Skip to main content
SpringerLink
Log in

Origin of several abundant proteins of amphibian oocytes

  • Focus
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Previous studies indicate that the genes controlling cell-specific functions in extant metazoans derive from housekeeping genes of their unicellular ancestors. Traces of such relationships can be found in the gene families controlling signal reception at cell surfaces and light condensation in eye lens. We present other examples of gene remodeling taken in the field of germ cell-specific proteins. In amphibian oocytes several proteins contribute to edification of an efficient translation machinery for the future embryo. Some RNA components of this machinery have to be protected against degradation during growth of the oocytes in the ovary. The protective function is served by a small group of RNA-binding proteins deriving from universal transcription or translation factors. Several of those proteins are bifunctional.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdallah B, Hourdry J, Deschamps S, Denis H, Mazabraud A (1991a) The genes encoding the major 42S storage particle proteins are expressed in male and female germ cells of Xenopus laevis. Development 113:851–856

    Google Scholar 

  • Abdallah B, Hourdry J, Krieg A, Denis H, Mazabraud A (1991b) Germ cell-specific expression of a gene encoding eukaryotic translation initiation factor 1α (eEF-1α) and generation of eEF-1α retropseudogenes in Xenopus laevis. Proc Natl Acad Sci USA 88:9277–9821

    Google Scholar 

  • Baker ME (1988a) Is vitellogenin an ancestor of apolipoprotein B-100 of human low-density lipoprotein and human lipoprotein lipase? Biochem J 255:1057–1060

    Google Scholar 

  • Baker ME (1988b) Invertebrate vitellogenin is homologous to human von Willebrand factor. Biochem J 2563:1059–1063

    Google Scholar 

  • Blanck A, Oesterhelt D (1987) The halo-opsin gene. II. Sequence, primary structure of halorhodopsin and comparison with bacteriorhodopsin. EMBO J 6:265–273

    Google Scholar 

  • Bourne HR (1988) Summary: signals past, present and future. Cold Spring Harb Symp Quant Biol 53:1019–1031

    Google Scholar 

  • Brown RS, Sander C, Argos P (1985) The primary structure of transcription factor TFIIIA has 12 consecutive repeats. FEBS Lett 186:271–274

    Google Scholar 

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Google Scholar 

  • Byrne BM, Gruber M, AB G (1989) The evolution of egg yolk proteins. Prog Biophys Mol Biol 53:33–69

    Google Scholar 

  • Darnbrough CH, Ford PJ (1981) Identification in Xenopus laevis of a class of oocyte-specific proteins bound to messenger RNA. Eur J Biochem 113:415–424

    Google Scholar 

  • de Jong WW, Hendriks W, Mulders JWM, Bloemendal H (1989) Evolution of eye lens crystallins: the stress connection. Trends Biochem Sci 14:365–368

    Google Scholar 

  • Denis H, le Maire M (1983) Thesaurisomes, a novel kind of nucleo-protein particles. Subcell Biochem 9:263–297

    Google Scholar 

  • Denis H, le Maire M (1985) Biochemical research on oogenesis. Aminoacyl tRNA turns over in the 42-S particles of Xenopus oocytes, but its ester bond is protected against hydrolysis. Eur J Biochem 149:549–556

    Google Scholar 

  • Deschamps S, Viet A, Garrigos M, Denis H, le Maire M (1992) mRNP4, a major mRNA-binding protein from Xenopus oocytes is identical to transcription factor FRG Y2. J Biol Chem 267:13799–13802

    Google Scholar 

  • Djé M, Mazabraud A, Viet A, le Maire M, Denis H, Crawford E, Brown DD (1990) Three genes under different developmental control encode elongation factor 1-α in Xenopus laevis. Nucleic Acids Res 18:3489–3493

    Google Scholar 

  • Doolittle RF (1985) The genealogy of some recently evolved vertebrate proteins. Trends Biochem Sci 10:233–237

    Google Scholar 

  • Dunn R, McCoy J, Simsek M, Majumdar A, Chang SH, RajBhandary UL, Khorana HG (1981) The bacteriorhodopsin gene. Proc Natl Acad Sci USA 78:6744–6748

    Google Scholar 

  • Fields S (1990) Pheromone response in yeast. Trends Biochem Sci 15:270–273

    Google Scholar 

  • Gilbert W, Marchionni M, McKnight G (1986) On the antiquity of introns. Cell 46:151–154

    Google Scholar 

  • Hellingwerf KH (1988) Phylogenetic relations between unicellular organisms and the mechanism of vertebrate signal transduction. Trends Biochem Sci 13:129

    Google Scholar 

  • Honda BM, Roeder RG (1980) Association of a 5S gene transcription factor with 5S RNA and altered levels of the factor during cell differentiation. Cell 22:119–126

    Google Scholar 

  • Ingram VM (1961) Gene evolution and the haemoglobins. Nature 189:704–708

    Google Scholar 

  • Joho KE, Darby MK, Crawford ET, Brown DD (1990) A finger protein structurally similar to TFIIIA that binds exclusively to 5S RNA in Xenopus. Cell 61:293–300

    Google Scholar 

  • Kaziro Y, Itoh H, Kozasa R, Toyama R, Tsukamoto T, Matsuoka M, Nakafuku M, Obara T, Kakagi T, Hernandez R (1988) Structure of the genes coding for G-proteins a subunits from mammalian and yeast cells. Cold Spring Harb Symp Quant Biol 53:209–220

    Google Scholar 

  • Kim SH, Darby MK, Joho K, Brown DD (1990) The characterization of the TFIIIA synthesized in somatic cells of Xenopus laevis. Genes Dev 4:1602–1610

