Home LiteratureArticle Details
PMID: 17178403 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies.

Neuron ·Vol. 52 ·No. 6 ·2006-12-21 ·Pages 997-1009

Barbee SA, Estes PS, Cziko AM, Hillebrand J, Luedeman RA, Coller JM, Johnson N, Howlett IC, Geng C, Ueda R, Brand AH, Newbury SF, Wilhelm JE, Levine RB, Nakamura A, Parker R, Ramaswami M

Abstract

Local control of mRNA translation modulates neuronal development, synaptic plasticity, and memory formation. A poorly understood aspect of this control is the role and composition of ribonucleoprotein (RNP) particles that mediate transport and translation of neuronal RNAs. Here, we show that staufen- and FMRP-containing RNPs in Drosophila neurons contain proteins also present in somatic "P bodies," including the RNA-degradative enzymes Dcp1p and Xrn1p/Pacman and crucial components of miRNA (argonaute), NMD (Upf1p), and general translational repression (Dhh1p/Me31B) pathways. Drosophila Me31B is shown to participate (1) with an FMRP-associated, P body protein (Scd6p/trailer hitch) in FMRP-driven, argonaute-dependent translational repression in developing eye imaginal discs; (2) in dendritic elaboration of larval sensory neurons; and (3) in bantam miRNA-mediated translational repression in wing imaginal discs. These results argue for a conserved mechanism of translational control critical to neuronal function and open up new experimental avenues for understanding the regulation of mRNA function within neurons.

MeSH Terms
Animals Animals, Genetically Modified Blotting, Northern Blotting, Western/methods Caspases/metabolism Cells, Cultured Central Nervous System/cytology Dendrites/metabolism,physiology Drosophila Drosophila Proteins/metabolism,physiology Exoribonucleases/metabolism Eye/metabolism,ultrastructure Fragile X Mental Retardation Protein/metabolism Green Fluorescent Proteins/metabolism Immunohistochemistry/methods Larva MicroRNAs/metabolism Microscopy, Electron, Scanning/methods Neurons/cytology,metabolism Protein Biosynthesis/physiology Protein Transport/physiology RNA-Binding Proteins/metabolism RNA-Induced Silencing Complex/metabolism Ribonucleoproteins/physiology
Chemicals
Drosophila Proteins MicroRNAs RNA-Binding Proteins RNA-Induced Silencing Complex Ribonucleoproteins Fragile X Mental Retardation Protein stau protein, Drosophila Green Fluorescent Proteins Exoribonucleases pcm protein, Drosophila Caspases Dcp-1 protein, Drosophila
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Barbee Scott A
Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85721, USA.
Estes Patricia S
Cziko Anne-Marie
Hillebrand Jens
Luedeman Rene A
Coller Jeff M
Johnson Nick
Howlett Iris C
Geng Cuiyun
Ueda Ryu
Brand Andrea H
Newbury Sarah F
Wilhelm James E
Levine Richard B
Nakamura Akira
Parker Roy
Ramaswami Mani
References (74)
74 references, click to expand
  1. Translational regulation and RNA localization in Drosophila oocytes and embryos.
    Annu Rev Genet. 2001;35:365-406 PMID: 11700288
  2. 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
  3. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation.
    Neuron. 2001 Nov 20;32(4):683-96 PMID: 11719208
  4. The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes.
    RNA. 2001 Dec;7(12):1717-27 PMID: 11780629
  5. Ypsilon Schachtel, a Drosophila Y-box protein, acts antagonistically to Orb in the oskar mRNA localization and translation pathway.
    Development. 2002 Jan;129(1):197-209 PMID: 11782413
  6. Selective translation of mRNAs at synapses.
    Curr Opin Neurobiol. 2002 Jun;12(3):300-4 PMID: 12049937
  7. Caenorhabditis elegans decapping proteins: localization and functional analysis of Dcp1, Dcp2, and DcpS during embryogenesis.
    Mol Biol Cell. 2005 Dec;16(12):5880-90 PMID: 16207815
  8. Disruption of GW bodies impairs mammalian RNA interference.
    Nat Cell Biol. 2005 Dec;7(12):1267-74 PMID: 16284622
  9. A role for the P-body component GW182 in microRNA function.
    Nat Cell Biol. 2005 Dec;7(12):1261-6 PMID: 16284623
  10. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila.
    Cell. 2006 Jan 13;124(1):191-205 PMID: 16413491
  11. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices.
    Neuron. 2002 Aug 1;35(3):535-45 PMID: 12165474
  12. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins.
    Genes Dev. 2002 Oct 1;16(19):2497-508 PMID: 12368261
  13. 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
  14. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila.
    Cell. 2003 Apr 4;113(1):25-36 PMID: 12679032
  15. Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion.
    Curr Biol. 2003 Apr 15;13(8):618-26 PMID: 12699617
  16. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies.
    Science. 2003 May 2;300(5620):805-8 PMID: 12730603
  17. 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
  18. The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies.
    RNA. 2003 Oct;9(10):1171-3 PMID: 13130130
  19. Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1.
    Development. 2003 Nov;130(22):5543-52 PMID: 14530299
  20. Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentsz.
    J Cell Biol. 2003 Dec 22;163(6):1197-204 PMID: 14691132
  21. Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis.
    Dev Cell. 2004 Jan;6(1):69-78 PMID: 14723848
  22. The enzymes and control of eukaryotic mRNA turnover.
    Nat Struct Mol Biol. 2004 Feb;11(2):121-7 PMID: 14749774
  23. Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons.
    Curr Biol. 2004 Feb 17;14(4):314-21 PMID: 14972682
  24. Cytoplasmic foci are sites of mRNA decay in human cells.
    J Cell Biol. 2004 Apr12;165(1):31-40 PMID: 15067023
  25. Evidence for cell autonomous AP1 function in regulation of Drosophila motor-neuron plasticity.
    BMC Neurosci. 2003 Sep 11;4:20 PMID: 12969508
  26. Local protein synthesis during axon guidance and synaptic plasticity.
    Curr Opin Neurobiol. 2004 Jun;14(3):305-10 PMID: 15194110
  27. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule.
    Neuron. 2004 Aug 19;43(4):513-25 PMID: 15312650
  28. Staufen, a gene required to localize maternal RNAs in the Drosophila egg.
    Cell. 1991 Jul 12;66(1):51-63 PMID: 1712672
  29. Genetics of nanos localization in Drosophila.
    Dev Dyn. 1994 Feb;199(2):103-15 PMID: 7515724
  30. 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
  31. Translocation of RNA granules in living neurons.
    J Neurosci. 1996 Dec 15;16(24):7812-20 PMID: 8987809
  32. Xp54, the Xenopus homologue of human RNA helicase p54, is an integral component of stored mRNP particles in oocytes.
    Nucleic Acids Res. 1997 Mar 1;25(5):965-73 PMID: 9023105
  33. Isolation and characterization of Dcp1p, the yeast mRNA decapping enzyme.
    EMBO J. 1998 Mar 2;17(5):1487-96 PMID: 9482745
  34. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells.
    Development. 1998 Feb;125(4):679-90 PMID: 9435288
  35. The mRNA 5' cap-binding protein eIF4E and control of cell growth.
    Curr Opin Cell Biol. 1998 Apr;10(2):268-75 PMID: 9561852
  36. The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis.
    J Neurosci. 1998 Nov 1;18(21):8886-99 PMID: 9786994
  37. 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
