Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1983 Apr 1;96(4):1159–1163. doi: 10.1083/jcb.96.4.1159

Membrane junctions in xenopus eggs: their distribution suggests a role in calcium regulation

DM Gardiner, RD Grey
PMCID: PMC2112324  PMID: 6682118

Abstract

We have observed the presence of membrane junctions formed between the plasma membrane and cortical endoplasmic reticulum of mature, unactivated eggs of xenopus laevis. The parallel, paired membranes of the junction are separated by a 10-mn gap within which electron-dense material is present. This material occurs in patches with an average center-to-center distance of approximately 30 nm. These junctions are rare in immature (but fully grown) oocytes (approximately 2 percent of the plasma membrane is associated with junctions) and increase dramatically during progesterone-induced maturation. Junctions in the mature, unactivated egg are two to three times more abundant in the animal hemisphere (25-30 percent of the plasma membrane associated with junction) as compared with the vegetal hemisphere (10-15 percent). Junction density decreases rapidly to values characteristic of immature oocytes in response to egg activation. The plasma membrane-ER junctions of xenopus eggs are strikingly similar in structure to membrane junctions in muscle cells thought to be essential in the triggering of intracellular calcium release from the sarcoplasmic reticulum. In addition, the junctions’ distinctive, animal-vegetal polarity of distribution, their dramatic appearance during maturation, and their disapperance during activation are correlated with previously documented patterns of calcium-mediated events in anuran eggs. We discuss several lines of evidence supporting the hypothesis that these junctions in xenopus eggs are sites that transduce extracellular events into intracellular calcium release during fertilization and activation of development.

Full Text

The Full Text of this article is available as a PDF (890.1 KB).

Selected References

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

  1. Barrett N., Barrett E. F. Excitation-contraction coupling in skeletal muscle: blockade by high extracellular concentrations of calcium buffers. Science. 1978 Jun 16;200(4347):1270–1272. doi: 10.1126/science.96524. [DOI] [PubMed] [Google Scholar]
  2. Browne C. L., Wiley H. S., Dumont J. N. Oocyte-follicle cell gap junctions in Xenopus laevis and the effects of gonadotropin on their permeability. Science. 1979 Jan 12;203(4376):182–183. doi: 10.1126/science.569364. [DOI] [PubMed] [Google Scholar]
  3. Campanella C., Andreuccetti P. Ultrastructural observations on cortical endoplasmic reticulum and on residual cortical granules in the egg of Xenopus laevis. Dev Biol. 1977 Mar;56(1):1–10. doi: 10.1016/0012-1606(77)90150-6. [DOI] [PubMed] [Google Scholar]
  4. Cardasis C. A., Schuel H., Herman L. Ultrastructural localization of calcium in unfertilized sea-urchin eggs. J Cell Sci. 1978 Jun;31:101–115. doi: 10.1242/jcs.31.1.101. [DOI] [PubMed] [Google Scholar]
  5. Cross N. L. Initiation of the activation potential by an increase in intracellular calcium in eggs of the frog, Rana pipiens. Dev Biol. 1981 Jul 30;85(2):380–384. doi: 10.1016/0012-1606(81)90269-4. [DOI] [PubMed] [Google Scholar]
  6. Eisenberg B. R., Gilai A. Structural changes in single muscle fibers after stimulation at a low frequency. J Gen Physiol. 1979 Jul;74(1):1–16. doi: 10.1085/jgp.74.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Elinson R. P. Site of sperm entry and a cortical contraction associated with egg activation in the frog Rana pipiens. Dev Biol. 1975 Dec;47(2):257–268. doi: 10.1016/0012-1606(75)90281-x. [DOI] [PubMed] [Google Scholar]
  8. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  9. Franzini-Armstrong C. Membrane particles and transmission at the triad. Fed Proc. 1975 Apr;34(5):1382–1389. [PubMed] [Google Scholar]
  10. Franzini-Armstrong C. STUDIES OF THE TRIAD : I. Structure of the Junction in Frog Twitch Fibers. J Cell Biol. 1970 Nov 1;47(2):488–499. doi: 10.1083/jcb.47.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gilkey J. C., Jaffe L. F., Ridgway E. B., Reynolds G. T. A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J Cell Biol. 1978 Feb;76(2):448–466. doi: 10.1083/jcb.76.2.448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gingell D. Contractile responses at the surface of an amphibian egg. J Embryol Exp Morphol. 1970 Jun;23(3):583–609. [PubMed] [Google Scholar]
  13. Grey R. D., Bastiani M. J., Webb D. J., Schertel E. R. An electrical block is required to prevent polyspermy in eggs fertilized by natural mating of Xenopus laevis. Dev Biol. 1982 Feb;89(2):475–484. doi: 10.1016/0012-1606(82)90335-9. [DOI] [PubMed] [Google Scholar]
  14. Grey R. D., Wolf D. P., Hedrick J. L. Formation and structure of the fertilization envelope in Xenopus laevis. Dev Biol. 1974 Jan;36(1):44–61. doi: 10.1016/0012-1606(74)90189-4. [DOI] [PubMed] [Google Scholar]
  15. Henkart M. P., Nelson P. G. Evidence for an intracellular calcium store releasable by surface stimuli ifibroblasts (L cells). J Gen Physiol. 1979 May;73(5):655–673. doi: 10.1085/jgp.73.5.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Henkart M., Landis D. M., Reese T. S. Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. J Cell Biol. 1976 Aug;70(2 Pt 1):338–347. doi: 10.1083/jcb.70.2.338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hollinger T. G., Dumont J. N., Wallace R. A. Calcium-induced dehiscence of cortical granules in Xenopus laevis oocytes. J Exp Zool. 1979 Oct;210(1):107–115. doi: 10.1002/jez.1402100111. [DOI] [PubMed] [Google Scholar]
  18. Jaffe L. F. Calcium explosions as triggers of development. Ann N Y Acad Sci. 1980;339:86–101. doi: 10.1111/j.1749-6632.1980.tb15971.x. [DOI] [PubMed] [Google Scholar]
  19. Johnson E. A., Sommer J. R. A strand of cardiac muscle. Its ultrastructure and the electrophysiological implications of its geometry. J Cell Biol. 1967 Apr;33(1):103–129. doi: 10.1083/jcb.33.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kelly D. E., Kuda A. M. Subunits of the triadic junction in fast skeletal muscle as revealed by freeze-fracture. J Ultrastruct Res. 1979 Aug;68(2):220–233. doi: 10.1016/s0022-5320(79)90156-4. [DOI] [PubMed] [Google Scholar]
  21. Miyamoto H., Racker E. Mechanism of calcium release from skeletal sarcoplasmic reticulum. J Membr Biol. 1982;66(3):193–201. doi: 10.1007/BF01868494. [DOI] [PubMed] [Google Scholar]
  22. Moreau M., Doree M., Guerrier P. Electrophoretic introduction of calcium ions into the cortex of Xenopus laevis oocytes triggers meiosis neinitiation. J Exp Zool. 1976 Sep;197(3):443–449. doi: 10.1002/jez.1401970318. [DOI] [PubMed] [Google Scholar]
  23. Moreau M., Vilain J. P., Guerrier P. Free calcium changes associated with hormone action in amphibian oocytes. Dev Biol. 1980 Jul;78(1):201–214. doi: 10.1016/0012-1606(80)90329-2. [DOI] [PubMed] [Google Scholar]
  24. O'Connor C. M., Robinson K. R., Smith L. D. Calcium, potassium, and sodium exchange by full-grown and maturing Xenopus laevis oocytes. Dev Biol. 1977 Nov;61(1):28–40. doi: 10.1016/0012-1606(77)90339-6. [DOI] [PubMed] [Google Scholar]
  25. Peachey L. D. Transverse tubules in excitation-contraction coupling. Fed Proc. 1965 Sep-Oct;24(5):1124–1134. [PubMed] [Google Scholar]
  26. ROSENBLUTH J. Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol. 1962 Jun;13:405–421. doi: 10.1083/jcb.13.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Robinson K. R. Electrical currents through full-grown and maturing Xenopus oocytes. Proc Natl Acad Sci U S A. 1979 Feb;76(2):837–841. doi: 10.1073/pnas.76.2.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Satir B. H., Wissig S. L. Alveolar sacs of Tetrahymena: ultrastructural characteristics and similarities to subsurface cisterns of muscle and nerve. J Cell Sci. 1982 Jun;55:13–33. doi: 10.1242/jcs.55.1.13. [DOI] [PubMed] [Google Scholar]
  29. Schlichter L. C., Elinson R. P. Electrical responses of immature and mature Rana pipiens oocytes to sperm and other activating stimuli. Dev Biol. 1981 Apr 15;83(1):33–41. doi: 10.1016/s0012-1606(81)80005-x. [DOI] [PubMed] [Google Scholar]
  30. Schroeder T. E., Strickland D. L. Ionophore A23187, calcium and contractility in frog eggs. Exp Cell Res. 1974 Jan;83(1):139–142. doi: 10.1016/0014-4827(74)90696-x. [DOI] [PubMed] [Google Scholar]
  31. Somlyo A. V. Bridging structures spanning the junctioning gap at the triad of skeletal muscle. J Cell Biol. 1979 Mar;80(3):743–750. doi: 10.1083/jcb.80.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Somlyo A. V., Gonzalez-Serratos H. G., Shuman H., McClellan G., Somlyo A. P. Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron-probe study. J Cell Biol. 1981 Sep;90(3):577–594. doi: 10.1083/jcb.90.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Steinhardt R. A., Epel D., Carroll E. J., Jr, Yanagimachi R. Is calcium ionophore a universal activator for unfertilised eggs? Nature. 1974 Nov 1;252(5478):41–43. doi: 10.1038/252041a0. [DOI] [PubMed] [Google Scholar]
  34. Wallace R. A., Jared D. W., Dumont J. N., Sega M. W. Protein incorporation by isolated amphibian oocytes. 3. Optimum incubation conditions. J Exp Zool. 1973 Jun;184(3):321–333. doi: 10.1002/jez.1401840305. [DOI] [PubMed] [Google Scholar]
  35. Wallace R. A., Steinhardt R. A. Maturation of Xenopus oocytes. II. Observations on membrane potential. Dev Biol. 1977 Jun;57(2):305–316. doi: 10.1016/0012-1606(77)90217-2. [DOI] [PubMed] [Google Scholar]
  36. Wasserman W. J., Masui Y. Initiation of meiotic maturation in Xenopus laevis oocytes by the combination of divalent cations and ionophore A23187. J Exp Zool. 1975 Sep;193(3):369–375. doi: 10.1002/jez.1401930313. [DOI] [PubMed] [Google Scholar]
  37. Wasserman W. J., Pinto L. H., O'Connor C. M., Smith L. D. Progesterone induces a rapid increase in [Ca2+]in of Xenopus laevis oocytes. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1534–1536. doi: 10.1073/pnas.77.3.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wolf D. P., Hedrick J. L. A molecular approach to fertilization. II. Viability and artificial fertilization of Xenopus laevis gemetes. Dev Biol. 1971 Jul;25(3):348–359. doi: 10.1016/0012-1606(71)90036-4. [DOI] [PubMed] [Google Scholar]
  39. Wolf D. P. The cortical response in Xenopus laevis ova. Dev Biol. 1974 Sep;40(1):102–115. doi: 10.1016/0012-1606(74)90112-2. [DOI] [PubMed] [Google Scholar]

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

RESOURCES