Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1990 Aug;10(8):4123–4129. doi: 10.1128/mcb.10.8.4123

Stability of maternal mRNA in Xenopus embryos: role of transcription and translation.

C Duval 1, P Bouvet 1, F Omilli 1, C Roghi 1, C Dorel 1, R LeGuellec 1, J Paris 1, H B Osborne 1
PMCID: PMC360935  PMID: 1695321

Abstract

The first 12 cell divisions of Xenopus laevis embryos do not require gene transcription. This means that the regulation of gene expression during this period is controlled at post transcriptional levels and makes Xenopus early development a potentially interesting biological system with which to study the mechanisms involved. We describe here the stability characteristics of several maternal Xenopus mRNAs which are deadenylated soon after fertilisation (J. Paris and M. Philippe, Dev. Biol., in press). We show that these mRNAs were only degraded in the embryo after the midblastula transition (MBT), when gene transcription was initiated. The kinetics with which the deadenylated maternal mRNAs decreased in the post-MBT embryos showed sequence specificity. The degradation of these mRNAs after the MBT was inhibited by cycloheximide but was not affected by dactinomycin. Therefore, the destabilization of these mRNAs does not appear to be initiated by new embryonic gene transcripts. Sequence comparisons of the 3' untranslated region of these mRNAs identified several motifs which may be involved in the posttranscriptional control of these gene products.

Full text

PDF
4123

Images in this article

Selected References

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

  1. Auffray C., Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. doi: 10.1111/j.1432-1033.1980.tb06030.x. [DOI] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernstein P., Peltz S. W., Ross J. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol Cell Biol. 1989 Feb;9(2):659–670. doi: 10.1128/mcb.9.2.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brewer G., Ross J. Poly(A) shortening and degradation of the 3' A+U-rich sequences of human c-myc mRNA in a cell-free system. Mol Cell Biol. 1988 Apr;8(4):1697–1708. doi: 10.1128/mcb.8.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cascio S., Gurdon J. B. The initiation of new gene transcription during Xenopus gastrulation requires immediately preceding protein synthesis. Development. 1987 Jun;100(2):297–305. doi: 10.1242/dev.100.2.297. [DOI] [PubMed] [Google Scholar]
  6. Casey J. L., Hentze M. W., Koeller D. M., Caughman S. W., Rouault T. A., Klausner R. D., Harford J. B. Iron-responsive elements: regulatory RNA sequences that control mRNA levels and translation. Science. 1988 May 13;240(4854):924–928. doi: 10.1126/science.2452485. [DOI] [PubMed] [Google Scholar]
  7. Colot H. V., Rosbash M. Behavior of individual maternal pA+ RNAs during embryogenesis of Xenopus laevis. Dev Biol. 1982 Nov;94(1):79–86. doi: 10.1016/0012-1606(82)90070-7. [DOI] [PubMed] [Google Scholar]
  8. Dani C., Blanchard J. M., Piechaczyk M., El Sabouty S., Marty L., Jeanteur P. Extreme instability of myc mRNA in normal and transformed human cells. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7046–7050. doi: 10.1073/pnas.81.22.7046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gurdon J. B., Brennan S., Fairman S., Mohun T. J. Transcription of muscle-specific actin genes in early Xenopus development: nuclear transplantation and cell dissociation. Cell. 1984 Oct;38(3):691–700. doi: 10.1016/0092-8674(84)90264-2. [DOI] [PubMed] [Google Scholar]
  10. Kelly R., Shaw D. R., Ennis H. L. Role of protein synthesis in decay and accumulation of mRNA during spore germination in the cellular slime mold Dictyostelium discoideum. Mol Cell Biol. 1987 Feb;7(2):799–805. doi: 10.1128/mcb.7.2.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kowalski J., Denhardt D. T. Regulation of the mRNA for monocyte-derived neutrophil-activating peptide in differentiating HL60 promyelocytes. Mol Cell Biol. 1989 May;9(5):1946–1957. doi: 10.1128/mcb.9.5.1946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Krieg P. A., Melton D. A. Developmental regulation of a gastrula-specific gene injected into fertilized Xenopus eggs. EMBO J. 1985 Dec 16;4(13A):3463–3471. doi: 10.1002/j.1460-2075.1985.tb04105.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Krowczynska A., Yenofsky R., Brawerman G. Regulation of messenger RNA stability in mouse erythroleukemia cells. J Mol Biol. 1985 Jan 20;181(2):231–239. doi: 10.1016/0022-2836(85)90087-7. [DOI] [PubMed] [Google Scholar]
  14. Kruijer W., Cooper J. A., Hunter T., Verma I. M. Platelet-derived growth factor induces rapid but transient expression of the c-fos gene and protein. Nature. 1984 Dec 20;312(5996):711–716. doi: 10.1038/312711a0. [DOI] [PubMed] [Google Scholar]
  15. Mercer J. F., Wake S. A. An analysis of the rate of metallothionein mRNA poly(A)-shortening using RNA blot hybridization. Nucleic Acids Res. 1985 Nov 25;13(22):7929–7943. doi: 10.1093/nar/13.22.7929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Müller R., Bravo R., Burckhardt J., Curran T. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature. 1984 Dec 20;312(5996):716–720. doi: 10.1038/312716a0. [DOI] [PubMed] [Google Scholar]
  17. Nakai H., Maxwell I. H., Pizer L. I. Herpesvirus infection alters the steady-state levels of cellular polyadenylated RNA in polyoma virus-transformed BHK cells. J Virol. 1982 Jun;42(3):1131–1134. doi: 10.1128/jvi.42.3.1131-1134.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nakakura N., Miura T., Yamana K., Ito A., Shiokawa K. Synthesis of heterogeneous mRNA-like RNA and low-molecular-weight RNA before the midblastula transition in embryos of Xenopus laevis. Dev Biol. 1987 Oct;123(2):421–429. doi: 10.1016/0012-1606(87)90400-3. [DOI] [PubMed] [Google Scholar]
  19. Owen D., Kühn L. C. Noncoding 3' sequences of the transferrin receptor gene are required for mRNA regulation by iron. EMBO J. 1987 May;6(5):1287–1293. doi: 10.1002/j.1460-2075.1987.tb02366.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Paris J., Osborne H. B., Couturier A., Le Guellec R., Philippe M. Changes in the polyadenylation of specific stable RNA during the early development of Xenopus laevis. Gene. 1988 Dec 10;72(1-2):169–176. doi: 10.1016/0378-1119(88)90139-4. [DOI] [PubMed] [Google Scholar]
  21. Petersen D. D., Koch S. R., Granner D. K. 3' noncoding region of phosphoenolpyruvate carboxykinase mRNA contains a glucocorticoid-responsive mRNA-stabilizing element. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7800–7804. doi: 10.1073/pnas.86.20.7800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Raj N. B., Pitha P. M. Two levels of regulation of beta-interferon gene expression in human cells. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3923–3927. doi: 10.1073/pnas.80.13.3923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Restifo L. L., Guild G. M. Poly(A) shortening of coregulated transcripts in Drosophila. Dev Biol. 1986 Jun;115(2):507–510. doi: 10.1016/0012-1606(86)90271-x. [DOI] [PubMed] [Google Scholar]
  24. Ross J. Messenger RNA turnover in eukaryotic cells. Mol Biol Med. 1988 Feb;5(1):1–14. [PubMed] [Google Scholar]
  25. 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]
  26. Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986 Aug 29;46(5):659–667. doi: 10.1016/0092-8674(86)90341-7. [DOI] [PubMed] [Google Scholar]
  27. Steel L. F., Jacobson A. Translational control of ribosomal protein synthesis during early Dictyostelium discoideum development. Mol Cell Biol. 1987 Mar;7(3):965–972. doi: 10.1128/mcb.7.3.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wilson M. C., Sawicki S. G., White P. A., Darnell J. E., Jr A correlation between the rate of poly(A) shortening and half-life of messenger RNA in adenovirus transformed cells. J Mol Biol. 1978 Nov 25;126(1):23–36. doi: 10.1016/0022-2836(78)90277-2. [DOI] [PubMed] [Google Scholar]
  29. Wilson T., Treisman R. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3' AU-rich sequences. Nature. 1988 Nov 24;336(6197):396–399. doi: 10.1038/336396a0. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES