Skip to main content

Neuronal P-bodies and Transport of microRNA-Repressed mRNAs

  • Chapter
  • First Online:
Macro Roles for MicroRNAs in the Life and Death of Neurons

Part of the book series: Research and Perspectives in Neurosciences ((NEUROSCIENCE))

  • 466 Accesses

Abstract

Highly polarized cells like neurons use specialized RNA transport systems to allow for local control of RNA translation, which is a key to neuronal plasticity in the brain. Several proteins, like ZPB1, FMRP, and Staufen, play an important role in transporting RNA along dendrites to the synapse, and a growing amount of evidence has highlighted the role of miRNA in the control of local RNA translation. P-bodies (Processing bodies) are cytoplasmic structures involved in both RNA degradation and storage of untranslated mRNAs. In neurons, dendritic P-body-like structures (dlP-bodies) are present in the soma and dendrites, sometimes in proximity with synapses. They contain miRNA-repressed mRNA and display motorized movement. Under synaptic activation, dlP-bodies relocalize to more distant sites, exchange molecules with the surrounding cytoplasm, and lose some of their components. We propose a model in which dlP-bodies participate in the transport and local regulation of miRNA targets in the dendrites of mammalian neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Ashraf SI, McLoon AL, Sclarsic SM, Kunes S (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124:191–205

    Article  PubMed  CAS  Google Scholar 

  • Bak M, Silahtaroglu A, Møller M, Christensen M, Rath MF, Skryabin B, Tommerup N, Kauppinen S (2008) MicroRNA expression in the adult mouse central nervous system. RNA 14:432–444

    Article  PubMed  CAS  Google Scholar 

  • 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 (2006) Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52:997–1009

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125:1111–1124

    Article  PubMed  CAS  Google Scholar 

  • Bicker S, Schratt G (2008) microRNAs: tiny regulators of synapse function in development and disease. J Cell Mol Med 12:1466–1476

    Article  PubMed  CAS  Google Scholar 

  • Chua JH, Armugam A, Jeyaseelan K (2009) MicroRNAs: Biogenesis, function and applications. Curr Opin Mol Ther 2:189–199

    Google Scholar 

  • Clark I, Giniger E, Ruohola-Baker H, Jan LY, Jan YN. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr Biol 1994:289–300

    Google Scholar 

  • Corbin R, Olsson-Carter K, Slack F (2009) The role of microRNAs in synaptic development and function. BMB Rept 42:131–135

    CAS  Google Scholar 

  • Cougot N, Babajko S, Seraphin B (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165:31–40

    Article  PubMed  CAS  Google Scholar 

  • Cougot N, Bhattacharyya SN, Tapia-Arancibia L, Bordonné R, Filipowicz W, Bertrand E, Rage F (2008) Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation. J Neurosci 28:13793–13804

    Article  PubMed  CAS  Google Scholar 

  • Duan R, Jin P (2006) Identification of messenger RNAs and microRNAs associated with fragile X mental retardation protein. Methods Mol Biol 342:267–276

    PubMed  CAS  Google Scholar 

  • Durand S, Cougot N, Mahuteau-Betzer F, Nguyen CH, Grierson DS, Bertrand E, Tazi J, Lejeune F (2007) Inhibition of nonsense-mediated mRNA decay (NMD) by a new chemical molecule reveals the dynamic of NMD factors in P-bodies. J Cell Biol 178:1145–1160

    Article  PubMed  CAS  Google Scholar 

  • Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C, Turrigiano G, Moore MJ (2007) The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression.Cell 130:179–191

    Article  PubMed  CAS  Google Scholar 

  • Hachet O, Ephrussi A (2001) Drosophila Y14 shuttles to the posterior of the oocyte and is required for oskar mRNA transport. Curr Biol 11:1666–1674

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N, Noda Y, Okada Y (1998) Kinesin and dynein superfamily proteins in organelle transport and cell division. Curr Opin Cell Biol 10:60–73

    Article  PubMed  CAS  Google Scholar 

  • Ingelfinger D, Arndt-Jovin DJ, Lührmann R, Achsel T (2002) The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8:1489–1501

    PubMed  CAS  Google Scholar 

  • Jin P, Alisch RS, Warren ST (2004) RNA and microRNAs in fragile X mental retardation. Nature Cell Biol:6:1048–1053

    Article  PubMed  CAS  Google Scholar 

  • Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nature Rev Mol Cell Biol 6:376–385

    Article  CAS  Google Scholar 

  • Le Hir H, Izaurralde E, Maquat LE, Moore MJ (2000) The spliceosome deposits multiple proteins 20–24 nucleotides upstream of mRNA exon-exon junctions. EMBO J 19:6860–6869

    Article  PubMed  Google Scholar 

  • Leung AK, Calabrese JM, Sharp PA (2006) Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc Natl Acad Sci USA 103:18125–18130

    Article  PubMed  CAS  Google Scholar 

  • Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115:787–798

    Article  PubMed  CAS  Google Scholar 

  • Ling SC, Fahrner PS, Greenough WT, Gelfand VI (2004) Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein. Proc Natl Acad Sci USA 101:17428–17433

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Rivas FV, Wohlschlegel J, Yates JR 3rd, Parker R, Hannon GJ (2005) A role for the P-body component GW182 in microRNA function. Nature Cell Biol. 7:1261–1266

    PubMed  Google Scholar 

  • Martin KC, Zukin RS (2006) RNA trafficking and local protein synthesis in dendrites: an overview. J Neurosci 26:7131–7134

    Article  PubMed  CAS  Google Scholar 

  • Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, Lührmann R, Tuschl T (2005) Identification of novel argonaute-associated proteins. Curr Biol 15:2149–2155

    Article  PubMed  CAS  Google Scholar 

  • Mohr SE Dillon ST, Boswell RE (2001) The RNA-binding protein Tsunagi interacts with Mago Nashi to establish polarity and localize oskar mRNA during Drosophila oogenesis. Genes Dev 15:2886–2899

    PubMed  CAS  Google Scholar 

  • Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W (2005) Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309:1573–1576

    Article  PubMed  CAS  Google Scholar 

  • Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439:283–289

    Article  PubMed  CAS  Google Scholar 

  • Sen GL, Blau HM (2005) Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nature Cell Biol 7:633–636

    Article  PubMed  CAS  Google Scholar 

  • Sheth U, Parker R (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300:805–808

    Article  PubMed  CAS  Google Scholar 

  • St Johnston D (2005) Moving messages: the intracellular localization of mRNAs. Nature Rev Mol Cell Biol 6:363–375

    Article  CAS  Google Scholar 

  • Van Eeden FJ Palacios IM, Petronczki M, Weston MJ, St Johnston D (2001) Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J Cell Biol 154:511–523

    Article  Google Scholar 

  • Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Bassell GJ (2003) Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23:3251–3261

    PubMed  CAS  Google Scholar 

  • Zeitelhofer M, Karra D, Macchi P, Tolino M, Thomas S, Schwarz M, Kiebler M, Dahm R (2008) Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons. J Neurosci 28:7555–7562

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Xing L, Singer RH, Bassell GJ (2007) QNQKE targeting motif for the SMN-Gemin multiprotein complexin neurons. J Neurosci Res 85:2657–2667

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Rage, F. (2010). Neuronal P-bodies and Transport of microRNA-Repressed mRNAs. In: De Strooper, B., Christen, Y. (eds) Macro Roles for MicroRNAs in the Life and Death of Neurons. Research and Perspectives in Neurosciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-04298-0_6

Download citation

Publish with us

Policies and ethics