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PMID: 17145503 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes.

Neuron ·Vol. 52 ·No. 5 ·2006-12-07 ·Pages 817-30

Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, Ehlers MD

Abstract

Dendritic spines are micron-sized membrane protrusions receiving most excitatory synaptic inputs in the mammalian brain. Spines form and grow during long-term potentiation (LTP) of synaptic strength. However, the source of membrane for spine formation and enlargement is unknown. Here we report that membrane trafficking from recycling endosomes is required for the growth and maintenance of spines. Using live-cell imaging and serial section electron microscopy, we demonstrate that LTP-inducing stimuli promote the mobilization of recycling endosomes and vesicles into spines. Preventing recycling endosomal transport abolishes LTP-induced spine formation. Using a pH-sensitive recycling cargo, we show that exocytosis from recycling endosomes occurs locally in spines, is triggered by activation of synaptic NMDA receptors, and occurs concurrently with spine enlargement. Thus, recycling endosomes provide membrane for activity-dependent spine growth and remodeling, defining a novel membrane trafficking mechanism for spine morphological plasticity and providing a mechanistic link between structural and functional plasticity during LTP.

MeSH Terms
Animals Biological Transport, Active/physiology Cell Size DNA/biosynthesis,genetics Dendritic Spines/physiology,ultrastructure Electrophysiology Endosomes/physiology,ultrastructure Exocytosis/physiology Hippocampus/cytology,growth & development Image Processing, Computer-Assisted Immunohistochemistry Long-Term Potentiation/physiology Microscopy, Electron Microscopy, Electron, Transmission Neuronal Plasticity/physiology Rats Receptors, N-Methyl-D-Aspartate/physiology
Chemicals
Receptors, N-Methyl-D-Aspartate DNA
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Park Mikyoung
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710, USA.
Salgado Jennifer M
Ostroff Linnaea
Helton Thomas D
Robinson Camenzind G
Harris Kristen M
Ehlers Michael D
References (48)
48 references, click to expand
  1. Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting.
    Neuron. 2000 Nov;28(2):511-25 PMID: 11144360
  2. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons.
    Neuron. 2001 Jan;29(1):243-54 PMID: 11182095
  3. Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex.
    Curr Biol. 2001 May 15;11(10):735-46 PMID: 11378383
  4. Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells.
    Nat Cell Biol. 2001 Jun;3(6):567-72 PMID: 11389441
  5. Remodeling of synaptic membranes after induction of long-term potentiation.
    J Neurosci. 2001 Aug 15;21(16):6245-51 PMID: 11487647
  6. Cell cycle regulation of myosin-V by calcium/calmodulin-dependent protein kinase II.
    Science. 2001 Aug 17;293(5533):1317-20 PMID: 11509731
  7. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons.
    Nat Neurosci. 2001 Nov;4(11):1086-92 PMID: 11687814
  8. Dendritic spines: structure, dynamics and regulation.
    Nat Rev Neurosci. 2001 Dec;2(12):880-8 PMID: 11733795
  9. 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
  10. Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD.
    J Cell Biol. 2002 Jun 24;157(7):1197-209 PMID: 12070131
  11. Dynamics of tubulovesicular recycling endosomes in hippocampal neurons.
    J Neurosci. 1999 Dec 1;19(23):10324-37 PMID: 10575030
  12. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite.
    Nature. 1999 Nov 25;402(6760):421-5 PMID: 10586883
  13. Role of AMPA receptor cycling in synaptic transmission and plasticity.
    Neuron. 1999 Nov;24(3):649-58 PMID: 10595516
  14. 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
  15. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines.
    Neuron. 2002 Oct 24;36(3):435-49 PMID: 12408846
  16. Long-term dendritic spine stability in the adult cortex.
    Nature. 2002 Dec 19-26;420(6917):812-6 PMID: 12490949
  17. Ras pathway signaling on endomembranes.
    Curr Opin Cell Biol. 2003 Apr;15(2):136-42 PMID: 12648668
  18. Hrs regulates early endosome fusion by inhibiting formation of an endosomal SNARE complex.
    J Cell Biol. 2003 Jul 7;162(1):125-37 PMID: 12847087
  19. Divergent functions of neuronal Rab11b in Ca2+-regulated versus constitutive exocytosis.
    J Neurosci. 2003 Nov 19;23(33):10531-9 PMID: 14627637
  20. Structural basis of long-term potentiation in single dendritic spines.
    Nature. 2004 Jun 17;429(6993):761-6 PMID: 15190253
  21. Lateral organization of endocytic machinery in dendritic spines.
    Nat Neurosci. 2004 Sep;7(9):917-8 PMID: 15322548
  22. Recycling endosomes supply AMPA receptors for LTP.
