Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation

Journal of Neuroscience

Volumn 27, Issue 48, 2007, Pages 13311-13315

  Brown, Tyler C ^a   Correia, Susana S ^a   Petrok, Cortney N ^a   Esteban, José A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Dendritic spine; Endosomes; GluR1; Hippocampus; Phosphorylation; Rab proteins; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; CARRIER PROTEIN; MUTANT PROTEIN; PROTEIN RAB11; RAB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; ENDOSOME; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SPINAL GANGLION; SYNAPSE; SYNAPTIC MEMBRANE;

ANALYSIS OF VARIANCE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; DENDRITES; ELECTRIC STIMULATION; ENDOSOMES; GYNECOMASTIA; HIPPOCAMPUS; LONG-TERM POTENTIATION; LUMINESCENT PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RATS; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; SYNAPTIC MEMBRANES; TRANSFORMATION, GENETIC;

EID: 36849089658     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4258-07.2007     Document Type: Article

References (46)

1. 2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor. J Biol Chem 272:32727-32730.
2. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR (1997b) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042-2045.
3. Barry MF, Ziff EB (2002) Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 12:279-286.
4. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
5. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
6. Brown TC, Tran IC, Backos DS, Esteban JA (2005) NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron 45:81-94.
7. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70:715-728.
8. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99:7877-7882.
9. Emery G, Hutterer A, Berdnik D, Mayer B, Wirtz-Peitz F, Gaitan MG, Knoblich JA (2005) Asymmetric Rab 11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 122:763-773.
10. Esteban JA (2003) AMPA receptor trafficking: a road map for synaptic plasticity. Mol Interv 3:375-385.
11. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143.
12. Gahwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci 20:471-477.
13. Gerges NZ, Backos DS, Esteban JA (2004a) Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J Biol Chem 279:43870-43878.
14. Gerges NZ, Tran IC, Backos DS, Harrell JM, Chinkers M, Pratt WB, Esteban JA (2004b) Independent functions of hsp90 in neurotransmitter release and in the continuous synaptic cycling of AMPA receptors. J Neurosci 24:4758-4766.
15. Gerges NZ, Brown TC, Correia SS, Esteban JA (2005) Analysis of Rab protein function in neurotransmitter receptor trafficking at hippocampal synapses. Methods Enzymol 403:153-166.
16. Gruart A, Munoz MD, Delgado-Garcia JM (2006) Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 26:1077-1087.
17. Gruenberg J (2001) The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol 2:721-730.
18. Harris KM, Kater SB (1994) Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
19. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
20. Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M (2005) Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121:437-450.
21. Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K (1993) Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 123:35-45.
22. Kennedy MJ, Ehlers MD (2006) Organelles and trafficking machinery for postsynaptic plasticity. Annu Rev Neurosci 29:325-362.
23. Kopec CD, 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.
24. Lo DC, McAllister AK, Katz LC (1994) Neuronal transfection in brain slices using particle-mediated gene transfer. Neuron 13:1263-1268.
25. Luscher 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.
26. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
27. Malinow R, Hayashi Y, Maletic-Savatic M, Zaman S, Poncer J-C, Shi SH, Esteban JA (1999) Introduction of green fluorescent protein into hippocampal neurons through viral infection. In: Imaging living neurons (Yuste R, Lanni F, Konnerth A, eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
28. Mammen AL, Kameyama K, Roche KW, Huganir RL (1997) Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J Biol Chem 272:32528-32533.
29. McGee AW, Bredt DS (2003) Assembly and plasticity of the glutamatergic postsynaptic specialization. Curr Opin Neurobiol 13:111-118.
30. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97.
31. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
32. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, Ehlers MD (2006) Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52:817-830.
33. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141-1144.
34. Pfeffer SR (2001) Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol 11:487-491.
35. Piccini A, Malinow R (2002) Critical postsynaptic density 95/disc large/zonula occludens-1 interactions by glutamate receptor 1 (GluR1) and GluR2 required at different subcellular sites. J Neurosci 22:5387-5392.
36. Sheng M, Hyoung Lee S (2003) AMPA receptor trafficking and synaptic plasticity: major unanswered questions. Neurosci Res 46:127-134.
37. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
38. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
39. Smith AC, Heo WD, Braun V, Jiang X, Macrae C, Casanova JE, Scidmore MA, Grinstein S, Meyer T, Brumell JH (2007) A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J Cell Biol 176:263-268.
40. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21:393-400.
41. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149:901-914.
42. Steiner P, Alberi S, Kulangara K, Yersin A, Sarria JC, Regulier E, Kasas S, Dietler G, Muller D, Catsicas S, Hirling H (2005) Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J 24:2873-2884.
43. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509-547.
44. van Ijzendoorn SC (2006) Recycling endosomes. J Cell Sci 119:1679-1681.
45. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.
46. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107-117.