CoChat
Sign Up
Cited by 37Neuroscience and Neuropharmacology ResearchCellular transport and secretionMemory and Neural Mechanisms

Mechanisms and Role of Dendritic Membrane Trafficking for Long-Term Potentiation

Open access
Hiester, Brian G., Becker, Matthew I., Bowen, Aaron B., Schwartz, Samantha L., Kennedy, Matthew J.·2018·Frontiers in Cellular Neuroscience
DOI 10.3389/fncel.2018.00391PMC PMC6218485
Open this paper in CoChat — free accountOpen PDF

Abstract

Long-term potentiation (LTP) of excitatory synapses is a major form of plasticity for learning and memory in the central nervous system. While the molecular mechanisms of LTP have been debated for decades, there is consensus that LTP induction activates membrane trafficking pathways within dendrites that are essential for synapse growth and strengthening. Current models suggest that key molecules for synaptic potentiation are sequestered within intracellular organelles, which are mobilized by synaptic activity to fuse with the plasma membrane following LTP induction. While the identity of the factors mobilized to the plasma membrane during LTP remain obscure, the field has narrowly focused on AMPA-type glutamate receptors. Here, we review recent literature and present new experimental data from our lab investigating whether AMPA receptors trafficked from intracellular organelles directly contribute to synaptic strengthening during LTP. We propose a modified model where membrane trafficking delivers distinct factors that are required to maintain synapse growth and AMPA receptor incorporation following LTP. Finally, we pose several fundamental questions that may guide further inquiry into the role of membrane trafficking for synaptic plasticity.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fncel.2018.00391

Cites

24 of 24 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • LTP expression is due to rapid postsynaptic accumulation of AMPARs.

    “Thus, it is now generally accepted that LTP expression is due to the rapid postsynaptic accumulation of AMPARs.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [237]

  • Many synaptic proteins are remarkably dynamic, including AMPARs, NMDARs, CaMKII, and scaffolding proteins such as PSD-95.

    “These studies show that many synaptic proteins are remarkably dynamic, including AMPARs (237, 249, 327, 328), NMDARs (329), CaMKII (330), and scaffolding proteins, such as PSD-95 (331).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [237]

    Citation 331 is attached to PSD-95, so the question is whether this source describes that scaffolding protein as dynamic. The Introduction section on lateral diffusion identifies PSD-95 as an anchor for mobile AMPA receptors, but does not describe PSD-95 itself as mobile or dynamically exchanged. Searches for PSD-95 mobility, turnover, and trafficking found no passage establishing that point. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 124

