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Mikyoung Park,1*
Esther C. Penick,3*
Jeffrey G. Edwards,3
Julie A. Kauer,3
Michael D. Ehlers1,2
Abstract:
Long-term potentiation (LTP) of synaptic strength, the mostestablished cellular model of information storage in the brain,is expressed by an increase in the number of postsynaptic AMPAreceptors. However, the source of AMPA receptors mobilized duringLTP is unknown. We report that AMPA receptors are transportedfrom recycling endosomes to the plasma membrane for LTP. Stimulithat triggered LTP promoted not only AMPA receptor insertionbut also generalized recycling of cargo and membrane from endocyticcompartments. Thus, recycling endosomes supply AMPA receptorsfor LTP and provide a mechanistic link between synaptic potentiationand membrane remodeling during synapse modification.
1 Department of Neurobiology, Duke University Medical Center, Box 3209, Durham, NC 27710, USA. 2 Department of Cell Biology, Department of Pharmacology and Cancer Biology, Department of Pathology, and Neuroproteomics Laboratory; Duke University Medical Center, Box 3209, Durham, NC 27710, USA. 3 Department of Molecular Pharmacology, Physiology, and Biotechnology, Brown University, Providence, RI 02912, USA.
Enhanced Recruitment of Endosomal Na+/H+ Exchanger NHE6 into Dendritic Spines of Hippocampal Pyramidal Neurons during NMDA Receptor-Dependent Long-Term Potentiation.
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|Abstract »|Full Text »|PDF »
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PNAS
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PNAS
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Rab11 and Its Effector Rab Coupling Protein Contribute to the Trafficking of {beta}1 Integrins during Axon Growth in Adult Dorsal Root Ganglion Neurons and PC12 Cells.
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PNAS
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Actin in dendritic spines: connecting dynamics to function.
Alterations of EHD1/EHD4 Protein Levels Interfere with L1/NgCAM Endocytosis in Neurons and Disrupt Axonal Targeting.
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Aberrant Rab11-Dependent Trafficking of the Neuronal Glutamate Transporter EAAC1 Causes Oxidative Stress and Cell Death in Huntington's Disease.
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The Stress Hormone Corticosterone Increases Synaptic {alpha}-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid (AMPA) Receptors via Serum- and Glucocorticoid-inducible Kinase (SGK) Regulation of the GDI-Rab4 Complex.
Contribution of the Global Subunit Structure and Stargazin on the Maturation of AMPA Receptors.
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Potassium Channel Silencing by Constitutive Endocytosis and Intracellular Sequestration.
S. Feliciangeli, M. P. Tardy, G. Sandoz, F. C. Chatelain, R. Warth, J. Barhanin, S. Bendahhou, and F. Lesage (2010)
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SNAP-25 Is a Target of Protein Kinase C Phosphorylation Critical to NMDA Receptor Trafficking.
C. G. Lau, Y. Takayasu, A. Rodenas-Ruano, A. V. Paternain, J. Lerma, M. V. L. Bennett, and R. S. Zukin (2010)
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Plasticity between Neuronal Pairs in Layer 4 of Visual Cortex Varies with Synapse State.
Myosin-Va-interacting protein, RILPL2, controls cell shape and neuronal morphogenesis via Rac signaling.
M.-F. Lise, D. P. Srivastava, P. Arstikaitis, R. L. Lett, R. Sheta, V. Viswanathan, P. Penzes, T. P. O'Connor, and A. El-Husseini (2009)
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I. L. Arancibia-Carcamo, E. Y. Yuen, J. Muir, M. J. Lumb, G. Michels, R. S. Saliba, T. G. Smart, Z. Yan, J. T. Kittler, and S. J. Moss (2009)
PNAS
106, 17552-17557
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Spine Modifications Associated with Long-Term Potentiation.
Y. Yang and Q. Zhou (2009)
Neuroscientist
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Axonal Targeting of Trk Receptors via Transcytosis Regulates Sensitivity to Neurotrophin Responses.
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Mechanism underlying activity-dependent insertion of TrkB into the neuronal surface.
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Uncoordinated 119 Protein Controls Trafficking of Lck via the Rab11 Endosome and Is Critical for Immunological Synapse Formation.
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Regulation of Postsynaptic Structure and Function by an A-Kinase Anchoring Protein-Membrane-Associated Guanylate Kinase Scaffolding Complex.
H. R. Robertson, E. S. Gibson, T. A. Benke, and M. L. Dell'Acqua (2009)
J. Neurosci.
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Eps15 Homology Domain 1-associated Tubules Contain Phosphatidylinositol-4-Phosphate and Phosphatidylinositol-(4,5)-Bisphosphate and Are Required for Efficient Recycling.
