Home LiteratureArticle Details
PMID: 18332108 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity.

Molecular and cellular biology ·Vol. 28 ·No. 10 ·2008-05-00 ·Pages 3114-26

Murano K, Okuwaki M, Hisaoka M, Nagata K

Abstract

It is well established that the transcription rate of the rRNA gene is closely associated with profound alterations in the cell growth rate. Regulation of rRNA gene transcription is likely to be dependent on the dynamic conversion of the chromatin structure. Previously, we identified B23/nucleophosmin, a multifunctional nucleolar phosphoprotein, as a component of template activating factor III that remodels the chromatin-like structure of the adenovirus genome complexed with viral basic proteins. It has also been shown that B23 has histone chaperone activity. Here, we examined the effect of B23 on rRNA gene transcription. B23 was found to be associated with the rRNA gene chromatin. Small-interfering-RNA-mediated down-regulation of the B23 expression level resulted in reduction of the transcription rate of the rRNA gene. We constructed a B23 mutant termed B23DeltaC, which lacks the domain essential for the histone chaperone activity and inhibited the histone binding activity of B23 in a dominant-negative manner. Expression of B23DeltaC decreased rRNA gene transcription and the rate of cell proliferation. These results suggest that B23 is involved in the transcription regulation of the rRNA gene as a nucleolar histone chaperone.

