Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Role of calcium in the localization of maternal poly(A)+RNA and tubulin mRNA in Xenopus oocytes

  • 33 Accesses

  • 16 Citations


Poly(A)+RNA and tubulin mRNA are localized in the periphery of Xenopus oocytes and become delocalized during meiotic maturation. Delocalization of this RNA can be triggered by incubation in agents which reduce entry of calcium ions into the cell (e.g. lanthanum chloride and verapamil). Although these agents ordinarily promote meiotic maturation, addition of theophylline to the medium will inhibit maturation but not delocalization. Manipulations which prevent calcium entry without inducing meiotic maturation (e.g. calcium-free buffer) are also shown to trigger disruption of the RNA localization. In addition, manipulations which reduce chloride efflux from the cell (e.g. increasing the external chloride ion concentration with choline chloride) result in disruption of the localization of poly (A)+ RNA and tubulin mRNA without inducing meiotic maturation. The calcium-dependent chloride efflux present in Xenopus oocytes disappears after the oocyte has been stimulated to proceed through meiotic maturation. We show that reduction of the influx of calcium ions or efflux of chloride ions induces the delocalization of poly (A)+RNA and tubulin mRNA without inducing meiotic maturation. We suggest, therefore, that reducing the transmembrane movement of these ions is likely to be the natural trigger for the delocalization of poly(A)+RNA and tubulin mRNA.

This is a preview of subscription content, log in to check access.


  1. Baker PF (1976) The regulation of intracellular calcium. Symp Soc Exptl Biol 30:67–88

  2. Balinsky BI, Devis RJ (1963) Origin and differentiation of cytoplasmic structures in the oocytes of Xenopus laevis. Acta Embryol Morphol Exp 6:55–108

  3. Barish ME (1983) A transient calcium-dependent chloride current in the immature Xenopus oocyte. J Physiol 342:309–325

  4. Beers RF Jr (1960) Hydrolysis of polyadenylic acid by pancreatic ribonuclease. J Biol Chem 235:2393–2398

  5. Borgens RB, Vanable JW Jr, Jaffe LF (1977) Bioelectricity and regeneration: large currents leave the stumps of regenerating newt limbs. Proc Natl Acad Sci USA 74:4528–4532

  6. Buchanan ES (1986) Distribution of specific mRNAs during oogenesis in Xenopus laevis. J Cell Biol 103:479a

  7. Capco DG (1982) The spatial pattern of RNA in fully grown oocytes of an amphibian, Xenopus laevis. J Exp Zool 219:147–154

  8. Capco DG, Jäckle H (1982) Localized protein synthesis during oogenesis of Xenopus laevis: analysis by in situ translation. Dev Biol 94:41–50

  9. Capco DG, Jeffery WR (1982) Transient localizations of messenger RNA in Xenopus laevis oocytes. Dev Biol 89:1–12

  10. Capco DG, McGaughey RW (1986) Cytoskeletal reorganization during early mammalian development: analysis using embedment-free sections. Dev Biol 115:446–458

  11. Capco DG, Mecca MD (1988) Analysis of proteins in the peripheral and central region of amphibian oocytes and eggs. Cell Differ 23:(in press)

  12. Charbonneau M, Grey RD (1984) The onset of activation responsiveness during maturation coincides with the formation of the cortical endoplasmic reticulum in oocytes of Xenopus laevis. Dev Biol 102:90–97

  13. Craig SW, Powell LD (1980) Regulation of actin polymerization by Villin, a 95,000 dalton cytoskeletal component of intestinal brush borders. Cell 22:739–746

  14. Darnell JE, Wall R, Tuchinski R (1971) An adenylic acid-rich sequence in messenger RNA of HeLa cells and its possible relationship to reiterated sites in DNA. Proc Natl Acad Sci USA 68:1321–1325

  15. Dworkin MB, Dworkin-Rastl E (1985) Changes in RNA titers and polyadenylation during oogenesis and oocyte maturation in Xenopus laevis. Dev Biol 112:451–457

  16. Fleckenstein A (1977) Specific pharmacology of calcium in myocardium, cardiac pacemakers, and vascular smooth muscle. Ann Rev Pharmacol Toxicol 17:149–166

  17. Galigher AE, Kozloff EN (1971) In: Essentials of practical microtechnique, Lea and Febiger, New York

  18. Glenney JR Jr, Glenney P, Weber K (1983) The spectrin-related molecule, TW-260/240 cross-links the actin bundles of the microvillus rootlets in the brush borders of intestinal epithelial cells. J Cell Biol 96:1491–1496

  19. Godsave F, Anderton BH, Heasman J, Wylie C (1984) Oocytes and early embryos of Xenopus laevis contain intermediate filaments which reach with anti-mammalian vimentin antibodies. J Embryol Exp Morphol 83:169–187

  20. Imoh H, Okamoto M, Eguchi G (1983) Accumulation of annulate lamellae in the subcortical layer during progesterone-induced oocyte maturation in Xenopus laevis. Dev Growth Differ 25:1–10

  21. Jaffe LF (1977) Electrophoresis along cell membranes. Nature 165:600–602

  22. Jaffe LF, Poo M (1979) Neurites grow faster towards the cathode than the anode in a steady field. J Exp Zool 209:115–128

  23. Jaffe LF, Stern CD (1979) Strong electrical currents leave the primitive streak of chick embryos. Science 206:569–571

  24. Jeffery WR (1982) Messenger RNA in the cytoskeletal framework: analysis by in situ hybridization. J Cell Biol 95:1–7

  25. Jeffery WR (1985) The spatial distribution of maternal mRNA is determined by a cortical cytoskeletal domain in Chaetopterus eggs. Dev Biol 110:217–229

  26. King ML, Barklis E (1985) Regional distribution of maternal messenger RNA in the amphibian oocyte. Dev Biol 112:203–212

  27. Langer GA, Frank JS (1972) Lanthanum in heart cell culture: effect on calcium exchange correlated with its localization. J Cell Biol 54:441–455

  28. Larabell CA, Chandler DE (1988) Freeze-fracture analysis of structural reorganization during meiotic maturation in Xenopus laevis oocytes. Cell Tissue Res 251:129–136

  29. Lenk R, Ranson L, Kaufmann Y, Penman S (1977) A cytoskeletal structure with associated polyribosomes obtained from HeLa cells. Cell 10:67–78

  30. Maller JL, Butcher FR, Krebs EG (1979) Early effect of progesterone on levels of cyclic adenosine 3′∶5′-monophosphate in Xenopus oocytes. J Biol Chem 254:579–582

  31. Miledi R (1971) Lanthanum ions abolish the “calcium response” of nerve terminals. Nature 229:410

  32. Mooseker MS (1983) Actin binding proteins of the brush border. Cell 35:11–13

  33. Moreau M, Vilain JP, Guerrier P (1980) Free calcium changes associated with hormone action in amphibian oocytes. Dev Biol 78:201–214

  34. Nachsen DA, Blaustein MP (1979) The effects of some organic “calcium antagonists” on calcium influx in presynaptic nerve terminals. Mol Pharmacol 16:579–586

  35. Nuccitelli R, Wiley LM (1985) Polarity of isolated blastomeres from mouse morulae: detection of transcellular ion currents. Dev Biol 109:452–463

  36. O'Connor CM, Smith LD (1976) Inhibition of oocyte maturation by theophylline: possible mechanism of action. Dev Biol 52:318–322

  37. O'Connor CM, Robinson KR, Smith LD (1977) Calcium, potassium, and sodium exchange by full-grown and maturing Xenopus laevis oocytes. Dev Biol 62:28–40

  38. Phillips CR (1985) Spatial changes in poly(A) concentrations during early embryogenesis in Xenopus laevis: analysis by in situ hybridization. Dev Biol 109:299–310

  39. Pinto JEB, Trifaro JM (1976) The different effects of D-600 (methoxyverapamil) on the release of adrenal catecholamines induced by acetylcholine, high potassium, or sodium deprivation. Br J Pharmacol 57:127–143

  40. Poo M (1981) In situ electrophoresis of membrane components. Ann Rev Bioeng 10:245–276

  41. Ritchie AK (1979) Catecholamine secretion in a rat pheochromocytoma cell line: two pathways for calcium entry. J Physiol 286:541–561

  42. Robinson KR (1979) Electrical currents through full-grown and maturing Xenopus oocytes. Proc Natl Acad Sci USA 76:837–841

  43. Schorderet-Slatkine S, Schorderet M, Baulieu EE (1976) Initiation of meiotic maturation in Xenopus laevis oocytes by lanthanum. Nature 262:289–290

  44. Schorderet-Slatkine S, Schorderet M, Baulieu EE (1977) Progesterone-induced meiotic reinitiation in vitro in Xenopus laevis oocytes: a role for displacement of membrane-bound calcium. Differentiation 9:67–76

  45. Steinhardt R, Zucker R, Schatten G (1977) Intracellular calcium release at fertilization in the sea urchin egg. Dev Biol 58:185–196

  46. Telfer WH, Woodruff RI, Huebner E (1981) Electrical polarity and cellular differentiation in meroistic ovaries. Am Zool 21:675–686

  47. Wallace RA, Steinhardt RA (1977) Maturation of Xenopus oocytes. II. Observations on membrane potential. Dev Biol 57:305–316

  48. Wasserman WJ, Pinto LH, O'Connor CR, Smith LD (1980) Progesterone induces a rapid increase in [Ca2+] in Xenopus laevis oocytes. Proc Natl Acad Sci USA 77:1534–1536

  49. Weinberger CP, Brick I (1980) Locomotion and adhesion of amphibian gastrula and neurula cells cultured on substrata of varied surface charge. Exp Cell Res 130:251–263

  50. Weiss GB (1974) Cellular pharmacology of lanthanum. Ann Rev Pharmacol 14:343–354

  51. Woodruff RI, Telfer WH (1973) Polarized intracellular bridges in ovarian follicles of the Cecropia moth. J Cell Biol 58:172–188

  52. Woodruff RI, Telfer WH (1980) Electrophoresis of proteins in intercellular bridges. Nature 286:84–86

  53. Wylie CC, Brown D, Godsave SF, Quarmby J, Heasman J (1985) The cytoskeleton of Xenopus oocytes and its role in development. J Embryol Exp Morphol [Suppl] 89:1–15

Download references

Author information

Correspondence to David G. Capco.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Larabell, C.A., Capco, D.G. Role of calcium in the localization of maternal poly(A)+RNA and tubulin mRNA in Xenopus oocytes. Roux's Arch Dev Biol 197, 175–183 (1988).

Download citation

Key words

  • Ca2+/Cl1− transmembrane flux
  • Oocytes
  • Meiotic maturation
  • mRNA