Home LiteratureArticle Details
PMID: 12456659 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B.

The EMBO journal ·Vol. 21 ·No. 23 ·2002-12-02 ·Pages 6527-38

Mosammaparast N, Ewart CS, Pemberton LF

Abstract

Import of core histones into the nucleus is a prerequisite for their deposition onto DNA and the assembly of chromatin. Here we demonstrate that nucleosome assembly protein 1 (Nap1p), a protein previously implicated in the deposition of histones H2A and H2B, is also involved in the transport of these two histones. We demonstrate that Nap1p can bind directly to Kap114p, the primary karyopherin/importin responsible for the nuclear import of H2A and H2B. Nap1p also serves as a bridge between Kap114p and the histone nuclear localization sequence (NLS). Nap1p acts cooperatively to increase the affinity of Kap114p for these NLSs. Nuclear accumulation of histone NLS-green fluorescent protein (GFP) reporters was decreased in deltanap1 cells. Furthermore, we demonstrate that Nap1p promotes the association of the H2A and H2B NLSs specifically with the karyopherin Kap114p. Localization studies demonstrate that Nap1p is a nucleocytoplasmic shuttling protein, and genetic experiments suggest that its shuttling is important for maintaining chromatin structure in vivo. We propose a model in which Nap1p links the nuclear transport of H2A and H2B to chromatin assembly.

