Recruitment of resting vesicles into recycling pools supports NMDA receptor-dependent synaptic potentiation in cultured hippocampal neurons

Journal of Physiology

Volumn 590, Issue 7, 2012, Pages 1585-1597

  Ratnayaka, Arjuna ^a   Marra, Vincenzo ^a   Bush, Daniel ^a   Burden, Jemima J ^b   Branco, Tiago ^b,c   Staras, Kevin ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE IMAGING; HEBBIAN PLASTICITY; HIPPOCAMPUS; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; RECYCLING POOL; RESTING VESICLE; SYNAPSE POTENTIATION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; SYNAPTOSOME; ULTRASTRUCTURE;

ANIMALS; CALCINEURIN; ENZYME INHIBITORS; HIPPOCAMPUS; NEURONS; NITRIC OXIDE SYNTHASE; NITROARGININE; PRESYNAPTIC TERMINALS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TACROLIMUS;

EID: 84859227369     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.226688     Document Type: Article

References (61)

1. Akbergenova Y & Bykhovskaia M (2009). Stimulation-induced formation of the reserve pool of vesicles in Drosophila motor boutons. J Neurophysiol 101, 2423-2433.
2. 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.
3. Antonova I, Lu FM, Zablow L, Udo H & Hawkins RD (2009). Rapid and long-lasting increase in sites for synapse assembly during late-phase potentiation in rat hippocampal neurons. PLoS One 4, e7690.
4. Betz WJ & Bewick GS (1992). Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255, 200-203.
5. 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.
6. Branco T, Marra V & Staras K (2010). Examining size-strength relationships at hippocampal synapses using an ultrastructural measurement of synaptic release probability. J Struct Biol 172, 203-210.
7. Branco T & Staras K (2009). The probability of neurotransmitter release: variability and feedback control at single synapses. Nat Rev Neurosci 10, 373-383.
8. Branco T, Staras K, Darcy KJ & Goda Y (2008). Local dendritic activity sets release probability at hippocampal synapses. Neuron 59, 475-485.
9. Chen X, Barg S & Almers W (2008). Release of the styryl dyes from single synaptic vesicles in hippocampal neurons. J Neurosci 28, 1894-1903.
10. Cousin MA & Evans GJ (2011). Activation of silent and weak synapses by cAMP-dependent protein kinase in cultured cerebellar granule neurons. J Physiol 589, 1943-1955.
11. Darcy KJ, Staras K, Collinson LM & Goda Y (2006a). Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 9, 315-321.
12. Darcy KJ, Staras K, Collinson LM & Goda Y (2006b). An ultrastructural readout of fluorescence recovery after photobleaching using correlative light and electron microscopy. Nat Protoc 1, 988-994.
13. Fernandez-Alfonso T & Ryan TA (2006). The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol 16, 413-420.
14. Fernandez-Alfonso T & Ryan TA (2008). A heterogeneous 'resting' pool of synaptic vesicles that is dynamically interchanged across boutons in mammalian CNS synapses. Brain Cell Biol. 36, 87-100.
15. Fisher-Lavie A, Zeidan A, Stern M, Garner CC & Ziv NE (2011). Use dependence of presynaptic tenacity. J Neurosci 31, 16770-16780.
16. Fredj NB & Burrone J (2009). A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci 12, 751-758.
17. Granseth B, Odermatt B, Royle SJ & Lagnado L (2006). Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51, 773-786.
18. Groemer TW & Klingauf J (2007). Synaptic vesicles recycle spontaneously and during activity belong to the same vesicle pool. Nat Neurosci 10, 145-147.
19. Harata N, Pyle JL, Aravanis AM, Mozhayeva M, Kavalali ET & Tsien RW (2001a). Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling. Trends Neurosci 24, 637-643.
20. Harata N, Ryan TA, Smith SJ, Buchanan J & Tsien RW (2001b). Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1-43 photoconversion. Proc Natl Acad Sci U S A 98, 12748-12753.
21. Herzog E, Nadrigny F, Silm K, Biesemann C, Helling I, Bersot T, Steffens H, Schwartzmann R, Nagerl UV, El Mestikawy S, Rhee J, Kirchhoff F & Brose N (2011). In vivo imaging of intersynaptic vesicle exchange using VGLUT1 Venus knock-in mice. J Neurosci 31, 15544-15559.
22. Hua Y, Sinha R, Martineau M, Kahms M & Klingauf J (2010). A common origin of synaptic vesicles undergoing evoked and spontaneous fusion. Nat Neurosci 13, 1451-1453.
23. Ikeda K & Bekkers JM (2009). Counting the number of releasable synaptic vesicles in a presynaptic terminal. Proc Natl Acad Sci U S A 106, 2945-2950.
24. Kim SH & Ryan TA (2010). CDK5 serves as a major control point in neurotransmitter release. Neuron 67, 797-809.
25. Krueger SR, Kolar A & Fitzsimonds RM (2003). The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40, 945-957.
26. Kumashiro S, Lu YF, Tomizawa K, Matsushita M, Wei FY & Matsui H (2005). Regulation of synaptic vesicle recycling by calcineurin in different vesicle pools. Neurosci Res 51, 435-443.
27. Kuromi H & Kidokoro Y (2000). Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 27, 133-143.
28. Li Z, Burrone J, Tyler WJ, Hartman KN, Albeanu DF & Murthy VN (2005). Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc Natl Acad Sci U S A 102, 6131-6136.
29. 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.
30. Malgaroli A, Ting AE, Wendland B, Bergamaschi A, Villa A, Tsien RW & Scheller RH (1995). Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268, 1624-1628.
31. Micheva KD & Smith SJ (2005). Strong effects of subphysiological temperature on the function and plasticity of mammalian presynaptic terminals. J Neurosci 25, 7481-7488.
32. 2+-dependent adenylyl cyclases in recovery from adaptive presynaptic silencing. J Neurosci 28, 5159-5168.
33. Murthy VN, Schikorski T, Stevens CF & Zhu Y (2001). Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32, 673-682.
34. Murthy VN, Sejnowski TJ & Stevens CF (1997). Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18, 599-612.
35. Ninan I & Arancio O (2004). Presynaptic CaMKII is necessary for synaptic plasticity in cultured hippocampal neurons. Neuron 42, 129-141.
36. Ninan I, Liu S, Rabinowitz D & Arancio O (2006). Early presynaptic changes during plasticity in cultured hippocampal neurons. EMBO J 25, 4361-4371.
37. Ostroff LE, Cain CK, Jindal N, Dar N & Ledoux JE (2011). Stability of presynaptic vesicle pools and changes in synapse morphology in the amygdala following fear learning in adult rats. J Comp Neurol 520, 295-314.
38. Pechstein A & Shupliakov O (2010). Taking a back seat: synaptic vesicle clustering in presynaptic terminals. Front Synaptic Neurosci 2, 143.
39. Ratnayaka A, Marra V, Branco T & Staras K (2011). Extrasynaptic vesicle recycling in mature hippocampal neurons. Nat Comms 2, 531.
40. Rizzoli SO & Betz WJ (2004). The structural organization of the readily releasable pool of synaptic vesicles. Science 303, 2037-2039.
41. Rizzoli SO & Betz WJ (2005). Synaptic vesicle pools. Nat Rev Neurosci 6, 57-69.
42. Ryan TA, Reuter H & Smith SJ (1997). Optical detection of a quantal presynaptic membrane turnover. Nature 388, 478-482.
43. Ryan TA, Reuter H, Wendland B, Schweizer FE, Tsien RW & Smith SJ (1993). The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713-724.
44. Ryan TA & Smith SJ (1995). Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14, 983-989.
45. Ryan TA, Ziv NE & Smith SJ (1996). Potentiation of evoked vesicle turnover at individually resolved synaptic boutons. Neuron 17, 125-134.
46. Sankaranarayanan S & Ryan TA (2001). Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 4, 129-136.
47. Sara Y, Virmani T, Deak F, Liu X & Kavalali ET (2005). An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45, 563-573.
48. Schikorski T & Stevens CF (2001). Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4, 391-395.
49. Schweizer FE & Ryan TA (2006). The synaptic vesicle: cycle of exocytosis and endocytosis. Curr Opin Neurobiol 16, 298-304.
50. 2+ flux during uncorrelated activity. Neuron 44, 835-849.
51. Staras K (2007). Share and share alike: trading of presynaptic elements between central synapses. Trends Neurosci 30, 292-298.
52. Staras K & Branco T (2010). Sharing vesicles between central presynaptic terminals: implications for synaptic function. Front Synaptic Neurosci 2, 20.
53. Staras K, Branco T, Burden JJ, Pozo K, Darcy KJ, Marra V, Ratnayaka A & Goda Y (2010). A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron 66, 37-44.
54. Sudhof TC (2004). The synaptic vesicle cycle. Annu Rev Neurosci 27, 509-547.
55. Thiagarajan TC, Lindskog M & Tsien RW (2005). Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47, 725-737.
56. Tyler WJ, Zhang XL, Hartman K, Winterer J, Muller W, Stanton PK & Pozzo-Miller L (2006). BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses. J Physiol 574, 787-803.
57. 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.
58. Welzel O, Henkel AW, Stroebel AM, Jung J, Tischbirek CH, Ebert K, Kornhuber J, Rizzoli SO & Groemer TW (2011). Systematic heterogeneity of fractional vesicle pool sizes and release rates of hippocampal synapses. Biophys J 100, 593-601.
59. Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R & Hell SW (2008). Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320, 246-249.
60. Wilhelm BG, Groemer TW & Rizzoli SO (2010). The same synaptic vesicles drive active and spontaneous release. Nat Neurosci 13, 1454-1456.
61. Zakharenko SS, Zablow L & Siegelbaum SA (2001). Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci 4, 711-717.