  1. Aoto J. Martinelli D. C. Malenka R. C. Tabuchi K. Su T. C. (2013). Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking. Cell 154, 75– 88. 10.1016/j.cell.2013.05.060 23827676 PMC3756801 · DOI
  2. Arendt K. L. Zhang Y. Jurado S. Malenka R. C. Südhof T. C. Chen L. (2015). Retinoic acid and LTP recruit postsynaptic AMPA receptors using distinct SNARE-dependent mechanisms. Neuron 86, 442– 456. 10.1016/j.neuron.2015.03.009 25843403 PMC4578641 · DOI
  3. Banke T. G. Bowie D. Lee H. Huganir R. L. Schousboe A. Traynelis S. F. (2000). Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J. Neurosci. 20, 89– 102. 10.1523/JNEUROSCI.20-01-00089.2000 10627585 PMC6774102 · DOI · Paper page
  4. Barcomb K. Goodell D. J. Arnold D. B. Bayer U. (2015). Live imaging of endogenous Ca2+/calmodulin-dependent protein kinase II in neurons reveals that ischemia-related aggregation does not require kinase activity. J. Neurochem. 135, 666– 673. 10.1111/jnc.13263 26212614 PMC4636925 · DOI
  5. Barria A. Muller D. Derkach V. Griffith L. C. Soderling T. R. (1997). Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276, 2042– 2046. 10.1126/science.276.5321.2042 9197267 · DOI · Paper page
  6. Bats C. Groc L. Choquet D. (2007). Article the interaction between stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53, 719– 734. 10.1016/j.neuron.2007.01.030 17329211 · DOI · Paper page
  7. Beaudoin G. M. J. Lee S. H. Singh D. Yuan Y. Ng Y. G. Reichardt L. F.. (2012). Culturing pyramidal neurons from the early postnatal mouse hippocampus and cortex. Nat. Protoc. 7, 1741– 1754. 10.1038/nprot.2012.099 22936216 · DOI
  8. Benke T. Traynelis S. F. (2018). AMPA-type glutamate receptor conductance changes and plasticity: still a lot of noise. Neurochem. Res. [Epub ahead of print]. 10.1007/s11064-018-2491-1 29476449 PMC6533624 · DOI
  9. Benke T. A. Luthi A. Isaac J. T. R. Collingridge G. L. (1998). Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393, 793– 797. 10.1038/31709 9655394 · DOI · Paper page
  10. Bhouri M. Morishita W. Temkin P. Goswami D. Kawabe H. Brose N.. (2018). Deletion of LRRTM1 and LRRTM2 in adult mice impairs basal AMPA receptor transmission and LTP in hippocampal CA1 pyramidal neurons. Proc. Natl. Acad. Sci. U.S.A. 115, E5382– E5389. 10.1073/pnas.1803280115 29784826 PMC6003336 · DOI
  11. Biederer T. Kaeser P. S. Blanpied T. A. (2017). Review transcellular nanoalignment of synaptic function. Neuron 96, 680– 696. 10.1016/j.neuron.2017.10.006 29096080 PMC5777221 · DOI · Paper page
  12. Bin N. Ma K. Harada H. Tien C.-W. Bergin F. Sugita K. (2018). Crucial role of postsynaptic syntaxin 4 in mediating basal neurotransmission and synaptic plasticity in article crucial role of postsynaptic syntaxin 4 in mediating basal neurotransmission and synaptic plasticity in hippocampal CA1 neurons. Cell Rep. 23, 2955– 2966. 10.1016/j.celrep.2018.05.026 29874582 · DOI · Paper page
  13. Bliss T. V. P. Collingridge G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31– 39. 10.1038/361031a0 8421494 · DOI · Paper page
  14. Bourke A. M. Bowen A. B. Kennedy M. J. (2018). New approaches for solving old problems in neuronal protein trafficking. Mol. Cell. Neurosci. 91, 48– 66. 10.1016/j.mcn.2018.04.004 29649542 PMC6128763 · DOI
  15. Bowen A. B. Bourke A. M. Hiester B. G. Hanus C. Kennedy M. J. (2017). Golgi-independent secretory trafficking through recycling endosomes in neuronal dendrites and spines. Elife 6: e27362. 10.7554/eLife.27362 28875935 PMC5624785 · DOI
  16. Bozdagi O. Nagy V. Kwei K. T. Huntley G. W. (2007). In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J. Neurophysiol. 98, 334– 344. 10.1152/jn.00202.2007 17493927 PMC4415272 · DOI · Paper page
  17. Bozdagi O. Shan W. Tanaka H. Benson D. L. Huntley G. W. (2000). Increasing numbers of synaptic puncta during late- phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28, 245– 259. 10.1016/S0896-6273(00)00100-8 11086998 · DOI
  18. Brigidi G. S. Santyr B. Shimell J. Jovellar B. Bamji S. X. (2015). Activity-regulated trafficking of the palmitoyl-acyl transferase DHHC5. Nat. Commun. 6: 8200. 10.1038/ncomms9200 26334723 PMC4569850 · DOI
