 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 6, 412-423, Copyright © 1986 by Society for Neuroscience
Protein-synthetic machinery at postsynaptic sites during synaptogenesis: a quantitative study of the association between polyribosomes and developing synapses
O Steward and PM Falk
Previous studies have revealed dramatic accumulations of polyribosomes
under growing spine synapses, suggesting a critical role for protein
synthesis at the postsynaptic site during synaptogenesis. The present study
quantitatively analyzes the distribution of polyribosomes under synapses
during developmental synaptogenesis in the rat's dentate gyrus. The middle
molecular layer of the suprapyramidal blade of the dentate gyrus was
examined electron-microscopically at 1, 4, 7, 10, 15, 20, and 28 d of age.
At each age, we evaluated (1) synapse density (the number of synapses/100
micron2 of neuropil), (2) the width of the molecular layer, (3) the
proportion of spine synapses with underlying polyribosomes, and (4) the
number of polyribosome-containing synapses/1000 micron2 of neuropil. From
the first two measures, an estimate was obtained of the total extent of
synaptogenesis, taking into account both the increase in synapse density
and the increase in total area of neuropil. At 1 d of age, very few
synapses were found in the molecular layer of the dentate gyrus, and those
that were present were quite immature in appearance. Synapse density
increased about 140- fold between 1 and 28 d of age, from an average of
0.36 synapses/100 micron2 at 1 d of age to 49 synapses/100 micron2 at 28 d
of age. An inverse relationship was found between synapse density and the
proportion of synapses with polyribosomes. Between 1 and 7 d of age, about
60% of the spine synapses had one or more polyribosomes under the spine
base. Thereafter, the proportion of spines with polyribosomes decreased as
synapse density increased. Similarly, the proportion of shaft synapses with
underlying polyribosomes was greatest between 1 and 7 d postnatal, and
decreased thereafter. While the proportion of synapses with polyribosomes
was greatest between 1 and 7 d, the actual number of
polyribosome-containing synapses/1000 micron2 of neuropil was negligible at
1 d, increased to a peak at 7 d of age, and then decreased as synapse
density increased. Qualitatively, the most dramatic accumulations of
polyribosomes were also found at 7 d of age. We conclude that
spine-associated polyribosomes represent a structural specialization of
dendrites at sites of synapse construction and as such may represent a
marker for growing synapses. We propose that these elements produce
protein(s) that are critically involved in the formation of the synaptic
contact.
This article has been cited by other articles:
|
|
|
|
 
J. Aoto, P. Ting, B. Maghsoodi, N. Xu, M. Henkemeyer, and L. Chen
Postsynaptic EphrinB3 Promotes Shaft Glutamatergic Synapse Formation
J. Neurosci.,
July 11, 2007;
27(28):
7508 - 7519.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. W. Grossman, G. M. Aldridge, I. J. Weiler, and W. T. Greenough
Local Protein Synthesis and Spine Morphogenesis: Fragile X Syndrome and Beyond
J. Neurosci.,
July 5, 2006;
26(27):
7151 - 7155.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. J. Weiler, C. C. Spangler, A. Y. Klintsova, A. W. Grossman, S. H. Kim, V. Bertaina-Anglade, H. Khaliq, F. E. de Vries, F. A. E. Lambers, F. Hatia, et al.
From the Cover: Fragile X mental retardation protein is necessary for neurotransmitter-activated protein translation at synapses
PNAS,
December 14, 2004;
101(50):
17504 - 17509.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Wang and H. Tiedge
Translational Control at the Synapse
Neuroscientist,
October 1, 2004;
10(5):
456 - 466.
[Abstract]
[PDF]
|
|
|
|
|
|
|
J. M. Alarcon, R. Hodgman, M. Theis, Y.-S. Huang, E. R. Kandel, and J. D. Richter
Selective Modulation of Some Forms of Schaffer Collateral-CA1 Synaptic Plasticity in Mice With a Disruption of the CPEB-1 Gene
Learn. Mem.,
May 1, 2004;
11(3):
318 - 327.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Wang, L. Ku, D. J. Osterhout, W. Li, A. Ahmadian, Z. Liang, and Y. Feng
Developmentally-programmed FMRP expression in oligodendrocytes: a potential role of FMRP in regulating translation in oligodendroglia progenitors
Hum. Mol. Genet.,
January 1, 2004;
13(1):
79 - 89.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. H. Woo and P. V. Nguyen
Protein Synthesis Is Required for Synaptic Immunity to Depotentiation
J. Neurosci.,
February 15, 2003;
23(4):
1125 - 1132.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. T. Greenough, A. Y. Klintsova, S. A. Irwin, R. Galvez, K. E. Bates, and I. J. Weiler
Synaptic regulation of protein synthesis and the fragile X protein
PNAS,
June 19, 2001;
98(13):
7101 - 7106.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. S. Moon, I. S. Park, L. T. Schenker, M. B. Kennedy, J.-I. Moon, and I. Jin
Presence of both Constitutive and Inducible Forms of Heat Shock Protein 70 in the Cerebral Cortex and Hippocampal Synapses
Cereb Cortex,
March 1, 2001;
11(3):
238 - 248.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. R. O'Kusky, P. Ye, and A. J. D'Ercole
Insulin-Like Growth Factor-I Promotes Neurogenesis and Synaptogenesis in the Hippocampal Dentate Gyrus during Postnatal Development
J. Neurosci.,
November 15, 2000;
20(22):
8435 - 8442.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Ganesh, K. L. Agarwala, K. Ueda, T. Akagi, K. Shoda, T. Usui, T. Hashikawa, H. Osada, A. V. Delgado-Escueta, and K. Yamakawa
Laforin, defective in the progressive myoclonus epilepsy of Lafora type, is a dual-specificity phosphatase associated with polyribosomes
Hum. Mol. Genet.,
September 1, 2000;
9(15):
2251 - 2261.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Jin and S. T. Warren
Understanding the molecular basis of fragile X syndrome
Hum. Mol. Genet.,
April 1, 2000;
9(6):
901 - 908.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. A. Muslimov, G. Banker, J. Brosius, and H. Tiedge
Activity-dependent Regulation of Dendritic BC1 RNA in Hippocampal Neurons in Culture
J. Cell Biol.,
June 29, 1998;
141(7):
1601 - 1611.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. B. Knowles and K. S. Kosik
Neurotrophin-3 signals redistribute RNA in neurons
PNAS,
December 23, 1997;
94(26):
14804 - 14808.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Wu, C. Aoki, A. Elste, A. A. Rogalski-Wilk, and P. Siekevitz
The synthesis of ATP by glycolytic enzymes in the postsynaptic density and the effect of endogenously generated nitric oxide
PNAS,
November 25, 1997;
94(24):
13273 - 13278.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z.-P. Feng, J. Klumperman, K. Lukowiak, and N. I. Syed
In Vitro Synaptogenesis between the Somata of Identified Lymnaea Neurons Requires Protein Synthesis But Not Extrinsic Growth Factors or Substrate Adhesion Molecules
J. Neurosci.,
October 15, 1997;
17(20):
7839 - 7849.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. J. Weiler, S. A. Irwin, A. Y. Klintsova, C. M. Spencer, A. D. Brazelton, K. Miyashiro, T. A. Comery, B. Patel, J. Eberwine, and W. T. Greenough
Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation
PNAS,
May 13, 1997;
94(10):
5395 - 5400.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Feng, C.-A. Gutekunst, D. E. Eberhart, H. Yi, S. T. Warren, and S. M. Hersch
Fragile X Mental Retardation Protein: Nucleocytoplasmic Shuttling and Association with Somatodendritic Ribosomes
J. Neurosci.,
March 1, 1997;
17(5):
1539 - 1547.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. G. J. M. VanderHorst and G. Holstege
Estrogen Induces Axonal Outgrowth in the Nucleus Retroambiguus-Lumbosacral Motoneuronal Pathway in the Adult Female Cat
J. Neurosci.,
February 1, 1997;
17(3):
1122 - 1136.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. B. Knowles, J. H. Sabry, M. E. Martone, T. J. Deerinck, M. H. Ellisman, G. J. Bassell, and K. S. Kosik
Translocation of RNA Granules in Living Neurons
J. Neurosci.,
December 15, 1996;
16(24):
7812 - 7820.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. E. Martone, J. A. Pollock, Y. Z. Jones, and M. H. Ellisman
Ultrastructural Localization of Dendritic Messenger RNA in Adult Rat Hippocampus
J. Neurosci.,
December 1, 1996;
16(23):
7437 - 7446.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Tiedge and J. Brosius
Translational Machinery in Dendrites of Hippocampal Neurons in Culture
J. Neurosci.,
November 15, 1996;
16(22):
7171 - 7181.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Eberwine, P. Crino, and M. Dichter
Review : Single-Cell mRNA Amplification: Implications for Basic and Clinical Neuroscience
Neuroscientist,
July 1, 1995;
1(4):
200 - 211.
[Abstract]
[PDF]
|
|
|
|
|
|
|
C. Bagni, L. Mannucci, C. G. Dotti, and F. Amaldi
Chemical Stimulation of Synaptosomes Modulates alpha -Ca2+/Calmodulin-Dependent Protein Kinase II mRNA Association to Polysomes
J. Neurosci.,
May 15, 2000;
20(10):
RC76 - RC76.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
