An antiserum against a specific component (a glycosamino glycan) of the cholinergic synaptic-vesicle of Torpedo marmorata has been used to investigate the localization of the component in the cell body, its movement within the electromotor axon and its fate within the nerve terminal upon electrical stimulation. After immunofluorescent staining, spots are observed throughout the cytoplasm of the lobe perikarya, although they are concentrated in the region of the axon hillock. Ligation of the electromotor nerves leading from the lobe to electric organ produces a proximal build-up of material which stains readily with the antivesicle antiserum, indicating that the vesicle antigen is transported from the cell body to the nerve terminal. A marked increase in indirect immunofluorescent staining of the electric organ is observed in the nerve ending upon electrical stimulation. We interpret this result as fusion of the vesicles with the presynaptic plasma membrane and exteriorization of the vesicle antigen to the extracellular space, thereby facilitating its staining. After recovery of the system the fluorescence declines, a result that is consistent with the reinternalization of the vesicle antigen into the core of reformed vesicles. The results support a mechanism whereby vesicles recycle within the nerve terminal and transmitter is released by exocytosis.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Boyne AF, McLeod S (1979) Ultrastructural plasticity in stimulated nerve terminals: pseudopodial invasions of abutted terminals in Torpedine ray electric organs. Neuroscience 4:615–624
Carlson SS, Kelly RB (1980) An antiserum specific for cholinergic synaptic vesicles from electric organ. J Cell Biol 87:98–103
Davies LP, Whittaker VP, Zimmermann H (1977) Axonal transport in the electromotor nerves of Torpedo marmorata. Exp Brain Res 30:493–510
Dowdall MJ, Fox G, Wächtler K, Whittaker VP, Zimmermann H (1976) Recent studies on the comparative biochemistry of the cholinergic neuron. Cold Spring Harbor Symposia on Quantitative Biology 40:65–81
Giannattasio G, Zanini A, Meldolesi J (1979) Complex carbohydrates of secretory organelles. In: Margolis RU, Margolis RK (eds) Complex carbohydrates of nervous tissue. Plenum, NY, pp 327–345
Heuser JE, Salpeter SR (1979) Organization of acetylcholine receptors in quick-frozen, deep-etched, and rotary-replicated Torpedo postsynaptic membrane. J Cell Biol 82:150–173
Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, Evans L (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81:275–300
Hooper JE, Carlson SS, Kelly RB (1980) Antibodies to synaptic vesicles purified from Narcine electric organ binds a subclass of mammalian nerve terminals. J Cell Biol 87:104–113
Jones RT, Walker JH, Richardson PJ, Fox GQ, Whittaker VP (1981 a) Immunohistochemical localization of cholinergic nerve terminals. Cell and Tissue Res 218:355–373
Jones RT, Walker JH, Richardson PJ, Fox GQ, Whittaker VP (1981 b) A specific method for the localization of cholinergic nerve terminals by indirect immunofluorescence. Abst 8th Meet int Soc Neurochem, Nottingham, Sept. 7–11th 1981, p9
Jones RT, Walker JH, Stadler H (1982) Further evidence that glycosaminoglycan specific to cholinergic synaptic vesicles recycles during electrical stimulation. Cell and Tissue Res (to be submitted)
Pastan I, Willingham M (1981) Receptor-mediated endocytosis of hormones in cultured cells. Ann Rev Physiol 43:239–250
Sheridan MN (1965) The fine structure of the electric organ of Torpedo marmorata. J Cell Biol 24:129–141
Sheridan MN, Whittaker VP, Israël M (1966) The subcellular fractionation of the electric organ of Torpedo. Z Zellforsch Mikrosk Anat 74:291–307
Stadler H, Füldner HH (1980) Proton NMR detection of acetylcholine status in synaptic vesicles. Nature 286:293–294
Stadler H, Tashiro T (1979) Isolation of synaptosomal plasma membranes from cholinergic nerve terminals and a comparison of their proteins with those of synaptic vesicles. Eur J Biochem 101:171–178
Stadler H, Whittaker VP (1978) Identification of vesiculin as a glycosaminoglycan. Brain Res 153:408–413
Suszkiw JB, Whittaker VP (1979) Role of vesicle recycling in vesicular storage and release of acetylcholine in Torpedo electroplaque synapses. Prog Brain Res 49:153–162
Ulmar G, Whittaker VP (1974a) Immunological approach to the characterization of cholinergic vesicular protein. J Neurochem 22:451–454
Ulmar G, Whittaker VP (1974b) Immunohistochemical localization and immunoelectrophoresis of cholinergic synaptic vesicle protein constituents from the Torpedo. Brain Res 71:155–159
Walker JH, Jones RT, Obrocki J, Richardson GP, Stadler H (1982) Presynaptic plasma membranes and synaptic vesicles of cholinergic nerve endings demonstrated by means of specific antisera. Cell and Tissue Res 223:101–116
Wedel RJ von, Carlson SS, Kelly RB (1981) Transfer of synaptic vesicle antigens to the presynaptic plasma membrane during exocytosis. Proc Natl Acad Sci USA 78:1014–1018
Zimmermann H (1979) Vesicle recycling and transmitter release. Neuroscience 4:1773–1804
Zimmermann H, Denston CR (1977) Recycling of synaptic vesicles in the cholinergic synapses of the Torpedo electric organ during induced transmitter release. Neuroscience 2:695–714
Zimmermann H, Whittaker VP (1974) Effect of electrical stimulation on the yield and composition of synaptic vesicles from the cholinergic synapse of the electric organ of Torpedo: a combined biochemical, electrophysiological and morphological study. J Neurochem 22:435–450
About this article
Cite this article
Theresa Jones, R., Walker, J.H., Stadler, H. et al. Immunohistochemical localization of a synaptic-vesicle antigen in a cholinergic neuron under conditions of stimulation and rest. Cell Tissue Res. 223, 117–126 (1982). https://doi.org/10.1007/BF00221503
- Cholinergic vesicle antigen
- Axonal transport
- Indirect immunofluorescence histochemistry
- Torpedo marmorata