    Google Scholar 

  • Kirk DL (1988) The ontogeny and phylogeny of cellular differentiation in Volvox. Trends Genet 4:32–36

    Google Scholar 

  • Kubo T, Fukuda K, Mikami A, Maeda A, Takahashi H, Mishina M, Haga T, Haga K, Ichiyama A, Kangawa K, Kojima M, Matsuo H, Hirose T, Numa S (1986) Cloning, sequencing and expression of complementary DNA encoding the muscarinic acetylcholine receptor. Nature 323:411–416

    Google Scholar 

  • Lagaye S, Barque JP, le Maire M, Denis H, Larsen CJ (1989) Characterization by human antibodies of two HeLa cell proteins which are related to Xenopus laevis transcription factor TFIIIA. Nucl Acids Res 105:11–16

    Google Scholar 

  • Masu Y, Nakayama K, Tamaki H, Harada Y, Kuno M, Nakanishi S (1988) cDNA cloning of bovine substance-K receptor through oocyte expression system. Nature 329:836–838

    Google Scholar 

  • Mattaj IW, Coppard NJ, Brown RS, Clark BFC, De Robertis EM (1987) 42Sp48—the most abundant protein in previtellogenic Xenopus oocytes—resembles elongation factor 1α structurally and functionally. EMBO J 6:2409–2413

    Google Scholar 

  • Miller J, McLachlan AD, Klug A (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J 4:1609–1614

    Google Scholar 

  • Murray MT, Schiller DL, Franke WW (1992) Sequence analysis of cytoplasmic mRNA-binding proteins of Xenopus oocytes identifies a family of RNA-binding proteins. Proc Natl Acad Sci USA 89:11–15

    Google Scholar 

  • Nardelli D, Gerber-Huber S, van het Schip FD, Gruber M, AB G, Wahli W (1987) Vertebrate and nematode genes coding for yolk proteins are derived from a common ancestor. Biochemistry 26:6397–6402

    Google Scholar 

  • Nathans J, Hogness DS (1983) Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell 34:807–814

    Google Scholar 

  • Pelham HRB, Brown DD (1980) A specific transcription factor that can bind either the 5S RNA gene or 5S RNA. Proc Natl Acad Sci USA 77:4170–4174

    Google Scholar 

  • Picard B, le Maire M, Wegnez M, Denis H (1980) Biochemical research on oogenesis. Composition of the 42-S storage particles of Xenopus laevis oocytes. Eur J Biochem 109:359–368

    Google Scholar 

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

    Google Scholar 

  • Saxe CL, Klein P, Sun TJ, Kimmel AR, Devreotes PN (1988) Structure and expression of the cAMP cell-surface receptor. Dev Genet 9:227–235

    Google Scholar 

  • Seifart KH, Wang L, Waldschmidt R, Jahn D, Wingender E (1989) Purification of human transcription factor IIIA and its interaction with a chemically synthesized gene encoding human 5 S RNA. J Biol Chem 264:1702–1709

    Google Scholar 

  • Shastry BS, Honda BM, Roeder RG (1984) Altered levels of a 5S gene-specific transcription factor (TFIIIA) during oogenesis and embryonic development of Xenopus laevis. J Biol Chem 259:11373–11382

    Google Scholar 

  • Starr RC (1969) Structure, reproduction, and differentiation in Volvox carteri f. nagariensis IYENGAR, strains HK 9 & 10. Arch Protistenk 111:204–222

    Google Scholar 

  • Tafuri SR, Wolffe AP (1990) Xenopus Y-box transcription factors: molecular cloning, functional analysis, and developmental regulation. Proc Natl Acad Sci USA 87:9028–9032

    Google Scholar 

  • Trewitt PM, Heilmann LJ, Degrugillier SS, Kumaran AK (1992) The boll weevil vitellogenin gene: nucleotide sequence, structure, and evolutionary relationship to nematode and vertebrate vitellogenin genes. J Mol Evol 34:478–492

    Google Scholar 

  • van den Eynde H, Mazabraud A, Denis H (1989) Biochemical research on oogenesis. RNA accumulation in the oocytes of the newt Pleurodeles waltl. Development 105:11–16

    Google Scholar 

  • Viet A, Armand MJ, Callen JC, Gomez de Gracia A, Denis H, le Maire M (1990) Elongation factor 1α (EF-1α) is concentrated in the Balbiani body and accumulates coordinately with the ribosomes during oogenesis of Xenopus laevis. Dev Biol 141:270–278

    Google Scholar 

  • Viet A, le Maire M, Philippe H, Morales J, Mazabraud A, Denis H (1991) Structural and functional properties of thesaurin a (42Sp50), the major protein of the 42 S particles present in Xenopus laevis previtellogenic oocytes. J Biol Chem 266:10392–10399

    Google Scholar 

  • Wang CK, Weil PA (1989) Purification and characterization of Saccharomyces cerevisiae transcription factor IIIA. J Biol Chem 264:1092–1099

    Google Scholar 

  • Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Ann Rev Biochem 57:479–504

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centre de Génétique Moléculaire, Laboratoire propre de CNRS, associé à l'Université P. et M. Curie (Paris VI), F-91198, Gif-sur-Yvette Cedex, France

    André Mazabraud & Herman Denis

  2. Laboratoire d'Embryologie Moléculaire et Expérimentale, Université de Paris XI, URA CNRS 1134, F-91405, Orsay Cedex, France

    Maurice Wegnez

Authors
  1. André Mazabraud
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maurice Wegnez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Herman Denis
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Offprint requests to: H. Denis

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mazabraud, A., Wegnez, M. & Denis, H. Origin of several abundant proteins of amphibian oocytes. J Mol Evol 35, 546–550 (1992). https://doi.org/10.1007/BF00160215

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00160215

Key words

Search

Navigation