Skip to main content
SpringerLink
Log in

Localization of mRNAs at Synaptic Sites on Dendrites

  • Chapter
Cell Polarity and Subcellular RNA Localization

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 34))

Abstract

It is becoming increasingly clear that an important aspect of gene expression in neurons involves the delivery of mRNAs to particular subcellular domains. Specifically, although the majority of the mRNAs that are expressed by neurons are found only in the neuronal cell body, a select population of mRNAs are transported into dendrites, and certain neurons also transport mRNA into axons. The nature and significance of this RNA targeting is now under intense investigation, and it is clear that mRNA targeting plays a key role in several aspects of neuronal function.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ainger K, Avossa D, Morgan F, Hill SJ, Barry C, Barbarese E, Carson JH (1993) Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J Cell Biol 123:431–441

    Article  PubMed  CAS  Google Scholar 

  • Ainger K, Avossa D, Diana AS, Barry C, Barbarese E, Carson JH (1997) Transport and localization elements in myelin basic protein mRNA. J Cell Biol 138:1077–1087

    Article  PubMed  CAS  Google Scholar 

  • Berry FB, Brown IR (1996) CaM I mRNA is localized to apical dendrites during postnatal development of neurons in the rat brain. J Neurosci Res 43:565–575

    Article  PubMed  CAS  Google Scholar 

  • Benson DL (1997) Dendritic compartmentation of NMDA receptor mRNA in cultured hippocampal neurons. Neuroreport 8:823–828

    Article  PubMed  CAS  Google Scholar 

  • Berry FB, Brown IR (1996) CaM I mRNA is localized to apical dendrites during postnatal development of neurons in the rat brain. J Neurosci Res 43:565–575

    Article  PubMed  CAS  Google Scholar 

  • Bian F, Chu T, Schilling K, Oberdick J (1996) Differential mRNA transport and the regulation of protein synthesis: selective sensitivity of Purkinje cell dendritic mRNAs to translational inhibition. Mol Cell Neurosci 7:116–133

    Article  PubMed  CAS  Google Scholar 

  • Blichenberg A, Schwanke B, Rehbein M, Garner CC, Richter D, Kindler S (1999) Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J Neurosci 19:8818–8829

    PubMed  CAS  Google Scholar 

  • Burgin KE, Washam MN, Rickling S, Westgate SA, Mobley WC, Kelly PT (1990) In situ hybridization histochemistry of Ca-H/calmodulin-dependent protein kinase in developing rat brain. J Neurosci 10:1788–1798

    PubMed  CAS  Google Scholar 

  • Chicurel ME, Terrian DM, Potter H (1990) Subcellular localization of mRNA: isolation and characterization of mRNA from an enriched preparation of hippocampal dendritic spines. Soc Neurosci Abstr 16:353

    Google Scholar 

  • Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, Greenough WT (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 94:5401–5404

    Article  PubMed  CAS  Google Scholar 

  • Davis L, Banker GA, Steward O (1987) Selective dendritic transport of RNA in hippocampal neurons in culture. Nature 330:447–479

    Article  Google Scholar 

  • Davis L, Burger B, Banker G, Steward O (1990) Dendritic transport: quantitative analysis of the time course of somatodendritic transport of recently synthesized RNA. J Neurosci 10:3056–3058

    PubMed  CAS  Google Scholar 

  • Dugich MM, Tocco G, Willoughby DA, Najm I, Pasinetti G, Thompson RF, Baudry M, Lapchak PA, Hefti F (1992) BDNF mRNA expression in the developing rat brain following kainic acidinduced seizure activity. Neuron 8:1127–1138

    Article  Google Scholar 

  • Feig S, Lipton P (1993) Pairing the cholinergic agonist carbachol with patterned Schaffer collateral stimulation initiates protein synthesis in hippocampal CA1 pyramidal cell dendrites via a muscarinic, NMDA-dependent mechanism. J Neurosci 13:1010–1021

    PubMed  CAS  Google Scholar 

  • Feng Y, Gutekunst C-A, Eberhart DE, Yi H, Warren ST, Hersch SM (1997) Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J Neurosci 17:1539–1547

    PubMed  CAS  Google Scholar 

  • Ferrandon D, Elphick L, Nusslein-Volhard C, Johnson DS (1994) Staufen protein associates with the 3’UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Ce11:1221–1232

    Google Scholar 

  • Furuichi T, Simon-Chazottes D, Fujino I, Yamada N, Hasegawa M, Miyawaki A, Yoshikawa S, Guenet J-L, Mikoshiba K (1993) Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene (Insp3r1) in the mouse central nervous system. Recept Chann 1:11–24

    CAS  Google Scholar 

  • Garner CC, Tucker RP, Matus A (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336:674–677

    Article  PubMed  CAS  Google Scholar 

  • Herb A, Wisden W, Catania dMV, Marechal D, Dresse A, Seeberg PH (1997) Prominent dendritic localization in forebrain neurons of a novel mRNA and its product, dendrin. Mol Cell Neurosci 8:367–374

    Article  PubMed  CAS  Google Scholar 

  • Hinds HL, Ashley CT, Sutcliffe JS, Nelson DL, Warren ST, Housman DE, Schalling M (1993) Tissue specific expression of FMR-1 provides evidence for a functional role in fragile X syndrome. Nat Gen 3:36–43

    Article  CAS  Google Scholar 

  • Kiebler MA, Hemraj I, Verkade P, Kohrmann M, Fortes P, Marion RM, Ortin J, Dotti CG (1999) The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons. J Neurosci 19:274–287

    Google Scholar 

  • Kislauskis EH, Zhu X, Singer RH (1994) Sequences responsible for intracellular localization of ßactin messenger RNA also affect cell phenotype. J Cell Biol 127:441–451

    Article  PubMed  CAS  Google Scholar 

  • Kleiman R, Banker G, Steward O (1994) Development of subcellular mRNA compartmentation in hippocampal neurons in culture. J Neurosci 14:1130–1140

    PubMed  CAS  Google Scholar 

  • Knowles RB, Kosik KS (1997) Neurotrophin-3 signals redistribute RNA in neurons. Proc Natl Acad Sci USA 94:14804–14808

    Article  PubMed  CAS  Google Scholar 

  • Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Ellisman MH, Bassell GJ, Kosik KS (1996) Translocation of RNA granules in living neurons. J Neurosci 16:7812–7820

    PubMed  CAS  Google Scholar 

  • Kohrmann M, Luo M, Kaether C, DesGroseillers L, Dotti CG, Keibler MA (1999) Microtubuledependent recruitment of staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol Biol Cell 10:2945–2953

    PubMed  CAS  Google Scholar 

  • Laudry CF, Watson JB, Handley VW, Campagnoni AT (1993) Distribution of neuronal and glial mRNAs within neuronal cell bodies and processes. Soc Neurosci Abstr 19:1745

    Google Scholar 

  • Leski ML, Steward O (1996) Synthesis of proteins within dendrites: ionic and neurotransmitter modulation of synthesis of particular polypeptides characterized by gel electrophoresis. Neurochem Res 21:681–690

    Article  PubMed  CAS  Google Scholar 

  • Link W, Konietzko G, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl K (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 92:5734–5738

    Article  PubMed  CAS  Google Scholar 

  • Lyford G, Yamagata K, Kaufmann W, Barnes C, Sanders L, Copeland N, Gilbert D, Jenkins N, Lanahan A, Worley P (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14:433–445

    Article  PubMed  CAS  Google Scholar 

  • MacDonald PM, Struhl G (1988) Cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. Nature 336:595–598

    Article  PubMed  CAS  Google Scholar 

  • Mayford M, Baranes D, Podsypania K, Kandel E (1996) The 3’-untranslated region of CAMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc Natl Acad Sci USA 93:13250–13255

    Article  PubMed  CAS  Google Scholar 

  • Miyashiro K, Dichter M, Eberwine J (1994) On the nature and differential distribution of mRNAs in hippocampal neuntes: implications for neuronal functioning. Proc Natl Acad Sci USA 91:10800–10804

    Article  PubMed  CAS  Google Scholar 

  • Mowry KL, Melton DA (1992) Vegetal messenger RNA localization directed by a 34-nt sequence element in Xenopus oocytes. Science 255:991–994

    Article  PubMed  CAS  Google Scholar 

  • Ouyang Y, Kreiman G, Kantor DB, Rosenstein AJ, Schuman EM, Kennedy MB (1998) Tetanic stimulation produces a similar increase in both nonphosphorylated and autophosphorylated CAMKII in dendrites of hippocampal CA1 neurons. Soc Neurosci Abstr 23:798

    Google Scholar 

  • Palacios-Pru EL, Palacios L, Mendoza RV (1981) Synaptogenetic mechanisms during chick cerebellar cortex development. J Submicros Cytol 13:145–167

    CAS  Google Scholar 

  • Palacios-Pru EL, Miranda-Contreras L, Mendoza RV, Zambrano E (1988) Dendritic RNA and postsynaptic density formation in chick cerebellar synaptogenesis. Neuroscience 24:111–118

    Article  PubMed  CAS  Google Scholar 

  • Paradies MA, Steward O (1997) Multiple subcellular mRNA distribution patterns in neurons: a nonisotopic in situ hybridization analysis. J Neurobiol 33:473–493

    Article  PubMed  CAS  Google Scholar 

  • Perlin JB, Gerwin CM, Panchision DM, Vick RS, Jakoi ER, DeLorenzo RJ (1993) Kindling produces long-lasting and selective changes in gene expression in hippocampal neurons. Proc Natl Acad Sci USA 90:1741–1745

    Article  PubMed  CAS  Google Scholar 

  • Pierce JP, van Leyen K, McCarthy JB (2000) Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines. Nat Neurosci 3:311–313

    Article  PubMed  CAS  Google Scholar 

  • Prakash N, Fehr S, Mohr E, Richter D (1997) Dendritic localization of rat vasopressin mRNA: ultrastructural analysis and mapping of targeting elements. Eur J Neurosci 9:523–532

    Article  PubMed  CAS  Google Scholar 

  • Racca C, Gardiol A, Triller A (1997) Dendritic and postsynaptic localizations of glycine receptor alpha subunit mRNAs. J Neurosci 17:1691–1700

    PubMed  CAS  Google Scholar 

  • Rao A, Steward O (1991a) Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: analysis of proteins synthesized within synaptosomes. J Neurosci 11:2881–2895

    PubMed  CAS  Google Scholar 

  • Rao A, Steward O (1991b) Synaptosomal RNA: assessment of contamination by glia and comparison with total RNA. Soc Neurosci Abstr 17:379

    Google Scholar 

  • Severt WL, Biber TUL, Wu X-Q, Hecht NB, DeLorenzo RJ, Jakoi ER (2000) The suppression of testis-brain RNA binding protein and kinesin heavy chain disrupts mRNA sorting in dendrites. J Cell Sci 112:3691–3702

    Google Scholar 

  • Sheetz AJ, Nairn AC, Constantine-Paton M (1997) N-methyl-D-aspartate receptor activation and visual activity induce elongation factor-2 phosphorylation in amphibian tecta: a role for Nmethyl-D-aspartate receptors in controlling protein synthesis. Proc Natl Acad Sci USA 94:14770–14775

    Article  Google Scholar 

  • Sheetz AJ, Nairn AC, Constantine-Paton M (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3:211–216.

    Article  Google Scholar 

  • Spacek J, Hartmann M (1983) Three-dimensional analysis of dendritic spines. I. Quantitative observations related to dendritic spines and synaptic morphology in cerebral and cerebellar cortices. Anat Embryol 167:289–310

    Article  PubMed  CAS  Google Scholar 

  • Steward O (1983) Polyribosomes at the base of dendritic spines of CNS neurons: their possible role in synapse construction and modification. Cold Spring Harbor Symp Quant Biol 48:745–759

    Article  PubMed  Google Scholar 

  • Steward O (1997) mRNA localization in neurons: a multipurpose mechanism. Neuron 18:9–12

    Article  PubMed  CAS  Google Scholar 

  • Steward O, Falk PM (1986) Protein synthetic machinery at postsynaptic sites during synaptogenesis; a quantitative study of the association between polyribosomes and developing synapses. J Neurosci 6:412–423

    PubMed  CAS  Google Scholar 

  • Steward O, Fass B (1983) Polyribosomes associated with dendritic spines in the denervated dentate gyrus: evidence for local regulation of protein synthesis during reinnervation. Prog Brain Res 58:131–136

    Article  PubMed  CAS  Google Scholar 

  • Steward O, Halpain S (1999) Lamina-specific synaptic activation causes domain-specific alterations in dendritic immunostaining for MAP2 and CAM kinase II. J Neurosci 15:78347845

    Google Scholar 

  • Steward O, Levy WB (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2:284–291

    PubMed  CAS  Google Scholar 

  • Steward O, Reeves TM (1988) Protein synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site. J Neurosci 8:176–184

    PubMed  CAS  Google Scholar 

  • Steward O, Ribak CE (1986) Polyribosomes associated with synaptic sites on axon initial segments: localization of protein synthetic machinery at inhibitory synapses. J Neurosci 6:3079–3085

    PubMed  CAS  Google Scholar 

  • Steward O, Singer RH (1997) The intracellular mRNA sorting system: postal zones, zip codes, mail bags and mail boxes. In: Hartford JB, Morris DR (eds) mRNA metabolism and posttranscriptional gene regulation. Wiley-Liss, New York, pp 127–146

    Google Scholar 

  • Steward O, Worley PF (submitted) Selective targeting of newly-synthesized Arc mRNA to synaptic sites is mediated by NMDA receptor activation

    Google Scholar 

  • Steward O, Pollack A, Rao A (1991) Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: time course of appearance of recently synthesized proteins in synaptic junctions. J Neurosci Res 30:649–660

    Article  PubMed  CAS  Google Scholar 

  • Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741–751

    Article  PubMed  CAS  Google Scholar 

  • Tongiorgi E, Righi M, Cattaneo A (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17:9492–9505

    PubMed  CAS  Google Scholar 

  • Torre ER, Steward O (1996) Protein synthesis within dendrites: distribution of the endoplasmic reticulum and the Golgi apparatus in dendrites of hippocampal neurons in culture. J Neurosci 16:5967–5978

    PubMed  CAS  Google Scholar 

  • Valentine G, Chakravarty S, Sarvey J, Bramham C, Herkenham M (2000) Fragile X (fmr1) mRNA expression is differentially regulated in two adult models of activity-dependent gene expression. Mol Brain Res 75:337–341

    Article  PubMed  CAS  Google Scholar 

  • Verity MA, Brown WJ, Cheung M (1980) Isolation of ribosome containing synaptosome subpopulation with active in vitro protein synthesis. J Neurosci Res 5:143–153

    Article  PubMed  CAS  Google Scholar 

  • Wallace CS, Lyford GL, Worley PF, Steward O (1998) Differential intracellular sorting of immediate early gene mRNAs depends on signals in the mRNA sequence. J Neurosci 18:26–35

    PubMed  CAS  Google Scholar 

  • Watson JB, Coulter PM, Margulies JE, de Lecea L, Danielson PE, Erlander MG, Sutcliffe JG (1994) G-protein gamma7 subunit is selectively expressed in medium-sized neurons and dendrites of the rat neostriatum. J Neurosci Res 39:108–116

    Article  PubMed  CAS  Google Scholar 

  • Weiler IJ, Greenough WT (1991) Potassium ion stimulation triggers protein translation in synaptoneurosomal polyribosomes. Mol Cell Neurosci 2:305–314

    Article  PubMed  CAS  Google Scholar 

  • Weiler IJ, Greenough WT (1993) Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc Nat Acad Sci USA 90:7168–7171

    Article  PubMed  CAS  Google Scholar 

  • Weiler IJ, Irwin SA, Klintsova AY, Spencer CM, Brazelton AD, Miyashiro K, Comery TA, Patel B, Eberwine J, Greenough WT (1997) Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc Nat! Acad Sci USA 94:5395–5400

    Article  CAS  Google Scholar 

  • Wu L, Wells D, Tay J, Mendis D, Abborr M-A, Barnitt A, Quinlan E, Heynen A, Fallon JR, Richter JD (1998) CPEB-mediated cytoplasmic polyadenylation and the regulation of experiencedependent translation of alpha-CaMKII at synapses. Neuron 21:1129–1139

    Article  PubMed  CAS  Google Scholar 

  • Yisraeli JK, Melton DA (1988) The maternal mRNA Vgl is correctly localized following injection into Xenopus oocytes. Nature 336:592–595

    Article  PubMed  CAS  Google Scholar 

  • Yisraeli JK, Sokol S, Melton DA (1990) A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vgl mRNA. Development 108:289–298

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Reeve-Irvine Research Center, Departments of Anatomy/Neurobiology and Neurobiology and Behavior, College of Medicine, University of California at Irvine, Irvine, CA, 92697, USA

    Oswald Steward

  2. Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA

    Paul Worley

Authors
  1. Oswald Steward
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul Worley
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institut für Zellbiochemie und klinische Neurobiologie, Universitäts-Krankenhaus Eppendorf, Martinistraße 52, 20246, Hamburg, Germany

    Dietmar Richter

Rights and permissions

Reprints and permissions

Copyright information

© 2001 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Steward, O., Worley, P. (2001). Localization of mRNAs at Synaptic Sites on Dendrites. In: Richter, D. (eds) Cell Polarity and Subcellular RNA Localization. Results and Problems in Cell Differentiation, vol 34. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-40025-7_1

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-40025-7_1

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-07436-3

  • Online ISBN: 978-3-540-40025-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation