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Translational Regulation of Gene Expression in Early Development

  • Joan V. Ruderman
  • Eric T. Rosenthal
  • Terese Tansey

Abstract

Fertilization of Spisula oocytes causes a rapid change in the overall pattern of protein synthesis. This change occurs independently of any new mRNA transcription: it is controlled entirely at the translational level. cDNA clones complementary to several translationally regulated mRNAs have been isolated and used to directly investigate fertilization-triggered changes in mRNA activity and structure. Several mRNAs gain a long poly(A) tail right after fertilization, whereas others lose their poly(A) tails. In general, there is a good correlation between possession of a poly(A) tail and translational activity in vivo. Except for these changes in poly(A), these mRNAs show no significant structural alterations. This result strongly suggests that the inactivity of maternal mRNAs in the oocyte is not due to their being stored as translationally incompetent larger precursor forms. Evidence for a role of masking components is also discussed.

Keywords

Xenopus Laevis Xenopus Oocyte Translation Product Translational Regulation Translational Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adamson, E.D. and Woodland, H.R. (1977). Changes in the rate of histone synthesis during oocyte maturation and very early development of Xenopus laevis. Develop. Biol. 57:136–149.CrossRefGoogle Scholar
  2. Alexandraki, D. and Ruderman, J.V. (1983). Changes in tubulin mRNA sequences during sea urchin early development. In preparation.Google Scholar
  3. Alexandraki, D. and Ruderman, J.V. (1981). Sequence heterogeneity, multiplicity and genomic organization of a- and β-tubulin genes in sea urchins. Mol. Cell. Biol. 1:1125–1137.Google Scholar
  4. Alexandraki, D. and Ruderman, J.V. (1982). Organization and expression of the tubulin gene families in the sea urchin. J. Submic. Cytol., in press.Google Scholar
  5. Angerer, R.C., Hughes, K.J., DeLeon, D.V., Lynn, D.A., and Angerer, L.M. (1983). [This volume].Google Scholar
  6. Aviv, H. and Leder, P. (1972). Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc. Natl. Acad. Sci. USA 69:1408–1413.CrossRefGoogle Scholar
  7. Ballantine, J.E.M., Woodland, H.R., and Sturgess, E.A. (1979). Changes in protein synthesis during development of Xenopus laevis. J. Embryol. Exp. Morphol. 51:135–153.Google Scholar
  8. Ballinger, D.G. and Hunt, T. (1981). Fertilization of sea urchin eggs is accompanied by 40S ribosomal subunit phosphorylation. Dev. Biol. 87:277–285.CrossRefGoogle Scholar
  9. Brandhorst, B.P. (1976). Two-dimensional gel patterns of protein synthesis before and after fertilization of sea urchin eggs. Develop. Biol. 52:310–317.CrossRefGoogle Scholar
  10. Brandis, J.W. and Raff, R.A. (1978). Translation of oogenetic mRNA in sea urchin eggs and early embryos. Demonstration of a change in translational efficiency following fertilization. Dev. Biol. 67:99–113.CrossRefGoogle Scholar
  11. Brandis, J.W. and Raff, R.A. (1979). Elevation of protein synthesis is a complex response to fertilization. Nature 278:476–469.CrossRefGoogle Scholar
  12. Braude, P., Pelham, H., Flach, T., and Lobatto, R. (1979). Post-transcriptional control in the early mouse embryo. Nature 282:102–105.CrossRefGoogle Scholar
  13. Cascio, H.V. and Wassarman, P.M. (1982). Program of early development in the mammal: Post-transcriptional control of a class of proteins synthesized by mouse oocytes and early embryos. Dev. Biol. 89:397–408.CrossRefGoogle Scholar
  14. Colot, H.V. and Rosbash, M. (1982). Behavior of individual maternal pA+ RNAs during embryogenesis of Xenopus laevis. Dev. Biol. 94:79–86.CrossRefGoogle Scholar
  15. Costantini, F.E., Britten, R.J., and Davidson, E.H. (1980). Message sequences and short repetitive sequences are interspersed in sea urchin egg poly(A) RNAs. Nature (London) 287:111–117.CrossRefGoogle Scholar
  16. Davidson, E.A. (1976). “Gene Activity in Early Development.” Academic Press, New York.Google Scholar
  17. Epel, D. (1967). Protein synthesis in sea urchin eggs: A “late” response to fertilization. Proc. Natl. Acad. Sci. USA 57:899–906.CrossRefGoogle Scholar
  18. Godefroy-Coburn, T. and Thach, R.E. (1982). The role of mRNA competition in regulating translation. IV. Kinetic Model. J. Biol. Chem. 256:11762–11773.Google Scholar
  19. Golden, L., Schafer, U., and Rosbash, M. (1981). Accumulation of individual pA RNAs during oogenesis of Xenopus laevis. Cell 22:835–844.CrossRefGoogle Scholar
  20. Gross, P.R. (1967). The control of protein synthesis in embryonic development and differentiation. Curr. Topics Dev. Biol. 2:1–29.CrossRefGoogle Scholar
  21. Gross, K.W., Jacobs-Lorena, M., Baglioni, C., and Gross, P.R. (1973). Cell-free translation of maternal messenger RNA from sea urchin eggs. P.N.A.S. 70:2614–2518.CrossRefGoogle Scholar
  22. Grunstein, M. and Hogness, D.S. (1975). Colony hybridization: a method for the isolation of clone DNAs that contain a specific gene. Proc. Natl. Acad. Sci. USA 75:5544.Google Scholar
  23. Hille, M.B. and Albers, A.A. (1979). Efficiency of protein synthesis after fertilization of sea urchin eggs. Nature 278:469–471.CrossRefGoogle Scholar
  24. Hough-Evans, B.R., Ernst, S.G., Britten, R.J., and Davidson, E.H. (1979). RNA complexity in developing sea urchin oocytes. Dev. Biol. 69:258–269.CrossRefGoogle Scholar
  25. Humphreys, T. (1971). Measurements of messenger RNA entering polysomes upon fertilization of sea urchin eggs. Dev. Biol. 26:201–208.CrossRefGoogle Scholar
  26. Ilan, J. and Ilan, J. (1978). Translation of maternal message ribonucleoprotein particles from sea urchin in a cell-free system and product analysis. Dev. Biol. 66:375–385.CrossRefGoogle Scholar
  27. Jacobson, A. and Favreau, M. (1983). Possible involvement of poly(A) in protein synthesis. Submitted for publication.Google Scholar
  28. Jeffery, W.R. and Brawerman, G. (1975). Association of the polyadenylate segment of messenger RNA with other polynucleotide sequences in mouse sarcoma 180 polyribosomes, Biochemistry 14:3445.CrossRefGoogle Scholar
  29. Jenkins, N.A., Kaumeyer, J.F., Young, E.M., and Raff, R.A. (1978). A test for masked message: The template activity of messenger of ribonucleprotein particles isolated from sea urchin eggs. Dev. Biol. 63:279–298.CrossRefGoogle Scholar
  30. Kaumeyer, J.F., Jenkins, N.A., and Raff, R.A. (1978). Messenger ribonucleoprotein particles in unfertilized sea urchin eggs. Dev. Biol. 63:266–278.CrossRefGoogle Scholar
  31. Laskey, R.A., Mills, A.D., Gurdon, J.R., and Partington, G.A. (1977). Protein synthesis in oocytes of Xenopus laevis is not regulated by the supply of messenger RNA. Cell 11:345–351.CrossRefGoogle Scholar
  32. Lifton, R.P. and Kedes, L.H. (1976). Size and sequence homology of masked maternal and embryonic histone mRNAs. Dev. Biol. 48:47–55.CrossRefGoogle Scholar
  33. Lingrel, J.B. and Woodland, H.R. (1974). Initiation does not limit the rate of globin synthesis in message-injected Xenopus oocytes. Eur. J. Biochem. 47:47–56.CrossRefGoogle Scholar
  34. Lodish, H.F. (1974). Model for the regulation of mRNA translation applied to haemoglobin synthesis. Nature 251:385–388.CrossRefGoogle Scholar
  35. Maniatis, R., Jeffrey, A., and van de Sande, H. (1975). Chain length determination of small double and single-stranded DNA molecules by polyacryalmide gel electrophoresis. Biochem. 14:3787–3794.CrossRefGoogle Scholar
  36. Martindale, M. and Brandhorst, B. (1982). Biol. Bull. (Abstracts) in press.Google Scholar
  37. Moon, R.T., Danilcheck, M.V., and Hille, M.B. (1982). An assessment of the masked message hypothesis: sea urchin egg messenger ribonucleoprotein complexes are efficient templates for in vitro protein synthesis. Dev. Biol. 93:389–403.CrossRefGoogle Scholar
  38. Palatnik, C.M., Wilkins, C., and Jacobson, A. (1982). Submitted for publication.Google Scholar
  39. Pelham, H.R.B. and Jackson, R.J. (1976). An efficient mRNA-dependent translation system from reticulocyte lysates. Eur. J. Biochem. 67:247–256.CrossRefGoogle Scholar
  40. Raff, R.A. and Showman, R.M. (1983). Maternal mRNA: quantitative, qualitative and spatial control of its expression in embryos. In “The Biology of Fertilization,” C.B. Metz and A. Monroy (eds.), in press.Google Scholar
  41. Rave, M., Crkvenjokov, R., and Boedtker, H. (1979). Identification of procollagen mRNAs transferred to diazabenzyloxymethyl paper from formaldehyde agarose gels. Nucleic Acids Res. 6:3559–3567.CrossRefGoogle Scholar
