognize transcription unit proteins on newt lampbrush chromosomes.
    J Cell Biol. 1987 Sep;105(3):1047-54 PMID: 3308902
  33. Functional characterization of X. laevis U5 snRNA genes.
    EMBO J. 1987 Oct;6(10):3071-8 PMID: 3691481
  34. Assembly of functional U1 and U2 human-amphibian hybrid snRNPs in Xenopus laevis oocytes.
    Science. 1988 Sep 9;241(4871):1328-31 PMID: 2970672
  35. Targeting of a chromosomal protein to the nucleus and to lampbrush chromosome loops.
    Proc Natl Acad Sci U S A. 1989 Feb;86(4):1269-72 PMID: 2919175
  36. 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
  37. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus.
    EMBO J. 1989 Oct;8(10):3113-9 PMID: 2531075
  38. Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus.
    Nature. 1990 Feb 1;343(6257):437-41 PMID: 2137203
  39. A monoclonal antibody that recognizes a phosphorylated epitope stains lampbrush chromosome loops and small granules in the amphibian germinal vesicle.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2217-23 PMID: 1703534
  40. Small nuclear ribonucleoproteins and heterogeneous nuclear ribonucleoproteins in the amphibian germinal vesicle: loops, spheres, and snurposomes.
    J Cell Biol. 1991 May;113(3):465-83 PMID: 1826687
  41. 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
  42. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies.
    Exp Cell Res. 1991 Jul;195(1):27-37 PMID: 2055273
  43. A conserved family of nuclear phosphoproteins localized to sites of polymerase II transcription.
    J Cell Biol. 1991 Nov;115(3):587-96 PMID: 1717489
  44. Two-step affinity purification of U7 small nuclear ribonucleoprotein particles using complementary biotinylated 2'-O-methyl oligoribonucleotides.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9784-8 PMID: 1835087
  45. Localization of the nucleolar protein NO38 in amphibian oocytes.
    J Cell Biol. 1992 Jan;116(1):1-14 PMID: 1730739
  46. Association of RNA with the B and C snurposomes of Xenopus oocyte nuclei.
    Chromosoma. 1991 Nov;101(2):69-82 PMID: 1722746
  47. SR proteins: a conserved family of pre-mRNA splicing factors.
    Genes Dev. 1992 May;6(5):837-47 PMID: 1577277
  48. Nopp140 shuttles on tracks between nucleolus and cytoplasm.
    Cell. 1992 Jul 10;70(1):127-38 PMID: 1623516
  49. Transcription on lampbrush chromosome loops in the absence of U2 snRNA.
    Mol Biol Cell. 1992 Mar;3(3):249-61 PMID: 1627829
  50. Assembly and localization of the U1-specific snRNP C protein in the amphibian oocyte.
    J Cell Biol. 1992 Dec;119(5):1037-46 PMID: 1447287
  51. Visualization of focal sites of transcription within human nuclei.
    EMBO J. 1993 Mar;12(3):1059-65 PMID: 8458323
  52. Positive patches and negative noodles: linking RNA processing to transcription?
    Trends Biochem Sci. 1993 Apr;18(4):117-9 PMID: 8493720
  53. The cellular organization of gene expression.
    Curr Opin Cell Biol. 1998 Jun;10(3):323-31 PMID: 9640532
  54. The snoRNA box C/D motif directs nucleolar targeting and also couples snoRNA synthesis and localization.
    EMBO J. 1998 Jul 1;17(13):3747-57 PMID: 9649444
  55. Localization and processing from a polycistronic precursor of novel snoRNAs in maize.
    J Cell Sci. 1998 Aug;111 ( Pt 15):2121-8 PMID: 9664033
  56. Nucleolar localization elements in U8 snoRNA differ from sequences required for rRNA processing.
    RNA. 1998 Jul;4(7):789-800 PMID: 9671052
  57. Of coiled bodies, gems, and salmon.
    J Cell Biochem. 1998 Aug 1;70(2):181-92 PMID: 9671224
  58. In vitro assembly of coiled bodies in Xenopus egg extract.
    Mol Biol Cell. 1994 Jun;5(6):633-44 PMID: 7949420
  59. Snurposomes and coiled bodies.
    Cold Spring Harb Symp Quant Biol. 1993;58:747-54 PMID: 7956092
  60. Characterization of cleavage and polyadenylation specificity factor and cloning of its 100-kilodalton subunit.
    Mol Cell Biol. 1994 Dec;14(12):8183-90 PMID: 7969155
  61. A polyadenylation factor subunit is the human homologue of the Drosophila suppressor of forked protein.
    Nature. 1994 Dec 1;372(6505):471-4 PMID: 7984242
  62. NAP57, a mammalian nucleolar protein with a putative homolog in yeast and bacteria.
    J Cell Biol. 1994 Dec;127(6 Pt 1):1505-14 PMID: 7798307
  63. 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
  64. Organization of small nucleolar ribonucleoproteins (snoRNPs) by fluorescence in situ hybridization and immunocytochemistry.
    Mol Biol Cell. 1994 Dec;5(12):1289-99 PMID: 7535131
  65. 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
  66. Is the sphere organelle/coiled body a universal nuclear component?
    Dev Genet. 1995;16(1):25-35 PMID: 7758244
  67. 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
  68. The small nucleolar RNAs.
    Annu Rev Biochem. 1995;64:897-934 PMID: 7574504
  69. Molecular analysis of the coiled body.
    J Cell Sci Suppl. 1995;19:107-13 PMID: 8655641
  70. In vivo evidence that TATA-binding protein/SL1 colocalizes with UBF and RNA polymerase I when rRNA synthesis is either active or inactive.
