Home LiteratureArticle Details
PMID: 9725903 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Partially processed pre-rRNA is preserved in association with processing components in nucleolus-derived foci during mitosis.

Molecular biology of the cell ·Vol. 9 ·No. 9 ·1998-09-00 ·Pages 2407-22

Dundr M, Olson MO

Abstract

Previous studies showed that components implicated in pre-rRNA processing, including U3 small nucleolar (sno)RNA, fibrillarin, nucleolin, and proteins B23 and p52, accumulate in perichromosomal regions and in numerous mitotic cytoplasmic particles, termed nucleolus-derived foci (NDF) between early anaphase and late telophase. The latter structures were analyzed for the presence of pre-rRNA by fluorescence in situ hybridization using probes for segments of pre-rRNA with known half-lives. The NDF did not contain the short-lived 5'-external transcribed spacer (ETS) leader segment upstream from the primary processing site in 47S pre-rRNA. However, the NDF contained sequences from the 5'-ETS core, 18S, internal transcribed spacer 1 (ITS1), and 28S segments and also had detectable, but significantly reduced, levels of the 3'-ETS sequence. Northern analyses showed that in mitotic cells, the latter sequences were present predominantly in 45S-46S pre-rRNAs, indicating that high-molecular weight processing intermediates are preserved during mitosis. Two additional essential processing components were also found in the NDF: U8 snoRNA and hPop1 (a protein component of RNase MRP and RNase P). Thus, the NDF appear to be large complexes containing partially processed pre-rRNA associated with processing components in which processing has been significantly suppressed. The NDF may facilitate coordinated assembly of postmitotic nucleoli.

