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EMBO J. Jan 2, 1998; 17(1): 278–287.
PMCID: PMC1170378

EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos.

Abstract

During Xenopus early development, gene expression is regulated mainly at the translational level by the length of the poly(A) tail of mRNAs. The Eg family and c-mos maternal mRNAs are deadenylated rapidly and translationally repressed after fertilization. Here, we characterize a short sequence element (EDEN) responsible for the rapid deadenylation of Eg5 mRNA. Determining the core EDEN sequence permitted us to localize the c-mos EDEN sequence. The c-mos EDEN confered a rapid deadenylation to a reporter gene. The EDEN-specific RNA-binding protein (EDEN-BP) was purified and a cDNA obtained. EDEN-BP is highly homologous to a human protein possibly involved in myotonic dystrophy. Immunodepleting EDEN-BP from an egg extract totally abolished the EDEN-mediated deadenylation activity, but did not affect the default deadenylation activity. Therefore, EDEN-BP constitutes the first trans-acting factor for which an essential role in the specificity of mRNA deadenylation has been directly demonstrated.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Audic Y, Omilli F, Osborne HB. Postfertilization deadenylation of mRNAs in Xenopus laevis embryos is sufficient to cause their degradation at the blastula stage. Mol Cell Biol. 1997 Jan;17(1):209–218. [PMC free article] [PubMed]
  • Audic Y, Omilli F, Osborne HB, Landais L. Design and use of easily made RNA size markers. Biotechniques. 1997 Oct;23(4):612–616. [PubMed]
  • Beelman CA, Parker R. Degradation of mRNA in eukaryotes. Cell. 1995 Apr 21;81(2):179–183. [PubMed]
  • Boeck R, Tarun S, Jr, Rieger M, Deardorff JA, Müller-Auer S, Sachs AB. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J Biol Chem. 1996 Jan 5;271(1):432–438. [PubMed]
  • Bouvet P, Omilli F, Arlot-Bonnemains Y, Legagneux V, Roghi C, Bassez T, Osborne HB. The deadenylation conferred by the 3' untranslated region of a developmentally controlled mRNA in Xenopus embryos is switched to polyadenylation by deletion of a short sequence element. Mol Cell Biol. 1994 Mar;14(3):1893–1900. [PMC free article] [PubMed]
  • Brown CE, Tarun SZ, Jr, Boeck R, Sachs AB. PAN3 encodes a subunit of the Pab1p-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol Cell Biol. 1996 Oct;16(10):5744–5753. [PMC free article] [PubMed]
  • Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994 Jul 29;265(5172):615–621. [PubMed]
  • Burd CG, Swanson MS, Görlach M, Dreyfuss G. Primary structures of the heterogeneous nuclear ribonucleoprotein A2, B1, and C2 proteins: a diversity of RNA binding proteins is generated by small peptide inserts. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9788–9792. [PMC free article] [PubMed]
  • Fox CA, Wickens M. Poly(A) removal during oocyte maturation: a default reaction selectively prevented by specific sequences in the 3' UTR of certain maternal mRNAs. Genes Dev. 1990 Dec;4(12B):2287–2298. [PubMed]
  • Fox CA, Sheets MD, Wickens MP. Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev. 1989 Dec;3(12B):2151–2162. [PubMed]
  • Funke B, Zuleger B, Benavente R, Schuster T, Goller M, Stévenin J, Horak I. The mouse poly(C)-binding protein exists in multiple isoforms and interacts with several RNA-binding proteins. Nucleic Acids Res. 1996 Oct 1;24(19):3821–3828. [PMC free article] [PubMed]
  • Gallie DR. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 1991 Nov;5(11):2108–2116. [PubMed]
  • Good PJ. A conserved family of elav-like genes in vertebrates. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4557–4561. [PMC free article] [PubMed]
  • Harland R, Misher L. Stability of RNA in developing Xenopus embryos and identification of a destabilizing sequence in TFIIIA messenger RNA. Development. 1988 Apr;102(4):837–852. [PubMed]
  • Huarte J, Stutz A, O'Connell ML, Gubler P, Belin D, Darrow AL, Strickland S, Vassalli JD. Transient translational silencing by reversible mRNA deadenylation. Cell. 1992 Jun 12;69(6):1021–1030. [PubMed]
  • Jackson RJ, Standart N. Do the poly(A) tail and 3' untranslated region control mRNA translation? Cell. 1990 Jul 13;62(1):15–24. [PubMed]
  • Jarzembowski JA, Malter JS. Cytoplasmic fate of eukaryotic mRNA: identification and characterization of AU-binding proteins. Prog Mol Subcell Biol. 1997;18:141–172. [PubMed]
