Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 Jun 1;93(3):839–848. doi: 10.1083/jcb.93.3.839

Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. I. Intracellular topography as revealed by OsFeCN staining and in situ Ca accumulation

PMCID: PMC2112144  PMID: 6181073

Abstract

Two ultrastructural approaches were used in photoreceptor cells of the leech, Hirudo medicinalis, to (a) investigate the intracellular topography of the smooth endoplasmic reticulum (SER) and (b) identify among the various subregions of the SER those which might function as Ca-sequestering sites. When the cells are prefixed with CaCl2- containing glutaraldehyde and postfixed with osmium tetroxide- ferricyanide (OsFeCN), only a part of the total SER is specifically stained. The stained SER cisternae include the submicrovillar cisternae (SMC), subsurface cisternae (SSC), the nuclear envelope, Golgi- associated SER, paracrystalline SER, and SER associated with glycogen areas. An extensive tubular SER cisternal system always remains unstained. When the cells are permeabilized by saponin and subsequently incubated with Ca2+, MgATP, and oxalate, the SMC (Walz, 1979, Eur. J. Cell Biol. 20:83-91), the SSC and the nuclear envelope contain electron- opaque Ca-oxalate precipitates indicating their ability to function as an effective Ca2+ sink. The results show that the very elaborate SER in this photoreceptor cell includes many functionally heterogeneous subregions. Of special physiological significance are those components (SMC and SSC) which are effective in Ca2+-buffering in the immediate vicinity of the plasma membrane.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Bader C., Baumann F., Bertrand D. Role of intracellular calcium and sodium in light adaptation in the retina of the honey bee drone (Apis mellifera, L). J Gen Physiol. 1976 Apr;67(4):475–491. doi: 10.1085/jgp.67.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blaustein M. P., McGraw C. F., Somlyo A. V., Schweitzer E. S. How is the cytoplasmic calcium concentration controlled in nerve terminals? J Physiol (Paris) 1980 Sep;76(5):459–470. [PubMed] [Google Scholar]
  3. Blaustein M. P., Ratzlaff R. W., Kendrick N. C., Schweitzer E. S. Calcium buffering in presynaptic nerve terminals. I. Evidence for involvement of a nonmitochondrial ATP-dependent sequestration mechanism. J Gen Physiol. 1978 Jul;72(1):15–41. doi: 10.1085/jgp.72.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown J. E., Blinks J. R. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol. 1974 Dec;64(6):643–665. doi: 10.1085/jgp.64.6.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown J. E., Brown P. K., Pinto L. H. Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J Physiol. 1977 May;267(2):299–320. doi: 10.1113/jphysiol.1977.sp011814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown J. E. Calcium ion, a putative intracellular messenger for light-adaptation in Limulus ventral photoreceptors. Biophys Struct Mech. 1977 Jun 29;3(2):141–143. doi: 10.1007/BF00535809. [DOI] [PubMed] [Google Scholar]
  7. Campbell K. P., Shamoo A. E. Phosphorylation of heavy sarcoplasmic reticulum vesicles: identification and characterization of three phosphorylated proteins. J Membr Biol. 1980 Oct 31;56(3):241–248. doi: 10.1007/BF01869479. [DOI] [PubMed] [Google Scholar]
  8. Cardell R. R., Jr Smooth endoplasmic reticulum in rat hepatocytes during glycogen deposition and depletion. Int Rev Cytol. 1977;48:221–279. doi: 10.1016/s0074-7696(08)61746-5. [DOI] [PubMed] [Google Scholar]
  9. Endo M., Iino M. Specific perforation of muscle cell membranes with preserved SR functions by saponin treatment. J Muscle Res Cell Motil. 1980 Mar;1(1):89–100. doi: 10.1007/BF00711927. [DOI] [PubMed] [Google Scholar]
  10. Fahrenbach W. H. The visual system of the horseshoe crab Limulus polyphemus. Int Rev Cytol. 1975;41:285–349. doi: 10.1016/s0074-7696(08)60970-5. [DOI] [PubMed] [Google Scholar]
