AGAP3 and Arf6 regulate trafficking of AMPA receptors and synaptic plasticity

Journal of Neuroscience

Volumn 33, Issue 31, 2013, Pages 12586-12598

  Oku, Yuko ^a   Huganir, Richard L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; AMPA RECEPTOR; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN AGAP3; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAT; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTORS; ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; FEMALE; GTP PHOSPHOHYDROLASES; GTPASE-ACTIVATING PROTEINS; HIPPOCAMPUS; HUMANS; LONG-TERM POTENTIATION; MALE; MAP KINASE SIGNALING SYSTEM; MUTATION; NEURONS; PROTEIN TRANSPORT; RATS; RECEPTORS, AMPA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84880785844     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0341-13.2013     Document Type: Article

References (42)

1. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609. CrossRef Medline
2. Bendor J, Lizardi-Ortiz JE, Westphalen RI, Brandstetter M, HemmingsHCJr, Sulzer D, Flajolet M, Greengard P (2010) AGAP1/AP-3-dependent endocytic recycling ofM5muscarinic receptors promotes dopamine release. EMBO J 29:2813-2826. CrossRef Medline
3. Blum S, Moore AN, Adams F, Dash PK (1999) A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term special memory. J Neurosci 19:3535-3544. Medline
4. Carlisle HJ, Manzerra P, Marcora E, Kennedy MB (2008) SynGAP regulates steady state and activity-dependent phosphorylation of cofilin. J Neurosci 28:13673-13683. CrossRef Medline
5. Chan CB, Chen Y, Liu X, Tang X, Lee CW, Mei L, Ye K (2011) PIKEmediated PI3-kinase activity is required for AMPA receptor surface expression. EMBO J 30:4274-4286. CrossRef Medline
6. Chen HJ, Rojas-Soto M, Oguni A, Kennedy MB (1998) A synaptic Ras-GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron 20:895-904. CrossRef Medline
7. Donaldson JG (2003) Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem 278:41573-41576. CrossRef Medline
8. English JD, Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase cascade in hippocampal long-term potentiation. J Biol Chem 271: 24329-24332. CrossRef Medline
9. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106. CrossRef Medline
10. Grant BD, Donaldson JG (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10:597-608. CrossRef Medline
11. Hayashi T, Thomas GM, Huganir RL (2009) Dual palmitoylation of NR2 subunits regulates NMDA receptor trafficking. Neuron 64:213-226. CrossRef Medline
12. Kamiya A, Kubo K, Tomoda T, Takaki M, Youn R, Ozeki Y, Sawamura N, Park U, Kudo C, Okawa M, Ross CA, Hatten ME, Nakajima K, Sawa A (2005) Disrupted-in-Schizophrenia-1 is required for neuronal migra-tion in the cerebral cortex: perturbation by schizophrenia-associated mutation. Nat Cell Biol 7:1167-1178. CrossRef Medline
13. Kim JH, Liao D, Lau LF, Huganir RL (1998) SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 20:683-691. CrossRef Medline
14. Kim MJ, Dunah AW, Wang YT, ShengM (2005) Differential roles of NR2Aand NR2B-containingNMDAreceptors in Ras-ERK signaling andAMPA receptor trafficking. Neuron 46:745-760. CrossRef Medline
15. Komiyama NH, Watabe AM, Carlisle HJ, Porter K, Charlesworth P, Monti J, Strathdee DJ, O'Carroll CM, Martin SJ, Morris RG, O'Dell TJ, Grant SG (2002) SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor. J Neurosci 22:9721-9732. Medline
16. Krapivinsky G, Medina I, Krapivinsky L, Gapon S, Clapham DE (2004) SynGAP-MUPP1-CaMKII synaptic complexes regulate p38 MAP kinase activity and NMDA receptor-dependent synaptic AMPA receptor potentiation. Neuron 43:563-574. CrossRef Medline
17. Liao D, Scannevin RH, Huganir R (2001) Activation of silent synapses by rapid activity-dependent synaptic recruitment ofAMPAreceptors. J Neurosci 21:6008-6017. Medline
18. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29:243-254. CrossRef Medline
19. Luo J, Wang Y, Yasuda RP, Dunah AW, Wolfe BB (1997) The majority of N-methyl-D-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B). Mol Pharmacol 51:79-86. Medline
20. Luo R, Akpan IO, Hayashi R, Sramko M, Barr V, Shiba Y, Randazzo PA (2012) GTP-binding protein-like domain of AGAP1 is protein binding site that allosterically regulates ArfGAP protein catalytic activity. J Biol Chem 287:17176-17185. CrossRef Medline
21. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126. CrossRef Medline
22. Nedyalkova L, Tempel W, Tong Y, Li Y, Arrowsmith CH, Edwards AM, Bountra C, Weigelt J, Bochkarev A, Park H Structural Genomics Consortium. Crystal structure of the Ras-like domain of CENTG3. PDB ID: 3IHW
23. Nie Z, Boehm M, Boja ES, Vass WC, Bonifacino JS, Fales HM, Randazzo PA (2003) Specific regulation of the adaptor protein complex AP-3 by the Arf GAP AGAP1. Dev Cell 5:513-521. CrossRef Medline
24. Nie Z, Fei J, Premont RT, Randazzo PA (2005) The Arf GAPs AGAP1 and AGAP2 distinguish between the adaptor protein complexes AP-1 and AP-3. J Cell Sci 118:3555-3566. CrossRef Medline
25. Pena V, Hothorn M, Eberth A, Kaschau N, Parret A, Gremer L, Bonneau F, Ahmadian MR, Scheffzek K (2008) The C2 domain of SynGAP is essential for stimulation of the Rap GTPase reaction. EMBO Rep 9:350-355. CrossRef Medline
26. Porat-Shliom N, Kloog Y, Donaldson JG (2008) A unique platform for H-ras signaling involving clathrin-independent endocytosis. Mol Biol Cell 19:765-775. Medline
27. Qin Q, Inatome R, Hotta A, Kojima M, Yamamura H, Hirai H, Yoshizawa T, Tanaka H, Fukami K, Yanagi S (2006) A novel GTPase, CRAG, mediates promyelocytic leukemia protein-associated nuclear body formation and degradation of expanded polyglutamine protein. J Cell Biol 172:497-504. CrossRef Medline
28. R Development Core Team (2008) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
29. Robertson SE, Setty SR, Sitaram A, Marks MS, Lewis RE, Chou MM (2006) Extracellular signal-regulated kinase regulates clathrin-independent endosomal trafficking. Mol Biol Cell 17:645-657. Medline
30. Rumbaugh G, Adams JP, Kim JH, Huganir RL (2006) SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons. Proc Natl Acad Sci U S A 103:4344-4351. CrossRef Medline
31. Sans N, Petralia RS, Wang YX, Blahos J 2nd, Hell JW, Wenthold RJ (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 20:1260-1271. Medline
32. Scholz R, Berberich S, Rathgeber L, Kolleker A, Köhr G, Kornau HC (2010) AMPA receptor signaling through BRAG2 and Arf6 critical for long-term synaptic depression. Neuron 66:768-780. CrossRef Medline
33. Selcher JC, Atkins CM, Trzaskos JM, Paylor R, Sweatt JD (1999) A necessity for MAP kinase activation in mammalian spatial learning. Learn Mem 6:478-490. CrossRef Medline
34. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613-643. CrossRef Medline
35. Soundararajan M, Yang X, Elkins JM, Sobott F, Doyle DA (2007) The centaurin gamma-1 GTPase-like domain functions as an NTPase. Biochem J 401:679-688. CrossRef Medline
36. Strack S, McNeill RB, Colbran RJ (2000) Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem 275: 23798-23806. CrossRef Medline
37. Tague SE, Muralidharan V, D'Souza-Schorey C (2004) Arf6 regulates tumor cell invasion via the activation of MEK/ERK signaling pathway. Proc Natl Acad Sci U S A 101:9671-9676. CrossRef Medline
38. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5:173-183. CrossRef Medline
39. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680. CrossRef Medline
40. Xia C, Ma W, Stafford LJ, Liu C, Gong L, Martin JF, LiuM (2003) GGAPs, a new family of bifunctional GTP-binding and GTPase-activating proteins. Mol Cell Biol 23:2476-2488. CrossRef Medline
41. Xia J, Zhang X, Staudinger J, Huganir RL (1999) Clustering ofAMPAreceptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22:179-187. CrossRef Medline
42. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R (2002) Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110:443-455. CrossRef Medline