M. Jovic, F. Kieken, N. Naslavsky, P. L. Sorgen, and S. Caplan (2009)
Mol. Biol. Cell
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Transducing Neuronal Activity into Dendritic Spine Morphology: New Roles for p38 MAP Kinase and N-cadherin.
H. Sugiura, H. Tanaka, S. Yasuda, T. Takemiya, and K. Yamagata (2009)
Neuroscientist
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X.-b. Wang, O. Bozdagi, J. S. Nikitczuk, Z. W. Zhai, Q. Zhou, and G. W. Huntley (2008)
PNAS
105, 19520-19525
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Y. Shinohara, H. Hirase, M. Watanabe, M. Itakura, M. Takahashi, and R. Shigemoto (2008)
PNAS
105, 19498-19503
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Monomeric IgG Is Neuroprotective via Enhancing Microglial Recycling Endocytosis and TNF-{alpha}.
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Janus-faced trafficking at glutamatergic synapses.
Region-Specific Changes in the Subcellular Distribution of AMPA Receptor GluR1 Subunit in the Rat Ventral Tegmental Area after Acute or Chronic Morphine Administration.
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Blood
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N. Hardel, N. Harmel, G. Zolles, B. Fakler, and N. Klocker (2008)
Cardiovasc Res
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UNC-108/Rab2 Regulates Postendocytic Trafficking in Caenorhabditis elegans.
D. K. Chun, J. M. McEwen, M. Burbea, and J. M. Kaplan (2008)
Mol. Biol. Cell
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Spine Expansion and Stabilization Associated with Long-Term Potentiation.
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Rapid Tumor Necrosis Factor {alpha}-Induced Exocytosis of Glutamate Receptor 2-Lacking AMPA Receptors to Extrasynaptic Plasma Membrane Potentiates Excitotoxicity.
D. Leonoudakis, P. Zhao, and E. C. Beattie (2008)
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The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM.
C. C. Yap, D. Wisco, P. Kujala, Z. M. Lasiecka, J. T. Cannon, M. C. Chang, H. Hirling, J. Klumperman, and B. Winckler (2008)
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Differential Trafficking of AMPA and NMDA Receptors during Long-Term Potentiation in Awake Adult Animals.
J. M. Williams, D. Guevremont, S. E. Mason-Parker, C. Luxmanan, W. P. Tate, and W. C. Abraham (2007)
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GluR1 Links Structural and Functional Plasticity at Excitatory Synapses.
C. D. Kopec, E. Real, H. W. Kessels, and R. Malinow (2007)
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PICK1 and Phosphorylation of the Glutamate Receptor 2 (GluR2) AMPA Receptor Subunit Regulates GluR2 Recycling after NMDA Receptor-Induced Internalization.
RAB-10 Regulates Glutamate Receptor Recycling in a Cholesterol-dependent Endocytosis Pathway.
D. R. Glodowski, C. C.-H. Chen, H. Schaefer, B. D. Grant, and C. Rongo (2007)
Mol. Biol. Cell
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Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation.
I. T. Bayazitov, R. J. Richardson, R. G. Fricke, and S. S. Zakharenko (2007)
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27, 11510-11521
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Real-Time Imaging of Discrete Exocytic Events Mediating Surface Delivery of AMPA Receptors.
G. A. Yudowski, M. A. Puthenveedu, D. Leonoudakis, S. Panicker, K. S. Thorn, E. C. Beattie, and M. von Zastrow (2007)
J. Neurosci.
27, 11112-11121
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CDK-5 Regulates the Abundance of GLR-1 Glutamate Receptors in the Ventral Cord of Caenorhabditis elegans.
P. Juo, T. Harbaugh, G. Garriga, and J. M. Kaplan (2007)
Mol. Biol. Cell
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Recycling Endosomes of Polarized Epithelial Cells Actively Sort Apical and Basolateral Cargos into Separate Subdomains.
A. Thompson, R. Nessler, D. Wisco, E. Anderson, B. Winckler, and D. Sheff (2007)
Mol. Biol. Cell
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EHD1 and Eps15 Interact with Phosphatidylinositols via Their Eps15 Homology Domains.
N. Naslavsky, J. Rahajeng, S. Chenavas, P. L. Sorgen, and S. Caplan (2007)
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EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration.
M. Jovic, N. Naslavsky, D. Rapaport, M. Horowitz, and S. Caplan (2007)
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Molecular determinants for the interaction between AMPA receptors and the clathrin adaptor complex AP-2.
K. Kastning, V. Kukhtina, J. T. Kittler, G. Chen, A. Pechstein, S. Enders, S. H. Lee, M. Sheng, Z. Yan, and V. Haucke (2007)
PNAS
104, 2991-2996
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Organization of {beta}-adrenoceptor signaling compartments by sympathetic innervation of cardiac myocytes.
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Biophysical Model of AMPA Receptor Trafficking and Its Regulation during Long-Term Potentiation/Long-Term Depression..