  11. Fein A., Charlton J. S. A quantitative comparison of the effects of intracellular calcium injection and light adaptation on the photoresponse of Limulus ventral photoreceptors. J Gen Physiol. 1977 Nov;70(5):591–600. doi: 10.1085/jgp.70.5.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fein A., Charlton J. S. Increased intracellular sodium mimics some but not all aspects of photoreceptor adaptation in the ventral eye of Limulus. J Gen Physiol. 1977 Nov;70(5):601–620. doi: 10.1085/jgp.70.5.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Forbes M. S., Plantholt B. A., Sperelakis N. Cytochemical staining procedures selective for sarcotubular systems of muscle: modifications and applications. J Ultrastruct Res. 1977 Sep;60(3):306–327. doi: 10.1016/s0022-5320(77)80016-6. [DOI] [PubMed] [Google Scholar]
  14. Forbes M. S., Sperelakis N. Structures located at the levels of the Z bands in mouse ventricular myocardial cells. Tissue Cell. 1980;12(3):467–489. doi: 10.1016/0040-8166(80)90037-3. [DOI] [PubMed] [Google Scholar]
  15. Hepler P. K. Membranes in the mitotic apparatus of barley cells. J Cell Biol. 1980 Aug;86(2):490–499. doi: 10.1083/jcb.86.2.490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Horridge G. A., Barnard P. B. Movement of palisade in locust retinula cells when illuminated. Q J Microsc Sci. 1965 Jun;106(2):131–135. [PubMed] [Google Scholar]
  18. Lasansky A. Cell junctions in ommatidia of Limulus. J Cell Biol. 1967 May;33(2):365–383. doi: 10.1083/jcb.33.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lasansky A., Fuortes M. G. The site of origin of electrical responses in visual cells of the leech, Hirudo medicinalis. J Cell Biol. 1969 Jul;42(1):241–252. doi: 10.1083/jcb.42.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lisman J. E., Brown J. E. Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J Gen Physiol. 1975 Oct;66(4):489–506. doi: 10.1085/jgp.66.4.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lisman J. E., Brown J. E. The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. J Gen Physiol. 1972 Jun;59(6):701–719. doi: 10.1085/jgp.59.6.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lisman J. E., Strong J. A. The initiation of excitation and light adaptation in Limulus ventral photoreceptors. J Gen Physiol. 1979 Feb;73(2):219–243. doi: 10.1085/jgp.73.2.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maaz G., Stieve H. The correlation of the receptor potential with the light induced transient increase in intracellular calcium-concentration measured by absorption change of arsenazo III injected into Limulus ventral nerve photoreceptor cell. Biophys Struct Mech. 1980;6(3):191–208. doi: 10.1007/BF00537293. [DOI] [PubMed] [Google Scholar]
  24. Margolis R. N., Cardell R. R., Curnow R. T. Association of glycogen synthase phosphatase and phosphorylase phosphatase activities with membranes of hepatic smooth endoplasmic reticulum. J Cell Biol. 1979 Nov;83(2 Pt 1):348–356. doi: 10.1083/jcb.83.2.348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McGraw C. F., Somlyo A. V., Blaustein M. P. Localization of calcium in presynaptic nerve terminals. An ultrastructural and electron microprobe analysis. J Cell Biol. 1980 May;85(2):228–241. doi: 10.1083/jcb.85.2.228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mullins L. J., Requena J. Calcium measurement in the periphery of an axon. J Gen Physiol. 1979 Sep;74(3):393–413. doi: 10.1085/jgp.74.3.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Perrelet A., Bader C. R. Morphological evidence for calcium stores in photoreceptors of the honeybee drone retina. J Ultrastruct Res. 1978 Jun;63(3):237–243. doi: 10.1016/s0022-5320(78)80048-3. [DOI] [PubMed] [Google Scholar]
  28. Tillotson D., Gorman A. L. Non-uniform Ca2+ buffer distribution in a nerve cell body. Nature. 1980 Aug 21;286(5775):816–817. doi: 10.1038/286816a0. [DOI] [PubMed] [Google Scholar]
  29. Walz B. Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements. J Cell Biol. 1982 Jun;93(3):849–859. doi: 10.1083/jcb.93.3.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Walz B. Subcellular calcium localization and AT0-dependent Ca2+-uptake by smooth endoplasmic reticulum in an invertebrate photoreceptor cell. An ultrastrucutral, cytochemical and X-ray microanalytical study. Eur J Cell Biol. 1979 Oct;20(1):83–91. [PubMed] [Google Scholar]
  31. Wick S. M., Hepler P. K. Localization of Ca++-containing antimonate precipitates during mitosis. J Cell Biol. 1980 Aug;86(2):500–513. doi: 10.1083/jcb.86.2.500. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES