Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 Oct 1;95(1):296–309. doi: 10.1083/jcb.95.1.296

Effect of barium and tetraethylammonium on membrane circulation in frog retinal photoreceptors

PMCID: PMC2112377  PMID: 6292233

Abstract

We studied the influence of altered ionic conditions on the recycling of synaptic vesicle membrane in frog retinal photoreceptors using horseradish peroxidase to monitor synaptic activity and trace the fate of internalized membrane. The addition of 1.2 mM barium or 20 mM tetraethylammonium to isolated retinas maintained in Ringer's solution, changes the usual balance of membrane circulation in the rod cells; the cone cells are much less affected. Retrieval of synaptic vesicle membrane in the rods, which normally regenerates small vesicles, becomes mediated predominantly by large sacs and vacuoles ("cisternae"). Because these cisternae can be labeled with peroxidase, they appear to arise from endocytized membrane. Morphometric analysis suggests strongly that the cisternae are formed of circulating synaptic vesicle membrane. The effects of barium and tetraethylammonium can be inhibited by high extracellular potassium, by high intensity light, and by 5 mM cobalt. They seem likely to depend on potassium channels, though additional more complex mediation may also be involved. The alterations in membrane retrieval that we find are of interest in terms of the multiple pathways of membrane cycling now being uncovered. They open potential experimental approaches to the controls of this circulation. In addition, the findings extend our previous ones demonstrating that rod cells and cone cells differ in their responses to divalent cations in ways that seem likely to be of physiological importance.

