Home LiteratureArticle Details
PMID: 9169532 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

RNA transport in dendrites: a cis-acting targeting element is contained within neuronal BC1 RNA.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 17 ·No. 12 ·1997-06-15 ·Pages 4722-33

Muslimov IA, Santi E, Homel P, Perini S, Higgins D, Tiedge H

Abstract

In nerve cells, a select group of RNAs has been localized to dendritic domains. Here we have examined dendritic RNA transport in sympathetic neurons in primary culture, using a microinjection protocol with neuronal BC1 RNA and with BC1-derived sequence segments. After cytoplasmic microinjection, full-length BC1 RNA was selectively transported to dendrites; in contrast, control RNAs such as nuclear RNAs and random-sequence irrelevant RNAs remained restricted to cytoplasmic areas proximal to the injection sites. Chimeric RNAs were constructed that contained the full-length BC1 sequence inserted upstream or downstream of the coding regions of nondendritic mRNAs. After microinjection, such chimeric RNAs were specifically targeted to dendrites; microinjected corresponding nonchimeric mRNAs were not. Dendritic transport of BC1 RNA was rapid: the average dendritic delivery rate within the first hour after microinjection was 242 +/- 25 microm/hr. Whereas a 5'-BC1 segment of 62 nucleotides was transported to dendrites to extents and at levels similar to full-length BC1 RNA, a 3'-BC1 segment of 60 nucleotides did not exit injected somata to any significant degree. A cis-acting dendritic targeting element is thus contained in the 5' part of neuronal BC1 RNA. These results demonstrate that mechanisms exist in neurons for fast and specific transport of selected RNAs to dendrites.

MeSH Terms
Animals Axonal Transport Cell Nucleus/metabolism Cells, Cultured DNA-Binding Proteins/biosynthesis Dendrites/metabolism Embryo, Mammalian Microinjections Neurons/metabolism RNA/administration & dosage,metabolism RNA, Long Noncoding RNA, Small Nuclear/metabolism RNA, Untranslated Rats Rats, Sprague-Dawley Ribonucleoproteins/biosynthesis Ribonucleoproteins, Small Cytoplasmic Superior Cervical Ganglion/metabolism Transcription, Genetic
Chemicals
Bc1 long-non-coding RNA, rat DNA-Binding Proteins RNA, Long Noncoding RNA, Small Nuclear RNA, Untranslated Ribonucleoproteins Ribonucleoproteins, Small Cytoplasmic RNA
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Muslimov I A
Department of Pharmacology, State University of New York, Health Science Center at Brooklyn, Brooklyn, New York 11203, USA.
Santi E
Homel P
Perini S
Higgins D
Tiedge H
References (53)
53 references, click to expand
  1. Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis.
    Neuron. 1996 Dec;17(6):1173-87 PMID: 8982164
  2. The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo.
    EMBO J. 1988 Jun;7(6):1749-56 PMID: 2901954
  3. Molecular characterization of dendritically localized transcripts encoding MAP2.
    Brain Res Mol Brain Res. 1996 Feb;36(1):63-9 PMID: 9011766
  4. Complete cDNA sequence encoding rat high and low molecular weight MAP2.
    Nucleic Acids Res. 1990 May 11;18(9):2822 PMID: 2339070
  5. U4 and U6 RNAs coexist in a single small nuclear ribonucleoprotein particle.
    Nucleic Acids Res. 1984 Apr 11;12(7):3283-93 PMID: 6201826
  6. Selective dendritic transport of RNA in hippocampal neurons in culture.
    Nature. 1987 Dec 3-9;330(6147):477-9 PMID: 2446139
  7. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  8. Somatodendritic expression of an immediate early gene is regulated by synaptic activity.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5734-8 PMID: 7777577
  9. Targeting of mRNAs to subsynaptic microdomains in dendrites.
    Curr Opin Neurobiol. 1995 Feb;5(1):55-61 PMID: 7773006
  10. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites.
    Neuron. 1995 Feb;14(2):433-45 PMID: 7857651
  11. Dendritic and postsynaptic localizations of glycine receptor alpha subunit mRNAs.
    J Neurosci. 1997 Mar 1;17(5):1691-700 PMID: 9030628
  12. Structure and expression of the rat inositol 1,4,5-trisphosphate receptor.
    J Biol Chem. 1990 Jul 25;265(21):12679-85 PMID: 2165071
  13. Cellular influences on RNA sorting in neurons and glia: an in situ hybridization histochemical study.
    Brain Res Mol Brain Res. 1994 Nov;27(1):1-11 PMID: 7877439
  14. Computer prediction of RNA structure.
    Methods Enzymol. 1989;180:262-88 PMID: 2482418
  15. Neural BC1 RNA: cDNA clones reveal nonrepetitive sequence content.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2624-8 PMID: 2437583
  16. Localized RNAs and their functions.
    Bioessays. 1993 Oct;15(10):651-8 PMID: 7506023
  17. mRNA localization in neurons: a multipurpose mechanism?
    Neuron. 1997 Jan;18(1):9-12 PMID: 9010200
  18. Structure and regulation of the gene encoding the neuron-specific protein kinase C substrate neurogranin (RC3 protein).
    J Biol Chem. 1995 Apr 28;270(17):10314-22 PMID: 7730337
  19. Improved green fluorescence.
    Nature. 1995 Feb 23;373(6516):663-4 PMID: 7854443
  20. In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain.
    J Neurosci. 1990 Jun;10(6):1788-98 PMID: 2162385
  21. On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10800-4 PMID: 7971965
  22. Superpolylinkers in cloning and expression vectors.
    DNA. 1989 Dec;8(10):759-77 PMID: 2558866
  23. The intracellular localization of messenger RNAs.
    Cell. 1995 Apr 21;81(2):161-70 PMID: 7736568
  24. Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites.
    Nature. 1988 Dec 15;336(6200):674-7 PMID: 3200318
  25. The use of UV light as a cross-linking agent for cells and tissue sections in in situ hybridization.
    DNA Cell Biol. 1991 Mar;10(2):143-7 PMID: 1706186
  26. mRNA at the synapse: analysis of a synaptosomal preparation enriched in hippocampal dendritic spines.
    J Neurosci. 1993 Sep;13(9):4054-63 PMID: 8396172
  27. Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene (Insp3r1) in the mouse central nervous system.
    Receptors Channels. 1993;1(1):11-24 PMID: 8081710
  28. Dendritic transport: quantitative analysis of the time course of somatodendritic transport of recently synthesized RNA.
    J Neurosci. 1990 Sep;10(9):3056-68 PMID: 1697901
  29. Evidence for base-pairing between mammalian U2 and U6 small nuclear ribonucleoprotein particles.
    Genes Dev. 1990 Dec;4(12A):2146-56 PMID: 2176635
  30. Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies.
    J Neurosci. 1992 Mar;12(3):762-72 PMID: 1545238
  31. Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site.
    J Neurosci. 1988 Jan;8(1):176-84 PMID: 3339407
  32. Evidence for the existence of snRNAs U4 and U6 in a single ribonucleoprotein complex and for their association by intermolecular base pairing.
    EMBO J. 1984 Jun;3(6):1357-63 PMID: 6204860
  33. Protein-RNA recognition.
    Annu Rev Biochem. 1995;64:593-620 PMID: 7574494
  34. Cell-cell signaling, microtubules, and the loss of symmetry in the Drosophila oocyte.
    Cell. 1995 Nov 3;83(3):353-6 PMID: 8521463
  35. Getting the message from the gene to the synapse: sorting and intracellular transport of RNA in neurons.
    Trends Neurosci. 1992 May;15(5):180-6 PMID: 1377425
  36. Dendritic location of neural BC1 RNA.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2093-7 PMID: 1706516
  37. BC1 RNA: transcriptional analysis of a neural cell-specific RNA polymerase III transcript.
    Mol Cell Biol. 1995 Mar;15(3):1642-50 PMID: 7862155
  38. Subcellular distribution of rRNA and poly(A) RNA in hippocampal neurons in culture.
    Brain Res Mol Brain Res. 1993 Dec;20(4):305-12 PMID: 7906850
  39. Brain-specific small RNA transcript of the identifier sequences is present as a 10 S ribonucleoprotein particle.
    J Biol Chem. 1991 Mar 15;266(8):4726-30 PMID: 1705932
  40. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity.
    Science. 1996 Sep 6;273(5280):1402-6 PMID: 8703078
  41. Functions of U-snRNPs.
    Mol Biol Rep. 1990;14(2-3):183-92 PMID: 2141907
  42. Distinct spatial localization of specific mRNAs in cultured sympathetic neurons.
    Neuron. 1990 Dec;5(6):809-19 PMID: 2148487
  43. Determinants of mRNA localization.
    Curr Opin Cell Biol. 1992 Dec;4(6):975-8 PMID: 1485968
  44. Translational machinery in dendrites of hippocampal neurons in culture.
    J Neurosci. 1996 Nov 15;16(22):7171-81 PMID: 8929426
  45. 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 U S A. 1996 Nov 12;93(23):13250-5 PMID: 8917577
  46. Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes.
    J Cell Biol. 1993 Oct;123(2):431-41 PMID: 7691830
  47. Dendrites as compartments for macromolecular synthesis.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10766-8 PMID: 7971959
  48. Translocation of RNA granules in living neurons.
    J Neurosci. 1996 Dec 15;16(24):7812-20 PMID: 8987809
  49. Development of subcellular mRNA compartmentation in hippocampal neurons in culture.
    J Neurosci. 1994 Mar;14(3 Pt 1):1130-40 PMID: 7509864
  50. Identification and characterization of BC1 RNP particles.
    DNA Cell Biol. 1996 Jul;15(7):549-59 PMID: 8756336
  51. Evaluation of RNAs present in synaptodendrosomes: dendritic, glial, and neuronal cell body contribution.
    J Neurochem. 1993 Sep;61(3):835-44 PMID: 7689643
  52. Differential subcellular localization of particular mRNAs in hippocampal neurons in culture.
    Neuron. 1990 Dec;5(6):821-30 PMID: 2148488
  53. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus.
    J Neurosci. 1982 Mar;2(3):284-91 PMID: 7062109
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-06-15
Pages
4722-33
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC1850620
Subset
IM
Grants
NCI NIH HHS · R01 CA094143 · United States
External Links
PubMed source 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