Home LiteratureArticle Details
PMID: 7841523 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis.

Molecular biology of the cell ·Vol. 5 ·No. 9 ·1994-09-00 ·Pages 955-66

Jiménez-García LF, Segura-Valdez ML, Ochs RL, Rothblum LI, Hannan R, Spector DL

Abstract

We have investigated the distribution of U3 snRNA and rRNA in HeLa cells and normal rat kidney cells during interphase and mitosis. U3 snRNA, known to be involved in pre-rRNA processing, was detected in nucleoli and coiled bodies during interphase, whereas rRNA was distributed in the nucleoli and throughout the cytoplasm. By comparison, ribosomal protein S6 was detected in nucleoli, coiled bodies, and in the cytoplasm. During nucleologenesis, pre-rRNA was observed in newly forming nucleoli during late telophase but not in prenucleolar bodies (PNBs), whereas U3 snRNA was detected in forming nucleoli and PNBs. Similar findings to those reported here for the localization of U3 snRNA have been reported previously for the U3 small nuclear ribonucleoprotein fibrillarin. These results suggest that components involved in pre-rRNA processing localize to discrete PNBs at the end of mitosis. The nucleolus is formed at specific telophase domains (nucleolar organizing regions) and the PNBs, containing factors essential for pre-rRNA processing, are recruited to these sites of rRNA transcription and processing.

MeSH Terms
Animals Cell Nucleolus/metabolism,ultrastructure Cells, Cultured HeLa Cells Humans Interphase Kidney Mitosis RNA Polymerase I/metabolism RNA Precursors/metabolism RNA, Small Nuclear/metabolism Rats Transcription, Genetic
Chemicals
RNA Precursors RNA, Small Nuclear RNA Polymerase I
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Jiménez-García L F
Laboratory of Electron Microscopy, Faculty of Sciences, National Autonomous University of Mexico, Mexico, D.F.
Segura-Valdez M L
Ochs R L
Rothblum L I
Hannan R
Spector D L
References (69)
69 references, click to expand
  1. The paranucleolar structure, accessory body of Cajal, sex chromatin, and related structures in nuclei of rat trigeminal neurons: a cytochemical and ultrastructural study.
    Anat Rec. 1969 Aug;164(4):403-31 PMID: 5797926
  2. 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
  3. Identification of the human U7 snRNP as one of several factors involved in the 3' end maturation of histone premessenger RNA's.
    Science. 1987 Dec 18;238(4834):1682-7 PMID: 2825355
  4. The primary structure of rat ribosomal protein S6.
    J Biol Chem. 1988 Feb 25;263(6):2891-6 PMID: 3277962
  5. Genes for human U3 small nucleolar RNA contain highly conserved flanking sequences.
    Biochim Biophys Acta. 1989 Jun 1;1008(1):14-22 PMID: 2719960
  6. 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
  7. 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
  8. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing.
    Cell. 1990 Mar 23;60(6):897-908 PMID: 2156625
  9. Functional and dynamic aspects of the mammalian nucleolus.
    Bioessays. 1990 Jan;12(1):14-21 PMID: 2181998
  10. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing.
    EMBO J. 1990 Jul;9(7):2299-308 PMID: 2357971
  11. 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
  12. Association between the nucleolus and the coiled body.
    J Struct Biol. 1990 Jul-Sep;104(1-3):120-7 PMID: 2088441
  13. 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
  14. In vivo detection of snRNP-rich organelles in the nuclei of mammalian cells.
    EMBO J. 1991 Jul;10(7):1863-73 PMID: 1710980
  15. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies.
    Exp Cell Res. 1991 Jul;195(1):27-37 PMID: 2055273
  16. Organization of nucleoli and nuclear bodies in osmotically stimulated supraoptic neurons of the rat.
    J Comp Neurol. 1991 Jun 15;308(3):329-39 PMID: 1865004
  17. Associations between distinct pre-mRNA splicing components and the cell nucleus.
    EMBO J. 1991 Nov;10(11):3467-81 PMID: 1833187
  18. 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
  19. A constitutive nucleolar protein identified as a member of the nucleoplasmin family.
    EMBO J. 1987 Jul;6(7):1881-90 PMID: 3308448
  20. LOCALIZATION OF DNA COMPLEMENTARY TO RIBOSOMAL RNA IN THE NUCLEOLUS ORGANIZER REGION OF DROSOPHILA MELANOGASTER.
    Proc Natl Acad Sci U S A. 1965 Apr;53:737-45 PMID: 14324529
  21. THE FINE STRUCTURE OF THE NUCLEOLUS DURING MITOSIS IN THE GRASSHOPPER NEUROBLAST CELL.
    J Cell Biol. 1965 Mar;24:349-68 PMID: 14326121
  22. A new staining procedure for electron microscopical cytology.
    J Ultrastruct Res. 1969 May;27(3):250-65 PMID: 4181256
  23. Fine structural organization of the interphase nucleus in some mammalian cells.
    J Ultrastruct Res. 1969 May;27(3):266-88 PMID: 5813971
  24. Depletion of U3 small nucleolar RNA inhibits cleavage in the 5' external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA.
    EMBO J. 1991 Dec;10(13):4231-9 PMID: 1756730
  25. U1 and U2 small nuclear RNAs are present in nuclear speckles.
    Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):305-8 PMID: 1530887
  26. Localization of U3 RNA molecules in nucleoli of HeLa and mouse 3T3 cells by high resolution in situ hybridization.
    Eur J Cell Biol. 1991 Dec;56(2):178-86 PMID: 1802706
  27. 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
  28. Differences in snRNP localization between transformed and nontransformed cells.
    Mol Biol Cell. 1992 May;3(5):555-69 PMID: 1535243
  29. Alterations of nucleolar ultrastructure and ribosome biogenesis by actinomycin D. Implications for U3 snRNP function.
    Eur J Cell Biol. 1992 Jun;58(1):149-62 PMID: 1386570
  30. In vitro assembly of prenucleolar bodies in Xenopus egg extract.
    J Cell Biol. 1992 Sep;118(6):1297-304 PMID: 1522108
  31. Assembly of snRNP-containing coiled bodies is regulated in interphase and mitosis--evidence that the coiled body is a kinetic nuclear structure.
    J Cell Biol. 1993 Feb;120(4):841-52 PMID: 7679389
  32. Immunocytochemical analysis of the coiled body in the cell cycle and during cell proliferation.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1947-51 PMID: 8446613
  33. In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism.
    Cell. 1993 Apr 9;73(1):47-59 PMID: 8462102
  34. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte.
    Cell. 1993 Jun 18;73(6):1233-45 PMID: 8513505
  35. 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
