Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 Apr 1;93(1):24–32. doi: 10.1083/jcb.93.1.24

Structural organization of actin in the sea urchin egg cortex: microvillar elongation in the absence of actin filament bundle formation

DA Begg, LI Rebhun, H Hyatt
PMCID: PMC2112110  PMID: 6802856

Abstract

We have investigated the relationship between the formation of actin filament bundles and the elongation of microvilli (MV) after fertilization in sea urchin eggs. In a previous study (1979, J Cell Biol. 83:241-248) we demonstrated that increased pH induced the formation of actin filaments in isolated sea urchin egg cortices with the concomitant elongation of MV. On the basis of these results we suggested that increased cytoplasmic pH after fertilization causes a reorganization of cortical actin, which in turn provides the force for MV elongation. To test this hypothesis, we compared the morphology of microvilli in eggs activated with and without the release of fertilization acid. Activation of eggs in normal sea water with the calcium ionophore A23187 causes the release of fertilization acid and the elongation of MV containing core bundles of actin filaments. Eggs activated with A23187 in NA(+)-free water do not undergo normal fertilization acid release but develop elongated, flaccid MV. These MV contain an irregular network of actin filaments rather than the parallel bundles of filaments found in normal MV. The addition of 40 mM NaCl to these eggs results in the release of H(+) and the concomitant conversion of flaccid MV to erect MV containing typical core bundles of actin filaments. Identical results are obtained when 10 mM NH(4)Cl is substituted for NaCl. The induction of cytoplasmic alkalinization in unactivated eggs with NH(4)Cl does not cause either MV elongation or the formation of actin filament bundles . These results suggest that: (a) the elongation of MV is stimulated by a rise in intracellular free Ca(++) concentration; (b) actin filament bundle formation is triggered by an increase in cytoplasmic pH; and (c) the formation of actin filament bundles is not necessary for MV elongation but is required to provide rigid support for MV.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

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

  1. Begg D. A., Rebhun L. I. pH regulates the polymerization of actin in the sea urchin egg cortex. J Cell Biol. 1979 Oct;83(1):241–248. doi: 10.1083/jcb.83.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Begg D. A., Rodewald R., Rebhun L. I. The visualization of actin filament polarity in thin sections. Evidence for the uniform polarity of membrane-associated filaments. J Cell Biol. 1978 Dec;79(3):846–852. doi: 10.1083/jcb.79.3.846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bryan J., Kane R. E. Separation and interaction of the major components of sea urchin actin gel. J Mol Biol. 1978 Oct 25;125(2):207–224. doi: 10.1016/0022-2836(78)90345-5. [DOI] [PubMed] [Google Scholar]
  4. Burgess D. R., Schroeder T. E. Polarized bundles of actin filaments within microvilli of fertilized sea urchin eggs. J Cell Biol. 1977 Sep;74(3):1032–1037. doi: 10.1083/jcb.74.3.1032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carron C. P., Longo F. J. Relation of cytoplasmic alkalinization to microvillar elongation and microfilament formation in the sea urchin egg. Dev Biol. 1982 Jan;89(1):128–137. doi: 10.1016/0012-1606(82)90301-3. [DOI] [PubMed] [Google Scholar]
  6. Chambers C., Grey R. D. Development of the structural components of the brush border in absorptive cells of the chick intestine. Cell Tissue Res. 1979;204(3):387–405. doi: 10.1007/BF00233651. [DOI] [PubMed] [Google Scholar]
  7. Chambers E. L., Hinkley R. E. Non-propagated cortical reactions induced by the divalent ionophore A23187 in eggs of the sea urchin, Lytechinus variegatus. Exp Cell Res. 1979 Dec;124(2):441–446. doi: 10.1016/0014-4827(79)90221-0. [DOI] [PubMed] [Google Scholar]
  8. Chambers E. L., Pressman B. C., Rose B. The activation of sea urchin eggs by the divalent ionophores A23187 and X-537A. Biochem Biophys Res Commun. 1974 Sep 9;60(1):126–132. doi: 10.1016/0006-291x(74)90181-8. [DOI] [PubMed] [Google Scholar]
  9. Chandler D. E., Heuser J. Membrane fusion during secretion: cortical granule exocytosis in sex urchin eggs as studied by quick-freezing and freeze-fracture. J Cell Biol. 1979 Oct;83(1):91–108. doi: 10.1083/jcb.83.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chandler D. E., Heuser J. Postfertilization growth of microvilli in the sea urchin egg: new views from eggs that have been quick-frozen, freeze-fractured, and deeply etched. Dev Biol. 1981 Mar;82(2):393–400. doi: 10.1016/0012-1606(81)90463-2. [DOI] [PubMed] [Google Scholar]
  11. Eddy E. M., Shapiro B. M. Changes in the topography of the sea urchin egg after fertilization. J Cell Biol. 1976 Oct;71(1):35–48. doi: 10.1083/jcb.71.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Epel D. Activation of an Na + -dependent amino acid transport system upon fertilization of sea urchin eggs. Exp Cell Res. 1972 May;72(1):74–89. doi: 10.1016/0014-4827(72)90569-1. [DOI] [PubMed] [Google Scholar]
  13. Epel D. Mechanisms of activation of sperm and egg during fertilization of sea urchin gametes. Curr Top Dev Biol. 1978;12:185–246. doi: 10.1016/s0070-2153(08)60597-9. [DOI] [PubMed] [Google Scholar]
  14. Epel D., Steinhardt R., Humphreys T., Mazia D. An analysis of the partial metabolic derepression of sea urchin eggs by ammonia: the existence of independent pathways. Dev Biol. 1974 Oct;40(2):245–255. doi: 10.1016/0012-1606(74)90127-4. [DOI] [PubMed] [Google Scholar]
  15. Grainger J. L., Winkler M. M., Shen S. S., Steinhardt R. A. Intracellular pH controls protein synthesis rate in the sea urchine egg and early embryo. Dev Biol. 1979 Feb;68(2):396–406. doi: 10.1016/0012-1606(79)90213-6. [DOI] [PubMed] [Google Scholar]
  16. Harris P. Cortical fibers in fertilized eggs of the sea urchin Strongylocentrotus purpuratus. Exp Cell Res. 1968 Oct;52(2):677–681. doi: 10.1016/0014-4827(68)90509-0. [DOI] [PubMed] [Google Scholar]
  17. Hartwig J. H., Tyler J., Stossel T. P. Actin-binding protein promotes the bipolar and perpendicular branching of actin filaments. J Cell Biol. 1980 Dec;87(3 Pt 1):841–848. doi: 10.1083/jcb.87.3.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jaffe L. A. Fast block to polyspermy in sea urchin eggs is electrically mediated. Nature. 1976 May 6;261(5555):68–71. doi: 10.1038/261068a0. [DOI] [PubMed] [Google Scholar]
  19. Jaffe L. A., Robinson K. R. Membrane potential of the unfertilized sea urchin egg. Dev Biol. 1978 Jan;62(1):215–228. doi: 10.1016/0012-1606(78)90103-3. [DOI] [PubMed] [Google Scholar]
  20. Johnson C. H., Epel D. Intracellular pH of sea urchin eggs measured by the dimethyloxazolidinedione (DMO) method. J Cell Biol. 1981 May;89(2):284–291. doi: 10.1083/jcb.89.2.284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johnson J. D., Epel D. Intracellular pH and activation of sea urchin eggs after fertilisation. Nature. 1976 Aug 19;262(5570):661–664. doi: 10.1038/262661a0. [DOI] [PubMed] [Google Scholar]
  22. Otto J. J., Kane R. E., Bryan J. Formation of filopodia in coelomocytes: localization of fascin, a 58,000 dalton actin cross-linking protein. Cell. 1979 Jun;17(2):285–293. doi: 10.1016/0092-8674(79)90154-5. [DOI] [PubMed] [Google Scholar]
  23. Otto J. J., Kane R. E., Bryan J. Redistribution of actin and fascin in sea urchin eggs after fertilization. Cell Motil. 1980;1(1):31–40. doi: 10.1002/cm.970010104. [DOI] [PubMed] [Google Scholar]
  24. Paul M., Epel D. Formation of fertilization acid by sea urchin eggs does not require specific cations. Exp Cell Res. 1975 Aug;94(1):1–6. doi: 10.1016/0014-4827(75)90524-8. [DOI] [PubMed] [Google Scholar]
  25. Schroeder T. E. Microvilli on sea urchin eggs: a second burst of elongation. Dev Biol. 1978 Jun;64(2):342–346. doi: 10.1016/0012-1606(78)90085-4. [DOI] [PubMed] [Google Scholar]
  26. Schroeder T. E. Surface area change at fertilization: resorption of the mosaic membrane. Dev Biol. 1979 Jun;70(2):306–326. doi: 10.1016/0012-1606(79)90030-7. [DOI] [PubMed] [Google Scholar]
  27. Shen S. S., Steinhardt R. A. Direct measurement of intracellular pH during metabolic derepression of the sea urchin egg. Nature. 1978 Mar 16;272(5650):253–254. doi: 10.1038/272253a0. [DOI] [PubMed] [Google Scholar]
  28. Shen S. S., Steinhardt R. A. Intracellular pH and the sodium requirement at fertilisation. Nature. 1979 Nov 1;282(5734):87–89. doi: 10.1038/282087a0. [DOI] [PubMed] [Google Scholar]
  29. Shen S. S., Steinhardt R. A. Intracellular pH controls the development of new potassium conductance after fertilization of the sea urchin egg. Exp Cell Res. 1980 Jan;125(1):55–61. doi: 10.1016/0014-4827(80)90188-3. [DOI] [PubMed] [Google Scholar]
  30. Spiegel E., Spiegel M. Microvilli in sea urchin eggs. Differences in their formation and type. Exp Cell Res. 1977 Oct 15;109(2):462–466. doi: 10.1016/0014-4827(77)90030-1. [DOI] [PubMed] [Google Scholar]
  31. Steinhardt R. A., Epel D. Activation of sea-urchin eggs by a calcium ionophore. Proc Natl Acad Sci U S A. 1974 May;71(5):1915–1919. doi: 10.1073/pnas.71.5.1915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Steinhardt R. A., Lundin L., Mazia D. Bioelectric responses of the echinoderm egg to fertilization. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2426–2430. doi: 10.1073/pnas.68.10.2426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Steinhardt R. A., Mazia D. Development of K + -conductance and membrane potentials in unfertilized sea urchin eggs after exposure to NH 4 OH. Nature. 1973 Feb 9;241(5389):400–401. doi: 10.1038/241400a0. [DOI] [PubMed] [Google Scholar]
  34. Tilney L. G., Hatano S., Ishikawa H., Mooseker M. S. The polymerization of actin: its role in the generation of the acrosomal process of certain echinoderm sperm. J Cell Biol. 1973 Oct;59(1):109–126. doi: 10.1083/jcb.59.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tilney L. G., Jaffe L. A. Actin, microvilli, and the fertilization cone of sea urchin eggs. J Cell Biol. 1980 Dec;87(3 Pt 1):771–782. doi: 10.1083/jcb.87.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tilney L. G., Kiehart D. P., Sardet C., Tilney M. Polymerization of actin. IV. Role of Ca++ and H+ in the assembly of actin and in membrane fusion in the acrosomal reaction of echinoderm sperm. J Cell Biol. 1978 May;77(2):536–550. doi: 10.1083/jcb.77.2.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wilt F. H., Mazia D. The stimulation of cytoplasmic polyadenylylation in sea urchin eggs by ammonia. Dev Biol. 1974 Apr;37(2):422–424. doi: 10.1016/0012-1606(74)90158-4. [DOI] [PubMed] [Google Scholar]
  38. Zucker R. S., Steinhardt R. A., Winkler M. M. Intracellular calcium release and the mechanisms of parthenogenetic activation of the sea urchin egg. Dev Biol. 1978 Aug;65(2):285–295. doi: 10.1016/0012-1606(78)90028-3. [DOI] [PubMed] [Google Scholar]

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

RESOURCES