  38. 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
  39. RNA and microRNAs in fragile X mental retardation.
    Nat Cell Biol. 2004 Nov;6(11):1048-53 PMID: 15516998
  40. Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay.
    Cell. 2005 Jan 28;120(2):195-208 PMID: 15680326
  41. The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway.
    Dev Cell. 2005 Mar;8(3):331-42 PMID: 15737929
  42. Processing bodies require RNA for assembly and contain nontranslating mRNAs.
    RNA. 2005 Apr;11(4):371-82 PMID: 15703442
  43. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies.
    RNA. 2005 May;11(5):717-27 PMID: 15840819
  44. A novel RNA-binding protein in neuronal RNA granules: regulatory machinery for local translation.
    J Neurosci. 2005 Apr 27;25(17):4420-34 PMID: 15858068
  45. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling.
    J Cell Biol. 2005 Jun 20;169(6):871-84 PMID: 15967811
  46. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies.
    Nat Cell Biol. 2005 Jul;7(7):719-23 PMID: 15937477
  47. Localization of FMRP-associated mRNA granules and requirement of microtubules for activity-dependent trafficking in hippocampal neurons.
    Genes Brain Behav. 2005 Aug;4(6):350-9 PMID: 16098134
  48. Inhibition of translational initiation by Let-7 MicroRNA in human cells.
    Science. 2005 Sep 2;309(5740):1573-6 PMID: 16081698
  49. The Elegance of the MicroRNAs: A Neuronal Perspective.
    Neuron. 2005 Sep 15;47(6):779-82 PMID: 16157272
  50. General translational repression by activators of mRNA decapping.
    Cell. 2005 Sep 23;122(6):875-86 PMID: 16179257
  51. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies.
    Science. 2005 Oct 21;310(5747):486-9 PMID: 16141371
  52. Contrasting mechanisms of regulating translation of specific Drosophila germline mRNAs at the level of 5'-cap structure binding.
    Biochem Soc Trans. 2005 Dec;33(Pt 6):1544-6 PMID: 16246166
  53. A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans.
    J Cell Biol. 2005 Oct 24;171(2):267-79 PMID: 16247027
  54. A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C. elegans.
    Development. 2005 Nov;132(22):4975-86 PMID: 16221731
  55. A brain-specific microRNA regulates dendritic spine development.
    Nature. 2006 Jan 19;439(7074):283-9 PMID: 16421561
  56. A repeated IMP-binding motif controls oskar mRNA translation and anchoring independently of Drosophila melanogaster IMP.
    J Cell Biol. 2006 Feb 13;172(4):577-88 PMID: 16476777
  57. Control of translation and mRNA degradation by miRNAs and siRNAs.
    Genes Dev. 2006 Mar 1;20(5):515-24 PMID: 16510870
  58. Characterization of an RNA granule from developing brain.
    Mol Cell Proteomics. 2006 Apr;5(4):635-51 PMID: 16352523
  59. RNA-associated protein 55 (RAP55) localizes to mRNA processing bodies and stress granules.
    RNA. 2006 Apr;12(4):547-54 PMID: 16484376
  60. Dendritic localization of the translational repressor Pumilio 2 and its contribution to dendritic stress granules.
    J Neurosci. 2006 Jun 14;26(24):6496-508 PMID: 16775137
  61. Targeting of aberrant mRNAs to cytoplasmic processing bodies.
    Cell. 2006 Jun 16;125(6):1095-109 PMID: 16777600
  62. Relief of microRNA-mediated translational repression in human cells subjected to stress.
    Cell. 2006 Jun 16;125(6):1111-24 PMID: 16777601
  63. Neuronal RNA granules: movers and makers.
    Neuron. 2006 Sep 21;51(6):685-90 PMID: 16982415
  64. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54.
    PLoS Biol. 2006 Jul;4(7):e210 PMID: 16756390
  65. Recognition of yeast mRNAs as "nonsense containing" leads to both inhibition of mRNA translation and mRNA degradation: implications for the control of mRNA decapping.
    Mol Biol Cell. 1999 Nov;10(11):3971-8 PMID: 10564284
  66. Isolation of a ribonucleoprotein complex involved in mRNA localization in Drosophila oocytes.
    J Cell Biol. 2000 Feb 7;148(3):427-40 PMID: 10662770
  67. Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions.
    Nature. 2000 Jun 29;405(6790):1062-5 PMID: 10890448
  68. Characterization of dFMR1, a Drosophila melanogaster homolog of the fragile X mental retardation protein.
    Mol Cell Biol. 2000 Nov;20(22):8536-47 PMID: 11046149
  69. Synaptic regulation of protein synthesis and the fragile X protein.
    Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7101-6 PMID: 11416194
  70. Abnormal development of dendritic spines in FMR1 knock-out mice.
    J Neurosci. 2001 Jul 15;21(14):5139-46 PMID: 11438589
  71. 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
  72. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility.
    Neuron. 2001 Aug 2;31(2):261-75 PMID: 11502257
  73. cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans.
    Development. 2001 Sep;128(17):3221-32 PMID: 11546739
  74. Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis.
    Development. 2001 Sep;128(17):3233-42 PMID: 11546740
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
0896-6273
DOI
10.1016/j.neuron.2006.10.028
Published
2006-12-21
Pages
997-1009
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC1955741
Subset
IM
Grants
NIGMS NIH HHS · GM54409 · United States
Biotechnology and Biological Sciences Research Council · BB/C005163/1 · United Kingdom
NIDA NIH HHS · R01 DA015495 · United States
Medical Research Council · G0300072 · United Kingdom
NIDA NIH HHS · DA17749 · United States
NIGMS NIH HHS · R37 GM045443 · United States
NIDA NIH HHS · DA15495 · United States
NIGMS NIH HHS · R01 GM054409 · United States
NIDA NIH HHS · K02 DA017749 · United States
External Links
PubMed source DOI: 10.1016/j.neuron.2006.10.028 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2