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PMID: 14729961 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

RanBP2/Nup358 provides a major binding site for NXF1-p15 dimers at the nuclear pore complex and functions in nuclear mRNA export.

Molecular and cellular biology ·Vol. 24 ·No. 3 ·2004-02-00 ·Pages 1155-67

Forler D, Rabut G, Ciccarelli FD, Herold A, Köcher T, Niggeweg R, Bork P, Ellenberg J, Izaurralde E

Abstract

Metazoan NXF1-p15 heterodimers promote the nuclear export of bulk mRNA across nuclear pore complexes (NPCs). In vitro, NXF1-p15 forms a stable complex with the nucleoporin RanBP2/Nup358, a component of the cytoplasmic filaments of the NPC, suggesting a role for this nucleoporin in mRNA export. We show that depletion of RanBP2 from Drosophila cells inhibits proliferation and mRNA export. Concomitantly, the localization of NXF1 at the NPC is strongly reduced and a significant fraction of this normally nuclear protein is detected in the cytoplasm. Under the same conditions, the steady-state subcellular localization of other nuclear or cytoplasmic proteins and CRM1-mediated protein export are not detectably affected, indicating that the release of NXF1 into the cytoplasm and the inhibition of mRNA export are not due to a general defect in NPC function. The specific role of RanBP2 in the recruitment of NXF1 to the NPC is highlighted by the observation that depletion of CAN/Nup214 also inhibits cell proliferation and mRNA export but does not affect NXF1 localization. Our results indicate that RanBP2 provides a major binding site for NXF1 at the cytoplasmic filaments of the NPC, thereby restricting its diffusion in the cytoplasm after NPC translocation. In RanBP2-depleted cells, NXF1 diffuses freely through the cytoplasm. Consequently, the nuclear levels of the protein decrease and export of bulk mRNA is impaired.

MeSH Terms
Animals DNA-(Apurinic or Apyrimidinic Site) Lyase/metabolism Dimerization Drosophila melanogaster/metabolism Humans Karyopherins/metabolism Molecular Chaperones Nuclear Pore/metabolism Nuclear Pore Complex Proteins/metabolism Nucleocytoplasmic Transport Proteins/metabolism RNA Interference RNA, Messenger/metabolism RNA-Binding Proteins/metabolism Receptors, Cytoplasmic and Nuclear
Chemicals
Karyopherins Molecular Chaperones NXF1 protein, human Nuclear Pore Complex Proteins Nucleocytoplasmic Transport Proteins RBM8A protein, human RNA, Messenger RNA-Binding Proteins Receptors, Cytoplasmic and Nuclear exportin 1 protein ran-binding protein 2 APEX1 protein, human DNA-(Apurinic or Apyrimidinic Site) Lyase
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Forler Daniel
EMBL, 69117 Heidelberg, Germany.
Rabut Gwénaël
Ciccarelli Francesca D
Herold Andrea
Köcher Thomas
Niggeweg Ricarda
Bork Peer
Ellenberg Jan
Izaurralde Elisa
References (38)
38 references, click to expand
  1. The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human.
    EMBO J. 1999 May 4;18(9):2593-609 PMID: 10228171
  2. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences.
    Genes Dev. 1999 May 1;13(9):1126-39 PMID: 10323864
  3. Identification of novel import and export signals of human TAP, the protein that binds to the constitutive transport element of the type D retrovirus mRNAs.
    Mol Cell Biol. 1999 Sep;19(9):6306-17 PMID: 10454577
  4. The human tap nuclear RNA export factor contains a novel transportin-dependent nuclear localization signal that lacks nuclear export signal function.
    J Biol Chem. 1999 Nov 5;274(45):32167-71 PMID: 10542253
  5. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates.
    RNA. 2000 Jan;6(1):136-58 PMID: 10668806
  6. The yeast nuclear pore complex: composition, architecture, and transport mechanism.
    J Cell Biol. 2000 Feb 21;148(4):635-51 PMID: 10684247
  7. The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm.
    Curr Opin Cell Biol. 2000 Jun;12(3):361-71 PMID: 10801463
  8. Kinetic analysis of translocation through nuclear pore complexes.
    EMBO J. 2001 Mar 15;20(6):1320-30 PMID: 11250898
  9. Overexpression of TAP/p15 heterodimers bypasses nuclear retention and stimulates nuclear mRNA export.
    J Biol Chem. 2001 Jun 8;276(23):20536-43 PMID: 11259411
  10. The nuclear pore complex as a transport machine.
    J Biol Chem. 2001 May 18;276(20):16593-6 PMID: 11283009
  11. Nucleocytoplasmic transport enters the atomic age.
    Curr Opin Cell Biol. 2001 Jun;13(3):310-9 PMID: 11343901
  12. Nuclear pores and nuclear assembly.
    Curr Opin Cell Biol. 2001 Jun;13(3):363-75 PMID: 11343909
  13. Genomic organization, expression, and localization of murine Ran-binding protein 2 (RanBP2) gene.
    Mamm Genome. 2001 Jun;12(6):406-15 PMID: 11353387
  14. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells.
    J Cell Biol. 2001 Jul 9;154(1):71-84 PMID: 11448991
  15. In vitro analysis of nuclear transport mediated by the C-terminal shuttle domain of Tap.
    J Biol Chem. 2001 Nov 9;276(45):42355-63 PMID: 11551912
  16. RNA export mediated by tap involves NXT1-dependent interactions with the nuclear pore complex.
    J Biol Chem. 2001 Nov 30;276(48):44953-62 PMID: 11579093
  17. Structural basis for the recognition of a nucleoporin FG repeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor.
    Mol Cell. 2001 Sep;8(3):645-56 PMID: 11583626
  18. The nucleoporin Nup153 is required for nuclear pore basket formation, nuclear pore complex anchoring and import of a subset of nuclear proteins.
    EMBO J. 2001 Oct 15;20(20):5703-14 PMID: 11598013
  19. Formation of Tap/NXT1 heterodimers activates Tap-dependent nuclear mRNA export by enhancing recruitment to nuclear pore complexes.
    Mol Cell Biol. 2002 Jan;22(1):245-56 PMID: 11739738
  20. Recent improvements to the SMART domain-based sequence annotation resource.
    Nucleic Acids Res. 2002 Jan 1;30(1):242-4 PMID: 11752305
  21. NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila.
    RNA. 2001 Dec;7(12):1768-80 PMID: 11780633
  22. The nucleoporin RanBP2 has SUMO1 E3 ligase activity.
    Cell. 2002 Jan 11;108(1):109-20 PMID: 11792325
  23. Nuclear export of mRNA by TAP/NXF1 requires two nucleoporin-binding sites but not p15.
    Mol Cell Biol. 2002 Aug;22(15):5405-18 PMID: 12101235
  24. The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import.
    J Cell Biol. 2002 Jul 8;158(1):63-77 PMID: 12105182
  25. Karyopherin beta 2B participates in mRNA export from the nucleus.
    Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14195-9 PMID: 12384575
  26. An efficient protein complex purification method for functional proteomics in higher eukaryotes.
    Nat Biotechnol. 2003 Jan;21(1):89-92 PMID: 12483225
  27. Structural basis for the interaction between the Tap/NXF1 UBA domain and FG nucleoporins at 1A resolution.
    J Mol Biol. 2003 Feb 21;326(3):849-58 PMID: 12581645
  28. Genome-wide analysis of nuclear mRNA export pathways in Drosophila.
    EMBO J. 2003 May 15;22(10):2472-83 PMID: 12743041
  29. Nup358 integrates nuclear envelope breakdown with kinetochore assembly.
    J Cell Biol. 2003 Sep 15;162(6):991-1001 PMID: 12963708
  30. CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP.
    Evolution. 1985 Jul;39(4):783-791 PMID: 28561359
  31. A giant nucleopore protein that binds Ran/TC4.
    Nature. 1995 Jul 13;376(6536):184-8 PMID: 7603572
  32. A conditional allele of the novel repeat-containing yeast nucleoporin RAT7/NUP159 causes both rapid cessation of mRNA export and reversible clustering of nuclear pore complexes.
    J Cell Biol. 1995 May;129(4):939-55 PMID: 7744966
  33. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region.
    J Biol Chem. 1995 Jun 9;270(23):14209-13 PMID: 7775481
  34. The human CAN protein, a putative oncogene product associated with myeloid leukemogenesis, is a nuclear pore complex protein that faces the cytoplasm.
    Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1519-23 PMID: 8108440
  35. Localization of the Ran-GTP binding protein RanBP2 at the cytoplasmic side of the nuclear pore complex.
    Eur J Cell Biol. 1995 Nov;68(3):211-9 PMID: 8603673
  36. G2 arrest and impaired nucleocytoplasmic transport in mouse embryos lacking the proto-oncogene CAN/Nup214.
    EMBO J. 1996 Oct 15;15(20):5574-83 PMID: 8896451
  37. CRM1 is an export receptor for leucine-rich nuclear export signals.
    Cell. 1997 Sep 19;90(6):1051-60 PMID: 9323133
  38. Major binding sites for the nuclear import receptor are the internal nucleoporin Nup153 and the adjacent nuclear filament protein Tpr.
    J Cell Biol. 1998 Apr 6;141(1):31-49 PMID: 9531546
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2004-02-00
Pages
1155-67
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC321439
Subset
IM
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