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. 1990 Mar 1;110(3):597–605. doi: 10.1083/jcb.110.3.597

Differential regulation of the levels of three gap junction mRNAs in Xenopus embryos

PMCID: PMC2116035  PMID: 2155241

Abstract

Xenopus mRNAs that potentially encode gap junction proteins in the oocyte and early embryo have been identified by low-stringency screening of cDNA libraries with cloned mammalian gap junction cDNAs. The levels of these mRNAs show strikingly different temporal regulation and tissue distribution. Using a nomenclature designed to stress important structural similarities of distinct gap junction gene products, the deduced polypeptides have been designated the Xenopus alpha 1 and alpha 2 gap junction proteins. The alpha 2 gap junction mRNA is a maternal transcript that disappears by the late gastrula stage. It is not detected in any organ of the adult except the ovary, and resides primarily, if not exclusively, in the oocytes and early embryos. The alpha 1 gap junction mRNA appears during organogenesis, and is detected in RNA from a wide variety of organs. It is also found in full-grown oocytes, but is rapidly degraded upon oocyte maturation, both in vivo and in vitro. The alpha 1 and alpha 2 mRNAs encode proteins with different degrees of amino acid sequence similarity to the predominant gap junction subunit of the mammalian heart (connexin 43). Together with our earlier report of a mid-embryonic (beta 1) gap junction mRNA, the results suggest that intercellular communication during oocyte growth and postfertilization development is a complex phenomenon involving the coordinated regulation of several genes.