    Science. 2004 Sep 24;305(5692):1972-5 PMID: 15448273
  23. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity.
    Nat Neurosci. 2004 Oct;7(10):1104-12 PMID: 15361876
  24. Quantal analysis and synaptic anatomy--integrating two views of hippocampal plasticity.
    Trends Neurosci. 1993 Apr;16(4):141-7 PMID: 7682347
  25. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella.
    J Cell Biol. 1994 Jun;125(6):1265-74 PMID: 7515888
  26. Rab11 regulates recycling through the pericentriolar recycling endosome.
    J Cell Biol. 1996 Nov;135(4):913-24 PMID: 8922376
  27. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat.
    J Neurosci. 1997 Jan 1;17(1):190-203 PMID: 8987748
  28. Postsynaptic membrane fusion and long-term potentiation.
    Science. 1998 Jan 16;279(5349):399-403 PMID: 9430593
  29. Rapid actin-based plasticity in dendritic spines.
    Neuron. 1998 May;20(5):847-54 PMID: 9620690
  30. Calcium-evoked dendritic exocytosis in cultured hippocampal neurons. Part I: trans-Golgi network-derived organelles undergo regulated exocytosis.
    J Neurosci. 1998 Sep 1;18(17):6803-13 PMID: 9712651
  31. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity.
    Science. 1999 Mar 19;283(5409):1923-7 PMID: 10082466
  32. Dendritic spine changes associated with hippocampal long-term synaptic plasticity.
    Nature. 1999 May 6;399(6731):66-70 PMID: 10331391
  33. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation.
    Science. 1999 Jun 11;284(5421):1811-6 PMID: 10364548
  34. Long-term potentiation--a decade of progress?
    Science. 1999 Sep 17;285(5435):1870-4 PMID: 10489359
  35. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation.
    Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16665-70 PMID: 15542587
  36. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses.
    Cell. 2004 Dec 17;119(6):873-87 PMID: 15607982
  37. NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD.
    Neuron. 2005 Jan 6;45(1):81-94 PMID: 15629704
  38. A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis.
    J Cell Biol. 2005 Jan 17;168(2):329-38 PMID: 15657400
  39. Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move!
    Trends Neurosci. 2005 Mar;28(3):133-9 PMID: 15749166
  40. Neurabin/protein phosphatase-1 complex regulates dendritic spine morphogenesis and maturation.
    Mol Biol Cell. 2005 May;16(5):2349-62 PMID: 15743906
  41. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells.
    Cell. 2005 May 20;121(4):593-606 PMID: 15907472
  42. Integration of biochemical signalling in spines.
    Nat Rev Neurosci. 2005 Jun;6(6):423-34 PMID: 15928715
  43. Essential role for the PKC target MARCKS in maintaining dendritic spine morphology.
    Neuron. 2005 Oct 6;48(1):77-90 PMID: 16202710
  44. Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane.
    Dev Cell. 2005 Sep;9(3):365-76 PMID: 16224820
  45. Retrograde signaling by Syt 4 induces presynaptic release and synapse-specific growth.
    Science. 2005 Nov 4;310(5749):858-63 PMID: 16272123
  46. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis.
    Neuron. 2005 Dec 8;48(5):757-71 PMID: 16337914
  47. A critical role for myosin IIb in dendritic spine morphology and synaptic function.
    Neuron. 2006 Jan 19;49(2):175-82 PMID: 16423692
  48. Molecular mechanisms of dendritic spine morphogenesis.
    Curr Opin Neurobiol. 2006 Feb;16(1):95-101 PMID: 16361095
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
0896-6273
DOI
10.1016/j.neuron.2006.09.040
Published
2006-12-07
Pages
817-30
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC1899130
Subset
IM
Grants
NINDS NIH HHS · R01 NS047574-01A2 · United States
NINDS NIH HHS · NS33574 · United States
NIA NIH HHS · R01 AG024492-01 · United States
NIBIB NIH HHS · EB002170 · United States
NIA NIH HHS · R01 AG024492 · United States
NINDS NIH HHS · R01 NS047574 · United States
NINDS NIH HHS · NS21184 · United States
NIMH NIH HHS · R01 MH064748-03 · United States
NIA NIH HHS · R01 AG024492-03 · United States
NIBIB NIH HHS · R01 EB002170 · United States
NIMH NIH HHS · R01 MH064748 · United States
NIA NIH HHS · R01 AG024492-02 · United States
NIMH NIH HHS · R01 MH064748-02 · United States
NIMH NIH HHS · R01 MH064748-04 · United States
NIA NIH HHS · AG024492 · United States
NINDS NIH HHS · R01 NS021184 · United States
NIMH NIH HHS · MH064748 · United States
NINDS NIH HHS · R01 NS033574 · United States
NINDS NIH HHS · R37 NS021184 · United States
NIMH NIH HHS · R01 MH064748-01 · United States
NIMH NIH HHS · R01 MH064748-05 · United States
Corrections
CommentIn
PMID: 17145496
External Links
PubMed source DOI: 10.1016/j.neuron.2006.09.040 PMC Full Text View journal details
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