MeSH Terms
5' Untranslated Regions Animals Apoptosis Regulatory Proteins Carrier Proteins Cell Line Cell Nucleolus/metabolism Endoribonucleases/metabolism Haplorhini Humans Mitosis/physiology RNA Precursors RNA Processing, Post-Transcriptional RNA, Catalytic/metabolism RNA, Ribosomal, 18S RNA, Ribosomal, 28S RNA, Small Nuclear Ribonuclease P Ribonucleoproteins/analysis
Chemicals
5' Untranslated Regions Apoptosis Regulatory Proteins Carrier Proteins POP1 protein, human RNA Precursors RNA, Catalytic RNA, Ribosomal, 18S RNA, Ribosomal, 28S RNA, Small Nuclear Ribonucleoproteins Endoribonucleases mitochondrial RNA-processing endoribonuclease RPP14 protein, human Ribonuclease P
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Dundr M
Department of Biochemistry, University of Mississippi Medical Center, Jackson, Mississippi 39216-4505, USA.
Olson M O
References (67)
67 references, click to expand
  1. Nucleolin is a sequence-specific RNA-binding protein: characterization of targets on pre-ribosomal RNA.
    J Mol Biol. 1996 Jul 5;260(1):34-53 PMID: 8676391
  2. A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis.
    J Cell Biol. 1995 May;129(3):561-75 PMID: 7730396
  3. U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing.
    Genes Dev. 1995 Oct 1;9(19):2433-43 PMID: 7557394
  4. Mitotic repression of RNA polymerase III transcription in vitro mediated by phosphorylation of a TFIIIB component.
    Science. 1994 Jan 7;263(5143):81-4 PMID: 8272869
  5. 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
  6. Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Mar;10(3):1145-52 PMID: 2406561
  7. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing.
    Cell. 1990 Mar 23;60(6):897-908 PMID: 2156625
  8. Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein.
    Mol Cell Biol. 1997 Aug;17(8):4230-7 PMID: 9234680
  9. 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
  10. 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
  11. Functional and dynamic aspects of the mammalian nucleolus.
    Bioessays. 1990 Jan;12(1):14-21 PMID: 2181998
  12. The RNA of RNase MRP is required for normal processing of ribosomal RNA.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):659-63 PMID: 8290578
  13. Cloning of murine RNA polymerase I-specific TAF factors: conserved interactions between the subunits of the species-specific transcription initiation factor TIF-IB/SL1.
    Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1733-8 PMID: 9050847
  14. Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis.
    EMBO J. 1995 Sep 1;14(17):4350-6 PMID: 7556076
  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. A molecular basis for discrete size variation in human ribosomal DNA.
    Am J Hum Genet. 1985 Mar;37(2):311-25 PMID: 2984926
  17. Structure and variation of human ribosomal DNA: molecular analysis of cloned fragments.
    Gene. 1981 Dec;16(1-3):1-9 PMID: 6282683
  18. Repopulation of postmitotic nucleoli by preformed RNA. II. Ultrastructure.
    J Cell Biol. 1973 Jul;58(1):54-63 PMID: 4726308
  19. Reassembly of functional nucleoli following in situ unraveling by low-ionic-strength treatment of cultured mammalian cells.
    Exp Cell Res. 1997 May 25;233(1):155-68 PMID: 9184085
  20. Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis.
    Eur J Biochem. 1993 Feb 15;212(1):211-5 PMID: 8444156
  21. hPop1: an autoantigenic protein subunit shared by the human RNase P and RNase MRP ribonucleoproteins.
    EMBO J. 1996 Nov 1;15(21):5936-48 PMID: 8918471
  22. The nucleolus.
    Annu Rev Cell Dev Biol. 1995;11:93-121 PMID: 8689574
  23. Identification and characterization of a new set of nucleolar ribonucleoproteins which line the chromosomes during mitosis.
    Exp Cell Res. 1992 May;200(1):5-15 PMID: 1563493
  24. Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridization.
    Chromosoma. 1997 Jun;105(7-8):481-95 PMID: 9211976
  25. Structure, function and assembly of the nucleolus.
    Trends Cell Biol. 1993 Jul;3(7):236-41 PMID: 14731759
  26. Mpp10p, a U3 small nucleolar ribonucleoprotein component required for pre-18S rRNA processing in yeast.
    Mol Cell Biol. 1997 Oct;17(10):5803-12 PMID: 9315638
  27. Cell cycle regulation of RNA polymerase III transcription.
    Mol Cell Biol. 1995 Dec;15(12):6653-62 PMID: 8524230
  28. STUDIES ON SYNCHRONOUS DIVISION OF TISSUE CULTURE CELLS INITIATED BY EXCESS THYMIDINE.
    Exp Cell Res. 1964 Jan;33:301-9 PMID: 14109144
  29. Rpp1, an essential protein subunit of nuclear RNase P required for processing of precursor tRNA and 35S precursor rRNA in Saccharomyces cerevisiae.
    Genes Dev. 1997 Nov 1;11(21):2926-37 PMID: 9353260
  30. The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs.
    J Cell Biol. 1996 Apr;133(2):235-46 PMID: 8609158
  31. Synthesis of RNA and protein during mitosis in mammalian tissue culture cells.
    Exp Cell Res. 1962 Mar;26:260-8 PMID: 14488623
  32. Nucleolar structure.
    Int Rev Cytol. 1984;87:107-58 PMID: 6201455
  33. Human DNA helicase IV is nucleolin, an RNA helicase modulated by phosphorylation.
    Gene. 1995 Jul 28;160(2):143-8 PMID: 7642087
  34. Mitotic repression of transcription in vitro.
    J Cell Biol. 1993 Feb;120(3):613-24 PMID: 8381119
  35. An RNase P RNA subunit mutation affects ribosomal RNA processing.
    Nucleic Acids Res. 1996 Aug 15;24(16):3158-66 PMID: 8774895
  36. A U3 small nuclear ribonucleoprotein-requiring processing event in the 5' external transcribed spacer of Xenopus precursor rRNA.
    Mol Cell Biol. 1993 Oct;13(10):5990-8 PMID: 8413202
  37. The POP1 gene encodes a protein component common to the RNase MRP and RNase P ribonucleoproteins.
    Genes Dev. 1994 Jun 15;8(12):1423-33 PMID: 7926742
  38. 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
  39. Relative distribution of rDNA and proteins of the RNA polymerase I transcription machinery at chromosomal NORs.
    Chromosoma. 1997 Jun;105(7-8):459-69 PMID: 9211974
  40. Processing of eukaryotic ribosomal RNA.
    Prog Nucleic Acid Res Mol Biol. 1994;49:197-239 PMID: 7863007
  41. Nucleolin functions in the first step of ribosomal RNA processing.
    EMBO J. 1998 Mar 2;17(5):1476-86 PMID: 9482744
  42. Yeast site-specific ribonucleoprotein endoribonuclease MRP contains an RNA component homologous to mammalian RNase MRP RNA and essential for cell viability.
    Genes Dev. 1992 Oct;6(10):1975-85 PMID: 1398074
  43. Electron tomography of metaphase nucleolar organizer regions: evidence for a twisted-loop organization.
    Mol Biol Cell. 1997 Nov;8(11):2199-216 PMID: 9362063
  44. Eukaryotic ribosomal RNA: the recent excitement in the nucleotide modification problem.
    Chromosoma. 1997 Jun;105(7-8):391-400 PMID: 9211966
  45. The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes.
    Genes Dev. 1993 Aug;7(8):1609-19 PMID: 8339936
  46. Constitutive and strong association of PAF53 with RNA polymerase I.
    Chromosoma. 1997 Sep;106(4):216-25 PMID: 9254723
  47. New host cell system for regulated simian virus 40 DNA replication.
    Mol Cell Biol. 1985 Nov;5(11):3231-40 PMID: 3018509
  48. Organization of small nucleolar ribonucleoproteins (snoRNPs) by fluorescence in situ hybridization and immunocytochemistry.
    Mol Biol Cell. 1994 Dec;5(12):1289-99 PMID: 7535131
  49. Location of the HIV-1 Rev protein during mitosis: inactivation of the nuclear export signal alters the pathway for postmitotic reentry into nucleoli.
    J Cell Sci. 1996 Sep;109 ( Pt 9):2239-51 PMID: 8886975
  50. Accurate processing of a eukaryotic precursor ribosomal RNA by ribonuclease MRP in vitro.
    Science. 1996 Apr 12;272(5259):268-70 PMID: 8602511
  51. The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs.
    J Cell Sci. 1996 Jun;109 ( Pt 6):1241-51 PMID: 8799814
  52. A class of nonribosomal nucleolar components is located in chromosome periphery and in nucleolus-derived foci during anaphase and telophase.
    Chromosoma. 1997 Jun;105(7-8):407-17 PMID: 9211968
  53. Mitotic regulation of TFIID: inhibition of activator-dependent transcription and changes in subcellular localization.
    Genes Dev. 1996 Oct 1;10(19):2389-400 PMID: 8843192
  54. Components of the nucleolar processing complex (Pre-rRNA, fibrillarin, and nucleolin) colocalize during mitosis and are incorporated to daughter cell nucleoli.
    Exp Cell Res. 1995 Nov;221(1):111-25 PMID: 7589236
  55. Transcription complex formation at the mouse rDNA promoter involves the stepwise association of four transcription factors and RNA polymerase I.
    J Biol Chem. 1991 Dec 25;266(36):24588-95 PMID: 1761556
  56. M phase phosphoprotein 10 is a human U3 small nucleolar ribonucleoprotein component.
    Mol Biol Cell. 1998 Feb;9(2):437-49 PMID: 9450966
  57. The small nucleolar RNAs.
    Annu Rev Biochem. 1995;64:897-934 PMID: 7574504
  58. Structure and variation of human ribosomal DNA: the external transcribed spacer and adjacent regions.
    Am J Hum Genet. 1982 Jan;34(1):32-49 PMID: 6282117
  59. Repression of RNA polymerase II and III transcription during M phase of the cell cycle.
    Exp Cell Res. 1996 Dec 15;229(2):282-8 PMID: 8986611
  60. When rDNA transcription is arrested during mitosis, UBF is still associated with non-condensed rDNA.
    J Cell Sci. 1997 Oct;110 ( Pt 19):2429-40 PMID: 9410881
  61. Function and synthesis of small nucleolar RNAs.
    Curr Opin Cell Biol. 1997 Jun;9(3):337-42 PMID: 9159079
  62. Mitotic repression of the transcriptional machinery.
    Trends Biochem Sci. 1997 Jun;22(6):197-202 PMID: 9204705
  63. The chromosome periphery during mitosis.
    Bioessays. 1994 Mar;16(3):179-85 PMID: 8166671
  64. Regulation of synthesis and processing of nucleolar components in metaphase-arrested cells.
    J Mol Biol. 1971 Jul 14;59(1):27-42 PMID: 5283755
  65. Nuclear domains of the RNA subunit of RNase P.
    J Cell Sci. 1997 Apr;110 ( Pt 7):829-37 PMID: 9133670
  66. Early stages of pre-rRNA formation within the nucleolar ultrastructure of mouse cells studied by in situ hybridization with a 5'ETS leader probe.
    Chromosoma. 1997 Jun;105(7-8):496-505 PMID: 9211977
  67. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing.
    EMBO J. 1990 Jul;9(7):2299-308 PMID: 2357971
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
1998-09-00
Pages
2407-22
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC25507
Subset
IM
Grants
NIAID NIH HHS · AI-34277 · United States
NIGMS NIH HHS · GM-28349 · 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]