  19. Brigidi G. S. Sun Y. Beccano-Kelly D. Pitman K. Mobasser M. Borgland S. L.. (2014). Palmitoylation of δ-catenin by DHHC5 mediates activity-induced synapse plasticity. Nat. Neurosci. 17, 522– 532. 10.1038/nn.3657 24562000 PMC5025286 · DOI
  20. Broutman G. Baudry M. (2001). Involvement of the secretory pathway for AMPA receptors in NMDA-induced potentiation in hippocampus. J. Neurosci. 21, 27– 34. 10.1523/JNEUROSCI.21-01-00027.2001 11150316 PMC6762437 · DOI
  21. Brown T. C. Correia S. S. Petrok C. N. Esteban J. A. (2007). Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J. Neurosci. 27, 13311– 13315. 10.1523/JNEUROSCI.4258-07.2007 18045925 PMC6673392 · DOI
  22. Chenaux G. Matt L. Hill T. C. Kaur I. Liu X. Kirk L. M. (2016). Loss of SynDIG1 reduces excitatory synapse maturation but not formation in vivo. ENeuro 3, 1– 17. 10.1523/ENEURO.0130-16.2016 PMC5073248 27800545 · DOI
  23. Cooney J. R. Hurlburt J. L. Selig D. K. Harris K. M. Fiala J. C. (2002). Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J. Neurosci. 22, 2215– 2224. 10.1523/JNEUROSCI.22-06-02215.2002 11896161 PMC6758269 · DOI · Paper page
  24. Derkach V. Barria A. Soderling T. R. (1999). Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc. Natl. Acad. Sci. U.S.A. 96, 3269– 3274. 10.1073/pnas.96.6.3269 10077673 PMC15931 · DOI · Paper page
  25. de Wit J. Sylwestrak E. O'Sullivan M. L. Otto S. Tiglio K. Savas J. N.. (2009). LRRTM2 interacts with neurexin1 and regulates excitatory synapse formation. Neuron 64, 799– 806. 10.1016/j.neuron.2009.12.019 20064388 PMC2829666 · DOI
  26. Diaz-Vera J. Palmer S. Hernandez-Fernaud J. R. Dornier E. Mitchell L. E. Macpherson I.. (2017). A proteomic approach to identify endosomal cargoes controlling cancer invasiveness. J. Cell Sci. 130, 697– 711. 10.1242/jcs.190835 28062852 PMC5339883 · DOI
  27. Ehlers M. D. (2000). Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28, 511– 525. 10.1016/S0896-6273(00)00129-X 11144360 · DOI · Paper page
  28. Ehlers M. D. Heine M. Groc L. Lee M. Choquet D. (2007). Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54, 447– 460. 10.1016/j.neuron.2007.04.010 17481397 PMC1993808 · DOI · Paper page
  29. Ehrlich I. Klein M. Rumpel S. Malinow R. (2007). PSD-95 is required for activity-driven synapse stabilization. Proc. Natl. Acad. Sci. U.S.A. 104, 4176– 4181. 10.1073/pnas.0609307104 17360496 PMC1820728 · DOI · Paper page
  30. Esteves da Silva M. Adrian M. Schätzle P. Lipka J. Watanabe T. Cho S.. (2015). Positioning of AMPA receptor-containing endosomes regulates synapse architecture. Cell Rep. 13, 933– 943. 10.1016/j.celrep.2015.09.062 26565907 · DOI
  31. Fossati M. Pizzarelli R. Schmidt E. R. Kupferman J. V. Stroebel D. Polleux F.. (2016). Regulate the development of excitatory and inhibitory synapses SRGAP2 and its human-specific paralog co-regulate the development of excitatory and inhibitory synapses. Neuron 91, 356– 369. 10.1016/j.neuron.2016.06.013 27373832 PMC5385270 · DOI · Paper page
  32. Garcia-Nafria J. Herguedas B. Watson J. F. Greger I. H. (2016). The dynamic AMPA receptor extracellular region: a platform for synaptic protein interactions. J. Physiol. 19, 5449– 5458. 10.1113/JP271844 PMC5043031 26891027 · DOI
  33. Gerges N. Z. Backos D. S. Rupasinghe C. N. Spaller M. R. Esteban J. A. (2006). Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane. EMBO J. 25, 1623– 1634. 10.1038/sj.emboj.7601065 16601687 PMC1440842 · DOI · Paper page
  34. Goo M. S. Sancho L. Slepak N. Boassa D. Deerinck T. J. Ellisman M. H.. (2017). Activity-dependent trafficking of lysosomes in dendrites and dendritic spines. J. Neurosci. 216, 2499– 2513. 10.1083/jcb.201704068 28630145 PMC5551717 · DOI · Paper page
  35. Granger A. J. Shi Y. Lu W. Cerpas M. Nicoll R. A. (2013). LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature 493, 495– 500. 10.1038/nature11775 23235828 PMC3998843 · DOI · Paper page
  36. Groc L. Heine M. Cognet L. Brickley K. Stephenson F. A. Lounis B.. (2004). Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat. Neurosci. 7, 695– 696. 10.1038/nn1270 15208630 · DOI
  37. Gross G. G. Junge J. A. Mora R. J. Kwon H. Olson C. A. Takahashi T. T.. (2013). Recombinant probes for visualizing endogenous synaptic proteins in living neurons. Neuron 78, 971– 985. 10.1016/j.neuron.2013.04.017 23791193 PMC3779638 · DOI