  42. Ricciardi, R.P., Miller, J.S., and Roberts, B.E. (1979). Purification and mapping of specific mRNAs by hybridization-selection and cell-free translation. Proc. Natl. Acad. Sci. USA 76:4927–4931.CrossRefGoogle Scholar
  43. Richter, J.D. and Smith, L.D. (1981). Differential capacity for translation and lack of competition between mRNAs that segregate to free- and membrane-bound polysomes. Cell 27:183–191.CrossRefGoogle Scholar
  44. Rosenthal, E., Hunt, T., and Ruderman, J.V. (1980). Selective translation of mRNA controls the pattern of protein synthesis during early development of the surf claim Spisula solidissima embryos. Cell 20:487–496.CrossRefGoogle Scholar
  45. Rosenthal, E.T., Brandhorst, B.P., and Ruderman, J.V. (1982). Translationally mediated changes in patterns of protein synthesis during maturation of starfish oocytes. Dev. Biol. 91:215–220.CrossRefGoogle Scholar
  46. Rosenthal, E.T., Tansey, T.R., and Ruderman, J.V. (1983). Sequence-specific adenylations and deodynylations accompany changes in the translation of maternal mRNA after fertilization of Spisula oocytes. J. Mol. Biol., in press.Google Scholar
  47. Roychoudhury, R., Jay, E., and Wu, R. (1976). Terminal labeling and addition of homopolymer tracts to duplex DNA fragments by teminal deoxynucleotidyl transferase. Nucleic Acids Res. 3:101–116.Google Scholar
  48. Ruderman, J.V. and Pardue, M.L. (1977). Analysis of mRNA in echinoderm and amphibian early development. Dev. Biol. 60:48–68.CrossRefGoogle Scholar
  49. Ruderman, J.V., Tansey, T.R., Rosenthal, E.T., Hunt, T., and Cheney, C.M. (1983). Spatial and temporal aspects of gene expression during Spisula embryogenesis. In “Embryos: Time, Space, and Pattern,” R.A. Raff and W. Jeffery (eds.). A.R. Liss, New York, in press.Google Scholar
  50. Ruderman, J.V., Woodland, H.R., and Sturgess, E.R. (1979). Modulations of histone messenger RNA during early development of Xenopus laevis. Dev. Biol. 71:71–82.CrossRefGoogle Scholar
  51. Showman, R.M., Wells, D.E., Anstrom, J., Hursh, D.A., and Raff, R.A. (1982). Message-specific sequestration of maternal histone mRNA in the sea urchin egg. Proc. Natl. Acad. Sci. 79:5944–5947.CrossRefGoogle Scholar
  52. Showman, R., Wells, D., Anstrom, J.A., Hursh, D.A., Leaf, D.S., and Raff, R.A. (1983). [This volume].Google Scholar
  53. Spirin, A.S. (1966). On “masked” forms of messenger RNA in early embryogenesis and in other differentiating systems. Curr. Top. Dev. Biol. 1:1–38.CrossRefGoogle Scholar
  54. Tansey, T.R. and Ruderman, J.V. (1983). Changing patterns of protein synthesis in Spisula embryos are controlled by changes in both mRNAs levels and translatable utilisation. Submitted.Google Scholar
  55. Thomas, T.L., Posakony, J.W., Anderson, D.M., Britten, R.J., and Davidson, E.R. (1981). Molecular structure of maternal mRNA. Chromosoma 84:319–335.CrossRefGoogle Scholar
  56. Thomas, P. (1980). Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. 77: 5201–5205.CrossRefGoogle Scholar
  57. Van Dongen, W., Zoal, R., Moorman, A., and Destree, O. (1981). Quantitation of the accumulation of histone messenger RNA during oogenesis in Xenopus laevis. Dev. Biol. 86:303–314.CrossRefGoogle Scholar
  58. Villa-Komaroff, L., Efstratiadis, A., Broome, S., Lomedico, P., Tizard, R., Naber, S.P., Chick, W.S., and Gilbert, W. (1978). A bacterial clone synthesizing proinsulin. Proc. Natl. Acad. Sci. USA 76:3683–3687.Google Scholar
  59. Vournakis, J.H., Efstratiadis, A., and Kafatos, F.C. (1975). Electrophoretic patterns of deadenylated chorian and globin mRNAs. P.N.A.S. 72:2959–2963.CrossRefGoogle Scholar
  60. Wells, D.E., Showman, R.M., Klein, W.H., and Raff, R.A. (1981). Delayed recruitment of maternal histone mRNA in sea urchin embryos. Nature (London) 292:477–479.CrossRefGoogle Scholar
  61. Winkler, M.M. and Steinhardt, R.A. (1981). Activation of protein synthesis in a sea urchin cell-free system. Dev. Biol. 84:432–439.CrossRefGoogle Scholar
  62. Young, E.M. and Raff, R.A. (1979). Messenger ribonucleoprotein particles in developing sea urchin embryos. Dev. Biol. 72:24–40.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Joan V. Ruderman
    • 1
  • Eric T. Rosenthal
    • 1
  • Terese Tansey
    • 1
  1. 1.Program in Cell and Developmental Biology, and Department of AnatomyHarvard Medical SchoolBostonUSA

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