MeSH Terms
Animals Base Sequence Cell Line Cell Proliferation Chromatin Assembly and Disassembly DNA, Complementary/genetics Gene Deletion Genes, p53 HeLa Cells Histones/metabolism Humans Mice Molecular Chaperones/metabolism Nuclear Proteins/antagonists & inhibitors,genetics,metabolism Nucleophosmin RNA, Ribosomal/genetics RNA, Small Interfering/genetics Transcription, Genetic
Chemicals
DNA, Complementary Histones Molecular Chaperones NPM1 protein, human Npm1 protein, mouse Nuclear Proteins RNA, Ribosomal RNA, Small Interfering Nucleophosmin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Murano Kensaku
Department of Infection Biology, Graduate School of Comprehensive Human Sciences and Institute of Basic Medical Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba 305-8575, Japan.
Okuwaki Mitsuru
Hisaoka Miharu
Nagata Kyosuke
References (58)
58 references, click to expand
  1. NoRC-dependent nucleosome positioning silences rRNA genes.
    EMBO J. 2006 Dec 13;25(24):5735-41 PMID: 17139253
  2. In vivo interaction of nucleophosmin/B23 and protein C23 during cell cycle progression in HeLa cells.
    Cancer Lett. 1999 Sep 20;144(1):45-54 PMID: 10503877
  3. RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components.
    Genes Dev. 2004 Oct 15;18(20):2506-17 PMID: 15489292
  4. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes.
    EMBO J. 2006 Apr 19;25(8):1669-79 PMID: 16601700
  5. Interaction of nucleolar phosphoprotein B23 with nucleic acids.
    Biochemistry. 1989 Nov 28;28(24):9495-501 PMID: 2482073
  6. Functional interaction of the DNA-binding transcription factor Sp1 through its DNA-binding domain with the histone chaperone TAF-I.
    J Biol Chem. 2003 Aug 1;278(31):28758-64 PMID: 12759364
  7. The histone chaperone TAF-I/SET/INHAT is required for transcription in vitro of chromatin templates.
    Mol Cell Biol. 2005 Jan;25(2):797-807 PMID: 15632079
  8. Template activating factor I, a novel host factor required to stimulate the adenovirus core DNA replication.
    J Biol Chem. 1993 May 15;268(14):10582-7 PMID: 8486711
  9. The structure and function of Xenopus NO38-core, a histone chaperone in the nucleolus.
    Structure. 2004 Dec;12(12):2149-60 PMID: 15576029
  10. Histone- and chromatin-binding activity of template activating factor-I.
    FEBS Lett. 1999 Dec 17;463(3):285-8 PMID: 10606739
  11. Involvement of template-activating factor I/SET in transcription of adenovirus early genes as a positive-acting factor.
    J Virol. 2006 Jan;80(2):794-801 PMID: 16378981
  12. Ternary complex formation between DNA-adenovirus core protein VII and TAF-Ibeta/SET, an acidic molecular chaperone.
    FEBS Lett. 2003 Dec 18;555(3):521-7 PMID: 14675767
  13. The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype.
    Mol Biol Cell. 2002 Jun;13(6):2016-30 PMID: 12058066
  14. Stimulation of DNA transcription by the replication factor from the adenovirus genome in a chromatin-like structure.
    J Biol Chem. 1995 Apr 21;270(16):9645-50 PMID: 7721897
  15. ARF impedes NPM/B23 shuttling in an Mdm2-sensitive tumor suppressor pathway.
    Mol Cell Biol. 2004 Nov;24(21):9327-38 PMID: 15485902
  16. Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription.
    Mol Cell Biol. 2005 Sep;25(17):7534-45 PMID: 16107701
  17. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone.
    FEBS Lett. 2001 Oct 12;506(3):272-6 PMID: 11602260
  18. Identification of nucleophosmin/B23, an acidic nucleolar protein, as a stimulatory factor for in vitro replication of adenovirus DNA complexed with viral basic core proteins.
    J Mol Biol. 2001 Aug 3;311(1):41-55 PMID: 11469856
  19. Regulation of mammalian ribosomal gene transcription by RNA polymerase I.
    Prog Nucleic Acid Res Mol Biol. 1999;62:109-54 PMID: 9932453
  20. Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23.
    Mol Cell Biol. 2004 Feb;24(3):985-96 PMID: 14729947
  21. The AgNORs.
    Micron. 2000 Apr;31(2):117-20 PMID: 10588056
  22. Physical and functional interaction between a nucleolar protein nucleophosmin/B23 and adenovirus basic core proteins.
    FEBS Lett. 2007 Jul 10;581(17):3283-8 PMID: 17602943
  23. NAP-I is a functional homologue of TAF-I that is required for replication and transcription of the adenovirus genome in a chromatin-like structure.
    Genes Cells. 1996 Dec;1(12):1045-56 PMID: 9077453
  24. The nuclear matrix protein, numatrin (B23), is associated with growth factor-induced mitogenesis in Swiss 3T3 fibroblasts and with T lymphocyte proliferation stimulated by lectins and anti-T cell antigen receptor antibody.
    J Cell Biol. 1988 Nov;107(5):1629-42 PMID: 3141428
  25. Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function.
    Mol Cell Biol. 2005 Feb;25(4):1258-71 PMID: 15684379
  26. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation.
    Mol Cell. 2003 Nov;12(5):1151-64 PMID: 14636574