  38. Gross G. G. Straub C. Perez-sanchez J. Dempsey W. P. Junge J. A. Roberts R. W.. (2016). An E3-ligase-based method for ablating inhibitory synapses. Nat. Methods 13, 673– 678. 10.1038/nmeth.3894 27271196 PMC5312699 · DOI
  39. Hanus C. Kochen L. Tom Dieck S. Racine V. Sibarita J. B. Schuman E. M.. (2014). Synaptic control of secretory trafficking in dendrites. Cell Rep. 7, 1771– 1778. 10.1016/j.celrep.2014.05.028 24931613 PMC5321479 · DOI
  40. Hara Y. Fukaya M. Hayashi K. Kawauchi T. Nakajima K. Sakagami H. (2016). ADP ribosylation factor 6 regulates neuronal migration in the developing cerebral cortex through FIP3/arfophilin-1-dependent endosomal trafficking of N-cadherin. ENeuro 3: ENEURO.0148– 16.2016. 10.1523/ENEURO.0148-16.2016 27622210 PMC5002984 · DOI
  41. Harward S. C. Hedrick N. G. Hall C. E. Parra-Bueno P. Milner T. A. Pan E.. (2016). Autocrine BDNF-TrkB signalling within a single dendritic spine. Nature 538, 99– 103. 10.1038/nature19766 27680698 PMC5398094 · DOI · Paper page
  42. Hashimoto K. Fukaya M. Qiao X. Sakimura K. Watanabe M. Kano M. (1999). Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J. Neurosci. 19, 6027– 6036. 10.1523/JNEUROSCI.19-14-06027.1999 10407040 PMC6783074 · DOI
  43. Hayashi Y. Shi S.-H. Esteban J. A. Piccini A. Poncer J.-C. Malinow R. (2000). Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262– 2268. 10.1126/science.287.5461.2262 10731148 · DOI · Paper page
  44. Heine M. Groc L. Frischknecht R. Beique J. C. Lounis B. Rumbaugh G.. (2008a). Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320, 201– 205. 10.1126/science.1152089 18403705 PMC2715948 · DOI · Paper page
  45. Heine M. Thoumine O. Mondin M. Tessier B. Giannone G. Choquet D. (2008b). Activity-independent and subunit-specific recruitment of functional AMPA receptors at neurexin/neuroligin contacts. Proc. Natl. Acad. Sci. U.S.A. 105, 20947– 20952. 10.1073/pnas.0804007106 19098102 PMC2634880 · DOI
  46. Heisler F. F. Lee H. K. Gromova K. V. Pechmann Y. Schurek B. Ruschkies L.. (2014). GRIP1 interlinks N-cadherin and AMPA receptors at vesicles to promote combined cargo transport into dendrites. Proc. Natl. Acad. Sci. U.S.A. 111, 5030– 5035. 10.1073/pnas.1304301111 24639525 PMC3977296 · DOI
  47. Heynen A. J. Quinlan E. M. Bae D. C. Bear M. F. (2000). Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron 28, 527– 536. 10.1016/S0896-6273(00)00130-6 11144361 · DOI
  48. Hiester B. G. Bourke A. M. Sinnen B. L. Cook S. G. Gibson E. S. Smith K. R.. (2017). L-Type voltage-gated Ca2+channels regulate synaptic-activity-triggered recycling endosome fusion in neuronal dendrites. Cell Rep. 21, 2134– 2146. 10.1016/j.celrep.2017.10.105 29166605 PMC6466620 · DOI
  49. Hruska M. Henderson N. Marchand S. J. Le J. H. Dalva M. B. (2018). Synaptic nanomodules underlie the organization and plasticity of spine synapses. Nat. Neurosci. 21, 671– 682. 10.1038/s41593-018-0138-9 29686261 PMC5920789 · DOI · Paper page
  50. Huang Z. Shimazu K. Woo N. H. Zang K. Mu U. Lu B.. (2006). Distinct roles of the beta-1-class integrins at the developing and the mature hippocampal excitatory synapse. J. Neurosci. 26, 11208– 11219. 10.1523/JNEUROSCI.3526-06.2006 17065460 PMC2693048 · DOI
  51. Isaac J. T. R. Nicoll R. A. Malenka R. C. (1995). Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427– 434. 10.1016/0896-6273(95)90046-2 7646894 · DOI · Paper page
  52. Jaafari N. Henley J. M. Hanley J. G. (2012). PICK1 mediates transient synaptic expression of GluA2- lacking AMPA receptors during glycine-induced AMPA receptor trafficking. J. Neurosci. 32, 11618– 11630. 10.1523/JNEUROSCI.5068-11.2012 22915106 PMC6703756 · DOI · Paper page
  53. Jaafari N. Konopacki F. A. Owen T. F. Kantamneni S. Rubin P. Craig T. J.. (2013). SUMOylation is required for glycine-induced increases in AMPA receptor surface expression (ChemLTP) in hippocampal neurons. PLoS ONE 8: e52345. 10.1371/journal.pone.0052345 23326329 PMC3543417 · DOI
  54. Jackson A. C. Nicoll R. A. (2011). The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70, 178– 199. 10.1016/j.neuron.2011.04.007 21521608 PMC3119519 · DOI · Paper page
  55. Jang S. Oh D. Lee Y. Hosy E. Shin H. Van Riesen C.. (2016). Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity. Nat. Neurosci. 19, 84– 93. 10.1038/nn.4176 26595655 PMC5010778 · DOI
  56. Jurado S. Goswami D. Zhang Y. Molina A. J. M. Südhof T. C. Malenka R. C. (2013). LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 77, 542– 558. 10.1016/j.neuron.2012.11.029 23395379 PMC3569727 · DOI · Paper page
  57. Kalashnikova E. Lorca R. A. Kaur I. Barisone G. A. Li B. Ishimaru T.. (2010). SynDIG1: an activity-regulated, AMPA- receptor-interacting transmembrane protein that regulates excitatory synapse development. Neuron 65, 80– 93. 10.1016/j.neuron.2009.12.021 20152115 PMC2822728 · DOI
  58. Kannan M. Gross G. G. Arnold X. D. B. Higley M. J. (2016). Visual deprivation during the critical period enhances layer 2/3 GABAergic inhibition in mouse V1. J. Neurosci. 36, 5914– 5919. 10.1523/JNEUROSCI.0051-16.2016 27251614 PMC4887562 · DOI
  59. Kawauchi T. Sekine K. Shikanai M. Chihama K. Tomita K. Kubo K. (2010). Article Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67, 588– 602. 10.1016/j.neuron.2010.07.007 20797536 · DOI
  60. Kennedy M. J. Davison I. G. Robinson C. G. Ehlers M. D. (2010). Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141, 524– 535. 10.1016/j.cell.2010.02.042 20434989 PMC2874581 · DOI · Paper page
  61. Kopec C. D. Li B. Wei W. Boehm J. Malinow R. (2006). Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 26, 2000– 2009. 10.1523/JNEUROSCI.3918-05.2006 16481433 PMC6674938 · DOI · Paper page
  62. Kopec C. D. Real E. Kessels H. W. Malinow R. (2007). GluR1 links structural and functional plasticity at excitatory synapses. J. Neurosci. 27, 13706– 13718. 10.1523/JNEUROSCI.3503-07.2007 18077682 PMC6673607 · DOI
  63. Liao D. Hessler N. Malinow R. (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400– 404. 10.1038/375400a0 7760933 · DOI · Paper page
  64. Lin D. Makino Y. Sharma K. Hayashi T. Neve R. Takamiya K.. (2009). Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat. Neurosci. 12, 879– 887. 10.1038/nn.2351 19503082 PMC2712131 · DOI · Paper page
  65. Lin L. Lo L. H-Y. Lyu Q. Lai K.-O. (2017). Determination of dendritic spine morphology by the striatin scaffold protein STRN4 through interaction with the phosphatase PP2A. J. Biol. Chem. 292, 9451– 9464. 10.1074/jbc.M116.772442 28442576 PMC5465475 · DOI
  66. Lledo P. M. Zhang X. Südhof T. C. Malenka R. C. Nicoll R. A. (1998). Postsynaptic membrane fusion and long-term potentiation. Science 279, 399– 403. 10.1126/science.279.5349.399 9430593 · DOI · Paper page
  67. Lu W. Man H. Ju W. Trimble W. S. MacDonald J. F. Wang Y. T. (2001). Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243– 254. 10.1016/S0896-6273(01)00194-5 11182095 · DOI
  68. Lu W. Shi Y. Jackson A. C. Bjorgan K. During M. J. Sprengel R.. (2009). Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62, 254– 268. 10.1016/j.neuron.2009.02.027 19409270 PMC3632349 · DOI · Paper page
  69. MacGillavry H. D. Song Y. Raghavachari S. Blanpied T. A. (2013). Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors. Neuron 78, 615– 622. 10.1016/j.neuron.2013.03.009 23719161 PMC3668352 · DOI · Paper page
  70. Malenka R. C. Nicoll R. A. (1999). Long-term potentiation—a decade of progress? Science 285, 1870– 1875. 10.1126/science.285.5435.1870 10489359 · DOI · Paper page
  71. Maletic-Savatic M. Malinow R. (1998). Calcium-evoked dendritic exocytosis in cultured hippocampal neurons. Part I: Trans-Golgi Network-derived organelles undergo regulated exocytosis. J. Neurosci. 18, 6803– 6813. 10.1523/JNEUROSCI.18-17-06803.1998 9712651 PMC6792980 · DOI
  72. Matt L. Kirk L. M. Chenaux G. Crawley J. N. Hell J. W. D.i E. (2018). SynDIG4/Prrt1 is required for excitatory synapse development and plasticity underlying cognitive function. Cell Rep. 22, 2246– 2253. 10.1016/j.celrep.2018.02.026 29490264 PMC5856126 · DOI
  73. Maxfield F. R. McGraw T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121– 132. 10.1038/nrm1315 15040445 · DOI
  74. Mcleod F. Bossio A. Marzo A. Ciani L. Sibilla S. Hannan S.. (2018). Wnt signaling mediates LTP-dependent spine plasticity and AMPAR localization through frizzled-7 receptors. Cell Rep. 23, 1060– 1071. 10.1016/j.celrep.2018.03.119 29694885 PMC5946458 · DOI
  75. Miesenbock G. De Angelis D. A. Rothman J. E. (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192– 195. 10.1038/28190 9671304 · DOI
  76. Mondin M. Labrousse V. Hosy E. Heine M. Levet F. Poujol C.. (2011). Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds. J. Neurosci. 31, 13500– 13515. 10.1523/JNEUROSCI.6439-10.2011 21940442 PMC6623291 · DOI
  77. Mora R. J. Roberts R. W. Arnold D. B. (2013). Recombinant probes reveal dynamic localization of CaMKII_within somata of cortical neurons. J. Neurosci. 33, 14579– 14590. 10.1523/JNEUROSCI.2108-13.2013 24005308 PMC3761057 · DOI
  78. Nagy V. Bozdagi O. Matynia A. Balcerzyk M. Okulski P. Dzwonek J.. (2006). Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J. Neurosci. 26, 1923– 1934. 10.1523/JNEUROSCI.4359-05.2006 16481424 PMC4428329 · DOI · Paper page
  79. Nicoll R. A. (2017). A brief history of long-term potentiation. Neuron 93, 281– 290. 10.1016/j.neuron.2016.12.015 28103477 · DOI · Paper page
  80. Nuriya M. Huganir R. L. (2006). Regulation of AMPA receptor trafficking by N-cadherin. J. Neurochem. 97, 652– 661. 10.1111/j.1471-4159.2006.03740.x 16515543 · DOI
  81. Opazo P. Labrecque S. Tigaret C. M. Frouin A. Wiseman P. W. De Koninck P.. (2010). CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67, 239– 252. 10.1016/j.neuron.2010.06.007 20670832 · DOI
  82. Padamsey Z. McGuinness L. Bardo S. J. Reinhart M. Tong R. Hedegaard A.. (2017). Activity-dependent exocytosis of lysosomes regulates the structural plasticity of dendritic spines. Neuron 93, 132– 146. 10.1016/j.neuron.2016.11.013 27989455 PMC5222721 · DOI · Paper page
  83. Park M. Salgado J. M. Ostroff L. Helton T. D. Robinson C. G. Harris K. M.. (2006). Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52, 817– 830. 10.1016/j.neuron.2006.09.040 17145503 PMC1899130 · DOI · Paper page
  84. Parton R. G. Simons K. Dotti C. G. (1992). Axonal and dentritic endocytic pathways in cultured neurons. J. Cell Biol. 119, 123– 137. 10.1083/jcb.119.1.123 1527164 PMC2289637 · DOI
  85. Penn A. C. Zhang C. L. Georges F. Royer L. Breillat C. Hosy E.. (2017). Hippocampal LTP and contextual learning require surface diffusion of AMPA receptors. Nature 549, 384– 388. 10.1038/nature23658 28902836 PMC5683353 · DOI · Paper page
  86. Petersen C. C. Malenka R. C. Nicoll R. A. Hopfield J. J. (1998). All-or-none potentiation at CA3-CA1 synapses. Proc. Natl. Acad. Sci. U.S.A. 95, 4732– 4737. 10.1073/pnas.95.8.4732 9539807 PMC22559 · DOI
  87. Petrini E. M. Lu J. Cognet L. Lounis B. Ehlers M. D. Choquet D. (2009). Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63, 92– 105. 10.1016/j.neuron.2009.05.025 19607795 PMC2847611 · DOI
  88. Plant K. Pelkey K. A. Bortolotto Z. A. Morita D. Terashima A. McBain C. J.. (2006). Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602– 604. 10.1038/nn1678 16582904 · DOI · Paper page
  89. Pozo K. Cingolani L. A. Bassani S. Laurent F. Passafaro M. Goda Y. (2012). β3 integrin interacts directly with GluA2 AMPA receptor subunit and regulates AMPA receptor expression in hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 109, 1323– 1328. 10.1073/pnas.1113736109 22232691 PMC3268285 · DOI
  90. Rácz B. Blanpied T. A. Ehlers M. D. Weinberg R. J. (2004). Lateral organization of endocytic machinery in dendritic spines. Nat. Neurosci. 7, 917– 918. 10.1038/nn1303 15322548 · DOI
  91. Rathje M. Fang H. Bachman J. L. Anggono V. Gether U. Huganir R. L.. (2013). AMPA receptor pHluorin-GluA2 reports NMDA receptor-induced intracellular acidification in hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 110, 14426– 14431. 10.1073/pnas.1312982110 23940334 PMC3761605 · DOI
  92. Roche K. W. Brien R. J. O. Mammen A. L. Bernhardt J. Huganir R. L. (1996). Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16, 1179– 1188. 10.1016/S0896-6273(00)80144-0 8663994 · DOI · Paper page
  93. Roman-Vendrell C. Chevalier M. Acevedo-Canabal A. M. Delgado-Peraza F. Flores-Otero J. Yudowski G. A. (2014). Imaging of kiss-and-run exocytosis of surface receptors in neuronal cultures. Front. Cell. Neurosci. 8: 363. 10.3389/fncel.2014.00363 25404895 PMC4217495 · DOI