    J Cell Biol. 1996 Apr;133(2):225-34 PMID: 8609157
  71. 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
  72. The Sm binding site targets U7 snRNA to coiled bodies (spheres) of amphibian oocytes.
    RNA. 1996 Aug;2(8):811-23 PMID: 8752090
  73. Nuclear domains involved in RNA synthesis, RNA processing, and replication.
    Crit Rev Eukaryot Gene Expr. 1996;6(2-3):215-46 PMID: 8855389
  74. Gene expression: increasing evidence for a transcriptosome.
    Trends Genet. 1996 May;12(5):161-3 PMID: 8984727
  75. Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA.
    J Cell Biol. 1997 Jan 13;136(1):19-28 PMID: 9008700
  76. The autoimmunity-inducing xenobiotic mercury interacts with the autoantigen fibrillarin and modifies its molecular and antigenic properties.
    J Immunol. 1997 Apr 1;158(7):3521-8 PMID: 9120314
  77. RNA polymerase II holoenzyme and transcriptional regulation.
    Curr Opin Cell Biol. 1997 Jun;9(3):310-9 PMID: 9159076
  78. Pre-mRNA processing and the CTD of RNA polymerase II: the tail that wags the dog?
    Cell. 1997 May 16;89(4):491-4 PMID: 9160740
  79. Sno storm in the nucleolus: new roles for myriad small RNPs.
    Cell. 1997 May 30;89(5):669-72 PMID: 9182752
  80. Guiding ribose methylation of rRNA.
    Trends Biochem Sci. 1997 Jul;22(7):257-61 PMID: 9255067
  81. 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
  82. Identification of an autonomously initiating RNA polymerase III holoenzyme containing a novel factor that is selectively inactivated during protein synthesis inhibition.
    Genes Dev. 1997 Sep 15;11(18):2371-82 PMID: 9308965
  83. Affinity purification of mammalian RNA polymerase I. Identification of an associated kinase.
    J Biol Chem. 1998 Jan 9;273(2):1257-67 PMID: 9422795
  84. Mammalian RNA polymerase I exists as a holoenzyme with associated basal transcription factors.
    J Mol Biol. 1998 Jan 9;275(1):43-53 PMID: 9451438
  85. Growth-related changes in phosphorylation of yeast RNA polymerase II.
    J Biol Chem. 1998 Feb 20;273(8):4689-94 PMID: 9468530
  86. Nucleolar localization elements of Xenopus laevis U3 small nucleolar RNA.
    Mol Biol Cell. 1998 Oct;9(10):2973-85 PMID: 9763456
  87. Coilin can form a complex with the U7 small nuclear ribonucleoprotein.
    Mol Biol Cell. 1998 Oct;9(10):2987-3001 PMID: 9763457
  88. RNA polymerase II holoenzymes and subcomplexes.
    J Biol Chem. 1998 Oct 23;273(43):27757-60 PMID: 9774381
  89. Regulatory targets in the RNA polymerase II holoenzyme.
    Curr Opin Genet Dev. 1998 Oct;8(5):565-70 PMID: 9794828
  90. The stem-loop binding protein (SLBP1) is present in coiled bodies of the Xenopus germinal vesicle.
    Mol Biol Cell. 1999 Feb;10(2):487-99 PMID: 9950690
  91. Regional specialization in human nuclei: visualization of discrete sites of transcription by RNA polymerase III.
    EMBO J. 1999 Apr 15;18(8):2241-53 PMID: 10205177
  92. Role of general and gene-specific cofactors in the regulation of eukaryotic transcription.
    Cold Spring Harb Symp Quant Biol. 1998;63:201-18 PMID: 10384284
  93. Coupling RNA polymerase II transcription with pre-mRNA processing.
    Curr Opin Cell Biol. 1999 Jun;11(3):347-51 PMID: 10395561
  94. mRNA polyadenylation and its coupling to other RNA processing reactions and to transcription.
    Curr Opin Cell Biol. 1999 Jun;11(3):352-7 PMID: 10395555
  95. Guided tours: from precursor snoRNA to functional snoRNP.
    Curr Opin Cell Biol. 1999 Jun;11(3):378-84 PMID: 10395551
  96. Structure and function of the nucleolus.
    Curr Opin Cell Biol. 1999 Jun;11(3):385-90 PMID: 10395554
  97. Role of the box C/D motif in localization of small nucleolar RNAs to coiled bodies and nucleoli.
    Mol Biol Cell. 1999 Jul;10(7):2131-47 PMID: 10397754
  98. Nuclear bodies: multifaceted subdomains of the interchromatin space.
    Trends Cell Biol. 1999 Aug;9(8):302-9 PMID: 10407409
  99. Purification and biochemical characterization of interchromatin granule clusters.
    EMBO J. 1999 Aug 2;18(15):4308-20 PMID: 10428969
  100. H3 uridine incorporation in lampbrush chromosomes.
    Proc Natl Acad Sci U S A. 1962 Apr 15;48:562-70 PMID: 13896377
  101. The relationship between RNA synthesis and loop structure in lampbrush chromosomes.
    Proc Natl Acad Sci U S A. 1963 Apr;49:544-51 PMID: 13957141
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
1999-12-00
Pages
4385-402
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC25765
Subset
IM
Grants
NIGMS NIH HHS · R01 GM033397 · United States
NIGMS NIH HHS · R37 GM033397 · United States
NIGMS NIH HHS · GM-33397 · United States
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