  • Kaminski A, Hunt SL, Patton JG, Jackson RJ. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA. 1995 Nov;1(9):924–938. [PMC free article] [PubMed]
  • Kohli V, Temsamani J. Comparison of in vitro transcriptions using various types of DNA templates. Anal Biochem. 1993 Feb 1;208(2):223–227. [PubMed]
  • Krieg PA, Melton DA. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 1984 Sep 25;12(18):7057–7070. [PMC free article] [PubMed]
  • Kunkel TA. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. [PMC free article] [PubMed]
  • Legagneux V, Bouvet P, Omilli F, Chevalier S, Osborne HB. Identification of RNA-binding proteins specific to Xenopus Eg maternal mRNAs: association with the portion of Eg2 mRNA that promotes deadenylation in embryos. Development. 1992 Dec;116(4):1193–1202. [PubMed]
  • Legagneux V, Omilli F, Osborne HB. Substrate-specific regulation of RNA deadenylation in Xenopus embryo and activated egg extracts. RNA. 1995 Dec;1(10):1001–1008. [PMC free article] [PubMed]
  • McGrew LL, Dworkin-Rastl E, Dworkin MB, Richter JD. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 1989 Jun;3(6):803–815. [PubMed]
  • Osborne HB, Duval C, Ghoda L, Omilli F, Bassez T, Coffino P. Expression and post-transcriptional regulation of ornithine decarboxylase during early Xenopus development. Eur J Biochem. 1991 Dec 5;202(2):575–581. [PubMed]
  • Paillard L, Legagneux V, Osborne HB. Poly(A) metabolism in Xenopus laevis embryos: substrate-specific and default poly(A) nuclease activities are mediated by two distinct complexes. Biochimie. 1996;78(6):399–407. [PubMed]
  • Paris J, Philippe M. Poly(A) metabolism and polysomal recruitment of maternal mRNAs during early Xenopus development. Dev Biol. 1990 Jul;140(1):221–224. [PubMed]
  • Paris J, Richter JD. Maturation-specific polyadenylation and translational control: diversity of cytoplasmic polyadenylation elements, influence of poly(A) tail size, and formation of stable polyadenylation complexes. Mol Cell Biol. 1990 Nov;10(11):5634–5645. [PMC free article] [PubMed]
  • Paris J, Osborne HB, Couturier A, Le Guellec R, Philippe M. Changes in the polyadenylation of specific stable RNA during the early development of Xenopus laevis. Gene. 1988 Dec 10;72(1-2):169–176. [PubMed]
  • Prussak CE, Almazan MT, Tseng BY. Peptide production from proteins separated by sodium dodecyl-sulfate polyacrylamide gel electrophoresis. Anal Biochem. 1989 May 1;178(2):233–238. [PubMed]
  • Sachs AB, Davis RW. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell. 1989 Sep 8;58(5):857–867. [PubMed]
  • Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature. 1988 Oct 6;335(6190):519–525. [PubMed]
  • Sagata N, Watanabe N, Vande Woude GF, Ikawa Y. The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature. 1989 Nov 30;342(6249):512–518. [PubMed]
  • Sallés FJ, Lieberfarb ME, Wreden C, Gergen JP, Strickland S. Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. Science. 1994 Dec 23;266(5193):1996–1999. [PubMed]
  • Sheets MD, Fox CA, Hunt T, Vande Woude G, Wickens M. The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 1994 Apr 15;8(8):926–938. [PubMed]
  • Simon R, Richter JD. Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryonic cytoplasmic polyadenylation element-binding proteins. Mol Cell Biol. 1994 Dec;14(12):7867–7875. [PMC free article] [PubMed]
  • Simon R, Tassan JP, Richter JD. Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev. 1992 Dec;6(12B):2580–2591. [PubMed]
  • Stebbins-Boaz B, Richter JD. Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early Xenopus development. Mol Cell Biol. 1994 Sep;14(9):5870–5880. [PMC free article] [PubMed]
  • Timchenko LT, Miller JW, Timchenko NA, DeVore DR, Datar KV, Lin L, Roberts R, Caskey CT, Swanson MS. Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res. 1996 Nov 15;24(22):4407–4414. [PMC free article] [PubMed]
  • Varnum SM, Wormington WM. Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. Genes Dev. 1990 Dec;4(12B):2278–2286. [PubMed]
  • Virtanen A, Aström J. Function and characterization of poly(A)-specific 3' exoribonucleases. Prog Mol Subcell Biol. 1997;18:199–220. [PubMed]
  • Wang J, Pegoraro E, Menegazzo E, Gennarelli M, Hoop RC, Angelini C, Hoffman EP. Myotonic dystrophy: evidence for a possible dominant-negative RNA mutation. Hum Mol Genet. 1995 Apr;4(4):599–606. [PubMed]

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