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PMID: 15121898 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNAs.

Nucleic acids research ·Vol. 32 ·No. 8 ·2004-00-00 ·Pages 2411-20

Villacé P, Marión RM, Ortín J

Abstract

hStaufen is the human homolog of dmStaufen, a double-stranded (ds)RNA-binding protein involved in early development of the fly. hStaufen-containing complexes were purified by affinity chromatography from human cells transfected with a TAP-tagged hStaufen gene. These complexes showed a size >10 MDa. Untagged complexes with similar size were identified from differentiated human neuroblasts. The identity of proteins present in purified hStaufen complexes was determined by mass spectrometry and the presence of these proteins and other functionally related ones was verified by western blot. Ribosomes and proteins involved in the control of protein synthesis (PABP1 and FMRP) were present in purified hStaufen complexes, as well as elements of the cytoskeleton (tubulins, tau, actin and internexin), cytoskeleton control proteins (IQGAP1, cdc42 and rac1) and motor proteins (dynein, kinesin and myosin). In addition, proteins normally found in the nucleus, like nucleolin and RNA helicase A, were also found associated with cytosolic hStaufen complexes. The co-localization of these components with hStaufen granules in the dendrites of differentiated neuroblasts, determined by confocal immunofluorescence, validated their association in living cells. These results support the notion that the hStaufen-containing granules are structures essential in the localization and regulated translation of human mRNAs in vivo.

MeSH Terms
ATP-Binding Cassette Transporters Biological Transport Cell Line Cytoplasmic Granules/chemistry Cytoskeletal Proteins/analysis Histocompatibility Antigens Class I/genetics Humans Macromolecular Substances Microtubule-Associated Proteins/analysis Neurons/chemistry,metabolism Nuclear Proteins/analysis Protein Biosynthesis RNA/analysis RNA, Messenger/metabolism RNA-Binding Proteins/analysis,genetics,physiology Recombinant Fusion Proteins/isolation & purification,metabolism Ribosomes/metabolism
Chemicals
ATP-Binding Cassette Transporters Cytoskeletal Proteins Histocompatibility Antigens Class I Macromolecular Substances Microtubule-Associated Proteins Nuclear Proteins RNA, Messenger RNA-Binding Proteins Recombinant Fusion Proteins STAU1 protein, human staufen protein, mammalian transporter associated with antigen processing (TAP) RNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Villacé Patricia
Centro Nacional de Biotecnología, Campus de Cantoblanco, 28049 Madrid, Spain.
Marión Rosa M
Ortín Juan
References (57)
57 references, click to expand
  1. The dsRNA binding protein family: critical roles, diverse cellular functions.
    FASEB J. 2003 Jun;17(9):961-83 PMID: 12773480
  2. IQGAP proteins are integral components of cytoskeletal regulation.
    EMBO Rep. 2003 Jun;4(6):571-4 PMID: 12776176
  3. Barentsz, a new component of the Staufen-containing ribonucleoprotein particles in mammalian cells, interacts with Staufen in an RNA-dependent manner.
    J Neurosci. 2003 Jul 2;23(13):5778-88 PMID: 12843282
  4. Genetic variability of Hong Kong (H3N2) influenza viruses: spontaneous mutations and their location in the viral genome.
    Gene. 1980 Nov;11(3-4):319-31 PMID: 6783473
  5. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system.
    Mol Cell Biol. 1987 Jan;7(1):379-87 PMID: 3031469
  6. RNA recognition by a Staufen double-stranded RNA-binding domain.
    EMBO J. 2000 Mar 1;19(5):997-1009 PMID: 10698941
  7. Molecular insights into mRNA transport and local translation in the mammalian nervous system.
    Neuron. 2000 Jan;25(1):19-28 PMID: 10707969
  8. Identification of two RNA-binding proteins associated with human telomerase RNA.
    Mol Biol Cell. 2000 Mar;11(3):999-1010 PMID: 10712515
  9. The molecular motor dynein is involved in targeting swallow and bicoid RNA to the anterior pole of Drosophila oocytes.
    Nat Cell Biol. 2000 Apr;2(4):185-90 PMID: 10783235
  10. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein.
    Science. 2000 Sep 22;289(5487):2120-2 PMID: 11000113
  11. She2p, a novel RNA-binding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p.
    EMBO J. 2000 Oct 16;19(20):5514-24 PMID: 11032818
  12. She2p is a novel RNA-binding protein that recruits the Myo4p-She3p complex to ASH1 mRNA.
    EMBO J. 2000 Dec 1;19(23):6592-601 PMID: 11101531
  13. mRNA localization: message on the move.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):247-56 PMID: 11283722
  14. The physiological significance of beta -actin mRNA localization in determining cell polarity and directional motility.
    Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7045-50 PMID: 11416185
  15. Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole.
    J Cell Biol. 2001 Aug 6;154(3):511-23 PMID: 11481346
  16. Getting the message across: the intracellular localization of mRNAs in higher eukaryotes.
    Annu Rev Cell Dev Biol. 2001;17:569-614 PMID: 11687499
  17. A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites.
    Neuron. 2001 Nov 8;32(3):463-75 PMID: 11709157
  18. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation.
    Neuron. 2001 Nov 20;32(4):683-96 PMID: 11719208
  19. The message and the messenger: delivering RNA in neurons.
    Sci STKE. 2002 Apr 2;2002(126):pe16 PMID: 11930084
  20. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170.
    Cell. 2002 Jun 28;109(7):873-85 PMID: 12110184
  21. Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles.
    J Cell Sci. 2002 Aug 15;115(Pt 16):3285-95 PMID: 12140260
  22. Identification of mRNA/protein (mRNP) complexes containing Puralpha, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor.
    J Biol Chem. 2002 Oct 4;277(40):37804-10 PMID: 12147688
  23. Regulation and function of local protein synthesis in neuronal dendrites.
    Trends Biochem Sci. 2002 Oct;27(10):506-13 PMID: 12368086
  24. Use of a hybrid vaccinia virus-T7 RNA polymerase system for expression of target genes.
    Mol Cell Biol. 1987 Jul;7(7):2538-44 PMID: 3112559
  25. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos.
    Cell. 1991 Jul 12;66(1):37-50 PMID: 2070417
  26. A new cationic liposome reagent mediating nearly quantitative transfection of animal cells.
    Biotechniques. 1991 Apr;10(4):520-5 PMID: 1867862
  27. A conserved double-stranded RNA-binding domain.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10979-83 PMID: 1438302
  28. Staufen protein associates with the 3'UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner.
    Cell. 1994 Dec 30;79(7):1221-32 PMID: 8001156
  29. Translational regulation in development.
    Cell. 1995 Apr 21;81(2):171-8 PMID: 7736569
  30. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential.
    Cell. 1995 May 5;81(3):403-12 PMID: 7736592
  31. NMR solution structure of a dsRNA binding domain from Drosophila staufen protein reveals homology to the N-terminal domain of ribosomal protein S5.
    EMBO J. 1995 Jul 17;14(14):3563-71 PMID: 7628456
  32. Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization.
    Nature. 1995 Oct 12;377(6549):524-7 PMID: 7566149
  33. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells.
    Cell. 1996 Mar 8;84(5):699-709 PMID: 8625408
  34. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene.
    Cell. 1996 Mar 8;84(5):711-22 PMID: 8625409
  35. IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs.
    EMBO J. 1996 Jun 17;15(12):2997-3005 PMID: 8670801
  36. mRNA localization in neurons: a multipurpose mechanism?
    Neuron. 1997 Jan;18(1):9-12 PMID: 9010200
  37. Characterization of a beta-actin mRNA zipcode-binding protein.
    Mol Cell Biol. 1997 Apr;17(4):2158-65 PMID: 9121465
  38. RNA-RNA interaction is required for the formation of specific bicoid mRNA 3' UTR-STAUFEN ribonucleoprotein particles.
    EMBO J. 1997 Apr 1;16(7):1751-8 PMID: 9130719
  39. Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum.
    Science. 1997 May 16;276(5315):1128-31 PMID: 9148809
  40. Inscuteable and Staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions.
    Cell. 1997 Aug 8;90(3):437-47 PMID: 9267024
  41. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast.
    Nature. 1997 Sep 4;389(6646):90-3 PMID: 9288973
  42. Identification of an actin cytoskeletal complex that includes IQGAP and the Cdc42 GTPase.
    J Biol Chem. 1997 Sep 26;272(39):24443-7 PMID: 9305904
  43. Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate.
    Nature. 1998 Feb 19;391(6669):792-5 PMID: 9486649
  44. hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA.
    Biochemistry. 1998 May 12;37(19):7021-9 PMID: 9578590
  45. Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila.
    Genes Dev. 1998 Jun 15;12(12):1837-46 PMID: 9637685
  46. The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport.
    J Neurosci. 1999 Jan 1;19(1):288-97 PMID: 9870958
  47. Identification of Miranda protein domains regulating asymmetric cortical localization, cargo binding, and cortical release.
    Mol Cell Neurosci. 1998 Dec;12(6):325-39 PMID: 9888987
  48. A human sequence homologue of Staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough endoplasmic reticulum.
    Mol Cell Biol. 1999 Mar;19(3):2212-9 PMID: 10022908
  49. Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum.
    Mol Cell Biol. 1999 Mar;19(3):2220-30 PMID: 10022909
  50. Synaptic plasticity: regulated translation in dendrites.
    Curr Biol. 1999 Mar 11;9(5):R168-70 PMID: 10074442
  51. Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons.
    Mol Biol Cell. 1999 Sep;10(9):2945-53 PMID: 10473638
  52. A generic protein purification method for protein complex characterization and proteome exploration.
    Nat Biotechnol. 1999 Oct;17(10):1030-2 PMID: 10504710
  53. A Xenopus protein related to hnRNP I has a role in cytoplasmic RNA localization.
    Mol Cell. 1999 Sep;4(3):431-7 PMID: 10518224
  54. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses.
    Cell. 2003 Feb 7;112(3):317-27 PMID: 12581522
  55. Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):2100-5 PMID: 12592035
  56. Sunrise at the synapse: the FMRP mRNP shaping the synaptic interface.
    Neuron. 2003 Feb 20;37(4):555-8 PMID: 12597853
  57. Nucleolin associates with a subset of the human Ro ribonucleoprotein complexes.
    J Mol Biol. 2002 Jul 12;320(3):475-88 PMID: 12096904
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2004-00-00
Epub
2004-00-30
Pages
2411-20
Language
English
Region
England
NLM ID
0411011
PMCID
PMC419443
Subset
IM
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