  27. The ribonuclease activity of nucleolar protein B23.
    Nucleic Acids Res. 1995 Oct 11;23(19):3974-9 PMID: 7479045
  28. Purification and initial characterization of a protein which facilitates assembly of nucleosome-like structure from mammalian cells.
    Eur J Biochem. 1984 Aug 1;142(3):431-9 PMID: 6468372
  29. Nucleophosmin, HDM2 and p53: players in UV damage incited nucleolar stress response.
    Cell Cycle. 2004 Aug;3(8):976-9 PMID: 15254398
  30. Intergenic transcripts regulate the epigenetic state of rRNA genes.
    Mol Cell. 2006 May 5;22(3):351-61 PMID: 16678107
  31. Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication.
    Cell. 2000 Sep 29;103(1):127-40 PMID: 11051553
  32. Positive and negative regulation of the cardiovascular transcription factor KLF5 by p300 and the oncogenic regulator SET through interaction and acetylation on the DNA-binding domain.
    Mol Cell Biol. 2003 Dec;23(23):8528-41 PMID: 14612398
  33. UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat.
    Mol Cell Biol. 2002 Jan;22(2):657-68 PMID: 11756560
  34. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption.
    Mol Cell Biol. 1998 Feb;18(2):1055-64 PMID: 9448003
  35. NoRC--a novel member of mammalian ISWI-containing chromatin remodeling machines.
    EMBO J. 2001 Sep 3;20(17):4892-900 PMID: 11532953
  36. Histone acetylation-independent transcription stimulation by a histone chaperone.
    Nucleic Acids Res. 2007;35(3):705-15 PMID: 17179179
  37. Nucleolin is required for RNA polymerase I transcription in vivo.
    Mol Cell Biol. 2007 Feb;27(3):937-48 PMID: 17130237
  38. Role of nucleophosmin in embryonic development and tumorigenesis.
    Nature. 2005 Sep 1;437(7055):147-53 PMID: 16007073
  39. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle.
    Cell. 1989 Jun 2;57(5):753-61 PMID: 2720786
  40. The structure of adenovirus chromatin in infected cells.
    J Gen Virol. 1985 Dec;66 ( Pt 12):2671-84 PMID: 4067582
  41. Nucleolin functions in the first step of ribosomal RNA processing.
    EMBO J. 1998 Mar 2;17(5):1476-86 PMID: 9482744
  42. Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing.
    Curr Opin Cell Biol. 2005 Jun;17(3):281-6 PMID: 15901498
  43. Protein NPM3 interacts with the multifunctional nucleolar protein B23/nucleophosmin and inhibits ribosome biogenesis.
    J Biol Chem. 2005 Feb 18;280(7):5496-502 PMID: 15596447
  44. Structure of the gene for rat nucleolar protein B23.
    J Biol Chem. 1990 Oct 25;265(30):18227-33 PMID: 2211699
  45. Binding mode of nucleosome-assembly protein (AP-I) and histones.
    Eur J Biochem. 1987 Jan 2;162(1):19-24 PMID: 3816782
  46. Synergistic action of MLL, a TRX protein with template activating factor-I, a histone chaperone.
    FEBS Lett. 2005 Jan 31;579(3):757-62 PMID: 15670842
  47. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis.
    Cell Mol Life Sci. 2007 Jan;64(1):29-49 PMID: 17171232
  48. Nucleophosmin regulates the stability and transcriptional activity of p53.
    Nat Cell Biol. 2002 Jul;4(7):529-33 PMID: 12080348
  49. Epigenetic mechanism of rRNA gene silencing: temporal order of NoRC-mediated histone modification, chromatin remodeling, and DNA methylation.
    Mol Cell Biol. 2005 Apr;25(7):2539-46 PMID: 15767661
  50. Can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3' half to different genes: characterization of the set gene.
    Mol Cell Biol. 1992 Aug;12(8):3346-55 PMID: 1630450
  51. Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease.
    Nucleic Acids Res. 1998 Oct 1;26(19):4508-15 PMID: 9742256
  52. Comparison of nucleolar proteins of normal rat liver and Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis.
    Proc Natl Acad Sci U S A. 1973 May;70(5):1316-20 PMID: 4351171
  53. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA.
    Nature. 1978 Oct 5;275(5679):416-20 PMID: 692721
  54. Different epigenetic layers engage in complex crosstalk to define the epigenetic state of mammalian rRNA genes.
    Hum Mol Genet. 2007 Apr 15;16 Spec No 1:R21-7 PMID: 17613545
  55. The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly.
    Mol Cell. 2001 Oct;8(4):841-53 PMID: 11684019
  56. Adenovirus chromatin I. Isolation and characterization of the major core protein VII and precursor Pro-VII.
    J Biol Chem. 1977 Jul 25;252(14):4981-7 PMID: 873925
  57. Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly.
    Mol Cell. 2007 Apr 27;26(2):217-29 PMID: 17466624
  58. Association of yeast RNA polymerase I with a nucleolar substructure active in rRNA synthesis and processing.
    J Cell Biol. 2000 May 1;149(3):575-90 PMID: 10791972
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
1098-5549
Published
2008-05-00
Epub
2008-00-10
Pages
3114-26
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC2423177
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: product@genelibs.com