Full Text

The Full Text of this article is available as a PDF (5.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ainsworth S. K., Karnovsky M. J. An ultrastructural staining method for enhancing the size and electron opacity of ferritin in thin sections. J Histochem Cytochem. 1972 Mar;20(3):225–229. doi: 10.1177/20.3.225. [DOI] [PubMed] [Google Scholar]
  2. Armstrong C. M., Hille B. The inner quaternary ammonium ion receptor in potassium channels of the node of Ranvier. J Gen Physiol. 1972 Apr;59(4):388–400. doi: 10.1085/jgp.59.4.388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong C. M., Taylor S. R. Interaction of barium ions with potassium channels in squid giant axons. Biophys J. 1980 Jun;30(3):473–488. doi: 10.1016/S0006-3495(80)85108-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baenziger J. U., Fiete D. Recycling of the hepatocyte asialoglycoprotein receptor does not require delivery of ligand to lysosomes. J Biol Chem. 1982 Jun 10;257(11):6007–6009. [PubMed] [Google Scholar]
  5. Baker P. F., Ravazzola M., Malaisse-Lagae F. Secretion-dependent uptake of extracellular fluid by the rat neurohypophysis. Nature. 1974 Jul 12;250(462):155–157. doi: 10.1038/250155a0. [DOI] [PubMed] [Google Scholar]
  6. Brown K. T., Flaming D. G. Opposing effects of calcium and barium in vertebrate rod photoreceptors. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1587–1590. doi: 10.1073/pnas.75.3.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ceccarelli B., Hurlbut W. P. Ca2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction. J Cell Biol. 1980 Oct;87(1):297–303. doi: 10.1083/jcb.87.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ceccarelli B., Hurlbut W. P., Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):499–524. doi: 10.1083/jcb.57.2.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chan K. Y., Haschke R. H. A re-evaluation of the retrograde axonal transport of horseradish peroxidase isoenzymes by semi-quantitative cytochemical analysis. Neuroscience. 1981;6(6):1145–1155. doi: 10.1016/0306-4522(81)90079-8. [DOI] [PubMed] [Google Scholar]
  10. Cornwall M. C., Gorman A. L. Contribution of calcium and potassium permeability changes to the off response of scallop hyperpolarizing photoreceptors. J Physiol. 1979 Jun;291:207–232. doi: 10.1113/jphysiol.1979.sp012808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DOUGLAS W. W., LYWOOD D. W., STRAUB R. W. The stimulant effect of barium on the release of acetylcholine from the superior cervical ganglion. J Physiol. 1961 May;156:515–522. doi: 10.1113/jphysiol.1961.sp006690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DOUGLAS W. W., RUBIN R. P. THE EFFECTS OF ALKALINE EARTHS AND OTHER DIVALENT CATIONS ON ADRENAL MEDULLARY SECRETION. J Physiol. 1964 Dec;175:231–241. doi: 10.1113/jphysiol.1964.sp007514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eaton D. C., Brodwick M. S. Effects of barium on the potassium conductance of squid axon. J Gen Physiol. 1980 Jun;75(6):727–750. doi: 10.1085/jgp.75.6.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Evans J. A., Liscum L., Hood D. C., Holtzman E. Uptake of horseradish peroxidase by presynaptic terminals of bipolar cells and photoreceptors of the from retina. J Histochem Cytochem. 1981 Apr;29(4):511–518. doi: 10.1177/29.4.6972957. [DOI] [PubMed] [Google Scholar]
  15. Fain G. L., Gerschenfeld H. M., Quandt F. N. Calcium spikes in toad rods. J Physiol. 1980 Jun;303:495–513. doi: 10.1113/jphysiol.1980.sp013300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fried R. C., Blaustein M. P. Retrieval and recycling of synaptic vesicle membrane in pinched-off nerve terminals (synaptosomes). J Cell Biol. 1978 Sep;78(3):685–700. doi: 10.1083/jcb.78.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gennaro J. F., Jr, Nastuk W. L., Rutherford D. T. Reversible depletion of synaptic vesicles induced by application of high external potassium to the frog neuromuscular junction. J Physiol. 1978 Jul;280:237–247. doi: 10.1113/jphysiol.1978.sp012382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gronowicz G., Masur S. K., Holtzman E. Quantitative analysis of exocytosis and endocytosis in the hydroosmotic response of toad bladder. J Membr Biol. 1980;52(3):221–235. doi: 10.1007/BF01869191. [DOI] [PubMed] [Google Scholar]
  19. Hagiwara S., Fukuda J., Eaton D. C. Membrane currents carried by Ca, Sr, and Ba in barnacle muscle fiber during voltage clamp. J Gen Physiol. 1974 May;63(5):564–578. doi: 10.1085/jgp.63.5.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hama K., Saito K. Fine structure of the afferent synapse of the hair cells in the saccular macula of the goldfish, with special reference to the anastomosing tubules. J Neurocytol. 1977 Aug;6(4):361–373. doi: 10.1007/BF01178223. [DOI] [PubMed] [Google Scholar]
  21. Hermann A., Gorman A. L. Blockade of voltage-dependent and Ca2+-dependent K+ current components by internal Ba2+ in molluscan pacemaker neurons. Experientia. 1979 Feb 15;35(2):229–231. doi: 10.1007/BF01920633. [DOI] [PubMed] [Google Scholar]
  22. Herzog V., Farquhar M. G. Luminal membrane retrieved after exocytosis reaches most golgi cisternae in secretory cells. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5073–5077. doi: 10.1073/pnas.74.11.5073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Heuser J. E., Reese T. S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):315–344. doi: 10.1083/jcb.57.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Holtzman E., Freeman A. R., Kashner L. A. Stimulation-dependent alterations in peroxidase uptake at lobster neuromuscular junctions. Science. 1971 Aug 20;173(3998):733–736. doi: 10.1126/science.173.3998.733. [DOI] [PubMed] [Google Scholar]
  25. Holtzman E. Membrane circulation: an overview. Methods Cell Biol. 1981;23:379–397. doi: 10.1016/s0091-679x(08)61510-1. [DOI] [PubMed] [Google Scholar]
  26. Holtzman E., Mercurio A. M. Membrane circulation in neurons and photoreceptors: some unresolved issues. Int Rev Cytol. 1980;67:1–67. doi: 10.1016/s0074-7696(08)62426-2. [DOI] [PubMed] [Google Scholar]
  27. Holtzman E. The origin and fate of secretory packages, especially synaptic vesicles. Neuroscience. 1977;2(3):327–355. doi: 10.1016/0306-4522(77)90001-x. [DOI] [PubMed] [Google Scholar]
  28. Hood D., Hock P. A. Light adaptation of the receptors: increment threshold functions for the frog's rods and cones. Vision Res. 1975 May;15(5):545–553. doi: 10.1016/0042-6989(75)90301-6. [DOI] [PubMed] [Google Scholar]
  29. Hubbard J. I., Kwanbunbumpen S. Evidence for the vesicle hypothesis. J Physiol. 1968 Feb;194(2):407–420. doi: 10.1113/jphysiol.1968.sp008415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Joseph K. C., Stieber A., Gonatas N. K. Endocytosis of cholera toxin in GERL-like structures of murine neuroblastoma cells pretreated with GM1 ganglioside. Cholera toxin internalization into Neuroblastoma GERL. J Cell Biol. 1979 Jun;81(3):543–554. doi: 10.1083/jcb.81.3.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kalina M., Pease D. C. The preservation of ultrastructure in saturated phosphatidyl cholines by tannic acid in model systems and type II pneumocytes. J Cell Biol. 1977 Sep;74(3):726–741. doi: 10.1083/jcb.74.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Katz B., Miledi R. Tetrodotoxin-resistant electric activity in presynaptic terminals. J Physiol. 1969 Aug;203(2):459–487. doi: 10.1113/jphysiol.1969.sp008875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kelly R. B., Deutsch J. W., Carlson S. S., Wagner J. A. Biochemistry of neurotransmitter release. Annu Rev Neurosci. 1979;2:399–446. doi: 10.1146/annurev.ne.02.030179.002151. [DOI] [PubMed] [Google Scholar]
  34. Koike H., Meldolesi J. Post-stimulation retrieval of luminal surface membrane in parotid acinar cells is calcium-dependent. Exp Cell Res. 1981 Aug;134(2):377–388. doi: 10.1016/0014-4827(81)90437-7. [DOI] [PubMed] [Google Scholar]
  35. Lynch K. The effects of chronic stimulation on the morphology of the frog neuromuscular junction. J Neurocytol. 1982 Feb;11(1):81–107. doi: 10.1007/BF01258006. [DOI] [PubMed] [Google Scholar]
  36. Mercurio A. M., Holtzman E. Smooth endoplasmic reticulum and other agranular reticulum in frog retinal photoreceptors. J Neurocytol. 1982 Apr;11(2):263–293. doi: 10.1007/BF01258247. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Morris J. F., Nordmann J. J., Dyball R. E. Structure-function correlation in mammalian neurosecretion. Int Rev Exp Pathol. 1978;18:1–95. [PubMed] [Google Scholar]
  39. Pastan I. H., Willingham M. C. Journey to the center of the cell: role of the receptosome. Science. 1981 Oct 30;214(4520):504–509. doi: 10.1126/science.6170111. [DOI] [PubMed] [Google Scholar]
  40. Reinecke M., Walther C. Ultrastructural changes with high activity and subsequent recovery at locust motor nerve terminals. A stereological analysis. Neuroscience. 1981;6(3):489–503. doi: 10.1016/0306-4522(81)90141-x. [DOI] [PubMed] [Google Scholar]
  41. Ross W. N., Stuart A. E. Voltage sensitive calcium channels in the presynaptic terminals of a decrementally conducting photoreceptor. J Physiol. 1978 Jan;274:173–191. doi: 10.1113/jphysiol.1978.sp012142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Schacher S., Holtzman E., Hood D. C. Synaptic activity of frog retinal photoreceptors. A peroxidase uptake study. J Cell Biol. 1976 Jul;70(1):178–192. doi: 10.1083/jcb.70.1.178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schaeffer S. F., Raviola E. Membrane recycling in the cone cell endings of the turtle retina. J Cell Biol. 1978 Dec;79(3):802–825. doi: 10.1083/jcb.79.3.802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Schnapf J. L., Copenhagen D. R. Differences in the kinetics of rod and cone synaptic transmission. Nature. 1982 Apr 29;296(5860):862–864. doi: 10.1038/296862a0. [DOI] [PubMed] [Google Scholar]
  46. Silverstein S. C., Steinman R. M., Cohn Z. A. Endocytosis. Annu Rev Biochem. 1977;46:669–722. doi: 10.1146/annurev.bi.46.070177.003321. [DOI] [PubMed] [Google Scholar]
  47. Standen N. B., Stanfield P. R. A potential- and time-dependent blockade of inward rectification in frog skeletal muscle fibres by barium and strontium ions. J Physiol. 1978 Jul;280:169–191. doi: 10.1113/jphysiol.1978.sp012379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Tartakoff A., Vassalli P., Détraz M. Comparative studies of intracellular transport of secretory proteins. J Cell Biol. 1978 Dec;79(3):694–707. doi: 10.1083/jcb.79.3.694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tomita T. Electrical activity of vertebrate photoreceptors. Q Rev Biophys. 1970 May;3(2):179–222. doi: 10.1017/s0033583500004571. [DOI] [PubMed] [Google Scholar]
  50. Ungar F., Piscopo I., Holtzman E. Calcium accumulation in intracellular compartments of frog retinal rod photoreceptors. Brain Res. 1981 Jan 26;205(1):200–206. doi: 10.1016/0006-8993(81)90733-2. [DOI] [PubMed] [Google Scholar]
  51. Vizi E. S. Na+-K+-activated adenosinetriphosphatase as a trigger in transmitter release. Neuroscience. 1978;3(4-5):367–384. doi: 10.1016/0306-4522(78)90040-4. [DOI] [PubMed] [Google Scholar]
  52. WERMAN R., GRUNDFEST H. Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J Gen Physiol. 1961 May;44:997–1027. doi: 10.1085/jgp.44.5.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Weibel E. R., Paumgartner D. Integrated stereological and biochemical studies on hepatocytic membranes. II. Correction of section thickness effect on volume and surface density estimates. J Cell Biol. 1978 May;77(2):584–597. doi: 10.1083/jcb.77.2.584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Wilschut J., Papahadjopoulos D. Ca2+-induced fusion of phospholipid vesicles monitored by mixing of aqueous contents. Nature. 1979 Oct 25;281(5733):690–692. doi: 10.1038/281690a0. [DOI] [PubMed] [Google Scholar]
  55. Zimmerberg J., Cohen F. S., Finkelstein A. Fusion of phospholipid vesicles with planar phospholipid bilayer membranes. I. Discharge of vesicular contents across the planar membrane. J Gen Physiol. 1980 Mar;75(3):241–250. doi: 10.1085/jgp.75.3.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Zimmermann H. Vesicle recycling and transmitter release. Neuroscience. 1979;4(12):1773–1804. doi: 10.1016/0306-4522(79)90058-7. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES