Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Aug 1;90(2):362–371. doi: 10.1083/jcb.90.2.362

Microfilament-mediated surface change in starfish oocytes in response to 1-methyladenine: implications for identifying the pathway and receptor sites for maturation-inducing hormones

PMCID: PMC2111864  PMID: 6270153

Abstract

Oocytes of the starfish Pisaster ochraceus exhibit an early response to 1-methyladenine (the maturation-inducing hormone), which is described for the first time. In this response approximately 6,500 spikelike surface projections, much larger than microvilli, emerge transiently from oocytes stripped of their follicle cells and then treated with the hormone in vitro. Each spike contains a prominent bundle of microfilaments, possibly composed of actin. The distribution of spikes when follicle cells are only partially removed and the morphological details of the normal junctional association between follicle cells and oocytes suggest that 1-methyladenine-sensitive sites (receptor sites) can be identified with the approximately 6,500 postjunctional specializations that are part of the oocyte surface. This finding in turn is employed to construct a set of hypotheses concerning the route that 1-methyladenine normally takes from the follicle cells to an oocyte during stimulation of maturation; it is postulated that, for each oocyte, 1-methyladenine is transported along approximately 6,500 thin follicle-cell processes, it is transmitted across the junctional gaps of an equivalent number of junctions between follicle cells and an oocyte, and then interacts with the postjunctional sites where 1- methyladenine receptors are thought to be clustered. Comparative aspects of this mode of intercellular communication are discussed.

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. Albertini D. F., Anderson E. The appearance and structure of intercellular connections during the ontogeny of the rabbit ovarian follicle with particular reference to gap junctions. J Cell Biol. 1974 Oct;63(1):234–250. doi: 10.1083/jcb.63.1.234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson E., Albertini D. F. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol. 1976 Nov;71(2):680–686. doi: 10.1083/jcb.71.2.680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson E. Oocyte-follicle cell differentiation in two species of amphineurans (Mollusca), Mopalia mucosa and Chaetopleura apiculata. J Morphol. 1969 Sep;129(1):89–125. doi: 10.1002/jmor.1051290107. [DOI] [PubMed] [Google Scholar]
  4. Bluemink J. G., Tertoolen L. G. The plasma-membrance IMP pattern as related to animal/vegetal polarity in the amphibian egg. Dev Biol. 1978 Feb;62(2):334–343. doi: 10.1016/0012-1606(78)90220-8. [DOI] [PubMed] [Google Scholar]
  5. Bou-Resli M. Ultrastructural studies on the intercellular bridges between the oocyte and follicle cells in the lizard Acanthodactylus scutellatus Hardyi. Z Anat Entwicklungsgesch. 1974;143(3):239–254. doi: 10.1007/BF00519868. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Cloud J. G., Schuetz A. W. Interaction of progesterone with all or isolated portions of the amphibian (Rana pipiens) oocyte surface. Physical and biological characteristics. Dev Biol. 1977 Oct 15;60(2):359–370. doi: 10.1016/0012-1606(77)90134-8. [DOI] [PubMed] [Google Scholar]
  9. Cloud J., Schuetz A. W. Spontaneous maturation of starfish oocytes: role of follicle cells and calcium ions. Exp Cell Res. 1973 Jun;79(2):446–450. doi: 10.1016/0014-4827(73)90465-5. [DOI] [PubMed] [Google Scholar]
  10. Dekel N., Beers W. H. Development of the rat oocyte in vitro: inhibition and induction of maturation in the presence or absence of the cumulus oophorus. Dev Biol. 1980 Mar 15;75(2):247–254. doi: 10.1016/0012-1606(80)90160-8. [DOI] [PubMed] [Google Scholar]
  11. Doree M., Guerrier P. Site of action of 1-methyladenine in inducing oocyte maturation in starfish. Kinetic evidence for receptors localized on the cell membrane. Exp Cell Res. 1975 Mar 15;91(2):296–300. doi: 10.1016/0014-4827(75)90107-x. [DOI] [PubMed] [Google Scholar]
  12. Dorée M., Moreau M., Guerrier P. Hormonal control of meiosis. In vitro induced release of calcium ions from the plasma membrane in starfish oocytes. Exp Cell Res. 1978 Sep;115(2):251–260. doi: 10.1016/0014-4827(78)90279-3. [DOI] [PubMed] [Google Scholar]
  13. Dumont J. N., Brummett A. R. Oogenesis in Xenopus laevis (Daudin). V. Relationships between developing oocytes and their investing follicular tissues. J Morphol. 1978 Jan;155(1):73–97. doi: 10.1002/jmor.1051550106. [DOI] [PubMed] [Google Scholar]
  14. Eppig J. J. Mouse oocyte development in vitro with various culture systems. Dev Biol. 1977 Oct 15;60(2):371–388. doi: 10.1016/0012-1606(77)90135-x. [DOI] [PubMed] [Google Scholar]
  15. Gilula N. B., Epstein M. L., Beers W. H. Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J Cell Biol. 1978 Jul;78(1):58–75. doi: 10.1083/jcb.78.1.58. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Godeau J. F., Schorderet-Slatkine S., Hubert P., Baulieu E. E. Induction of maturation in Xenopus laevis oocytes by a steroid linked to a polymer. Proc Natl Acad Sci U S A. 1978 May;75(5):2353–2357. doi: 10.1073/pnas.75.5.2353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Guerrier P., Dorée M., Freyssinet G. Stimulation précoce des activités protéines kinases au cours du processus hormonal de réinitiation de la méiose dans les ovocytes d'Etoiles de mer. C R Acad Sci Hebd Seances Acad Sci D. 1975 Nov 17;281(20):1475–1478. [PubMed] [Google Scholar]
  18. Guerrier P., Moreau M., Doree M. Hormonal control of meiosis in starfish: stimulation of protein phosphorylation induced by 1-methyladenine. Mol Cell Endocrinol. 1977 Apr;7(2):137–150. doi: 10.1016/0303-7207(77)90063-6. [DOI] [PubMed] [Google Scholar]
  19. Gwatkin R. B., Andersen O. F. Hamster oocyte maturation in vitro: inhibition by follicular components. Life Sci. 1976 Aug 15;19(4):527–536. doi: 10.1016/0024-3205(76)90232-0. [DOI] [PubMed] [Google Scholar]
  20. Heller D. T., Schultz R. M. Ribonucleoside metabolism by mouse oocytes: metabolic cooperativity between the fully grown oocyte and cumulus cells. J Exp Zool. 1980 Dec;214(3):355–364. doi: 10.1002/jez.1402140314. [DOI] [PubMed] [Google Scholar]
  21. Hillensjö T., LeMaire W. J. Gonadotropin releasing hormone agonists stimulate meiotic maturation of follicle-enclosed rat oocytes in vitro. Nature. 1980 Sep 11;287(5778):145–146. doi: 10.1038/287145a0. [DOI] [PubMed] [Google Scholar]
  22. Hirai S., Kanatani H. Site of production of meiosis-inducing substance in ovary of starfish. Exp Cell Res. 1971 Jul;67(1):224–227. doi: 10.1016/0014-4827(71)90642-2. [DOI] [PubMed] [Google Scholar]
  23. Houk M. S., Epel D. Protein synthesis during hormonally induced meiotic maturation and fertilization in starfish oocytes. Dev Biol. 1974 Oct;40(2):298–310. doi: 10.1016/0012-1606(74)90132-8. [DOI] [PubMed] [Google Scholar]
  24. Ishikawa H., Bischoff R., Holtzer H. Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J Cell Biol. 1969 Nov;43(2):312–328. [PMC free article] [PubMed] [Google Scholar]
  25. Kanatani H., Hiramoto Y. Site of action of 1-methyladenine in inducing oocyte maturation in starfish. Exp Cell Res. 1970 Aug;61(2):280–284. doi: 10.1016/0014-4827(70)90448-9. [DOI] [PubMed] [Google Scholar]
  26. Kanatani H. Maturation-inducing substance in starfishes. Int Rev Cytol. 1973;35:253–298. doi: 10.1016/s0074-7696(08)60356-3. [DOI] [PubMed] [Google Scholar]
  27. Kishimoto T., Cayer M. L., Kanatani H. Starfish oocyte maturation and reduction of disulfide-bond on oocyte surface. Exp Cell Res. 1976 Aug;101(1):104–110. doi: 10.1016/0014-4827(76)90418-3. [DOI] [PubMed] [Google Scholar]
  28. Masui Y. Relative roles of the pituitary, follicle cells, and progesterone in the induction of oocyte maturation in Rana pipiens. J Exp Zool. 1967 Dec;166(3):365–375. doi: 10.1002/jez.1401660309. [DOI] [PubMed] [Google Scholar]
  29. Moor R. M., Smith M. W., Dawson R. M. Measurement of intercellular coupling between oocytes and cumulus cells using intracellular markers. Exp Cell Res. 1980 Mar;126(1):15–29. doi: 10.1016/0014-4827(80)90466-8. [DOI] [PubMed] [Google Scholar]
  30. Moreau M., Guerrier P., Doree M., Ashley C. C. Hormone-induced release of intracellular Ca2+ triggers meiosis in starfish oocytes. Nature. 1978 Mar 16;272(5650):251–253. doi: 10.1038/272251a0. [DOI] [PubMed] [Google Scholar]
  31. Moreau M., Guerrier P., Dorée M. Hormonal control of meiosis reinitation in starfish oocytes. New evidence for the absence of efficient intracellular receptors for l-methyladenine recognition. Exp Cell Res. 1978 Sep;115(2):245–249. doi: 10.1016/0014-4827(78)90278-1. [DOI] [PubMed] [Google Scholar]
  32. Schorderet-Slatkine S., Schorderet M., Baulieu E. Initiation of meiotic maturation in Xenopus laevis oocytes by lanthanum. Nature. 1976 Jul 22;262(5566):289–290. doi: 10.1038/262289a0. [DOI] [PubMed] [Google Scholar]
  33. Schroeder P. C. Active contraction of Starfish oocyte follicle cells after treatment with 1-methyl adenine. Naturwissenschaften. 1971 May;58(5):270–271. doi: 10.1007/BF00602999. [DOI] [PubMed] [Google Scholar]
  34. Schroeder P. C., Larsen J. H., Jr, Waldo A. E. Oocyte-follicle cell relationships in a starfish. Cell Tissue Res. 1979;203(2):249–256. doi: 10.1007/BF00237239. [DOI] [PubMed] [Google Scholar]
  35. Schuetz A. W. Action of hormones on germinal vesicle breakdown in frog (Rana pipiens) oocytes. J Exp Zool. 1967 Dec;166(3):347–354. doi: 10.1002/jez.1401660307. [DOI] [PubMed] [Google Scholar]
  36. Schuetz A. W. Cytoplasmic activation of starfish oocytes by sperm and divalent ionophore A-23187. J Cell Biol. 1975 Jul;66(1):86–94. doi: 10.1083/jcb.66.1.86. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shirai H. Effect of L-phenylalanine on I-methyladenine production and spontaneous oocyte maturation in starfish. Exp Cell Res. 1974 Jul;87(1):31–38. doi: 10.1016/0014-4827(74)90523-0. [DOI] [PubMed] [Google Scholar]
  38. Tokarz R. R. An autoradiographic study of the effects of mammalian gonadotropins (follicle-stimulating hormone and luteinizing hormone) and estradiol-17beta on [3H]thymidine labeling of surface epithelial cells, prefollicular cells, and oogonia in the ovary of the lizard Anolis carolinensis. Gen Comp Endocrinol. 1978 Jun;35(2):179–188. doi: 10.1016/0016-6480(78)90160-0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES