Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1987 Apr 1;104(4):933–937. doi: 10.1083/jcb.104.4.933

Inositol 1,4,5 trisphosphate releases calcium from specialized sites within Limulus photoreceptors

PMCID: PMC2114430  PMID: 3494019

Abstract

We have investigated the subcellular distribution and identity of inositol trisphosphate (InsP3)-sensitive calcium stores in living Limulus ventral photoreceptor cells, where light and InsP3 are known to raise intracellular calcium. We injected ventral photoreceptor cells with the photoprotein aequorin and viewed its luminescence with an image intensifier. InsP3 only elicited detectable aequorin luminescence when injected into the light-sensitive rhabdomeral (R)-lobe where aequorin luminescence induced by light was also confined. Calcium stores released by light and InsP3 are therefore localized to the R- lobe. Within the R-lobe, InsP3-induced aequorin luminescence was further confined around the injection site, due to rapid dilution and/or degradation of injected InsP3. Prominent cisternae of smooth endoplasmic reticulum are uniquely localized within the cell beneath the microvillar surface of the R-lobe (Calman, B., and S. Chamberlain, 1982, J. Gen. Physiol., 80:839-862). These cisternae are the probable site of InsP3 action.

Full Text

The Full Text of this article is available as a PDF (1.0 MB).

Selected References

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

  1. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  2. Berridge M. J. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J. 1983 Jun 15;212(3):849–858. doi: 10.1042/bj2120849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Brown J. E., Rubin L. J. A direct demonstration that inositol-trisphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochem Biophys Res Commun. 1984 Dec 28;125(3):1137–1142. doi: 10.1016/0006-291x(84)91402-5. [DOI] [PubMed] [Google Scholar]
  5. Brown J. E., Rubin L. J., Ghalayini A. J., Tarver A. P., Irvine R. F., Berridge M. J., Anderson R. E. myo-Inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature. 1984 Sep 13;311(5982):160–163. doi: 10.1038/311160a0. [DOI] [PubMed] [Google Scholar]
  6. Calman B. G., Chamberlain S. C. Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. J Gen Physiol. 1982 Dec;80(6):839–862. doi: 10.1085/jgp.80.6.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Corson D. W., Fein A. Quantitative pressure injection of picoliter volumes into Limulus ventral photoreceptors. Biophys J. 1983 Dec;44(3):299–304. doi: 10.1016/S0006-3495(83)84303-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fein A., Charlton J. S. Enhancement and phototransduction in the ventral eye of limulus. J Gen Physiol. 1977 May;69(5):553–569. doi: 10.1085/jgp.69.5.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fein A., Charlton J. S. Local adaptation in the ventral photoreceptors of Limulus. J Gen Physiol. 1975 Dec;66(6):823–836. doi: 10.1085/jgp.66.6.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fein A., Payne R., Corson D. W., Berridge M. J., Irvine R. F. Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature. 1984 Sep 13;311(5982):157–160. doi: 10.1038/311157a0. [DOI] [PubMed] [Google Scholar]
  11. GRADO C., BALLOU C. E. Myo-inositol phosphates obtained by alkaline hydrolysis of beef brain phosphoinositide. J Biol Chem. 1961 Jan;236:54–60. [PubMed] [Google Scholar]
  12. Harary H. H., Brown J. E. Spatially nonuniform changes in intracellular calcium ion concentrations. Science. 1984 Apr 20;224(4646):292–294. doi: 10.1126/science.6710144. [DOI] [PubMed] [Google Scholar]
  13. Levy S., Fein A. Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes. J Gen Physiol. 1985 Jun;85(6):805–841. doi: 10.1085/jgp.85.6.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. II. The basic photoresponse. J Gen Physiol. 1969 Sep;54(3):310–330. doi: 10.1085/jgp.54.3.310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Payne R., Corson D. W., Fein A., Berridge M. J. Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5 triphosphate result from a rise in intracellular calcium. J Gen Physiol. 1986 Jul;88(1):127–142. doi: 10.1085/jgp.88.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Payne R., Corson D. W., Fein A. Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors. J Gen Physiol. 1986 Jul;88(1):107–126. doi: 10.1085/jgp.88.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Payne R., Fein A. Localized adaptation within the rhabdomeral lobe of Limulus ventral photoreceptors. J Gen Physiol. 1983 May;81(5):767–769. doi: 10.1085/jgp.81.5.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Prentki M., Biden T. J., Janjic D., Irvine R. F., Berridge M. J., Wollheim C. B. Rapid mobilization of Ca2+ from rat insulinoma microsomes by inositol-1,4,5-trisphosphate. Nature. 1984 Jun 7;309(5968):562–564. doi: 10.1038/309562a0. [DOI] [PubMed] [Google Scholar]
  20. SHIMOMURA O., JOHNSON F. H., SAIGA Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol. 1962 Jun;59:223–239. doi: 10.1002/jcp.1030590302. [DOI] [PubMed] [Google Scholar]
  21. Stern J., Chinn K., Bacigalupo J., Lisman J. Distinct lobes of Limulus ventral photoreceptors. I. Functional and anatomical properties of lobes revealed by removal of glial cells. J Gen Physiol. 1982 Dec;80(6):825–837. doi: 10.1085/jgp.80.6.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Streb H., Bayerdörffer E., Haase W., Irvine R. F., Schulz I. Effect of inositol-1,4,5-trisphosphate on isolated subcellular fractions of rat pancreas. J Membr Biol. 1984;81(3):241–253. doi: 10.1007/BF01868717. [DOI] [PubMed] [Google Scholar]
  23. Streb H., Irvine R. F., Berridge M. J., Schulz I. Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature. 1983 Nov 3;306(5938):67–69. doi: 10.1038/306067a0. [DOI] [PubMed] [Google Scholar]
  24. TOMLINSON R. V., BALLOU C. E. Complete characterization of the myo-inositol polyphosphates from beef brain phosphoinositide. J Biol Chem. 1961 Jul;236:1902–1906. [PubMed] [Google Scholar]
  25. Walz B. Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. I. Intracellular topography as revealed by OsFeCN staining and in situ Ca accumulation. J Cell Biol. 1982 Jun;93(3):839–848. doi: 10.1083/jcb.93.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES