Home LiteratureArticle Details
PMID: 15084657 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Endoplasmic reticulum export site formation and function in dendrites.

Aridor M, Guzik AK, Bielli A, Fish KN

Abstract

The elongated and polarized characteristics of neurons render targeting of receptors to the plasma membrane of distal axonal projections and dendritic branches a major sorting task. Although the majority of biosynthetic cargo synthesis, transport, and sorting are believed to occur in the soma, local membrane protein translation and sorting has been reported recently to take place in dendrites and axons. We investigated where endoplasmic reticulum (ER) export occurs in dendrites using an in vitro permeabilized neuron system that enables us to specifically control the assembly of ER export sites. We show that ER export sites are assembled regularly throughout the entire dendritic tree by the regulated sequential recruitment of Sar1 and COPII (coat protein complex II). Moreover, activation of metabotropic glutamate receptors leads to the recruitment of the NMDA receptor subunit NR1 to remodeled ER export sites. We propose that regulation of receptor assembly and export from the ER in dendrites plays an important role in modulating receptor surface expression and neuronal function.

MeSH Terms
Animals COP-Coated Vesicles/metabolism Cell Membrane Permeability Cells, Cultured Dendrites/drug effects,physiology,ultrastructure Endoplasmic Reticulum/drug effects,metabolism Excitatory Amino Acid Agents/pharmacology Glycine/analogs & derivatives,pharmacology Macromolecular Substances Membrane Proteins/metabolism Monomeric GTP-Binding Proteins/genetics,metabolism Nuclear Pore Complex Proteins Protein Transport/physiology Rats Rats, Sprague-Dawley Receptors, Metabotropic Glutamate/agonists,metabolism Receptors, N-Methyl-D-Aspartate/metabolism Resorcinols/pharmacology Saccharomyces cerevisiae Proteins
Chemicals
Excitatory Amino Acid Agents Macromolecular Substances Membrane Proteins NR1 NMDA receptor Nuclear Pore Complex Proteins Receptors, Metabotropic Glutamate Receptors, N-Methyl-D-Aspartate Resorcinols SEC13 protein, S cerevisiae Saccharomyces cerevisiae Proteins 3,5-dihydroxyphenylglycine SAR1 protein, rat Monomeric GTP-Binding Proteins Glycine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Aridor Meir
Department of Cell Biology and Physiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261, USA.
Guzik Amy K
Bielli Anna
Fish Kenneth N
References (55)
55 references, click to expand
  1. Regulation of back-propagating action potentials in hippocampal neurons.
    Curr Opin Neurobiol. 1999 Jun;9(3):288-92 PMID: 10395568
  2. Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines.
    Nat Neurosci. 2000 Apr;3(4):311-3 PMID: 10725917
  3. Kinase signaling initiates coat complex II (COPII) recruitment and export from the mammalian endoplasmic reticulum.
    J Biol Chem. 2000 Nov 17;275(46):35673-6 PMID: 11001944
  4. Stimulation of glutamate receptor protein synthesis and membrane insertion within isolated neuronal dendrites.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11545-50 PMID: 11027353
  5. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly.
    J Cell Biol. 2001 Jan 8;152(1):213-29 PMID: 11149932
  6. Evidence for a satellite secretory pathway in neuronal dendritic spines.
    Curr Biol. 2001 Mar 6;11(5):351-5 PMID: 11267872
  7. Protein synthesis at synaptic sites on dendrites.
    Annu Rev Neurosci. 2001;24:299-325 PMID: 11283313
  8. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue.
    Neuron. 2001 Mar;29(3):779-96 PMID: 11301036
  9. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation.
    Neuron. 2001 Apr;30(1):227-40 PMID: 11343657
  10. Local translation of classes of mRNAs that are targeted to neuronal dendrites.
    Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7080-5 PMID: 11416191
  11. Protein synthetic machinery in the dendrites of the magnocellular neurosecretory neurons of wild-type Long-Evans and homozygous Brattleboro rats.
    J Chem Neuroanat. 2002 Mar;23(3):171-86 PMID: 11861124
  12. The protein kinase A inhibitor H89 acts on cell morphology by inhibiting Rho kinase.
    J Pharmacol Exp Ther. 2002 Mar;300(3):1000-7 PMID: 11861809
  13. Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane.
    J Neurosci. 2002 Mar 15;22(6):2215-24 PMID: 11896161
  14. Measures for quantifying dendritic arborizations.
    Network. 2002 Aug;13(3):397-414 PMID: 12222821
  15. Trafficking of NMDA receptors.
    Annu Rev Pharmacol Toxicol. 2003;43:335-58 PMID: 12540744
  16. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging.
    J Neurosci. 2003 Jul 16;23(15):6188-99 PMID: 12867502
  17. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles.
    Cell. 2003 Aug 22;114(4):497-509 PMID: 12941277
  18. Ca2+ stores in Purkinje neurons: endoplasmic reticulum subcompartments demonstrated by the heterogeneous distribution of the InsP3 receptor, Ca(2+)-ATPase, and calsequestrin.
    J Neurosci. 1992 Feb;12(2):489-505 PMID: 1311032
  19. Molecular diversity of glutamate receptors and implications for brain function.
    Science. 1992 Oct 23;258(5082):597-603 PMID: 1329206
  20. The endoplasmic reticulum of Purkinje neuron body and dendrites: molecular identity and specializations for Ca2+ transport.
    Neuroscience. 1992 Jul;49(2):467-77 PMID: 1331857
  21. 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
  22. Morphological analysis of protein transport from the ER to Golgi membranes in digitonin-permeabilized cells: role of the P58 containing compartment.
    J Cell Biol. 1992 Dec;119(5):1097-116 PMID: 1447290
  23. Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors.
    Neuron. 2003 Oct 30;40(3):581-94 PMID: 14642281
  24. 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
  25. Distribution of the intermediate elements operating in ER to Golgi transport.
    J Cell Sci. 1991 Nov;100 ( Pt 3):415-30 PMID: 1808196
  26. Physiological learning theory.
    J Abnorm Child Psychol. 1976;4(4):309-14 PMID: 187637
  27. Heterogeneous distribution of the cAMP receptor protein RII in the nervous system: evidence for its intracellular accumulation on microtubules, microtubule-organizing centers, and in the area of the Golgi complex.
    J Cell Biol. 1986 Jul;103(1):189-203 PMID: 3522603
  28. Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability.
    J Neurophysiol. 1995 Jul;74(1):122-9 PMID: 7472317
  29. Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport.
    J Cell Biol. 1995 Nov;131(4):875-93 PMID: 7490291
  30. Evaluation of RNAs present in synaptodendrosomes: dendritic, glial, and neuronal cell body contribution.
    J Neurochem. 1993 Sep;61(3):835-44 PMID: 7689643
  31. Differential subcellular mRNA targeting: deletion of a single nucleotide prevents the transport to axons but not to dendrites of rat hypothalamic magnocellular neurons.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4377-81 PMID: 7753814
  32. Targeting of mRNAs to subsynaptic microdomains in dendrites.
    Curr Opin Neurobiol. 1995 Feb;5(1):55-61 PMID: 7773006
  33. Dendrites as compartments for macromolecular synthesis.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10766-8 PMID: 7971959
  34. 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
  35. Polarized distribution of the trans-Golgi network marker TGN38 during the in vitro development of neocortical neurons: effects of nocodazole and brefeldin A.
    Eur J Neurosci. 1994 Sep 1;6(9):1453-65 PMID: 8000569
  36. 3,5-dihydroxyphenylglycine is a highly selective agonist for phosphoinositide-linked metabotropic glutamate receptors in the rat hippocampus.
    J Neurochem. 1994 Aug;63(2):769-72 PMID: 8035201
  37. Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments.
    J Cell Biol. 1994 Apr;125(1):51-65 PMID: 8138575
  38. Three-dimensional visualization of the smooth endoplasmic reticulum in Purkinje cell dendrites.
    J Neurosci. 1993 Nov;13(11):4636-46 PMID: 8229189
  39. Differential inhibition of multiple vesicular transport steps between the endoplasmic reticulum and trans Golgi network.
    J Biol Chem. 1993 Feb 25;268(6):4216-26 PMID: 8382697
  40. The organization of the endoplasmic reticulum and the intermediate compartment in cultured rat hippocampal neurons.
    Mol Biol Cell. 1995 Oct;6(10):1315-32 PMID: 8573789
  41. Expression and purification of mammalian Sarl.
    Methods Enzymol. 1995;257:49-53 PMID: 8583938
  42. Protein synthesis within dendrites: glycosylation of newly synthesized proteins in dendrites of hippocampal neurons in culture.
    J Neurosci. 1996 Oct 1;16(19):5967-78 PMID: 8815879
  43. Active properties of neuronal dendrites.
    Annu Rev Neurosci. 1996;19:165-86 PMID: 8833440
  44. The organization of endoplasmic reticulum export complexes.
    J Cell Biol. 1996 Oct;135(1):19-35 PMID: 8858160
  45. COPII vesicles derived from mammalian endoplasmic reticulum microsomes recruit COPI.
    J Cell Biol. 1996 Nov;135(4):895-911 PMID: 8922375
  46. Translational machinery in dendrites of hippocampal neurons in culture.
    J Neurosci. 1996 Nov 15;16(22):7171-81 PMID: 8929426
  47. A regulatory role for cAMP-dependent protein kinase in protein traffic along the exocytic route.
    J Biol Chem. 1996 Nov 29;271(48):30935-41 PMID: 8940080
  48. mRNA localization in neurons: a multipurpose mechanism?
    Neuron. 1997 Jan;18(1):9-12 PMID: 9010200
  49. Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells.
    Science. 1997 Oct 17;278(5337):463-7 PMID: 9334305
  50. Protein kinase A activity is required for the budding of constitutive transport vesicles from the trans-Golgi network.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14461-6 PMID: 9405635
  51. Presence and phosphorylation of transcription factors in developing dendrites.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2313-8 PMID: 9482882
  52. Cargo selection by the COPII budding machinery during export from the ER.
    J Cell Biol. 1998 Apr 6;141(1):61-70 PMID: 9531548
  53. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes.
    Cell. 1998 Jul 10;94(1):131-41 PMID: 9674434
  54. Dendritic and postsynaptic protein synthetic machinery.
    J Neurosci. 1999 Jan 1;19(1):168-79 PMID: 9870948
  55. Cargo can modulate COPII vesicle formation from the endoplasmic reticulum.
    J Biol Chem. 1999 Feb 12;274(7):4389-99 PMID: 9933643
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2004-04-14
Pages
3770-6
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6729346
Subset
IM
Grants
NIMH NIH HHS · MH064372 · United States
NIDDK NIH HHS · R01 DK062318 · United States
NIMH NIH HHS · K01 MH064372-02 · United States
NIMH NIH HHS · K01 MH064372-01 · United States
NIMH NIH HHS · K01 MH064372-03 · United States
NIMH NIH HHS · K01 MH064372-05 · United States
NIMH NIH HHS · K01 MH064372 · United States
NIMH NIH HHS · K01 MH064372-04 · United States
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: [email protected]