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In vivo storage of XR family interspersed RNA in Xenopus oocytes

Published online by Cambridge University Press:  26 September 2008

Chengyu Liu  and
L. Dennis Smith
Chengyu Liu*
Affiliation:
Department of Developmental and Cell Biology and Developmental Biology Center, University of California at Irvine, Irvine, California, USA
L. Dennis Smith
Affiliation:
Department of Developmental and Cell Biology and Developmental Biology Center, University of California at Irvine, Irvine, California, USA
*
1 Dr Chengyu liu, Roche Institute of Molecular Biology, 340 Kingsland Street, Nutley, NJ 07110, USA. Telephone: (201)-235-4574. Fax: (201)-235-2839.
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Summary

Interspersed RNA is an abundant class of cytoplasmic poly(A)+ RNA which contains repetitive elements within mostly heterogeneous single copy sequences. In spite of its quantitative importance in oocytes or eggs (two-thirds of the total poly(A)+ RNA), very little is known about its synthesis, its interaction with other molecules, and its functional significance. Here, we analysed a prevalent family of interspersed RNa (XR family) during Xenopus oogenesis. We found that XR interspersed RNA, unlike extracted interspersed RNA, did not form RNA duplexes in vivo. Im small oocytes (stage III), XR RNA interacted with proteins forming rapidly sedimenting ribonucleoprotein particles (RNPs) with a median sedimentaion constant of 80S. However, towards the end of oogenesis (stage VI), these XR RNPs changed into smaller particles with a median sedimentaion constant of 40S. By analysing the proteins associated with XR RNA sequence, we have identified a 42 kilodalton protein in small oocytes, which was replaced by a 45 kilodalton protein at stage V of oogenesis.

Keywords

Interspersed RNARibonucleoprotein particleRNA binding proteinXenopus oocyte
Type
Article
Information
Zygote , Volume 3 , Issue 1 , February 1995 , pp. 37 - 44
Copyright
Copyright © Cambridge University Press 1995

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Footnotes

1PO Box 830745, University of Nebraska, Lincoln, Nebraska, 68583–0745., USA.

References

Allison, L.A., Romaniuk, P.J.. & Bakken, A.H.. (1991). RNA protein interactions of stored 5S RNA with TFIIIA and ribosomal protein L5 during Xenopus oogenesis. Dev. Biol. 144, 129–44.CrossRefGoogle ScholarPubMed
Anderson, D.M., Richter, J.D., Chamberlin, M.E., Price, D.H., Britten, R.J., Smith, L.D.. & Davidson, E.H.. (1982). Sequence organization of poly(A) RNA synthesized and accumulated in lampbrush chromosome stage Xenopus laevis. J. Mol. Biol. 155, 281–309.CrossRefGoogle ScholarPubMed
Bandziulis, R.J., Swanson, M.S.. & Dreyfuss, G.. (1989). RNA-binding proteins proteins as developmental regulators. Genes Dev 3, 431–7.CrossRefGoogle ScholarPubMed
Bass, B.L.. & Weintraub, H.. (1987). A developmentally regulated activity that unwinds RNA duplexes. Cell 48, 607–13.CrossRefGoogle ScholarPubMed
Burd, C.G.. & Dreyfuss, G.. (1994). Conserved structures and diversity of functions of RNA-binding proteins. Science 265, 615–21.CrossRefGoogle ScholarPubMed
Calzone, F.J., Jacobs, H.T., Flytzanis, C.N., Posakony, J.W.. & Davidson, E.H.. (1985). Interspersed maternal RNA of sea urchin and amphibian eggs. In Biology of Fertilization: The Fertilization Response of the Eggs, ed. C.B., Mertz. & A., Monroy, vol. 3, pp 347–66. Orlando, Florida: Academic Press.Google Scholar
Calzone, F.J., Lee, J.J., Le, N., Britten, R.J.. & Davidson, E.H.. (1988). A long, nontranslatable poly(A) RNA stored in the egg of the sea urchin Strongylocentrotus purpuratus. Genes Dev. 2, 305–18.CrossRefGoogle ScholarPubMed
Costantini, F.D., Britten, R.J.. & Davidson, E.H.. (1980). Message sequences and short repetitive sequences are interspersed in sea urchin egg poly(A)+ RNAs. Nature 287, 111–17.CrossRefGoogle ScholarPubMed
Cummings, A.. & Sommerville, J.. (1988). Protein kinase activity associated with stored messenger ribonucleoprotein particles of xenopus oocytes. J. Cell Biol. 107, 45–56.CrossRefGoogle ScholarPubMed
Darnbrough, C.H.. & Ford, P.J.. (1981). Identification in Xenopus laevis of a class of oocyte-specific proteins bound to messenger RNA. Eur. J. Biochem. 113, 415–26.CrossRefGoogle ScholarPubMed
Davidson, E.H. (1986). Gene Activity in Early Development, 3rd edn. Orlando, Florida: Academic Press.Google Scholar
Davidson, E.H.. & Hough, B.R.. (1971). Genetic information in oocyte RNA. J. Mol. Biol. 56, 491–506.CrossRefGoogle ScholarPubMed
Dearsly, A.L., Johnson, R.M., Barrett, P.. & Sommerville, J.. (1985). Identification of a 60-kda phosphoprotein that binds stored messenger rna of Xenopus oocytes. Eur. J. Biochem. 150, 95–103.CrossRefGoogle ScholarPubMed
Denis, H.. & LeMaire, M.. (1983). Thesaurisomes, a novel king of nucleoprotein particles. Subcell. Biochem. 9, 263–7.CrossRefGoogle Scholar
Deschamps, S., Viel, A., Garrigos, M., Denis, H.. & Maire, M.. (1992). mRNP4, a major mRNA-binding protein from Xenopus oocytes is identical to transcription factor frg Y2. J. Biol. Chem. 267, 13799–802.CrossRefGoogle Scholar
Dreyfuss, G.. (1986). Structure and function of nuclear and cytoplasmic ribonucleoprotein particles. Annu. Rev. Cell Biol. 2, 459–98.CrossRefGoogle ScholarPubMed
Dreyfuss, G., Philipson, L.. & Mattaj, I.W.. (1988a). Ribonucleoprotein particles in cellular processes. J. Cell Biol. 106, 1419–25.CrossRefGoogle ScholarPubMed
Dreyfuss, G., Swanson, M.S.. & Pinol-Roma, S.. (1988b). Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation. Trends Biochem. Sci. 13, 86–91.CrossRefGoogle ScholarPubMed
Dreyfuss, G., Choi, Y.D.. & Adam, S.A.. (1989). The ribonucleoprotein structures along the pathway of mRNA formation. Endocrine Res. 15, 441–74.CrossRefGoogle ScholarPubMed
Dumont, J.N.. (1972). Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morphol. 136, 153–80.CrossRefGoogle ScholarPubMed
Federoff, N., Wellauer, P.K.. & Wall, R.. (1977). Intermolecular duplexes in heterogeneous neclear rna from Hela cells. Cell 10, 597–610.CrossRefGoogle Scholar
Ford, P.J.. (1971). Non-coordinated accumulation and synthesis of 5S ribonucleic acid by ovaries of Xenopus laevis. Nature 233, 561–4.CrossRefGoogle ScholarPubMed
Honda, B.M.. & Roeder, R.G.. (1980). Association of 5S gene transcription factor with 5S RNA and altered levels of the factor during cell differentiation. Cell 22, 119–26.CrossRefGoogle ScholarPubMed
Hough-Evans, B.R., Ernst, S.G., Britten, R.J.. & Davidson, E.H.. (1979). RNA complexity of developing sea urchin oocytes. Dev. Biol. 69, 225–36.CrossRefGoogle ScholarPubMed
Keem, K., Smith, L.D., Wallace, R.A.. & Wolf, D.. (1979). Growth rate of oocytes in laboratory-maintained Xenopus laevis. Camete Res. 2, 125–35.Google Scholar
Kick, D., Barrett, P., Cummings, A.. & Sommerville, J.. (1987). Phosphorylation of a 60 kDa polypeptide from Xenopus oocytes blocks messenger RNA translation. Nucleic Acids Res. 15, 4099–109.CrossRefGoogle ScholarPubMed
LeMaire, M.. & Denis, H.. (1987). Biochemical research on oogenesis: binding of tRNA to the nucleoprotein particles of Xenopus laevis previtellogenic oocytes. J. Biol. Chem. 262, 654–9.CrossRefGoogle Scholar
Liu, C., Smith, L.D.. (1994). Differential accumulation of mRNA and interspersed RNA during Xenopus oogenesis and embryogenesis. Zygote 2, 307–16.CrossRefGoogle ScholarPubMed
Liu, C.. & Smith, L.D.. (1995). Evidence that XR family interspersed RNA may regulate translation in Xenopus oocytes. Mol. Reprod. Dev., in press.CrossRefGoogle Scholar
Marello, K., LaRovere, J.. & Sommerville, J.. (1992). Binding of Xenopus oocyte masking protein to mRNA sequences. Nucleic Acids Res. 20, 5593–600.CrossRefGoogle ScholarPubMed
Mattaj, I.W., Coppad, N.J., Brown, R.S., Clark, B.F.C.. & DeRobertis, E.M.. (1987). 42S p48 – the most abundant protein in previtellogenic Xenopus oocytes – resembles elongation factor 1a structurally and functionally. EMBO J. 6, 2409–13.CrossRefGoogle Scholar
McGrew, L.L.. & Richter, J.D.. (1989). Xenopus oocyte poly(A) RNAs that hybridize to a cloned interspersed repeat sequence are not translatable. Dev. Biol. 134, 267–70.CrossRefGoogle Scholar
Murray, M.T., Krohne, G.. & Franke, W.W.. (1991). Different forms of soluble cytoplasmic mRNa binding proteins and particles in Xenopus laevis oocytes and embryos. J. Cell Biol. 112, 1–11.CrossRefGoogle ScholarPubMed
Murray, M.T., Schiller, D.L.. & Franke, W.W.. (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.CrossRefGoogle ScholarPubMed
Newport, J.. & Kirschner, M.. (1982). A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at midblastula stage. Cell 30, 675–86.CrossRefGoogle Scholar
Nieuwkoop, P.D.. & Faber, J.. (1967). Normal Table of Xenopus laevis (Daudin). Amsterdam: North-Holland.Google Scholar
Pelham, H.R.B.. & Brown, D.D.. (1980). A specific transcription factor that can bind either the 5s genes of 5s RNA. Natl. Acad. Sci. USA 78, 1760–4.CrossRefGoogle Scholar
Posakony, J.W., Scheller, R.H., Anderson, D.M., Britten, R.J.. & Davidson, E.H.. (1981). Repetitive sequences of sea urching genome. III. Nuclotide sequences of cloned repeat elements. J. Mol. Biol. 149, 41–67.CrossRefGoogle Scholar
Ranjan, M., Tafuri, S.R.. & Wolffe, A.P.. (1993). Masking mRNA from translantion in somatic cells. Genes Dev. 7, 1725–6.CrossRefGoogle ScholarPubMed
Rebagliati, M.R.. & Melton, D.A.. (1987). Antisense RNA injections in fertilized frog eggs reveal an RNA duplex unwinding activity. Cell 48, 599–605.CrossRefGoogle ScholarPubMed
Richter, J.D.. & Smith, L.D. (1983). Developmentally regulated RNA binding proteins during oogenesis in Xenopus laevis. J. Biol. Chem. 258, 4864–9.CrossRefGoogle ScholarPubMed
Richter, J.D.. & Smith, L.D.. (1984). The reversible inhibition of translation by Xenopus oocyte specific proteins. Nature 309, 378–80.CrossRefGoogle ScholarPubMed
Richter, J.D., Anderson, D.M., Davidson, E.H. & Smith, L.D.. (1984). Interspersed poly(A) RNAs of amphibian oocytes are not translatable. J. Mol. Biol. 173, 227–41.CrossRefGoogle Scholar
Rosbash, M. & Ford, P.J.. (1974). Polyadenylic acid-containing RNA in Xenopus laevis oocytes. J. Mol. Biol. 85, 87–101.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F.. & Maniatis, T.. (1989). Molecular Cloning: A Laboratory Manual, 2nd edn. ColdSpring, Harbor, New York: Cold Spring Harbor Laboratory Press.Google Scholar
Smith, L.D., Xu, W.L.. & Varnold, R.L.. (1991). Oogenesis and oocyte isolation. In Xenopus laevis: Practial Uses in Cell and Molecular Biology, ed. B.J., Kay. & H.B., Peng, Methods in Cell Biology, vol. 36, pp 45–59. San Diego, California: Academic PressGoogle ScholarPubMed
Sommerville, J.. (1990). RNA-binding phosphoproteins and the regulation of maternal mRNA in Xenopus. J. Reprod. Fert. Suppl. 42. 225–33.Google ScholarPubMed
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
Swiderski, R.E.. & Richter, J.D.. (1988). Photocrosslinking of proteins to maternal mRNA in Xenopus oocytes. Dev. Biol. 128, 349–58.CrossRefGoogle ScholarPubMed
Tafuri, R.S.. & Wolffe, A.P.. (1993). Selective recruitment of masked maternal mRNA from messenger ribonucleoprotein particles containing FRGY2 (mRNP4). J. Biol. Chem. 268, 24 255–61.CrossRefGoogle ScholarPubMed
Taylor, M.A.. & Smith, L.D.. (1987). Induction of maturation in small Xenopus laevis oocytes. Dev. Biol. 121, 111–18.CrossRefGoogle ScholarPubMed
Viel, A., Armand, M.J., Callen, J.C., DeGracia, A.G., Denis, H.. & LeMaire, M.. (1990). Elongation factor 1-a (EF1-a) is concentrated in the balbiani body and accumulates coordinately with the ribosomes during oogenesis of Xenopus laevis. Dev. Biod. 141, 270–8.CrossRefGoogle Scholar
Wallace, R.A., Jared, D.W., Dumont, J.N.. & Sega, M.W.. (1973). Protein incorporation by isolated amphibian oocytes. III. Optimum incubation conditions. J. Exp. Zool. 184, 321–34.CrossRefGoogle Scholar