Plasticity of expression of a synaptic vesicle antigen in adult rat superior cervical ganglion

Abstract

The effects of deafferentation and alterations of synaptic activity on levels of a synaptic vesicle-specific membrane protein (SV) were studied in the adult rat superior cervical ganglion (SCG) in viva, using a monoclonal antibody directed against the protein. Levels of SV were quantified by radioimmunoassay. Deafferentation of the SCG results in a transient increase in SV levels in the SCG on days 7 and 10 after surgery, with levels then dropping below control levels on days 14, 21, and 30 after surgery. Immunohistochemical labeling of deafferented ganglia indicates that the increase is confined to the perikarya of principal ganglionic neurons. Levels of SV in an SCG target tissue, the iris, do not differ from control levels on day 7 after deafferentation, but are elevated at days 10, 14, and 30 after surgery. After reinnervation of the SCG, levels of SV in the SCG are elevated above control values, but do not differ from control values in the iris. Treatment with chlorisondamine, which blocks synaptic transmission in sympathetic ganglia, produces a significant increase in SV levels in the SCG after 7 d of treatment. Long-term chlorisondamine treatment results in reductions in SV in the SCG after 14 and 28 d. Treatment with phenoxybenzamine for 6 d, which reflexly increases synaptic activity, produces a marked decrease in SV in the SCG. These results suggest that activity, mediated by transsynaptic factors, contributes to the regulation of synthesis of a synaptic vesicle protein in the SCG. The results further suggest that accumulation of synaptic vesicles in terminals of the principal ganglion neurons may help regulate the maintenance of normal synaptic vesicle pools within sympathetic neurons.While ample evidence for neural plasticity exists in the developing nervous system, studies of responses in adult systems have in general shown considerable limitations in the ability to respond to and recover from alterations in connectivity and activity. Among peripheral systems, the adult rat superior cervical ganglion (SCG) is one in which several studies have documented plasticity in response to experimental manipulations. Deafferentation of the SCG by section of the cervical sympathetic trunk (CST) in adult animals has been reported to produce only limited changes in ganglion size in the absence of regeneration of the CST (Gabella, 1976). If the CST is permitted to reinnervate the SCG, recovery of normal numbers of synapses occurs, as assessed by morphometric analysis, and restoration of normal

Depolarization regulates expression of a synaptic vesicle protein in rat superior cervical ganglia in vitro

“…Levels of a 65 kilodalton integral membrane protein (p65) of the synaptic vesicles (Matthew,Tsavaler and Reichardt,198 1) increase significantly during the second postnatal week in vivo (Greif and Reichardt, 1982). Neonatal deafferentation prevents normal postnatal increases in p65 levels (Greif and Trenchard, 1988), as does treatment for 14 days with the ganglionic blocker, chlorisondamine (Greif and Linderman, 1986). These experiments suggest that membrane depolarization is essential for normal postnatal development of p65 in the SCG.…”

“…Deafferentdtion zn vzvo blocks neuronal activity, disrupts the physical environment and alters trophic factors. However, at least part of the change in p65 levels caused by deafferentation in vivo is due to the loss of neuronal activity since it can be mimicked by pharmacological blockade of preganglionic transmission in neonates and adults (Greif, 1986;Greif and Linderman, 1986 In ciliary ganglia, cholinergic agonists and antagonists appear to modulate the number of acetylcholine receptors (Smith ct al., 1986). Following dcafferentation of the SCG, an 85% decrease in calmodulin-binding to postsynaptic densities is observed (Wu and Black, 1988).…”

Most Synaptic Vesicles Isolated from Rat Brain Carry Three Membrane Proteins, SV2, Synaptophysin, and p65

“…It is not known whether subpopulations differing in number of copies of SV2, synaptophysin, or p65 per vesicle may also be present in isolated brain synaptic vesicles. Nevertheless, the presence of these proteins, especially SV2, 011 virtually all brain synaptic vesicles provides a useful marker in studies of synaptic vesicle subclasses or of synaptic vesicle levels altered by developmental or physiological factors (Greif, 1986;Bullock et al, 1987;Chun and Shatz, 1988). SV2, synaptophysin, and p65 have been identified on several vesicle types in addition to the small presynaptic vesicles studied here.…”

Neonatal deafferentation prevents normal expression of synaptic vesicle antigens in the developing rat superior cervical ganglion

“…However, immunohistochemical methods are inappropriate for such quantitative determinants. It has not been possible to determine directly the relative pools of SV in the SCG, since deafferentation in adult animals results in a transient increase in SV levels in ganglion neuron cytoplasm after short survival periods (Greif, 1986). However, 30 days after SCG deafferentation in adult rats, levels of SV are 33% of control values (Greif, 1986).…”