  94. Saglietti L. Dequidt C. Kamieniarz K. Rousset M. Valnegri P. Thoumine O.. (2007). Extracellular Interactions between GluR2 and N-cadherin in spine regulation. Neuron 54, 461– 477. 10.1016/j.neuron.2007.04.012 17481398 · DOI · Paper page
  95. Schnell E. Sizemore M. Karimzadegan S. Chen L. Bredt D. S. Nicoll R. A. (2002). Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. U.S.A. 99, 13902– 13907. 10.1073/pnas.172511199 12359873 PMC129795 · DOI · Paper page
  96. Schwenk J. Baehrens D. Haupt A. Bildl W. Boudkkazi S. Roeper J. (2014). Neuroresource regional diversity and developmental dynamics of the AMPA-receptor proteome in the mammalian brain. Neuron 84, 41– 54. 10.1016/j.neuron.2014.08.044 25242221 · DOI
  97. Schwenk J. Harmel N. Brechet A. Zolles G. Berkefeld H. Müller C. S.. (2012). High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes. Neuron 74, 621– 633. 10.1016/j.neuron.2012.03.034 22632720 · DOI · Paper page
  98. Shi S.-H. Hayashi Y. Petralia R. S. Zaman S. H. Wenthold R. J. Svoboda K.. (1999). Rapid spine delivery and redestribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811– 1816. 10.1126/science.284.5421.1811 10364548 · DOI · Paper page
  99. Sinnen B. L. Bowen A. B. Forte J. S. Hiester B. G. Crosby K. C. Gibson E. S.. (2017). Optogenetic control of synaptic composition and function. Neuron 93, 646– 660. 10.1016/j.neuron.2016.12.037 28132827 PMC5300939 · DOI · Paper page
  100. Soler-llavina G. J. Arstikaitis P. Morishita W. Ahmad M. Sudhof T. C. (2013). Report leucine-rich repeat transmembrane proteins are essential for maintenance of long-term potentiation. Neuron 79, 439– 446. 10.1016/j.neuron.2013.06.007 23931994 PMC3741667 · DOI
  101. Son J. Keefe M. D. Stevenson T. J. Barrios J. P. Anjewierden S. Newton J. B.. (2016). Transgenic fingRs for live mapping of synaptic dynamics in genetically-defined neurons. Sci. Rep. 6: 18734. 10.1038/srep18734 26728131 PMC4700522 · DOI
  102. Spacek J. Harris K. M. (1997). Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature Rat. J. Neurosci. 17, 190– 203. 10.1523/JNEUROSCI.17-01-00190.1997 8987748 PMC6793680 · DOI · Paper page
  103. Spence E. F. Kanak D. J. Carlson B. R. Soderling S. H. (2016). The Arp2/3 complex is essential for distinct stages of spine synapse maturation, including synapse unsilencing. J. Neurosci. 36, 9696– 9709. 10.1523/JNEUROSCI.0876-16.2016 27629719 PMC5039249 · DOI · Paper page
  104. Sun X. Zhao Y. Wolf M. E. (2005). Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons. J. Neurosci. 25, 7342– 7351. 10.1523/JNEUROSCI.4603-04.2005 16093384 PMC6725299 · DOI · Paper page
  105. Szepesi Z. Hosy E. Ruszczycki B. Bijata M. Pyskaty M. Bikbaev A.. (2014). Synaptically released matrix metalloproteinase activity in control of structural plasticity and the cell surface distribution of GluA1-AMPA receptors. PLoS ONE 9: e98274. 10.1371/journal.pone.0098274 24853857 PMC4031140 · DOI · Paper page
  106. Szymczak A. L. Workman C. J. Wang Y. Vignali K. M. Dilioglou S. Vanin E. F.. (2004). Correction of multi-gene deficiency in vivo using a single ‘self-cleaving' 2A peptide-based retroviral vector. Nat. Biotechnol. 22, 589– 595. 10.1038/nbt957 15064769 · DOI
  107. Tao-Cheng J.-H. Crocker V. T. Winters C. A. Azzam R. Chludzinski J. Reese T. S. (2011). Trafficking of AMPA receptors at plasma membranes of hippocampal neurons. J. Neurosci. 31, 4834– 4843. 10.1523/JNEUROSCI.4745-10.2011 21451021 PMC3138201 · DOI · Paper page
  108. Tardin C. Cognet L. Bats C. Lounis B. Choquet D. (2003). Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J. 22, 4656– 4665. 10.1093/emboj/cdg463 12970178 PMC212729 · DOI · Paper page
  109. Tomita S. Chen L. Kawasaki Y. Petralia R. S. Wenthold R. J. Nicoll R. A.. (2003). Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell Biol. 161, 805– 816. 10.1083/jcb.200212116 12771129 PMC2199354 · DOI
  110. Tomita S. Fukata M. Nicoll R. Bredt D. (2004). Dynamic interaction of stargazing-like TARPs with cycling AMPA receptors at synapses. Science 303, 1508– 1511. 10.1126/science.1090262 15001777 · DOI
  111. Uezu A. Kanak D. J. Bradshaw T. W. A. Soderblum E. J. Catavero C. M. Burette A. C.. (2016). Identification of an elaborate complex mediating postsynaptic inhibition. Science 353, 960– 962. 10.1126/science.aag0821 27609886 PMC5432043 · DOI · Paper page
  112. Wakayama S. Kiyonaka S. Arai I. Kakegawa W. Matsuda S. Ibata K.. (2017). Chemical labelling for visualizing native AMPA receptors in live neurons. Nat. Commun. 8: 14850. 10.1038/ncomms14850 28387242 PMC5385570 · DOI
  113. Walker A. S. Neves G. Grillo F. Jackson R. E. Rigby M. Donnell C. O.. (2017). Distance-dependent gradient in NMDAR-driven spine calcium signals along tapering dendrites. Proc. Natl. Acad. Sci. U.S.A. 114, E1986– E1995. 10.1073/pnas.1607462114 28209776 PMC5347575 · DOI
  114. Wang R. Walker C. S. Brockie P. J. Francis M. M. Mellem J. E. Madsen D. M.. (2008a). Evolutionary conserved role for TARPs in the gating of glutamate receptors and tuning of synaptic function. Neuron 59, 997– 1008. 10.1016/j.neuron.2008.07.023 18817737 PMC2754846 · DOI
  115. Wang Z. Edwards J. G. Riley N. Provance D. W. Karcher R. Li X.-D.. (2008c). Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135, 535– 548. 10.1016/j.cell.2008.09.057 18984164 PMC2585749 · DOI · Paper page
  116. Werner C. T. Murray C. H. Reimers J. M. Chauhan N. M. Woo K. K. Y. Molla H. M.. (2017). Trafficking of calcium-permeable and calcium-impermeable AMPA receptors in nucleus accumbens medium spiny neurons co-cultured with prefrontal cortex neurons. Neuropharmacology 116, 224– 232. 10.1016/j.neuropharm.2016.12.014 27993521 PMC5385156 · DOI
  117. Woolfrey K. M. Sanderson J. L. Dell'Acqua M. L. (2015). The palmitoyl acyltransferase DHHC2 regulates recycling endosome exocytosis and synaptic potentiation through palmitoylation of AKAP79/150. J. Neurosci. 35, 442– 456. 10.1523/JNEUROSCI.2243-14.2015 25589740 PMC4293401 · DOI
  118. Wu D. Bacaj T. Morishita W. Goswami D. Arendt K. L. Xu W.. (2017a). Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP. Nature 544, 316– 321. 10.1038/nature21720 28355182 PMC5734942 · DOI · Paper page
  119. Wu Y. Whiteus C. Xu C. S. Hayworth K. J. Weinberg R. J. Hess H. F. (2017b). Contacts between the endoplasmic reticulum and other membranes in neurons. Proc. Natl. Acad. Sci. U.S.A. 114, E4859– E4867. 10.1073/pnas.1701078114 PMC5474793 28559323 · DOI
  120. Yang Y. Wang X.-B. Frerking M. Zhou Q. (2008a). Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 105, 11388– 11393. 10.1073/pnas.0802978105 18682558 PMC2496888 · DOI
  121. Ye T. Ip J. P. K. Fu A. K. Y. Ip N. Y. (2014). Cdk5-mediated phosphorylation of RapGEF2 controls neuronal migration in the developing cerebral cortex. Nat. Commun. 5: 4826. 10.1038/ncomms5826 25189171 PMC4164783 · DOI
  122. Yudowski G. A. Puthenveedu M. A. Leonoudakis D. Panicker S. Thorn K. S. Beattie E. C.. (2007). Real-time imaging of discrete exocytic events mediating surface delivery of AMPA receptors. J. Neurosci. 27, 11112– 11121. 10.1523/JNEUROSCI.2465-07.2007 17928453 PMC3249441 · DOI · Paper page
  123. Zhang Y. Cudmore R. H. Lin D. Linden D. J. Huganir R. L. (2015). Visualization of NMDA receptor–dependent AMPA receptor synaptic plasticity in vivo. Nat. Neurosci. 18, 402– 407. 10.1038/nn.3936 25643295 PMC4339371 · DOI
  124. Zheng N. Jeyifous O. Munro C. Montgomery J. M. Green W. N. (2015). Synaptic activity regulates AMPA receptor trafficking through different recycling pathways. Elife 4: e06878. 10.7554/eLife.06878 25970033 PMC4451724 · DOI

Cited by

Sorted by citations

Authors
Hiester, B. G., Becker, M. I., Bowen, A. B., Schwartz, S. L., & Kennedy, M. J.
Affiliations
University of Colorado Anschutz (US)
Corresponding author
Kennedy, Matthew J.
ORCID
Venue
Frontiers in Cellular Neuroscience
Publisher
Frontiers Media SA
Published
2018-10-30
Volume
12
Pages
391-391
ISSN
1662-5102 (ISSN-L)
DOI
10.3389/fncel.2018.00391
PMC
PMC6218485
OpenAlex
W2899312143
Cited by
37
References
24
Citations by year
2024: 4 · 2023: 11 · 2022: 5 · 2021: 7 · 2020: 7 · 2019: 2 · 2018: 1
FWCI
1.94
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institute of Neurological Disorders and Stroke (NS082271, NS103328, NS092421)
  • National Institute on Aging (AG058005)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
long-term potentiation, synaptic plasticity, AMPA receptors, intracellular organelles, membrane fusion, excitatory synapses, learning and memory

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review