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Selected References

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

  1. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  2. Beyer E. C., Kistler J., Paul D. L., Goodenough D. A. Antisera directed against connexin43 peptides react with a 43-kD protein localized to gap junctions in myocardium and other tissues. J Cell Biol. 1989 Feb;108(2):595–605. doi: 10.1083/jcb.108.2.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beyer E. C., Paul D. L., Goodenough D. A. Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J Cell Biol. 1987 Dec;105(6 Pt 1):2621–2629. doi: 10.1083/jcb.105.6.2621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blackshaw S. E., Warner A. E. Low resistance junctions between mesoderm cells during development of trunk muscles. J Physiol. 1976 Feb;255(1):209–230. doi: 10.1113/jphysiol.1976.sp011276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Dahl G., Miller T., Paul D., Voellmy R., Werner R. Expression of functional cell-cell channels from cloned rat liver gap junction complementary DNA. Science. 1987 Jun 5;236(4806):1290–1293. doi: 10.1126/science.3035715. [DOI] [PubMed] [Google Scholar]
  7. Decker R. S., Friend D. S. Assembly of gap junctions during amphibian neurulation. J Cell Biol. 1974 Jul;62(1):32–47. doi: 10.1083/jcb.62.1.32. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  9. Ebihara L., Beyer E. C., Swenson K. I., Paul D. L., Goodenough D. A. Cloning and expression of a Xenopus embryonic gap junction protein. Science. 1989 Mar 3;243(4895):1194–1195. doi: 10.1126/science.2466337. [DOI] [PubMed] [Google Scholar]
  10. Epstein M. L., Gilula N. B. A study of communication specificity between cells in culture. J Cell Biol. 1977 Dec;75(3):769–787. doi: 10.1083/jcb.75.3.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  12. Fraser S. E., Bryant P. J. Patterns of dye coupling in the imaginal wing disk of Drosophila melanogaster. Nature. 1985 Oct 10;317(6037):533–536. doi: 10.1038/317533a0. [DOI] [PubMed] [Google Scholar]
  13. Fraser S. E., Green C. R., Bode H. R., Gilula N. B. Selective disruption of gap junctional communication interferes with a patterning process in hydra. Science. 1987 Jul 3;237(4810):49–55. doi: 10.1126/science.3037697. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Gimlich R. L., Kumar N. M., Gilula N. B. Sequence and developmental expression of mRNA coding for a gap junction protein in Xenopus. J Cell Biol. 1988 Sep;107(3):1065–1073. doi: 10.1083/jcb.107.3.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goodenough D. A., Paul D. L., Jesaitis L. Topological distribution of two connexin32 antigenic sites in intact and split rodent hepatocyte gap junctions. J Cell Biol. 1988 Nov;107(5):1817–1824. doi: 10.1083/jcb.107.5.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Guthrie S. C., Gilula N. B. Gap junctional communication and development. Trends Neurosci. 1989 Jan;12(1):12–16. doi: 10.1016/0166-2236(89)90150-1. [DOI] [PubMed] [Google Scholar]
  18. Guthrie S. C. Patterns of junctional communication in the early amphibian embryo. Nature. 1984 Sep 13;311(5982):149–151. doi: 10.1038/311149a0. [DOI] [PubMed] [Google Scholar]
  19. Guthrie S., Turin L., Warner A. Patterns of junctional communication during development of the early amphibian embryo. Development. 1988 Aug;103(4):769–783. doi: 10.1242/dev.103.4.769. [DOI] [PubMed] [Google Scholar]
  20. Kumar N. M., Gilula N. B. Cloning and characterization of human and rat liver cDNAs coding for a gap junction protein. J Cell Biol. 1986 Sep;103(3):767–776. doi: 10.1083/jcb.103.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Larsen W. J., Wert S. E., Brunner G. D. A dramatic loss of cumulus cell gap junctions is correlated with germinal vesicle breakdown in rat oocytes. Dev Biol. 1986 Feb;113(2):517–521. doi: 10.1016/0012-1606(86)90187-9. [DOI] [PubMed] [Google Scholar]
  22. Lee S., Gilula N. B., Warner A. E. Gap junctional communication and compaction during preimplantation stages of mouse development. Cell. 1987 Dec 4;51(5):851–860. doi: 10.1016/0092-8674(87)90108-5. [DOI] [PubMed] [Google Scholar]
  23. Michalke W., Loewenstein W. R. Communication between cells of different type. Nature. 1971 Jul 9;232(5306):121–122. doi: 10.1038/232121b0. [DOI] [PubMed] [Google Scholar]
  24. Milks L. C., Kumar N. M., Houghten R., Unwin N., Gilula N. B. Topology of the 32-kd liver gap junction protein determined by site-directed antibody localizations. EMBO J. 1988 Oct;7(10):2967–2975. doi: 10.1002/j.1460-2075.1988.tb03159.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mohana Rao J. K., Argos P. A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta. 1986 Jan 30;869(2):197–214. doi: 10.1016/0167-4838(86)90295-5. [DOI] [PubMed] [Google Scholar]
  26. Paul D. L. Molecular cloning of cDNA for rat liver gap junction protein. J Cell Biol. 1986 Jul;103(1):123–134. doi: 10.1083/jcb.103.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sargent T. D., Jamrich M., Dawid I. B. Cell interactions and the control of gene activity during early development of Xenopus laevis. Dev Biol. 1986 Mar;114(1):238–246. doi: 10.1016/0012-1606(86)90399-4. [DOI] [PubMed] [Google Scholar]
  28. Slack C., Warner A. E. Intracellular and intercellular potentials in the early amphibian embryo. J Physiol. 1973 Jul;232(2):313–330. doi: 10.1113/jphysiol.1973.sp010272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Spray D. C., Harris A. L., Bennett M. V. Voltage dependence of junctional conductance in early amphibian embryos. Science. 1979 Apr 27;204(4391):432–434. doi: 10.1126/science.312530. [DOI] [PubMed] [Google Scholar]
  30. Swenson K. I., Jordan J. R., Beyer E. C., Paul D. L. Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell. 1989 Apr 7;57(1):145–155. doi: 10.1016/0092-8674(89)90180-3. [DOI] [PubMed] [Google Scholar]
  31. Turin L., Warner A. E. Intracellular pH in early Xenopus embryos: its effect on current flow between blastomeres. J Physiol. 1980 Mar;300:489–504. doi: 10.1113/jphysiol.1980.sp013174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Warner A. E., Guthrie S. C., Gilula N. B. Antibodies to gap-junctional protein selectively disrupt junctional communication in the early amphibian embryo. Nature. 1984 Sep 13;311(5982):127–131. doi: 10.1038/311127a0. [DOI] [PubMed] [Google Scholar]
  33. Warner A. E., Lawrence P. A. Permeability of gap junctions at the segmental border in insect epidermis. Cell. 1982 Feb;28(2):243–252. doi: 10.1016/0092-8674(82)90342-7. [DOI] [PubMed] [Google Scholar]
  34. Weir M. P., Lo C. W. Gap-junctional communication compartments in the Drosophila wing imaginal disk. Dev Biol. 1984 Mar;102(1):130–146. doi: 10.1016/0012-1606(84)90181-7. [DOI] [PubMed] [Google Scholar]
  35. Young J. D., Cohn Z. A., Gilula N. B. Functional assembly of gap junction conductance in lipid bilayers: demonstration that the major 27 kd protein forms the junctional channel. Cell. 1987 Mar 13;48(5):733–743. doi: 10.1016/0092-8674(87)90071-7. [DOI] [PubMed] [Google Scholar]
  36. Zhang J. T., Nicholson B. J. Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. J Cell Biol. 1989 Dec;109(6 Pt 2):3391–3401. doi: 10.1083/jcb.109.6.3391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zimmer D. B., Green C. R., Evans W. H., Gilula N. B. Topological analysis of the major protein in isolated intact rat liver gap junctions and gap junction-derived single membrane structures. J Biol Chem. 1987 Jun 5;262(16):7751–7763. [PubMed] [Google Scholar]
  38. de Laat S. W., Tertoolen L. G., Dorresteijn A. W., van den Biggelaar J. A. Intercellular communication patterns are involved in cell determination in early molluscan development. Nature. 1980 Oct 9;287(5782):546–548. doi: 10.1038/287546a0. [DOI] [PubMed] [Google Scholar]

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