Early presynaptic changes during plasticity in cultured hippocampal neurons

EMBO Journal

Volumn 25, Issue 18, 2006, Pages 4361-4371

  Ninan, Ipe ^a   Liu, Shumin ^a   Rabinowitz, Daniel ^a   Arancio, Ottavio ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Cultures; Plasticity; Synapse; Terminal

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; GREEN FLUORESCENT PROTEIN; MOLECULAR MARKER; SYNAPTOBREVIN 2;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FLUORESCENCE; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; STAINING; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; CELLS, CULTURED; ELECTRIC STIMULATION; EVOKED POTENTIALS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MICE; NEURONAL PLASTICITY; NEURONS; PRESYNAPTIC TERMINALS; RECEPTORS, AMPA; RECOMBINANT FUSION PROTEINS; TRANSFECTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 33748932135     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601318     Document Type: Article

References (45)

1. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3: 445-451
2. Allen C, Stevens CF (1994) An evaluation of causes for unreliability of synaptic transmission. Proc Natl Acad Sci USA 91: 10380-10383
3. Antonova I, Arancio O, Trillat AC, Wang HG, Zablow L, Udo H, Kandel ER, Hawkins RD (2001) Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294: 1547-1550
4. Arancio O, Kandel ER, Hawkins RD (1995) Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons. Nature 376: 74-80
5. Benke TA, Luthi A, Isaac JT, Collingridge GL (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393: 793-797
6. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18: 10464-10472
7. Buchs PA, Muller D (1996) Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc Natl Acad Sci USA 93: 8040-8045
8. Carroll RC, Lissin DV, von Zastrow M, Nicoll RA, Malenka RC (1999) Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat Neurosci 2: 454-460
9. Choi S, Klingauf J, Tsien RW (2000) Postfusional regulation of cleft glutamate concentration during LTP at 'silent synapses'. Nat Neurosci 3: 330-336
10. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008
11. East SJ, Garthwaite J (1991) NMDA receptor activation in rat hippocampus induces cyclic GMP formation through the L-arginine-nitric oxide pathway. Neurosci Lett 123: 17-19
12. Emptage NJ, Reid CA, Fine A, Bliss TV (2003) Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron 38: 797-804
13. 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
14. Hessler NA, Shirke AM, Malinow R (1993) The probability of transmitter release at a mammalian central synapse. Nature 366: 569-572
15. Humeau Y, Shaban H, Bissiere S, Luthi A (2003) Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain. Nature 426: 841-845
16. Kase H (1988) New inhibitors of protein kinases from microbial source. In Proceedings of Seventh International Symposium on Biology of Actinomycetes, Okami Y, Beppu T, Ogawara H (eds) pp 159-164. Tokyo: Japan Scientific Societies Press
17. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375: 400-404
18. Lissin DV, Carroll RC, Nicoll RA, Malenka RC, von Zastrow M (1999) Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J Neurosci 19: 1263-1272
19. Liu G, Choi S, Tsien RW (1999) Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22: 395-409
20. Liu G, Tsien RW (1995) Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375: 404-408
21. Liu S, Ninan I, Antonova I, Battaglia F, Trinchese F, Narasanna A, Kolodilov N, Dauer W, Hawkins RD, Arancio O (2004) alpha-Synuclein produces a long-lasting increase in neurotransmitter release. EMBO J 23: 4506-4516
22. 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
23. Ma L, Zablow L, Kandel ER, Siegelbaum SA (1999) Cyclic AMP induces functional presynaptic boutons in hippocampal CA3-CA1 neuronal cultures. Nat Neurosci 2: 24-30
24. Malgaroli A, Tsien RW (1992) Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature 357: 134-139
25. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-766
26. Murthy VN, Stevens CF (1998) Synaptic vesicles retain their identity through the endocytic cycle. Nature 392: 497-501
27. Neuhoff H, Roeper J, Schweizer M (1999) Activity-dependent formation of perforated synapses in cultured hippocampal neurons. Eur J Neurosci 11: 4241-4250
28. Ninan I, Arancio O (2004) Presynaptic CaMKII is necessary for synaptic plasticity in cultured hippocampal neurons. Neuron 42: 129-141
29. Ninan I, Liu S, Arancio O (2005) Tetanus-induced presynaptic remodeling in cultured hippocampal neurons. Soc Neurosci Abstracts, Washington, p 2005 2610.2012
30. Palmer MJ, Isaac JT, Collingridge GL (2004) Multiple, developmentally regulated expression mechanisms of long-term potentiation at CA1 synapses. J Neurosci 24: 4903-4911
31. Pickard L, Noel J, Duckworth JK, Fitzjohn SM, Henley JM, Collingridge GL, Molnar E (2001) Transient synaptic activation of NMDA receptors leads to the insertion of native AMPA receptors at hippocampal neuronal plasma membranes. Neuropharmacology 41: 700-713
32. Reid CA, Dixon DB, Takahashi M, Bliss TV, Fine A (2004) Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses. J Neurosci 24: 3618-3626
33. Renger JJ, Egles C, Liu G (2001) A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron 29: 469-484
34. Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262: 754-757
35. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207
36. Ryan TA, Ziv NE, Smith SJ (1996) Potentiation of evoked vesicle turnover at individually resolved synaptic boutons. Neuron 17: 125-134
37. Sampo B, Kaech S, Kunz S, Banker G (2003) Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37: 611-624
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. 2+ flux during uncorrelated activity. Neuron 44: 835-849
40. Stevens CF, Sullivan JM (1998) Regulation of the readily releasable vesicle pool by protein kinase C. Neuron 21: 885-893
41. Stewart MG, Medvedev NI, Popov VI, Schoepfer R, Davies HA, Murphy K, Dallerac GM, Kraev IV, Rodriguez JJ (2005) Chemically induced long-term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices. Eur J Neurosci 21: 3368-3378
42. 2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem Biophys Res Commun 181: 968-975
43. 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
44. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D (2001) Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 21: 6245-6251
45. Wang HG, Lu FM, Jin I, Udo H, Kandel ER, de Vente J, Walter U, Lohmann SM, Hawkins RD, Antonova I (2005) Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 45: 389-403