MeSH Terms
Active Transport, Cell Nucleus Cell Cycle Proteins Cell Nucleus/metabolism Histones/metabolism In Vitro Techniques Karyopherins/metabolism Nuclear Proteins/metabolism Nucleosome Assembly Protein 1 Protein Binding Proteins/metabolism Retroelements/genetics Saccharomyces cerevisiae Proteins Yeasts/genetics,metabolism beta Karyopherins
Chemicals
Cell Cycle Proteins Histones KAP114 protein, S cerevisiae Karyopherins NAP1 protein, S cerevisiae Nuclear Proteins Nucleosome Assembly Protein 1 Proteins Retroelements Saccharomyces cerevisiae Proteins beta Karyopherins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Mosammaparast Nima
Center for Cell Signaling, University of Virginia, Charlottesville, VA 22908, USA.
Ewart Courtney S
Pemberton Lucy F
References (43)
43 references, click to expand
  1. The nuclear pore complex.
    J Cell Sci. 2000 Nov;113 ( Pt 22):3885-6 PMID: 11058073
  2. Control of neurulation by the nucleosome assembly protein-1-like 2.
    Nat Genet. 2000 Aug;25(4):431-5 PMID: 10932189
  3. The Sda1 protein is required for passage through start.
    Mol Biol Cell. 2001 Jan;12(1):201-19 PMID: 11160833
  4. SPT genes: key players in the regulation of transcription, chromatin structure and other cellular processes.
    J Biochem. 2001 Feb;129(2):185-91 PMID: 11173517
  5. Nuclear import of histone H2A and H2B is mediated by a network of karyopherins.
    J Cell Biol. 2001 Apr 16;153(2):251-62 PMID: 11309407
  6. Multiple pathways contribute to nuclear import of core histones.
    EMBO Rep. 2001 Aug;2(8):690-6 PMID: 11493596
  7. Transport into and out of the nucleus.
    Microbiol Mol Biol Rev. 2001 Dec;65(4):570-94, table of contents PMID: 11729264
  8. Pathways mediating the nuclear import of histones H3 and H4 in yeast.
    J Biol Chem. 2002 Jan 4;277(1):862-8 PMID: 11694505
  9. Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains.
    EMBO J. 2002 Feb 1;21(3):377-86 PMID: 11823430
  10. Nuclear import of Upf3p is mediated by importin-alpha/-beta and export to the cytoplasm is required for a functional nonsense-mediated mRNA decay pathway in yeast.
    Genetics. 2002 Aug;161(4):1465-82 PMID: 12196393
  11. Binding mode of nucleosome-assembly protein (AP-I) and histones.
    Eur J Biochem. 1987 Jan 2;162(1):19-24 PMID: 3816782
  12. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses.
    Cell. 1987 Mar 27;48(6):1035-46 PMID: 3030556
  13. Changes in histone gene dosage alter transcription in yeast.
    Genes Dev. 1988 Feb;2(2):150-9 PMID: 2834270
  14. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport.
    J Cell Biol. 1991 Oct;115(1):1-17 PMID: 1717476
  15. Ssn6-Tup1 is a general repressor of transcription in yeast.
    Cell. 1992 Feb 21;68(4):709-19 PMID: 1739976
  16. Functional analysis of nucleosome assembly protein, NAP-1. The negatively charged COOH-terminal region is not necessary for the intrinsic assembly activity.
    J Biol Chem. 1992 Oct 15;267(29):20980-6 PMID: 1400414
  17. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1.
    Genes Dev. 1994 Oct 1;8(19):2257-69 PMID: 7958893
  18. Members of the NAP/SET family of proteins interact specifically with B-type cyclins.
    J Cell Biol. 1995 Aug;130(3):661-73 PMID: 7622566
  19. NAP1 acts with Clb1 to perform mitotic functions and to suppress polar bud growth in budding yeast.
    J Cell Biol. 1995 Aug;130(3):675-85 PMID: 7622567
  20. Stimulation of transcription factor binding and histone displacement by nucleosome assembly protein 1 and nucleoplasmin requires disruption of the histone octamer.
    Mol Cell Biol. 1995 Nov;15(11):6178-87 PMID: 7565770
  21. Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays.
    Mol Cell Biol. 1996 Jun;16(6):3112-24 PMID: 8649423
  22. Kap104p: a karyopherin involved in the nuclear transport of messenger RNA binding proteins.
    Science. 1996 Oct 25;274(5287):624-7 PMID: 8849456
  23. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4.
    Cell. 1996 Oct 4;87(1):95-104 PMID: 8858152
  24. Histones in transit: cytosolic histone complexes and diacetylation of H4 during nucleosome assembly in human cells.
    Biochemistry. 1997 Jan 21;36(3):469-80 PMID: 9012662
  25. A distinct nuclear import pathway used by ribosomal proteins.
    Cell. 1997 May 30;89(5):715-25 PMID: 9182759
  26. Control of mitotic events by Nap1 and the Gin4 kinase.
    J Cell Biol. 1997 Jul 14;138(1):119-30 PMID: 9214386
  27. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export.
    Curr Biol. 1997 Oct 1;7(10):767-75 PMID: 9368759
  28. A distinct and parallel pathway for the nuclear import of an mRNA-binding protein.
    J Cell Biol. 1997 Dec 29;139(7):1645-53 PMID: 9412460
  29. Chromatin assembly factors: a dual function in nucleosome formation and mobilization?
    Genes Cells. 1997 Oct;2(10):593-600 PMID: 9427281
  30. Assembly, remodeling, and histone binding capabilities of yeast nucleosome assembly protein 1.
    J Biol Chem. 1998 Mar 13;273(11):6582-90 PMID: 9497395
  31. Transport routes through the nuclear pore complex.
    Curr Opin Cell Biol. 1998 Jun;10(3):392-9 PMID: 9640541
  32. Karyopherins and kissing cousins.
    Trends Cell Biol. 1998 May;8(5):184-8 PMID: 9695836
  33. Specific binding of the karyopherin Kap121p to a subunit of the nuclear pore complex containing Nup53p, Nup59p, and Nup170p.
    J Cell Biol. 1998 Dec 28;143(7):1813-30 PMID: 9864357
  34. Specific components of the SAGA complex are required for Gcn4- and Gcr1-mediated activation of the his4-912delta promoter in Saccharomyces cerevisiae.
    Genetics. 1999 Apr;151(4):1365-78 PMID: 10101163
  35. Chromatin assembly: biochemical identities and genetic redundancy.
    Curr Opin Genet Dev. 1999 Apr;9(2):185-90 PMID: 10322140
  36. All aboard the cyclin train: subcellular trafficking of cyclins and their CDK partners.
    Trends Cell Biol. 1999 Jun;9(6):207-10 PMID: 10354564
  37. Nuclear import of the TATA-binding protein: mediation by the karyopherin Kap114p and a possible mechanism for intranuclear targeting.
    J Cell Biol. 1999 Jun 28;145(7):1407-17 PMID: 10385521
  38. Functional characterization of human nucleosome assembly protein-2 (NAP1L4) suggests a role as a histone chaperone.
    Genomics. 1997 Sep 15;44(3):253-65 PMID: 9325046
  39. The RCAF complex mediates chromatin assembly during DNA replication and repair.
    Nature. 1999 Dec 2;402(6761):555-60 PMID: 10591219
  40. The yeast nuclear pore complex: composition, architecture, and transport mechanism.
    J Cell Biol. 2000 Feb 21;148(4):635-51 PMID: 10684247
  41. De novo nucleosome assembly: new pieces in an old puzzle.
    Genes Dev. 2000 Jun 15;14(12):1430-8 PMID: 10859162
  42. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone.
    Genes Dev. 2000 Aug 1;14(15):1899-907 PMID: 10921904
  43. Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators.
    Mol Cell Biol. 2000 Dec;20(23):8933-43 PMID: 11073993
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2002-12-02
Pages
6527-38
Language
English
Region
England
NLM ID
8208664
PMCID
PMC136951
Subset
IM
Grants
NIGMS NIH HHS · R01 GM065385 · United States
NIGMS NIH HHS · R01 GM65385 · 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: product@genelibs.com