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Xenopus interspersed RNA families, Ocr and XR, bind DNA-binding proteins

Published online by Cambridge University Press:  26 September 2008

Katherine Ladner Guttridge  and
L. Dennis Smith
Katherine Ladner Guttridge*
Affiliation:
Developmental Biology Center, University of California-Irvine, Irvine, California, USA
L. Dennis Smith
Affiliation:
Developmental Biology Center, University of California-Irvine, Irvine, California, USA
*
Dr Katherine L. Guttridge, Department of Microbiology and Molecular Genetics, University of California-Irvine, Irvine, CA 92717, USA. Telephone: (714) 725-3096. Fax: (714)856-8598.
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Summary

Interspersed RNA makes up two-thirds of cytoplasmic polyadenylated RNA in Xenopus and sea urchin eggs.Although it has no known function, previous work has suggested that at least one family of interspersed RNA, XR, binds Xenopus oocyte proteins, and can influence the rate of translation. We have used two Xenopus repeat families, Ocr and XR, to explore their protein binding abilities. Ocr RNA binds the same pattern of highly abundant oocyte proteins that XR RNA binds, which are believed to be messenger ribonucleoprotein (mRNP) particle proteins. In addition, we show that Ocr RNA binds the Oct-60 protein, a member of the POU-domain family of transcription factors found in Xenopus oocytes. Using a 32 base pair sequence from the XR repeat in a DNA affinity column two proteins were isolated, 66KDa and 92KDa, that together form a complex with XR DNA. One of these proteins (92KDa) also binds XR RNA. We suggest that the role of at least a subset of interspersed RNAs in development may be to bind, and sequester in the cytoplasm, DNA-binding proteins until the end of oogenesis

Keywords

DNA-binding proteinsInterspersed RNAOogenesisXenopus
Type
Article
Information
Zygote , Volume 3 , Issue 2 , May 1995 , pp. 111 - 122
Copyright
Copyright © Cambridge University Press 1995

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References

Anderson, D.M., Scheller, R.H., Posakony, J.W., McAllister, L.B., Trabert, S.G., Beall, D., Britten, R.J. & Davidson, E.H. (1981). Repetitive sequences of the sea urchin genome: distribution of members of specific repetitive families. J. Mol. Biol. 145, 5–28.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 the poly(A) RNA synthesized and accumulated in lampbrush chromosome stage Xenopus laevis oocytes. J. Mol. Biol. 155, 281–309.CrossRefGoogle ScholarPubMed
Baulieu, E.-E., Godeau, F., Schorderet, M. & Schorderet-Slatkine, S. (1978). Steroid–induced meiotic division in Xenopus laevis oocytes: surface and calcium. Nature 275, 593–8.CrossRefGoogle ScholarPubMed
Calzone, F.J., Thézé, N., Thiebaud, P., Hill, R.L., Britten, T.J. & Davidson, E.H. (1988). Developmental appearance of factors that bind specifically to cis-regulatory sequences of a gene expressed in the sea urchin embryo. Genes Dev. 2, 1074–88.Google Scholar
Calzone, F.J., Höög, C., Teplow, D.B., Cutting, A.E., Zeller, R.W., Britten, R.J. & Davidson, E.H.(1991). Gene regulatory factors of the sea urchin embryo. I. Purification by affinity chromatography and cloning of P3A2, a novel DNA–binding protein. Development 112, 335–50.Google Scholar
Clemens, K.R., Wolf, V., McBryant, S.J., Zhang, P., Liao, X., Wright, P.E. & Gottesfeld, J.M. (1993). Molecular basis for specific recognition of both RNA and DNA by a zinc finger protein. Science 260, 530–3.Google Scholar
Costantini, F.D., Scheller, R.H., 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.Google Scholar
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, 415–24.CrossRefGoogle ScholarPubMed
Davidson, E.H. (1986). Gene Activity in Early Development. New York: Academic Press.Google Scholar
Davidson, E.H. & Britten, R.J. (1973). Organization, transcription and regulation in the animal genome. Q. Rev. Biol. 48, 565–613.CrossRefGoogle ScholarPubMed
Denegre, J.D. & Danilchik, M.V. (1993). Deep cytoplasmic rearrangements in axis– respecified Xenopus embryos. Dev. Biol. 160, 157–64.Google Scholar
Deschamps, S., Viel, A., Garrigos, M., Denis, H. & le Maire, M. (1992). mRNP4, a major mRNA – binding protein from Xenopus oocytes, is identical to transcription factor FRGY2. J. Biol. Chem. 267, 13799–802.Google Scholar
Dumont, J.N. (1972). Oogenesis in Xenopus laevis. I. Stage of oocyte development in laboratory maintained animals. J. Morphol. 136, 153–80.Google Scholar
Graham, D.E., Neufeld, B.R., Davidson, E.H. & Britten, R.J. (1974).Interspersion of repetitive and non–repetitive DNA sequences in the sea urchin genome. Cell 1, 127–37.Google Scholar
Hinkley, C.S., Martin, J.F., Leibham, D. & Perry, M. (1992). Sequential expression of multiple POU proteins during amphibian early development. Mol. Cell. Biol. 12, 638–49.Google Scholar
Höög, C., Calzone, F.J., Cutting, A.E., Britten, R.J. & Davidson, E.H. (1991). Gene regulatory factors of the sea urchin embryo. II.Two similar proteins, P3A1 and P3A2, bind to the same target sites that are required for early territorial gene expression. Development 112, 351–64.Google Scholar
Klein, W.H., Thomas, T.L., Lai, C., Scheller, R.H., Britten, R.J. & Davidson, E.H. (1978). Characteristics of individual repetitve sequence families in the sea urchin genome studied with cloned repeats. Cell 13, 889–900.CrossRefGoogle Scholar
Kloc, M. & Etkin, L.D. (1994). Delocalization of Vg1 mRNA from the vegetal cortex in Xenopus oocytes after destruction of XLsirt RNA. Science 265, 1101–3.Google Scholar
Kloc, M., Spohr, G. & Etkin, L.D. (1994). Translocation of repetitive RNA sequences with the germ plasm in Xenopus oocytes. Science 262, 1712–14.Google Scholar
Liu, C. (1992). Accumulation, polyadenylation, storage, and function of interspersed RNA during Xenopus oogenesis and embryogenesis. University of California, Irvine.Google Scholar
Liu, C. & Smith, L.D. (1994a). Differential accumulation of mRNA and interspersed RNA during Xenopus oogenesis and embryogenesis. Zygote 2, 307–16.Google Scholar
Liu, C. & Smith, L.D. (1994b). Evidence that XR family interspersed RNA may regulate translation in Xenopus oocytes. Mol. Reprod. Dev. (in Press).Google Scholar
Marello, K., LaRovere, J. &Sommerville, J. (1992). Binding of Xenopus oocyte masking proteins to mRNA sequences. Nucleic Acids Res. 20, 5593–600.CrossRefGoogle ScholarPubMed
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.Google Scholar
Morgan, G.T. & Middleton, K.M. (1990). Short interspersed repeats from Xenopus that contain mulitiple octamer motifs are related to know transposable elements. Nucleic Acids Res. 18, 5781–6.CrossRefGoogle Scholar
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.Google Scholar
Posakony, J.W., Scheller, R.H., Anderson, D.M., Britten, R.J. & Davidson, E.H. (1981). Repetitive sequences of sea urchin genome. III.Nucleotide sequences of cloned repeat elements. J. Mol. Biol. 149, 41–67.CrossRefGoogle ScholarPubMed
Ranjan, M., Tafuri, S.R. & Wolffe, A.P. (1993). Masking mRNA from translation in somatic cell. Genes Dev. 7, 1725–36.CrossRefGoogle Scholar
Richter, J.D. (1988). Information relay from gene to protein: the mRNP connection. Trends Biochem. 13, 483–6.Google Scholar
Richter, J.D. & Smith, L.D. (1981). Differential capacity for translation and lack of competition between mRNAs that segregate to free and membrane–bound polysomes. Cell 27, 183–91.CrossRefGoogle ScholarPubMed
Richter, J.D. & Smith, L.D. (1984a). Interspersed poly(A) RNAs of amphibian oocytes are not translatable. J. Mol. Biol. 173, 227–41.Google Scholar
Richter, J.D. & Smith, L.D. (1984b). Reversible inhibition of translation by Xenopus oocyte–specific proteins. Nature 309, 378–80.Google Scholar
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
Scheller, R.H., Anderson, D.M., Posakony, J.W., McAllister, L.B., Britten, R.J. & Davidson, E.H. (1981). Repetitive sequences of the sea urchin genome: subfamily structure and evolutionary conservation. J. Mol. Biol. 149, 15–39.Google Scholar
Sommerville, J. (1990). RNA-binding phosphoproteins and the regulation of maternal mRNA in Xenopus. J.Reprod. Fert. 42. 225–33.Google Scholar
Tafuri, S.R. & Wolffe, A.P. (1993). Selective recruitment of masked maternal mRNA from messenger ribonucleoprotein particle containing FRGY2 (mRNP4). J. Biol. Chem. 268. 24255–61.Google Scholar
Thézé, N., Calzone, F.J., Thiebaud, P., Hill, R.L., Britten, R.J. & Davidson, E.H. (1990). Sequences of the CyIIIa actin gene regulatory domain bound specifically by sea urchin embryo nuclear proteins. Mol. Reprod. Dev. 25, 110–22.Google 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. 18, 321–34.CrossRefGoogle Scholar
Wu, M. & Gerhart, J. (1991). Raising Xenopus in the laboratory. In: Methods in Cell Biology, Xenopus laevis: Practical Uses and Molecular Biology, ed. Kay, B.K. & Peng, H.B., 3–18. San Diego, California: Academic Press.Google Scholar