Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation

Journal of Neuroscience

Volumn 26, Issue 7, 2006, Pages 2000-2009

  Kopec, Charles D ^a   Li, Bo ^a   Wei, Wei ^a   Boehm, Jannic ^a   Malinow, Roberto ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

AMPA receptor; Exocytosis; Long term potentiation; NMDA receptor; Trafficking; Two photon microscopy

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; GREEN FLUORESCENT PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; BIOLOGICAL MONITORING; CELL ENLARGEMENT; CELL STIMULATION; CELL SURFACE; CELL VOLUME; CHEMICAL MODIFICATION; CONTROLLED STUDY; DENDRITIC SPINE; EXOCYTOSIS; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN CONTENT; SENSITIVITY ANALYSIS;

ANIMALS; EXOCYTOSIS; HIPPOCAMPUS; LONG-TERM POTENTIATION; RATS; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; SPINE; SYNAPSES; TRANSFECTION;

EID: 33644560354     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3918-05.2006     Document Type: Article

References (74)

1. Anderson RGFJ, Goldstein JL, Brown MS (1984) Visualization of acidic organelles in intact cells by electron microscopy. Proc Natl Acad Sci USA 81:4838-4842.
2. Arnold D, Feng L, Kim J, Heintz N (1994) A strategy for the analysis of gene expression during neural development. Proc Natl Acad Sci USA 91:9970-9974.
3. Ashby MCDLRS, Ralph GS, Uney J, Collingridge GL, Henley JM (2004) Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 24:5172-5176.
4. Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345-353.
5. Barria A, Malinow R (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48:289-301.
6. Baude A, Nusser Z, Molnar E, McIlhinney RA, Somogyi P (1995) High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69:1031-1055.
7. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
8. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
9. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3:243-293.
10. Campbell RETO, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99:7877-7882.
11. Carroll RC, Zukin RS (2002) NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 25:571-577.
12. Collingridge GL, Isaac JT, Wang YT (2004) Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5:952-962.
13. Desmond NL, Levy WB (1983) Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus. Brain Res 265:21-30.
14. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
15. Fischer M, Kaech S, Knutti D, Matus A (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20:847-854.
16. Fonseca R, Nagerl UV, Morris RG, Bonhoeffer T (2004) Competing for memory: hippocampal LTP under regimes of reduced protein synthesis. Neuron 44:1011-1020.
17. Fukazawa YSY, Ozawa F, Ohta Y, Mizuno K, Inokuchi K (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447-460.
18. Gandhi SPSC (2003) Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423:607-613.
19. Harris KM, Kater SB (1994) Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
20. 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.
21. Hosokawa T, Rusakov DA, Bliss TV, Fine A (1995) Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J Neurosci 15:5560-5573.
22. Huh KH, Wenthold RJ (1999) Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 274:151-157.
23. Jia Z, Agopyan N, Miu P, Xiong Z, Henderson J, Gerlai R, Taverna FA, Velumian A, MacDonald J, Carlen P, Abramow-Newerly W, Roder J (1996) Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17:945-956.
24. Jiang M, Lee CL, Smith KL, Swann JW (1998) Spine loss and other persistent alterations of hippocampal pyramidal cell dendrites in a model of early-onset epilepsy. J Neurosci 18:8356-8368.
25. Johnston D, Christie BR, Frick A, Gray R, Hoffman DA, Schexnayder LK, Watanabe S, Yuan LL (2003) Active dendrites, potassium channels and synaptic plasticity. Philos Trans R Soc Lond B Biol Sci 358:667-674.
26. Kauer JA, Malenka RC, Nicoll RA (1988) A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron 1:911-917.
27. Lang CBA, Zablow L, Kandel ER, Siegelbaum SA, Zakharenko SS (2004) Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc Natl Acad Sci USA 101:16665-16670.
28. Li B, Otsu Y, Murphy TH, Raymond LA (2003) Developmental decrease in NMDA receptor desensitization associated with shift to synapse and interaction with postsynaptic density-95. J Neurosci 23:11244-11254.
29. Lisman J (2003) Long-term potentiation: outstanding questions and attempted synthesis. Philos Trans R Soc Lond B Biol Sci 358:829-842.
30. Lisman JE (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38-43.
31. Lledo PM, Zhang X, Sudhof TC, Malenka RC, Nicoll RA (1998) Postsynaptic membrane fusion and long-term potentiation. Science 279:399-403.
32. Maletic-Savatic M, Malinow R, Svoboda K (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923-1927.
33. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
34. Matsuzaki MHN, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
35. Mayer ML, Armstrong N (2004) Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66:161-181.
36. Miesenbock GDAD, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
37. Mizrahi A, Crowley JC, Shtoyerman E, Katz LC (2004) High-resolution in vivo imaging of hippocampal dendrites and spines. J Neurosci 24:3147-3151.
38. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
39. Morgan SL, Teyler TJ (2001) Epileptic-like activity induces multiple forms of plasticity in hippocampal area CA1. Brain Res 917:90-96.
40. Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C (2003) Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773-786.
41. Muller D, Joly M, Lynch G (1988) Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242:1694-1697.
42. Nevander G, Ingvar M, Auer R, Siesjo BK (1985) Status epilepticus in well-oxygenated rats causes neuronal necrosis. Ann Neurol 18:281-290.
43. Okamoto K, Nagai T, Miyawaki A, Hayashi Y (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
44. Ostroff LE, Fiala JC, Allwardt B, Harris KM (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535-545.
45. Otmakhov N, Khibnik L, Otmakhova N, Carpenter S, Riahi S, Asrican B, Lisman J (2004) Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91:1955-1962.
46. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
47. Passafaro M, Piech V, Sheng M (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4:917-926.
48. Passafaro M, Nakagawa T, Sala C, Sheng M (2003) Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature 424:677-681.
49. Perez-Otano I, Ehlers MD (2004) Learning from NMDA receptor trafficking: clues to the development and maturation of glutamatergic synapses. Neurosignals 13:175-189.
50. Petralia RS, Wenthold RJ (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318:329-354.
51. Quinlan EM, Olstein DH, Bear MF (1999) Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc Natl Acad Sci USA 96:12876-12880.
52. Quinlan EM, Lebel D, Brosh I, Barkai E (2004) A molecular mechanism for stabilization of learning-induced synaptic modifications. Neuron 41:185-192.
53. Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P (2000) NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20:2512-2522.
54. Rensing N, Ouyang Y, Yang XF, Yamada KA, Rothman SM, Wong M (2005) In vivo imaging of dendritic spines during electrographic seizures. Ann Neurol 58:888-898.
55. Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83-88.
56. Sankaranarayanan SDAD, Rothman JE, Ryan TA (2000) The use of pHluorins for optical measurements of presynaptic activity. Biophys J 79:2199-2208.
57. Sheng M, Kim MJ (2002) Postsynaptic signaling and plasticity mechanisms. Science 298:776-780.
58. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147.
59. 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.
60. 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.
61. Song I, Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25:578-588.
62. Sorra KE, Harris KM (1998) Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J Neurosci 18:658-671.
63. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
64. Swann JW, Al-Noori S, Jiang M, Lee CL (2000) Spine loss and other dendritic abnormalities in epilepsy. Hippocampus 10:617-625.
65. Takahashi T, Svoboda K, Malinow R (2003) Experience strengthening transmission by driving AMPA receptors into synapses. Science 299:1585-1588.
66. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
67. Tonegawa S, Nakazawa K, Wilson MA (2003) Genetic neuroscience of mammalian learning and memory. Philos Trans R Soc Lond B Biol Sci 358:787-795.
68. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402:421-425.
69. Traub RD, Wong RK (1982) Cellular mechanism of neuronal synchronization in epilepsy. Science 216:745-747.
70. Wenthold RJ, Petralia RS, Blahos Jr J, Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16:1982-1989.
71. 2+. J Physiol (Lond) 506:13-32.
72. Wong M (2005) Modulation of dendritic spines in epilepsy: Cellular mechanisms and functional implications. Epilepsy Behav 7:569-577.
73. Zador A, Koch C, Brown TH (1990) Biophysical model of a Hebbian synapse. Proc Natl Acad Sci USA 87:6718-6722.
74. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T, Worley P, Lubke J, Frotscher M, Kelly PH, Sommer B, Andersen P, Seeburg PH, Sakmann B (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284:1805-1811.