Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1990 Feb;10(2):816–822. doi: 10.1128/mcb.10.2.816

The 5' untranslated region of mRNA for ribosomal protein S19 is involved in its translational regulation during Xenopus development.

P Mariottini 1, F Amaldi 1
PMCID: PMC360883  PMID: 2300060

Abstract

During Xenopus development, the synthesis of ribosomal proteins is regulated at the translational level. To identify the region of the ribosomal protein mRNAs responsible for their typical translational behavior, we constructed a fused gene in which the upstream sequences (promoter) and the 5' untranslated sequence (first exon) of the gene coding for Xenopus ribosomal protein S19 were joined to the coding portion of the procaryotic chloramphenicol acetyltransferase (CAT) gene deleted of its own 5' untranslated region. This fused gene was introduced in vivo by microinjection into Xenopus fertilized eggs, and its activity was monitored during embryogenesis. By analyzing the pattern of appearance of CAT activity and the distribution of the S19-CAT mRNA between polysomes and messenger ribonucleoproteins, it was concluded that the 35-nucleotide-long 5' untranslated region of the S19 mRNA is able to confer to the fused S19-CAT mRNA the translational behavior typical of ribosomal proteins during Xenopus embryo development.

Full text

PDF
816

Images in this article

Selected References

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

  1. Amaldi F., Beccari E., Bozzoni I., Luo Z. X., Pierandrei-Amaldi P. Nucleotide sequences of cloned cDNA fragments specific for six Xenopus laevis ribosomal proteins. Gene. 1982 Mar;17(3):311–316. doi: 10.1016/0378-1119(82)90147-0. [DOI] [PubMed] [Google Scholar]
  2. Amaldi F., Bozzoni I., Beccari E., Pierandrei-Amaldi P. Expression of ribosomal protein genes and regulation of ribosome biosynthesis in Xenopus development. Trends Biochem Sci. 1989 May;14(5):175–178. doi: 10.1016/0968-0004(89)90269-7. [DOI] [PubMed] [Google Scholar]
  3. Baum E. Z., Wormington W. M. Coordinate expression of ribosomal protein genes during Xenopus development. Dev Biol. 1985 Oct;111(2):488–498. doi: 10.1016/0012-1606(85)90500-7. [DOI] [PubMed] [Google Scholar]
  4. Beccari E., Mazzetti P., Mileo A., Bozzoni I., Pierandrei-Amaldi P., Amaldi F. Sequences coding for the ribosomal protein L14 in Xenopus laevis and Xenopus tropicalis; homologies in the 5' untranslated region are shared with other r-protein mRNAs. Nucleic Acids Res. 1986 Oct 10;14(19):7633–7646. doi: 10.1093/nar/14.19.7633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bowman L. H. The synthesis of ribosomal proteins S16 and L32 is not autogenously regulated during mouse myoblast differentiation. Mol Cell Biol. 1987 Dec;7(12):4464–4471. doi: 10.1128/mcb.7.12.4464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bozzoni I., Beccari E., Luo Z. X., Amaldi F. Xenopus laevis ribosomal protein genes: isolation of recombinant cDNA clones and study of the genomic organization. Nucleic Acids Res. 1981 Mar 11;9(5):1069–1086. doi: 10.1093/nar/9.5.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bozzoni I., Fragapane P., Annesi F., Pierandrei-Amaldi P., Amaldi F., Beccari E. Expression of two Xenopus laevis ribosomal protein genes in injected frog oocytes. A specific splicing block interferes with the L1 RNA maturation. J Mol Biol. 1984 Dec 25;180(4):987–1005. doi: 10.1016/0022-2836(84)90267-5. [DOI] [PubMed] [Google Scholar]
  8. Dudov K. P., Perry R. P. The gene family encoding the mouse ribosomal protein L32 contains a uniquely expressed intron-containing gene and an unmutated processed gene. Cell. 1984 Jun;37(2):457–468. doi: 10.1016/0092-8674(84)90376-3. [DOI] [PubMed] [Google Scholar]
  9. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hentze M. W., Rouault T. A., Caughman S. W., Dancis A., Harford J. B., Klausner R. D. A cis-acting element is necessary and sufficient for translational regulation of human ferritin expression in response to iron. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6730–6734. doi: 10.1073/pnas.84.19.6730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hyman L. E., Wormington W. M. Translational inactivation of ribosomal protein mRNAs during Xenopus oocyte maturation. Genes Dev. 1988 May;2(5):598–605. doi: 10.1101/gad.2.5.598. [DOI] [PubMed] [Google Scholar]
