Dynamics of synapsin I gene expression during the establishment and restoration of functional synapses in the rat hippocampus

Synapse development and injury-induced reorganization have been extensively characterized morphologically, yet relatively little is known about the underlying molecular and biochemical events. To examine molecular mechanisms of synaptic development and rearrangement, we looked at the developmental p...

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Published inNeuroscience Vol. 58; no. 4; pp. 683 - 703
Main Authors Melloni, R.H., Apostolides, P.J., Hamos, J.E., DeGennaro, L.J.
Format Journal Article
LanguageEnglish
Published Oxford Elsevier Ltd 01.02.1994
Elsevier
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Abstract Synapse development and injury-induced reorganization have been extensively characterized morphologically, yet relatively little is known about the underlying molecular and biochemical events. To examine molecular mechanisms of synaptic development and rearrangement, we looked at the developmental pattern of expression of the neuron-specific gene synapsin I in granule cell neurons of the dentate gyrus and their accompanying mossy fibers during the main period of synaptogenic differentiation in the rat hippocampus. We found a significant difference between the temporal expression of synapsin I messenger RNA in dentate granule somata and the appearence of protein in their mossy fiber terminals during the postnatal development of these neurons. Next, to investigate the regulation of neuron-specific gene expression during the restoration of synaptic contacts in the central nervous system, we examined the expression of the synapsin I gene following lesions of hippocampal circuitry. These studies show marked changes in the pattern and intensity of synapsin I immunoreactivity in the dendritic fields of dentate granule cell neurons following perforant pathway transection. In contrast, changes in synapsin I messenger RNA expression in target neurons, and in those neurons responsible for the reinnervation of this region of the hippocampus, were not found to accompany new synapse formation. On a molecular level, both developmental and lesion data suggest that the expression of the synapsin I gene is tightly regulated in the central nervous system, and that considerable changes in synapsin I protein may occur in neurons without concomitant changes in the levels of its messenger RNA. Finally, our results suggest that the appearance of detectable levels of synapsin I protein in developing and sprouting synapses coincides with the acquisition of function by those central synapses.
AbstractList Synapse development and injury-induced reorganization have been extensively characterized morphologically, yet relatively little is known about the underlying molecular and biochemical events. To examine molecular mechanisms of synaptic development and rearrangement, we looked at the developmental pattern of expression of the neuron-specific gene synapsin I in granule cell neurons of the dentate gyrus and their accompanying mossy fibers during the main period of synaptogenic differentiation in the rat hippocampus. We found a significant difference between the temporal expression of synapsin I messenger RNA in dentate granule somata and the appearance of protein in their mossy fiber terminals during the postnatal development of these neurons. Next, to investigate the regulation of neuron-specific gene expression during the restoration of synaptic contacts in the central nervous system, we examined the expression of the synapsin I gene following lesions of hippocampal circuitry. These studies show marked changes in the pattern and intensity of synapsin I immunoreactivity in the dendritic fields of dentate granule cell neurons following perforant pathway transection. In contrast, changes in synapsin I messenger RNA expression in target neurons, and in those neurons responsible for the reinnervation of this region of the hippocampus, were not found to accompany new synapse formation. On a molecular level, both developmental and lesion data suggest that the expression of the synapsin I gene is tightly regulated in the central nervous system, and that considerable changes in synapsin I protein may occur in neurons without concomitant changes in the levels of its messenger RNA. Finally, our results suggest that the appearance of detectable levels of synapsin I protein in in developing and sprouting synapses coincides with the acquisition of function by those central synapses.
Synapse development and injury-induced reorganization have been extensively characterized morphologically, yet relatively little is known about the underlying molecular and biochemical events. To examine molecular mechanisms of synaptic development and rearrangement, we looked at the developmental pattern of expression of the neuron-specific gene synapsin I in granule cell neurons of the dentate gyrus and their accompanying mossy fibers during the main period of synaptogenic differentiation in the rat hippocampus. We found a significant difference between the temporal expression of synapsin I messenger RNA in dentate granule somata and the appearance of protein in their mossy fiber terminals during the postnatal development of these neurons. The studies show marked changes in the pattern and intensity of synapsin I immunoreactivity in the dendritic fields of dentate granule cell neurons following perforant pathway transection. In contrast, changes in synapsin I messenger RNA expression in target neurons, and in those neurons responsible for the reinnervation of this region of the hippocampus, were not found to accompany new synapse formation.
Synapse development and injury-induced reorganization have been extensively characterized morphologically, yet relatively little is known about the underlying molecular and biochemical events. To examine molecular mechanisms of synaptic development and rearrangement, we looked at the developmental pattern of expression of the neuron-specific gene synapsin I in granule cell neurons of the dentate gyrus and their accompanying mossy fibers during the main period of synaptogenic differentiation in the rat hippocampus. We found a significant difference between the temporal expression of synapsin I messenger RNA in dentate granule somata and the appearence of protein in their mossy fiber terminals during the postnatal development of these neurons. Next, to investigate the regulation of neuron-specific gene expression during the restoration of synaptic contacts in the central nervous system, we examined the expression of the synapsin I gene following lesions of hippocampal circuitry. These studies show marked changes in the pattern and intensity of synapsin I immunoreactivity in the dendritic fields of dentate granule cell neurons following perforant pathway transection. In contrast, changes in synapsin I messenger RNA expression in target neurons, and in those neurons responsible for the reinnervation of this region of the hippocampus, were not found to accompany new synapse formation. On a molecular level, both developmental and lesion data suggest that the expression of the synapsin I gene is tightly regulated in the central nervous system, and that considerable changes in synapsin I protein may occur in neurons without concomitant changes in the levels of its messenger RNA. Finally, our results suggest that the appearance of detectable levels of synapsin I protein in developing and sprouting synapses coincides with the acquisition of function by those central synapses.
Author Melloni, R.H.
Hamos, J.E.
DeGennaro, L.J.
Apostolides, P.J.
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  surname: Apostolides
  fullname: Apostolides, P.J.
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IsPeerReviewed true
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Issue 4
Keywords P
PBS
AChE
SSC
EC
Vertebrata
Synapse
Mammalia
Rat
Phosphoproteins
Rodentia
Central nervous system
Development
Gene expression
Hippocampus
Brain (vertebrata)
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SSID ssj0000543
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Snippet Synapse development and injury-induced reorganization have been extensively characterized morphologically, yet relatively little is known about the underlying...
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StartPage 683
SubjectTerms acetylcholinesterase
Acetylcholinesterase - metabolism
AChE
Animals
Animals, Newborn
Biological and medical sciences
Blotting, Western
Denervation
Development. Senescence. Regeneration. Transplantation
DNA Probes
entorhinal cortex
Fundamental and applied biological sciences. Psychology
Gene Expression Regulation - physiology
Hippocampus - growth & development
Hippocampus - metabolism
Hippocampus - physiology
Image Processing, Computer-Assisted
Immunohistochemistry
In Situ Hybridization
Male
PBS
phosphate-buffered saline
postnatal day
Rats
Rats, Sprague-Dawley
RNA - biosynthesis
RNA, Messenger - biosynthesis
SSC
standard saline citrate
Synapses - metabolism
Synapses - physiology
Synapsins - biosynthesis
Synapsins - genetics
Vertebrates: nervous system and sense organs
Title Dynamics of synapsin I gene expression during the establishment and restoration of functional synapses in the rat hippocampus
URI https://dx.doi.org/10.1016/0306-4522(94)90448-0
https://www.ncbi.nlm.nih.gov/pubmed/7514766
https://search.proquest.com/docview/16925777
https://search.proquest.com/docview/76499747
Volume 58
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