Retinoic acid and LTP recruit postsynaptic AMPA receptors using distinct SNARE-dependent mechanisms

Neuron

Volumn 86, Issue 2, 2015, Pages 442-456

  Arendt, Kristin L ^a   Zhang, Yingsha ^a   Jurado, Sandra ^a,b   Malenka, Robert C ^a   Südhof, Thomas C ^a   Chen, Lu ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; COMPLEXIN; NERVE PROTEIN; PROTEIN SNAP 47; Q SNARE PROTEIN; RETINOIC ACID; SNARE PROTEIN; SYNAPTOBREVIN; SYNATOBREVIN 2; SYNTAXIN; SYNTAXIN 3; SYNTAXIN 4; UNCLASSIFIED DRUG; SYNTAXIN 4, HUMAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL FUSION; CONTROLLED STUDY; EXOCYTOSIS; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANIMAL; DRUG EFFECTS; DRUG POTENTIATION; HIPPOCAMPUS; HOMEOSTASIS; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SYNAPSE; SYNAPTIC POTENTIAL;

ANIMALS; DRUG SYNERGISM; EXOCYTOSIS; HIPPOCAMPUS; HOMEOSTASIS; LONG-TERM POTENTIATION; MICE; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; PROTEIN TRANSPORT; QA-SNARE PROTEINS; RECEPTORS, AMPA; SNARE PROTEINS; SYNAPSES; SYNAPTIC POTENTIALS; TRETINOIN;

EID: 84929296242     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.009     Document Type: Article

References (59)

1. Adesnik H., Nicoll R.A. Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J.Neurosci. 2007, 27:4598-4602.
2. Ahmad M., Polepalli J.S., Goswami D., Yang X., Kaeser-Woo Y.J., Südhof T.C., Malenka R.C. Postsynaptic complexin controls AMPA receptor exocytosis during LTP. Neuron 2012, 73:260-267.
3. Aoto J., Nam C.I., Poon M.M., Ting P., Chen L. Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 2008, 60:308-320.
4. Arendt K.L., Sarti F., Chen L. Chronic inactivation of a neural circuit enhances LTP by inducing silent synapse formation. J.Neurosci. 2013, 33:2087-2096.
5. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 2008, 31:47-67.
6. Campanac E., Debanne D. Plasticity of neuronal excitability: Hebbian rules beyond the synapse. Arch. Ital. Biol. 2007, 145:277-287.
7. Chapellier B., Mark M., Garnier J.M., LeMeur M., Chambon P., Ghyselinck N.B. A conditional floxed (loxP-flanked) allele for the retinoic acid receptor alpha (RARalpha) gene. Genesis 2002, 32:87-90.
8. Chen L., Lau A.G., Sarti F. Synaptic retinoic acid signaling and homeostatic synaptic plasticity. Neuropharmacology 2014, 78:3-12.
9. Chiang M.Y., Misner D., Kempermann G., Schikorski T., Giguère V., Sucov H.M., Gage F.H., Stevens C.F., Evans R.M. An essential role for retinoid receptors RARbeta and RXRgamma in long-term potentiation and depression. Neuron 1998, 21:1353-1361.
10. Cocco S., Diaz G., Stancampiano R., Diana A., Carta M., Curreli R., Sarais L., Fadda F. Vitamin A deficiency produces spatial learning and memory impairment in rats. Neuroscience 2002, 115:475-482.
11. Collingridge G.L., Kehl S.J., McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J.Physiol. 1983, 334:33-46.
12. Davis G.W., Muller M. Homeostatic control of presynaptic neurotransmitter release. Annu. Rev. Physiol. 2015, 77:251-270.
13. Dugani C.B., Klip A. Glucose transporter 4: cycling, compartments and controversies. EMBO Rep. 2005, 6:1137-1142.
14. Giraudo C.G., Eng W.S., Melia T.J., Rothman J.E. A clamping mechanism involved in SNARE-dependent exocytosis. Science 2006, 313:676-680.
15. Grasselli G., Hansel C. Cerebellar long-term potentiation: cellular mechanisms and role in learning. Int. Rev. Neurobiol. 2014, 117:39-51.
16. Gray E.E., Fink A.E., Sariñana J., Vissel B., O'Dell T.J. Long-term potentiation in the hippocampal CA1 region does not require insertion and activation of GluR2-lacking AMPA receptors. J.Neurophysiol. 2007, 98:2488-2492.
17. Guire E.S., Oh M.C., Soderling T.R., Derkach V.A. Recruitment of calcium-permeable AMPA receptors during synaptic potentiation is regulated by CaM-kinase I. J.Neurosci. 2008, 28:6000-6009.
18. Holt M., Varoqueaux F., Wiederhold K., Takamori S., Urlaub H., Fasshauer D., Jahn R. Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression. J.Biol. Chem. 2006, 281:17076-17083.
19. Huganir R.L., Nicoll R.A. AMPARs and synaptic plasticity: the last 25 years. Neuron 2013, 80:704-717.
20. Huntwork S., Littleton J.T. A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat. Neurosci. 2007, 10:1235-1237.
21. Isaac J.T., Nicoll R.A., Malenka R.C. Evidence for silent synapses: implications for the expression of LTP. Neuron 1995, 15:427-434.
22. Jurado S., Goswami D., Zhang Y., Molina A.J., Südhof T.C., Malenka R.C. LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 2013, 77:542-558.
23. Kennedy M.J., Davison I.G., Robinson C.G., Ehlers M.D. Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 2010, 141:524-535.
24. Lau C.G., Takayasu Y., Rodenas-Ruano A., Paternain A.V., Lerma J., Bennett M.V., Zukin R.S. SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking. J.Neurosci. 2010, 30:242-254.
25. Liao D., Hessler N.A., Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 1995, 375:400-404.
26. Link E., Edelmann L., Chou J.H., Binz T., Yamasaki S., Eisel U., Baumert M., Südhof T.C., Niemann H., Jahn R. Tetanus toxin action: inhibition of neurotransmitter release linked to synaptobrevin proteolysis. Biochem. Biophys. Res. Commun. 1992, 189:1017-1023.
27. Lledo P.M., Zhang X., Südhof T.C., Malenka R.C., Nicoll R.A. Postsynaptic membrane fusion and long-term potentiation. Science 1998, 279:399-403.
28. Maden M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 2007, 8:755-765.
29. Magee J.C., Johnston D. Plasticity of dendritic function. Curr. Opin. Neurobiol. 2005, 15:334-342.
30. Maghsoodi B., Poon M.M., Nam C.I., Aoto J., Ting P., Chen L. Retinoic acid regulates RARalpha-mediated control of translation in dendritic RNA granules during homeostatic synaptic plasticity. Proc. Natl. Acad. Sci. USA 2008, 105:16015-16020.
31. Makino H., Malinow R. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 2009, 64:381-390.
32. Maximov A., Tang J., Yang X., Pang Z.P., Südhof T.C. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 2009, 323:516-521.
33. McMahon H.T., Missler M., Li C., Südhof T.C. Complexins: cytosolic proteins that regulate SNAP receptor function. Cell 1995, 83:111-119.
34. Misner D.L., Jacobs S., Shimizu Y., de Urquiza A.M., Solomin L., Perlmann T., De Luca L.M., Stevens C.F., Evans R.M. Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity. Proc. Natl. Acad. Sci. USA 2001, 98:11714-11719.
35. Morita D., Rah J.C., Isaac J.T. Incorporation of inwardly rectifying AMPA receptors at silent synapses during hippocampal long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369:20130156.
36. Nomoto M., Takeda Y., Uchida S., Mitsuda K., Enomoto H., Saito K., Choi T., Watabe A.M., Kobayashi S., Masushige S., et al. Dysfunction of the RAR/RXR signaling pathway in the forebrain impairs hippocampal memory and synaptic plasticity. Mol. Brain 2012, 5:8.
37. Olson A.L., Knight J.B., Pessin J.E. Syntaxin 4, VAMP2, and/or VAMP3/cellubrevin are functional target membrane and vesicle SNAP receptors for insulin-stimulated GLUT4 translocation in adipocytes. Mol. Cell. Biol. 1997, 17:2425-2435.
38. Pabst S., Hazzard J.W., Antonin W., Südhof T.C., Jahn R., Rizo J., Fasshauer D. Selective interaction of complexin with the neuronal SNARE complex. Determination of the binding regions. J.Biol. Chem. 2000, 275:19808-19818.
39. Patterson M.A., Szatmari E.M., Yasuda R. AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc. Natl. Acad. Sci. USA 2010, 107:15951-15956.
40. Petrini E.M., Lu J., Cognet L., Lounis B., Ehlers M.D., Choquet D. Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 2009, 63:92-105.
41. Plant K., Pelkey K.A., Bortolotto Z.A., Morita D., Terashima A., McBain C.J., Collingridge G.L., Isaac J.T. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 2006, 9:602-604.
42. Poon M.M., Chen L. Retinoic acid-gated sequence-specific translational control by RARalpha. Proc. Natl. Acad. Sci. USA 2008, 105:20303-20308.
43. Reim K., Mansour M., Varoqueaux F., McMahon H.T., Südhof T.C., Brose N., Rosenmund C. Complexins regulate a late step in Ca2+-dependent neurotransmitter release. Cell 2001, 104:71-81.
44. Rizo J., Rosenmund C. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 2008, 15:665-674.
45. Sala C., Segal M. Dendritic spines: the locus of structural and functional plasticity. Physiol. Rev. 2014, 94:141-188.
46. Sarti F., Schroeder J., Aoto J., Chen L. Conditional RARα knockout mice reveal acute requirement for retinoic acid and RARα in homeostatic plasticity. Front. Mol. Neurosci. 2012, 5:16.
47. Sarti F., Zhang Z., Schroeder J., Chen L. Rapid suppression of inhibitory synaptic transmission by retinoic acid. J.Neurosci. 2013, 33:11440-11450.
48. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B.R., Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 1992, 359:832-835.
49. Südhof T.C. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 2013, 80:675-690.
50. Südhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
51. Tang J., Maximov A., Shin O.H., Dai H., Rizo J., Südhof T.C. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 2006, 126:1175-1187.
52. Toyoizumi T., Kaneko M., Stryker M.P., Miller K.D. Modeling the dynamic interaction of Hebbian and homeostatic plasticity. Neuron 2014, 84:497-510.
53. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391:892-896.
54. Wang H.L., Zhang Z., Hintze M., Chen L. Decrease in calcium concentration triggers neuronal retinoic acid synthesis during homeostatic synaptic plasticity. J.Neurosci 2011, 31:17764-17771.
55. Xu W., Morishita W., Buckmaster P.S., Pang Z.P., Malenka R.C., Südhof T.C. Distinct neuronal coding schemes in memory revealed by selective erasure of fast synchronous synaptic transmission. Neuron 2012, 73:990-1001.
56. Xue M., Lin Y.Q., Pan H., Reim K., Deng H., Bellen H.J., Rosenmund C. Tilting the balance between facilitatory and inhibitory functions of mammalian and Drosophila Complexins orchestrates synaptic vesicle exocytosis. Neuron 2009, 64:367-380.
57. Yang X., Kaeser-Woo Y.J., Pang Z.P., Xu W., Südhof T.C. Complexin clamps asynchronous release by blocking a secondary Ca(2+) sensor via its accessory α helix. Neuron 2010, 68:907-920.
58. Yu X., Zuo Y. Spine plasticity in the motor cortex. Curr. Opin. Neurobiol. 2011, 21:169-174.
59. Yudowski G.A., Puthenveedu M.A., Leonoudakis D., Panicker S., Thorn K.S., Beattie E.C., von Zastrow M. Real-time imaging of discrete exocytic events mediating surface delivery of AMPA receptors. J.Neurosci. 2007, 27:11112-11121.