  12. Kay M. A., Jacobs-Lorena M. Selective translational regulation of ribosomal protein gene expression during early development of Drosophila melanogaster. Mol Cell Biol. 1985 Dec;5(12):3583–3592. doi: 10.1128/mcb.5.12.3583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Loreni F., Ruberti I., Bozzoni I., Pierandrei-Amaldi P., Amaldi F. Nucleotide sequence of the L1 ribosomal protein gene of Xenopus laevis: remarkable sequence homology among introns. EMBO J. 1985 Dec 16;4(13A):3483–3488. doi: 10.1002/j.1460-2075.1985.tb04107.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Marini N. J., Etkin L. D., Benbow R. M. Persistence and replication of plasmid DNA microinjected into early embryos of Xenopus laevis. Dev Biol. 1988 Jun;127(2):421–434. doi: 10.1016/0012-1606(88)90328-4. [DOI] [PubMed] [Google Scholar]
  15. Mariottini P., Bagni C., Annesi F., Amaldi F. Isolation and nucleotide sequences of cDNAs for Xenopus laevis ribosomal protein S8: similarities in the 5' and 3' untranslated regions of mRNAs for various r-proteins. Gene. 1988 Jul 15;67(1):69–74. doi: 10.1016/0378-1119(88)90009-1. [DOI] [PubMed] [Google Scholar]
  16. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  17. Meyuhas O., Thompson E. A., Jr, Perry R. P. Glucocorticoids selectively inhibit translation of ribosomal protein mRNAs in P1798 lymphosarcoma cells. Mol Cell Biol. 1987 Aug;7(8):2691–2699. doi: 10.1128/mcb.7.8.2691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nomura M., Gourse R., Baughman G. Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem. 1984;53:75–117. doi: 10.1146/annurev.bi.53.070184.000451. [DOI] [PubMed] [Google Scholar]
  19. Parkin N., Darveau A., Nicholson R., Sonenberg N. cis-acting translational effects of the 5' noncoding region of c-myc mRNA. Mol Cell Biol. 1988 Jul;8(7):2875–2883. doi: 10.1128/mcb.8.7.2875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pelletier J., Kaplan G., Racaniello V. R., Sonenberg N. Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5' noncoding region. Mol Cell Biol. 1988 Mar;8(3):1103–1112. doi: 10.1128/mcb.8.3.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pierandrei-Amaldi P., Beccari E., Bozzoni I., Amaldi F. Ribosomal protein production in normal and anucleolate Xenopus embryos: regulation at the posttranscriptional and translational levels. Cell. 1985 Aug;42(1):317–323. doi: 10.1016/s0092-8674(85)80127-6. [DOI] [PubMed] [Google Scholar]
  22. Pierandrei-Amaldi P., Bozzoni I., Cardinali B. Expression of the gene for ribosomal protein L1 in Xenopus embryos: alteration of gene dosage by microinjection. Genes Dev. 1988 Jan;2(1):23–31. doi: 10.1101/gad.2.1.23. [DOI] [PubMed] [Google Scholar]
  23. Pierandrei-Amaldi P., Campioni N., Beccari E., Bozzoni I., Amaldi F. Expression of ribosomal-protein genes in Xenopus laevis development. Cell. 1982 Aug;30(1):163–171. doi: 10.1016/0092-8674(82)90022-8. [DOI] [PubMed] [Google Scholar]
  24. Pierandrei-Amaldi P., Campioni N., Gallinari P., Beccari E., Bozzoni I., Amaldi F. Ribosomal-protein synthesis is not autogenously regulated at the translational level in Xenopus laevis. Dev Biol. 1985 Feb;107(2):281–289. doi: 10.1016/0012-1606(85)90311-2. [DOI] [PubMed] [Google Scholar]
  25. Probst E., Kressmann A., Birnstiel M. L. Expression of sea urchin histone genes in the oocyte of Xenopus laevis. J Mol Biol. 1979 Dec 15;135(3):709–732. doi: 10.1016/0022-2836(79)90173-6. [DOI] [PubMed] [Google Scholar]
  26. Rhoads D. D., Dixit A., Roufa D. J. Primary structure of human ribosomal protein S14 and the gene that encodes it. Mol Cell Biol. 1986 Aug;6(8):2774–2783. doi: 10.1128/mcb.6.8.2774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rouault T. A., Hentze M. W., Dancis A., Caughman W., Harford J. B., Klausner R. D. Influence of altered transcription on the translational control of human ferritin expression. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6335–6339. doi: 10.1073/pnas.84.18.6335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rubin C. M., Schmid C. W. Pyrimidine-specific chemical reactions useful for DNA sequencing. Nucleic Acids Res. 1980 Oct 24;8(20):4613–4619. doi: 10.1093/nar/8.20.4613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schmidt T., Chen P. S., Pellegrini M. The induction of ribosome biosynthesis in a nonmitotic secretory tissue. J Biol Chem. 1985 Jun 25;260(12):7645–7650. [PubMed] [Google Scholar]
  30. 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]
  31. Wagner M., Perry R. P. Characterization of the multigene family encoding the mouse S16 ribosomal protein: strategy for distinguishing an expressed gene from its processed pseudogene counterparts by an analysis of total genomic DNA. Mol Cell Biol. 1985 Dec;5(12):3560–3576. doi: 10.1128/mcb.5.12.3560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wiedemann L. M., Perry R. P. Characterization of the expressed gene and several processed pseudogenes for the mouse ribosomal protein L30 gene family. Mol Cell Biol. 1984 Nov;4(11):2518–2528. doi: 10.1128/mcb.4.11.2518. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES