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Expression of Ribosomal Protein Genes during Xenopus Development

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The Molecular Biology of Cell Determination and Cell Differentiation

Part of the book series: Developmental Biology ((DEBO,volume 5))

Abstract

Biosynthesis of the eukaryotic ribosome encompasses the expression of genes encoding approximately 60 integral proteins and two distinct classes of rRNA genes in the nucleus and the nucleolus. The regulation of ribosome production is an important aspect of gene expression during Xenopus laevis development. During oogenesis in Xenopus and other amphibia, ribosomes are accumulated at least 1000 times more rapidly than in the most synthetically active somatic cells (Korn and Gurdon, 1981). This massive stockpile of 1012 ribosomes within a single egg is sufficient to support protein synthesis through development of the swimming tadpole, which consists of approximately 106 cells (Brown and Gurdon, 1964). The enormous synthesis of ribosomes during oogenesis and the requirement to impose somatic regulation of ribosome production during embryogenesis renders Xenopus an exquisite model system for the analysis of ribosome biogenesis during vertebrate development.

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References

  • Abovich, N., and Rosbash, M., 1984, Two genes for ribosomal protein 51 of Saccharomyces cere-visiae complement and contribute to the ribosomes, Mol. Cell. Biol. 4:1871–1879.

    PubMed  CAS  Google Scholar 

  • Abovich, N., Gritz, L., Tung, L., and Rosbash, M., 1985, Effect of RP51 gene dosage alterations on ribosome synthesis in Saccharomyces cerevisiae, Mol. Cell. Biol. 5:3429–3435.

    PubMed  CAS  Google Scholar 

  • Anderson, D. M., Richter, J. D., Chamberlin, M. E., Price, D. H., Britten, R. J., Smith, L. D., and Davidson, E. H., 1982, Sequence organization of the poly(A) RNA synthesized and accumulated in lampbrush chromosome stage Xenopus laevis oocytes, J. Mol. Biol. 155:281–309.

    Article  PubMed  CAS  Google Scholar 

  • Baum, E. Z., 1986, Developmental regulation of Xenopus ribosomal protein genes: Control at the translational level, Ph.D. thesis, Brandeis University, Waltham, Massachusetts.

    Google Scholar 

  • Baum, E. Z., and Wormington, W. M., 1985, Coordinate expression of ribosomal protein genes during Xenopus development, Dev. Biol. 111:488–498.

    Article  PubMed  CAS  Google Scholar 

  • Bozzoni, I., Beccari, E., Luo, Z. X., and Amaldi, F., 1981, Xenopus laevis ribosomal protein genes: Isolation of recombinant cDNA clones and study of the genomic organization, Nucl. Acids Res. 9:1069–1086.

    Article  PubMed  CAS  Google Scholar 

  • Bozzoni, I., Tognoni, A., Pierandrei-Amaldi, P., Beccari, E., Buongiorno-Nardelli, M., and Amaldi, F., 1982, Isolation and structural analysis of ribosomal protein genes in Xenopus laevis, J. Mol. Biol. 161:353–371.

    Article  PubMed  CAS  Google Scholar 

  • Bozzoni, I., Fragapane, P., Annesi, F., Pierandrei-Amaldi, P., Amaldi, F., and Beccari, E., 1984, Expression of two X. laevis ribosomal protein genes in injected frog oocytes: A specific splicing block interferes with L1 RNA maturation, J. Mol. Biol. 180:987–1005.

    Article  PubMed  CAS  Google Scholar 

  • Brown, D. D., and Dawid, I. B., 1968, Specific gene amplification in oocytes, Science 160:272–280.

    Article  PubMed  CAS  Google Scholar 

  • Brown, D. D., and Gurdon, J. B., 1964, Absence of rRNA synthesis in the anucleolate mutant of X. laevis, Proc. Natl. Acad. Sci. USA 51:139–146.

    Article  PubMed  CAS  Google Scholar 

  • Brown, D. D., and Littna, E., 1964, RNA synthesis during the development of Xenopus laevis the South African clawed toad, J. Mol. Biol. 8:669–687.

    Article  PubMed  CAS  Google Scholar 

  • Brown, D. D., and Schlissel, M. S., 1985, The molecular basis of differential gene expression of two 5S RNA genes, Cold Spring Harbor Symp. Quant. Biol. 50:549–554.

    Article  PubMed  Google Scholar 

  • Colot, H. V., and Rosbash, M., 1982, Behavior of individual maternal pA + RNAs during embryogenesis of Xenopus laevis, Dev. Biol. 94:79–86.

    Article  PubMed  CAS  Google Scholar 

  • Dixon, L. K., and Ford, P. J., 1982, Regulation of protein synthesis and accumulation during oogenesis in Xenopus laevis, Dev. Biol. 93:478–497.

    Article  PubMed  CAS  Google Scholar 

  • Dumont, J. N., 1972, Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals, J. Morphol. 136:153–180.

    Article  PubMed  CAS  Google Scholar 

  • Dworkin, M. B., and Hershey, J. W. B., 1981, Cellular titers and subcellular distributions of abundant polyadenylate-containing ribonucleic acid species during early development in the frog Xenopus laevis, Mol. Cell. Biol. 1:983–993.

    PubMed  CAS  Google Scholar 

  • Fried, H. M., Pearson, N. J., Kim, K. H., and Warner, R. J., 1981, The genes for fifteen ribosomal proteins of Saccharomyces cerevisiae, J. Biol. Chem. 256:10176–10183.

    PubMed  CAS  Google Scholar 

  • Gall, J. G., 1968, Differential synthesis of the genes for rRNA during amphibian oogenesis, Proc. Natl. Acad. Sci. USA 60:553–560.

    Article  PubMed  CAS  Google Scholar 

  • Golden, L., Schafer, U., and Rosbash, M., 1980, Accumulation of individual pA+ RNAs during oogenesis of Xenopus laevis, Cell 22:835–844.

    Article  PubMed  CAS  Google Scholar 

  • Gurdon, J. B., and Melton, D. A., 1981, Gene transfer in amphibian eggs and oocytes, Annu. Rev. Genet. 15:189–218.

    Article  PubMed  CAS  Google Scholar 

  • Hadjiolov, A. A., 1985, The Nucleolus and Ribosome Biogenesis, Cell Biology Monographs, Vol. 12, Springer-Verlag, New York.

    Google Scholar 

  • Hallberg, R. L., and Brown, D. D., 1969, Coordinated synthesis of some ribosomal proteins and ribosomal DNA in embryos of Xenopus laevis, J. Mol. Biol. 46:393–411.

    Article  PubMed  CAS  Google Scholar 

  • Hallberg, R. L., and Smith, D. C., 1975, Ribosomal protein synthesis in Xenopus laevis oocytes, Dev. Biol. 42:40–52.

    Article  PubMed  CAS  Google Scholar 

  • Hyman, L. E., Colot, H. V., and Rosbash, M., 1984, Accumulation and behavior of mRNA during oogenesis and early embryogenesis of Xenopus laevis, in: Molecular Aspects of Early Development (G. M. Malacinski and W. Klein, eds.), pp. 142–151, Plenum, New York.

    Google Scholar 

  • Kalthoff, H., and Richter, D., 1982, Subcellular transport and ribosomal incorporation of microinjected protein S6 in oocytes from Xenopus laevis, Biochemistry 18:4144–4147.

    Article  Google Scholar 

  • Kay, M. A., and Jacobs-Lorena, M., 1985, Selective translational regulation of ribosomal protein gene expression during early development of Drosophila melanogaster, Mol. Cell. Biol. 5:3583–3592.

    PubMed  CAS  Google Scholar 

  • Korn, L. J., and Gurdon, J. B., 1981, The reactivation of developmentally inert 5S RNA genes in somatic nuclei injected into Xenopus oocytes, Nature (Lond.) 289:461–465.

    Article  CAS  Google Scholar 

  • Krämer, A., 1985, 55 Ribosomal gene transcription during Xenopus oogenesis, in: Developmental Biology: A Comprehensive Synthesis, Vol. 1, Oogenesis (L. W. Browder, ed.), pp. 431–448, Plenum, New York.

    Google Scholar 

  • Lastick, S. M., and McConkey, E. H., 1976, Exchange and stability of HeLa ribosomal proteins in vivo, J. Biol. Chem. 251:2867–2875.

    PubMed  CAS  Google Scholar 

  • Lee, G., Hynes, R., and Kirschner, M., 1984, Temporal and spatial regulation of fibronectin in early Xenopus development, Cell 36:729–740.

    Article  PubMed  CAS  Google Scholar 

  • Loreni, F., Ruberti, I., Bozzoni, I., Pierandrei-Amaldi, P., and Amaldi, F., 1985, Nucleotide sequence of the L1 ribosomal protein gene of Xenopus Jaevis: remarkable sequence homology among introns, EMBO J. 4:3483–3488.

    PubMed  CAS  Google Scholar 

  • Meyuhas, O., and Perry, R. P., 1980, Construction and identification of cDNA clones for mouse ribosomal proteins: Application for the study of r-protein gene expression, Gene 10:113–129.

    Article  PubMed  CAS  Google Scholar 

  • Miller, L., 1974, Metabolism of 5S RNA in the absence of ribosome production, Cell 3:275–281.

    Article  PubMed  CAS  Google Scholar 

  • Monk, R. J., Meyuhas, O., and Perry, R. P., 1981, Mammals have multiple genes for individual ribosomal proteins, Cell 24:301–306.

    Article  PubMed  CAS  Google Scholar 

  • Nomura, M., Gourse, R., and Baughman, G., 1984, Regulation of the synthesis of ribosomes and ribosomal components, Annu. Rev. Biochem. 53:75–118.

    Article  PubMed  CAS  Google Scholar 

  • Pelham, H. R. B., and Brown, D. D., 1980, A specific transcription factor that can bind either the 5S RNA gene or 5S RNA, Proc. Natl. Acad. Sci. USA 77:4170–4174.

    Article  PubMed  CAS  Google Scholar 

  • Picard, B., and Wegnez, M., 1979, Isolation of 7S particle from Xenopus laevis oocytes: A 5S RNA-protein complex, Proc. Natl. Acad. Sci. USA 76:241–245.

    Article  PubMed  CAS  Google Scholar 

  • Pierandrei-Amaldi, P., and Beccari, E., 1980, Messenger RNA for ribosomal proteins in Xenopus laevis oocytes, Eur. J. Biochem. 106:603–611.

    Article  PubMed  CAS  Google Scholar 

  • Pierandrei-Amaldi, P., Campioni, N., Beccari, E., Bozzoni, I., and Amaldi, F., 1982, Expression of ribosomal protein genes in Xenopus laevis, Cell 30:163–171.

    Article  PubMed  CAS  Google Scholar 

  • Pierandrei-Amaldi, P., Campioni, N., Gallinari, P., Beccari, E., Bozzoni, I., and Amaldi, F., 1985a, Ribosomal protein synthesis is not autogenously regulated at the translational level in Xenopus laevis, Dev. Biol. 107:281–289.

    Article  PubMed  CAS  Google Scholar 

  • Pierandrei-Amaldi, P., Beccari, E., Bozzoni, I., and Amaldi, F., 1985b, Ribosomal protein production in normal and anucleolate Xenopus embryos: Regulation at the post-transcriptional and translational levels, Cell 42:317–323.

    Article  PubMed  CAS  Google Scholar 

  • Reeder, R. H., and Roan, J. G., 1984, The mechanism of nucleolar dominance in Xenopus hybrids, Cell 38:39–44.

    Article  CAS  Google Scholar 

  • Richter, J. D., and Smith, L. D., 1983, Developmentally regulated RNA binding proteins during oogenesis in Xenopus laevis, J. Biol. Chem. 258:4864–4869.

    PubMed  CAS  Google Scholar 

  • Richter, J. D., and Smith, L. D., 1984, Reversible inhibition of translation by Xenopus oocytespecific proteins, Nature (Lond.) 309:378–380.

    Article  CAS  Google Scholar 

  • Richter, J. D., Smith, L. D., Anderson, D. M., and Davidson, E. H., 1984, Interspersed poly(A) RNAs of amphibian oocytes are not translatable. J. Mol. Biol. 173:227–241.

    Article  PubMed  CAS  Google Scholar 

  • Rosbash, M., and Ford, P. J., 1974, Polyadenylic acid-containing RNA in Xenopus laevis oocytes, Dev. Biol. 85:87–101.

    CAS  Google Scholar 

  • Sagata, N., Shiokawa, K., and Yamana, K., 1980, A study on the steady-state population of poly(A)+ RNA during early development of Xenopus laevis, Dev. Biol. 77:431–438.

    Article  PubMed  CAS  Google Scholar 

  • Santon, J. B., and Pellegrini, M., 1981, Rates of ribosomal protein and total protein synthesis during Drosophila early embryogenesis, Dev. Biol. 85:252–257.

    Article  PubMed  CAS  Google Scholar 

  • Smith, L. D., and Richter, J. D., 1984, Synthesis, accumulation, and utilization of maternal macromolecules during oogenesis and oocyte maturation, in: Biology of Fertilization, Vol. 1 (C. B. Metz, and A. Monroy, eds.), pp. 141–188, Academic, New York.

    Google Scholar 

  • Sturgess, E. A., Ballantine, J. E. M., Woodland, H. R., Mohun, T. R., Lane, C. D., and Dimitriades, G. J., 1980, Actin synthesis during the early development of Xenopus laevis, J. Embryol. Exp. Morphol. 58:303–320.

    PubMed  CAS  Google Scholar 

  • Taylor, M. A., and Smith, L. D., 1985, Quantitative changes in protein synthesis during oogenesis in Xenopus laevis, Dev. Biol. 110:230–237.

    Article  PubMed  CAS  Google Scholar 

  • Warner, J. R., 1977, In the absence of ribosomal RNA synthesis, the ribosomal proteins of HeLa cells are synthesized normally and degraded rapidly, J. Mol. Biol. 155:315–333.

    Article  Google Scholar 

  • Warner, J. R., Mitra, G., Schwindinger, W. F., Studeny, M., and Fried, H. M., 1985, Saccharomyces cerevisiae coordinates accumulation of yeast ribosomal proteins by modulating mRNA splicing, translational initiation, and turnover, Mol. Cell. Biol. 5:1512–1521.

    PubMed  CAS  Google Scholar 

  • Weiss, Y. C., Vaslet, C. A., and Rosbash, M., 1981, Ribosomal protein mRNAs increase dramatically during Xenopus development, Dev. Biol. 87:330–339.

    Article  PubMed  CAS  Google Scholar 

  • Woodland, H. R., 1974, Changes in the polysome content of developing Xenopus laevis embryos, Dev. Biol. 40:90–101.

    Article  PubMed  CAS  Google Scholar 

  • Woodland, H. R., Flynn, J. M., and Wylie, A. J., 1979, Utilization of stored mRNA in Xenopus embryos and its replacement by newly synthesized transcripts: Histone H1 synthesis using interspecies hybrids, Cell 18:165–171.

    Article  PubMed  CAS  Google Scholar 

  • Wormington, W. M., and Brown, D. D., 1983, Onset of 5S RNA gene regulation during Xenopus embryogenesis, Dev. Biol. 99:248–257.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, Massachusetts, 02254, USA

    W. Michael Wormington

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  1. W. Michael Wormington
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Editors and Affiliations

  1. University of Calgary, Calgary, Alberta, Canada

    Leon W. Browder

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© 1988 Plenum Press, New York

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Wormington, W.M. (1988). Expression of Ribosomal Protein Genes during Xenopus Development. In: Browder, L.W. (eds) The Molecular Biology of Cell Determination and Cell Differentiation. Developmental Biology, vol 5. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-6817-9_8

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  • DOI: https://doi.org/10.1007/978-1-4615-6817-9_8

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4615-6819-3

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