 |
Previous Article | Next Article 
The Journal of Neuroscience, February 1, 2002, 22(3):654-665
Development of Vesicle Pools during Maturation of Hippocampal
Synapses
Marina G.
Mozhayeva,
Yildirim
Sara,
Xinran
Liu, and
Ege T.
Kavalali
Center for Basic Neuroscience and Department of Physiology,
University of Texas Southwestern Medical Center, Dallas, Texas
75390-9111
We studied the emergence of vesicle pool organization at developing
hippocampal synapses by monitoring vesicle recycling and neurotransmitter release as well as examining electron micrographs. Our
analysis suggests that presynaptic boutons go through three distinct
functional states to mature. At the onset the synapses lack readily
releasable vesicles although they possess a pool of recycling vesicles
that can release neurotransmitters under strong stimulation. In the
next stage the majority of these recycling vesicles switches to a
functionally docked state and forms the readily releasable pool (RRP).
After assembly of the RRP, new vesicles build the reserve pool. At the
mature state the size of the RRP increases linearly with increasing
recycling pool size. Furthermore, this preferential filling of the RRP
during early synapse maturation is reduced strikingly in
synapses deficient in synapsin I and II. Taken together, these results
expose a mechanism that ensures functionally effective allocation of a
limited number of vesicles in a CNS synapse.
Key words:
synapse maturation; readily releasable pool; synapsins; FM1-43; patch clamp; hippocampal culture
Copyright © 2002 Society for Neuroscience 0270-6474/02/223654-12$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
C. Chung, F. Deak, and E. T. Kavalali
Molecular Substrates Mediating Lanthanide-Evoked Neurotransmitter Release in Central Synapses
J Neurophysiol,
October 1, 2008;
100(4):
2089 - 2100.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. L. Coleman, C. A. Bill, F. Simsek-Duran, G. Lonart, D. Samigullin, and M. Bykhovskaia
Synapsin II and calcium regulate vesicle docking and the cross-talk between vesicle pools at the mouse motor terminals
J. Physiol.,
October 1, 2008;
586(19):
4649 - 4673.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Corradi, A. Zanardi, C. Giacomini, F. Onofri, F. Valtorta, M. Zoli, and F. Benfenati
Synapsin-I- and synapsin-II-null mice display an increased age-dependent cognitive impairment
J. Cell Sci.,
September 15, 2008;
121(18):
3042 - 3051.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Leal-Ortiz, C. L. Waites, R. Terry-Lorenzo, P. Zamorano, E. D. Gundelfinger, and C. C. Garner
Piccolo modulation of Synapsin1a dynamics regulates synaptic vesicle exocytosis
J. Cell Biol.,
May 28, 2008;
181(5):
831 - 846.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Busetto, M. J. Higley, and B. L. Sabatini
Developmental presence and disappearance of postsynaptically silent synapses on dendritic spines of rat layer 2/3 pyramidal neurons
J. Physiol.,
March 15, 2008;
586(6):
1519 - 1527.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. D. Nelson, E. T. Kavalali, and L. M. Monteggia
Activity-Dependent Suppression of Miniature Neurotransmission through the Regulation of DNA Methylation
J. Neurosci.,
January 9, 2008;
28(2):
395 - 406.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. T. Kavalali
Multiple vesicle recycling pathways in central synapses and their impact on neurotransmission
J. Physiol.,
December 15, 2007;
585(3):
669 - 679.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Baldelli, A. Fassio, F. Valtorta, and F. Benfenati
Lack of Synapsin I Reduces the Readily Releasable Pool of Synaptic Vesicles at Central Inhibitory Synapses
J. Neurosci.,
December 5, 2007;
27(49):
13520 - 13531.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Moulder, X. Jiang, A. A. Taylor, W. Shin, K. D. Gillis, and S. Mennerick
Vesicle Pool Heterogeneity at Hippocampal Glutamate and GABA Synapses
J. Neurosci.,
September 12, 2007;
27(37):
9846 - 9854.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Delgado-Martinez, R. B. Nehring, and J. B. Sorensen
Differential Abilities of SNAP-25 Homologs to Support Neuronal Function
J. Neurosci.,
August 29, 2007;
27(35):
9380 - 9391.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Bronk, F. Deak, M. C. Wilson, X. Liu, T. C. Sudhof, and E. T. Kavalali
Differential Effects of SNAP-25 Deletion on Ca2+-Dependent and Ca2+-Independent Neurotransmission
J Neurophysiol,
August 1, 2007;
98(2):
794 - 806.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. F. G. Toonen, K. Wierda, M. S. Sons, H. de Wit, L. N. Cornelisse, A. Brussaard, J. J. Plomp, and M. Verhage
Munc18-1 expression levels control synapse recovery by regulating readily releasable pool size
PNAS,
November 28, 2006;
103(48):
18332 - 18337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Huang, K. Shimazu, N. H. Woo, K. Zang, U. Muller, B. Lu, and L. F. Reichardt
Distinct Roles of the beta1-Class Integrins at the Developing and the Mature Hippocampal Excitatory Synapse
J. Neurosci.,
October 25, 2006;
26(43):
11208 - 11219.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Mahgoub, Y. Sara, E. T. Kavalali, and L. M. Monteggia
Reciprocal Interaction of Serotonin and Neuronal Activity in Regulation of cAMP-Responsive Element-Dependent Gene Expression
J. Pharmacol. Exp. Ther.,
April 1, 2006;
317(1):
88 - 96.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Virmani, D. Atasoy, and E. T. Kavalali
Synaptic vesicle recycling adapts to chronic changes in activity.
J. Neurosci.,
February 22, 2006;
26(8):
2197 - 2206.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Sun, P. Bronk, X. Liu, W. Han, and T. C. Sudhof
Synapsins regulate use-dependent synaptic plasticity in the calyx of Held by a Ca2+/calmodulin-dependent pathway
PNAS,
February 21, 2006;
103(8):
2880 - 2885.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Moulder and S. Mennerick
Synaptic vesicles: turning reluctance into action.
Neuroscientist,
February 1, 2006;
12(1):
11 - 15.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Virmani, M. Ertunc, Y. Sara, M. Mozhayeva, and E. T. Kavalali
Phorbol Esters Target the Activity-Dependent Recycling Pool and Spare Spontaneous Vesicle Recycling
J. Neurosci.,
November 23, 2005;
25(47):
10922 - 10929.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Moulder and S. Mennerick
Reluctant Vesicles Contribute to the Total Readily Releasable Pool in Glutamatergic Hippocampal Neurons
J. Neurosci.,
April 13, 2005;
25(15):
3842 - 3850.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Sara, T. Biederer, D. Atasoy, A. Chubykin, M. G. Mozhayeva, T. C. Sudhof, and E. T. Kavalali
Selective Capability of SynCAM and Neuroligin for Functional Synapse Assembly
J. Neurosci.,
January 5, 2005;
25(1):
260 - 270.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Chandra, F. Fornai, H.-B. Kwon, U. Yazdani, D. Atasoy, X. Liu, R. E. Hammer, G. Battaglia, D. C. German, P. E. Castillo, et al.
Double-knockout mice for {alpha}- and {beta}-synucleins: Effect on synaptic functions
PNAS,
October 12, 2004;
101(41):
14966 - 14971.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Rohrbough, E. Rushton, L. Palanker, E. Woodruff, H. J. G. Matthies, U. Acharya, J. K. Acharya, and K. Broadie
Ceramidase Regulates Synaptic Vesicle Exocytosis and Trafficking
J. Neurosci.,
September 8, 2004;
24(36):
7789 - 7803.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Palmer, J. T. R. Isaac, and G. L. Collingridge
Multiple, Developmentally Regulated Expression Mechanisms of Long-Term Potentiation at CA1 Synapses
J. Neurosci.,
May 26, 2004;
24(21):
4903 - 4911.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. G. Mozhayeva, M. F. Matos, X. Liu, and E. T. Kavalali
Minimum Essential Factors Required for Vesicle Mobilization at Hippocampal Synapses
J. Neurosci.,
February 18, 2004;
24(7):
1680 - 1688.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Cousin, C. S. Malladi, T. C. Tan, C. R. Raymond, K. J. Smillie, and P. J. Robinson
Synapsin I-associated Phosphatidylinositol 3-Kinase Mediates Synaptic Vesicle Delivery to the Readily Releasable Pool
J. Biol. Chem.,
August 1, 2003;
278(31):
29065 - 29071.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Li and R. E. Burke
Developmental Changes in Short-Term Synaptic Depression in the Neonatal Mouse Spinal Cord
J Neurophysiol,
December 1, 2002;
88(6):
3218 - 3231.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Kirischuk and R. Grantyn
Inter-Bouton Variability of Synaptic Strength Correlates With Heterogeneity of Presynaptic Ca2+ Signals
J Neurophysiol,
October 1, 2002;
88(4):
2172 - 2176.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Biederer, Y. Sara, M. Mozhayeva, D. Atasoy, X. Liu, E. T. Kavalali, and T. C. Sudhof
SynCAM, a Synaptic Adhesion Molecule That Drives Synapse Assembly
Science,
August 30, 2002;
297(5586):
1525 - 1531.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Sara, M. G. Mozhayeva, X. Liu, and E. T. Kavalali
Fast Vesicle Recycling Supports Neurotransmission during Sustained Stimulation at Hippocampal Synapses
J. Neurosci.,
March 1, 2002;
22(5):
1608 - 1617.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|