Clathrin-independent trafficking of AMPA receptors

Journal of Neuroscience

Volumn 35, Issue 12, 2015, Pages 4830-4836

  Glebov, Oleg O ^a,b   Tigaret, Cezar M ^a   Mellor, Jack R ^a   Henley, Jeremy M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

AMPA receptors; Endocytosis; Membrane trafficking; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; CLATHRIN; DYNAMIN; F ACTIN; 4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; ACTIN; AMINOQUINOLINE DERIVATIVE; HYDRAZONE DERIVATIVE; N'-(3,4-DIHYDROXYBENZYLIDENE)-3-HYDROXY-2-NAPHTHAHYDRAZIDE; PYRIMIDINE DERIVATIVE; RAC1 PROTEIN; RAC1 PROTEIN, RAT; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOFLUORESCENCE TEST; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE TECHNIQUE; DRUG EFFECTS; HIPPOCAMPUS; LONG TERM DEPRESSION; MALE; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN TRANSPORT;

ACTINS; AMINOQUINOLINES; ANIMALS; CELL CULTURE TECHNIQUES; CLATHRIN; DYNAMINS; HIPPOCAMPUS; HYDRAZONES; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEURONS; PROTEIN TRANSPORT; PYRIMIDINES; RAC1 GTP-BINDING PROTEIN; RATS; RECEPTORS, AMPA; RNA, SMALL INTERFERING;

EID: 84925856963     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3571-14.2015     Document Type: Article

References (37)

1. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22:461–469. CrossRef Medline
2. Bonanomi D, Fornasiero EF, Valdez G, Halegoua S, Benfenati F, Menegon A, Valtorta F (2008) Identification of a developmentally regulated pathway of membrane retrieval in neuronal growth cones. J Cell Sci 121:3757– 3769. CrossRef Medline
3. Borroni V, Barrantes FJ (2011) Cholesterol modulates the rate and mechanism of acetylcholine receptor internalization. J Biol Chem 286:17122– 17132. CrossRef Medline
4. Chung C, Barylko B, Leitz J, Liu X, Kavalali ET (2010) Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J Neurosci 30:1363–1376. CrossRef Medline
5. Cinar H, Barnes EM Jr (2001) Clathrin-independent endocytosis of GABA A receptors in HEK 293 cells. Biochemistry 40:14030–14036. CrossRef Medline
6. Collingridge GL, Peineau S, Howland JG, Wang YT (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459–473. CrossRef Medline
7. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127:915–934. CrossRef Medline
8. Damke H, Baba T, van der Bliek AM, Schmid SL (1995) Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol 131:69–80. CrossRef Medline
9. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5:410–421. CrossRef Medline
10. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. CrossRef Medline
11. Dutta D, Williamson CD, Cole NB, Donaldson JG (2012) Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis. PLoS One 7:e45799. CrossRef Medline
12. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511–525. CrossRef Medline
13. Ford MG, Pearse BM, Higgins MK, Vallis Y, Owen DJ, Gibson A, Hopkins CR, Evans PR, McMahon HT (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291:1051–1055. CrossRef Medline
14. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y (2004) Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A 101:7618–7623. CrossRef Medline
15. Gu J, Lee CW, Fan Y, Komlos D, Tang X, Sun C, Yu K, Hartzell HC, Chen G, Bamburg JR, Zheng JQ (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13:1208–1215. CrossRef Medline
16. Hansen CG, Nichols BJ (2009) Molecular mechanisms of clathrinindependent endocytosis. J Cell Sci 122:1713–1721. CrossRef Medline
17. He Z, Fan J, Kang L, Lu J, Xue Y, Xu P, Xu T, Chen L (2008) Ca2+ triggers a novel clathrin-independent but actin-dependent fast endocytosis in pancreatic beta cells. Traffic 9:910–923. CrossRef Medline
18. Henley JM, Barker EA, Glebov OO (2011) Routes, destinations and delays: recent advances in AMPA receptor trafficking. Trends Neurosci 34:258– 268. CrossRef Medline
19. Hill TA, Gordon CP, McGeachie AB, Venn-Brown B, Odell LR, Chau N, Quan A, Mariana A, Sakoff JA, Chircop M, Robinson PJ, McCluskey A (2009) Inhibition of dynamin mediated endocytosis by the dynoles— synthesis and functional activity of a family of indoles. J Med Chem 52: 3762–3773. CrossRef Medline
20. Hotulainen P, Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189:619–629. CrossRef Medline
21. Jockusch WJ, Praefcke GJ, McMahon HT, Lagnado L (2005) Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46:869–878. CrossRef Medline
22. Joset A, Dodd DA, Halegoua S, Schwab ME (2010) Pincher-generated Nogo-A endosomes mediate growth cone collapse and retrograde signaling. J Cell Biol 188:271–285. CrossRef Medline
23. Kumari S, Borroni V, Chaudhry A, Chanda B, Massol R, Mayor S, Barrantes FJ (2008) Nicotinic acetylcholine receptor is internalized via a Rac-dependent, dynamin-independent endocytic pathway. J Cell Biol 181: 1179–1193. CrossRef Medline
24. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, Wyszynski M, Wang YT, Sheng M (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3:1282–1290. CrossRef Medline
25. Lu J, Helton TD, Blanpied TA, Rácz B, Newpher TM, Weinberg RJ, Ehlers MD (2007) Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron 55:874–889. CrossRef Medline
26. Lüscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24:649–658. CrossRef Medline
27. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10:839–850. CrossRef Medline
28. Man HY, Lin JW, Ju WH, Ahmadian G, Liu L, Becker LE, Sheng M, Wang YT (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25:649–662. CrossRef Medline
29. Martin S, Henley JM (2004) Activity-dependent endocytic sorting of kai nate receptors to recycling or degradation pathways. EMBO J 23:4749– 4759. CrossRef Medline
30. Owen DJ, Wigge P, Vallis Y, Moore JD, Evans PR, McMahon HT (1998) Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation. EMBO J 17:5273–5285. CrossRef Medline
31. Park RJ, Shen H, Liu L, Liu X, Ferguson SM, De Camilli P (2013) Dynamin triple knockout cells reveal off target effects of commonly used dynamin inhibitors. J Cell Sci 126:5305–5312. CrossRef Medline
32. Rocca DL, Martin S, Jenkins EL, Hanley JG (2008) Inhibition of Arp2/3- mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis. Nat Cell Biol 10:259–271. CrossRef Medline
33. von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, Robertson MJ, MacGregor KA, Tomilin N, Pechstein A, Chau N, Chircop M, Sakoff J, von Kries JP, Saenger W, Kräusslich HG, Shupliakov O, Robinson PJ, McCluskey A, Haucke V (2011) Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146:471–484. CrossRef Medline
34. Wiens KM, Lin H, Liao D (2005) Rac1 induces the clustering of AMPA receptors during spinogenesis. J Neurosci 25:10627–10636. CrossRef Medline
35. Willox AK, Sahraoui YME, Royle SJ (2014) Non-specificity of Pitstop 2 in clathrin-mediated endocytosis. Biol Open 3:326–331. CrossRef Medline
36. Xu J, McNeil B, Wu W, Nees D, Bai L, Wu LG (2008) GTP-independent rapid and slow endocytosis at a central synapse. Nat Neurosci 11:45–53. CrossRef Medline
37. Zhou Q, Xiao M, Nicoll RA (2001) Contribution of cytoskeleton to the internalization of AMPA receptors. Proc Natl Acad Sci U S A 98:1261– 1266. CrossRef Medline