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. 1978 Dec 1;79(3):802–825. doi: 10.1083/jcb.79.3.802

Membrane recycling in the cone cell endings of the turtle retina

PMCID: PMC2110281  PMID: 730768

Abstract

The ultrastructural effects of dark, light, and low temperature were investigated in the cone cell endings of the red-eared turtle (Pseudemys scripta elegans). Thin sections revealed that in dark- adapted retinas maintained at 22 degrees C, the neural processes which contact the cone cells at the invaginating synapses penetrated deeply into the photoreceptor endings. When dark-adapted retinas were illuminated for 1 h at 22 degrees C, the invaginating processes were apparently extruded from the synaptic endings. On the other hand, 1-h exposure to a temperature of 4 degrees C in the dark caused the invaginating processes to become much more strikingly inserted than at room temperature. A morphometric analysis showed that the ratio between the synaptic surface density of the endings and their total surface density decreased in the light and increased in the dark and cold. Freeze-fracturing documented fusion of synaptic vesicles with the presynaptic membrane in all conditions tested. These observations suggest that the changes in configuration of the pedicles in the light, dark, and cold reflect a different balance between addition and retrieval of synaptic vesicle membrane from the plasmalemma; in the dark, the rate of vesicle fusion is increased, whereas in the cold, membrane retrieval is blocked. When the eyecups were warmed up and illuminated for 30-45 min after cold exposure, a striking number of vacuoles and cisterns appeared in the cytoplasm and coated vesicles were commonly seen budding from the plasmalemma. 60-90 min after returning to room temperature, the endings had reverted to their normal configuration, and the vast majority of vacuoles, cisterns, and coated vesicles had disappeared. When horseradish peroxidase was included in the incubation medium, very few synaptic vesicles were labeled at the end of the period of cold exposure. 30-45 min after returning to 22 degrees C, vacuoles and cisterns contained peroxidase, whereas most synaptic vesicles were devoid of reaction product. 2 h after returning to 22 degrees C, coated vesicles, vacuoles, and cisterns had disappeared and a number of synaptic vesicles were labeled. These experiments suggest that vacuoles, cisterns, and coated vesicles mediate the retrieval of the synaptic vesicle membrane that has been added to the plasmalemma during cold exposure.

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Selected References

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  1. Clark A. W., Hurlbut W. P., Mauro A. Changes in the fine structure of the neuromuscular junction of the frog caused by black widow spider venom. J Cell Biol. 1972 Jan;52(1):1–14. doi: 10.1083/jcb.52.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Fuortes M. G., Schwartz E. A., Simon E. J. Colour-dependence of cone responses in the turtle retina. J Physiol. 1973 Oct;234(1):199–216. doi: 10.1113/jphysiol.1973.sp010341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  4. Gray E. G., Pease H. L. On understanding the organisation of the retinal receptor synapses. Brain Res. 1971 Dec 10;35(1):1–15. doi: 10.1016/0006-8993(71)90591-9. [DOI] [PubMed] [Google Scholar]
  5. Heuser J. E., Reese T. S., Landis D. M. Functional changes in frog neuromuscular junctions studied with freeze-fracture. J Neurocytol. 1974 Mar;3(1):109–131. doi: 10.1007/BF01111936. [DOI] [PubMed] [Google Scholar]
  6. Holtzman E., Peterson E. R. Uptake of protein by mammalian neurons. J Cell Biol. 1969 Mar;40(3):863–869. doi: 10.1083/jcb.40.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kristensson K., Olsson Y., Sjöstrand J. Axonal uptake and retrograde transport of exogenous proteins in the hypoglossal nerve. Brain Res. 1971 Sep 24;32(2):399–406. doi: 10.1016/0006-8993(71)90332-5. [DOI] [PubMed] [Google Scholar]
  8. Model P. G., Highstein S. M., Bennett M. V. Depletion of vesicles and fatigue of transmission at a vertebrate central synapse. Brain Res. 1975 Nov 14;98(2):209–228. doi: 10.1016/0006-8993(75)90002-5. [DOI] [PubMed] [Google Scholar]
  9. Pfenninger K., Akert K., Moor H., Sandri C. Freeze-fracturing of presynaptic membranes in the central nervous system. Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):387–387. doi: 10.1098/rstb.1971.0071. [DOI] [PubMed] [Google Scholar]
  10. Pysh J. J., Wiley R. G. Synaptic vesicle depletion and recovery in cat sympathetic ganglia electrically stimulated in vivo. Evidence for transmitter secretion by exocytosis. J Cell Biol. 1974 Feb;60(2):365–374. doi: 10.1083/jcb.60.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Raviola E., Gilula N. B. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol. 1975 Apr;65(1):192–222. doi: 10.1083/jcb.65.1.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Richter A., Simon E. J. Properties of centre-hyperpolarizing, red-sensitive bipolar cells in the turtle retina. J Physiol. 1975 Jun;248(2):317–334. doi: 10.1113/jphysiol.1975.sp010976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ripps H., Shakib M., MacDonald E. D. Peroxidase uptake by photoreceptor terminals of the skate retina. J Cell Biol. 1976 Jul;70(1):86–96. doi: 10.1083/jcb.70.1.86. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Schacher S. M., Holtzman E., Hood D. C. Uptake of horseradish peroxidase by frog photoreceptor synapses in the dark and the light. Nature. 1974 May 17;249(454):261–263. doi: 10.1038/249261a0. [DOI] [PubMed] [Google Scholar]
  15. Schaeffer S. F., Raviola E. Ultrastructural analysis of functional changes in the synaptic endings of turtle cone cells. Cold Spring Harb Symp Quant Biol. 1976;40:521–528. doi: 10.1101/sqb.1976.040.01.048. [DOI] [PubMed] [Google Scholar]
  16. Teichberg S., Holtzman E., Crain S. M., Peterson E. R. Circulation and turnover of synaptic vesicle membrane in cultured fetal mammalian spinal cord neurons. J Cell Biol. 1975 Oct;67(1):215–230. doi: 10.1083/jcb.67.1.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Theodosis D. T., Dreifuss J., Harris M. C., Orci L. Secretion-related uptake of horseradish peroxidase in neurohypophysial axons. J Cell Biol. 1976 Aug;70(2 Pt 1):294–303. doi: 10.1083/jcb.70.2.294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Weisman R. A., Korn E. D. Phagocytosis of latex beads by Acanthamoeba. I. Biochemical properties. Biochemistry. 1967 Feb;6(2):485–497. doi: 10.1021/bi00854a017. [DOI] [PubMed] [Google Scholar]

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