  36. Identification and characterization of a sphere organelle protein.
    J Cell Biol. 1993 Aug;122(4):767-73 PMID: 8349728
  37. Coiled bodies in the nucleolus of breast cancer cells.
    J Cell Sci. 1994 Feb;107 ( Pt 2):385-99 PMID: 8207070
  38. Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleolus remnant and in the prenucleolar bodies at telophase.
    J Cell Sci. 1994 Feb;107 ( Pt 2):463-75 PMID: 8207073
  39. Snurposomes and coiled bodies.
    Cold Spring Harb Symp Quant Biol. 1993;58:747-54 PMID: 7956092
  40. Structure and mode of formation of the nucleolus in meristematic cells of Vicia faba and Allium cepa.
    J Biophys Biochem Cytol. 1958 Nov 25;4(6):777-84 PMID: 13610944
  41. A correlated light and electron microscope study of the nucleolar material during mitosis in Vicia faba.
    J Cell Biol. 1963 Apr;17:167-201 PMID: 13928037
  42. Organization of argyrophilic nucleolar material throughout the division cycle of meristematic cells.
    Protoplasma. 1970;69(2):265-78 PMID: 4190596
  43. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  44. Regulation of synthesis and processing of nucleolar components in metaphase-arrested cells.
    J Mol Biol. 1971 Jul 14;59(1):27-42 PMID: 5283755
  45. Localisation of rapidly and slowly labelled nuclear RNA as visualized by high resolution autoradiography.
    Exp Cell Res. 1971 Jul;67(1):129-41 PMID: 4105558
  46. Nucleoli formation under inhibited RNA synthesis.
    Exp Cell Res. 1975 Jul;93(2):458-67 PMID: 1157830
  47. Rate of nucleologenesis as a measure of gene activity.
    Nature. 1975 Aug 7;256(5517):503-5 PMID: 1160996
  48. Visualization of nucleolar organizer regions im mammalian chromosomes using silver staining.
    Chromosoma. 1975 Nov 20;53(1):37-50 PMID: 53131
  49. Localization and characterization of newly synthesized nuclear RNA in isolate rat hepatocytes.
    Exp Cell Res. 1976 Apr;99(1):155-64 PMID: 944140
  50. The isolation of eukaryotic ribosomal proteins. The purification and characterization of the 40 S ribosomal subunit proteins S2, S3, S4, S5, S6, S7, S8, S9, S13, S23/S24, S27, and S28.
    J Biol Chem. 1976 Aug 10;251(15):4666-72 PMID: 947902
  51. Processing of RNA.
    Annu Rev Biochem. 1976;45:605-29 PMID: 786158
  52. Nucleolar transcription during plant mitosis. In situ assay for RNA polymerase activity.
    Exp Cell Res. 1976 Oct 15;102(2):311-6 PMID: 976350
  53. 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
  54. Histone genes are located at the sphere loci of newt lampbrush chromosomes.
    Chromosoma. 1981;84(2):159-71 PMID: 7327042
  55. Isolation and characterization of rat ribosomal DNA clones.
    Gene. 1982 Jan;17(1):75-7 PMID: 6281138
  56. Localization of acid phosphatase activity, phosphate ions and inorganic cations in plant nuclear coiled bodies.
    Cell Biol Int Rep. 1982 Jun;6(6):601-7 PMID: 6179638
  57. Nucleotide sequence of the region between the 18S rRNA sequence and the 28S rRNA sequence of rat ribosomal DNA.
    Nucleic Acids Res. 1982 Jun 25;10(12):3667-80 PMID: 6287418
  58. The "accessory body" of Cajal in the neuronal nucleus. A light and electron microscopic approach.
    Anat Embryol (Berl). 1983;166(1):19-30 PMID: 6301310
  59. Localization of nucleolar phosphoproteins B23 and C23 during mitosis.
    Exp Cell Res. 1983 Jun;146(1):139-49 PMID: 6345184
  60. Ultrastructural distribution of nuclear ribonucleoproteins as visualized by immunocytochemistry on thin sections.
    J Cell Biol. 1984 Jan;98(1):358-63 PMID: 6231300
  61. 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
  62. Nucleolar structure.
    Int Rev Cytol. 1984;87:107-58 PMID: 6201455
  63. Primary and secondary structure of rat 28 S ribosomal RNA.
    Nucleic Acids Res. 1984 Apr 25;12(8):3677-93 PMID: 6328433
  64. Nucleologenesis: composition and fate of prenucleolar bodies.
    Chromosoma. 1985;92(5):330-6 PMID: 3902398
  65. Purification and partial characterization of a nucleolar scleroderma antigen (Mr = 34,000; pI, 8.5) rich in NG,NG-dimethylarginine.
    J Biol Chem. 1985 Nov 15;260(26):14304-10 PMID: 2414294
  66. Fibrillarin: a new protein of the nucleolus identified by autoimmune sera.
    Biol Cell. 1985;54(2):123-33 PMID: 2933102
  67. Phosphoprotein pp135 is an essential component of the nucleolus organizer region (NOR).
    Exp Cell Res. 1986 Jan;162(1):11-22 PMID: 2415379
  68. Redistribution of U-snRNPs during mitosis.
    Exp Cell Res. 1986 Mar;163(1):87-94 PMID: 2935418
  69. Behaviour of nucleolus during mitosis. A comparative ultrastructural study of various cancerous cell lines using the Ag-NOR staining procedure.
    Chromosoma. 1987;95(2):95-107 PMID: 2439263
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
1994-09-00
Pages
955-66
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC301119
Subset
IM
Grants
NIGMS NIH HHS · R01 GM042694 · United States
NCI NIH HHS · 5P30CA-45508-06 · United States
NIGMS NIH HHS · GM-42694 · United States
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]