Literature DB >> 19364820

Spatially restricted translation of the xCR1 mRNA in Xenopus embryos.

Yan Zhang1, Kara D Forinash, Jered McGivern, Brian Fritz, Karel Dorey, Michael D Sheets.   

Abstract

The xCR1 protein is a maternal determinant and cofactor for nodal signaling in vertebrate embryos. The xCR1 protein accumulates specifically in the animal cells of Xenopus embryos, but maternal xCR1 mRNA is distributed equally throughout all embryonic cells. Here, we show that vegetal cell-specific translational repression of xCR1 mRNA contributes to this spatially restricted accumulation of the xCR1 protein in Xenopus embryos. xCR1 mRNA was associated with polyribosomes in animal cells but not vegetal cells. A 351-nucleotide region of xCR1 mRNA's 3' untranslated region was sufficient to confer a spatially restricted pattern of translation to a luciferase reporter mRNA by repressing translation in vegetal cells. Repression depended upon the mRNA's 5' cap but not its 3' poly(A) tail. Furthermore, the region of xCR1 mRNA sufficient to confer vegetal cell-specific repression contained both Pumilio binding elements (PBEs) and binding sites for the CUG-BP1 protein. The PBEs and the CUG-BP1 sites were necessary but not sufficient for translation repression. Our studies of xCR1 mRNA document the first example of spatially regulated translation in controlling the asymmetric distribution of a maternal determinant in vertebrates.

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Year:  2009        PMID: 19364820      PMCID: PMC2698763          DOI: 10.1128/MCB.01865-08

Source DB:  PubMed          Journal:  Mol Cell Biol        ISSN: 0270-7306            Impact factor:   4.272


  55 in total

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Authors:  Aaron C Goldstrohm; Marvin Wickens
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2.  A combinatorial code for CPE-mediated translational control.

Authors:  Maria Piqué; José Manuel López; Sylvain Foissac; Roderic Guigó; Raúl Méndez
Journal:  Cell       Date:  2008-02-08       Impact factor: 41.582

3.  Recruitment of Nanos to hunchback mRNA by Pumilio.

Authors:  J Sonoda; R P Wharton
Journal:  Genes Dev       Date:  1999-10-15       Impact factor: 11.361

4.  CUG repeat binding protein (CUGBP1) interacts with the 5' region of C/EBPbeta mRNA and regulates translation of C/EBPbeta isoforms.

Authors:  N A Timchenko; A L Welm; X Lu; L T Timchenko
Journal:  Nucleic Acids Res       Date:  1999-11-15       Impact factor: 16.971

5.  Poly(A)-independent regulation of maternal hunchback translation in the Drosophila embryo.

Authors:  D Chagnovich; R Lehmann
Journal:  Proc Natl Acad Sci U S A       Date:  2001-09-18       Impact factor: 11.205

6.  Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein.

Authors:  S Nakahata; Y Katsu; K Mita; K Inoue; Y Nagahama; M Yamashita
Journal:  J Biol Chem       Date:  2001-03-29       Impact factor: 5.157

7.  Translation of ASH1 mRNA is repressed by Puf6p-Fun12p/eIF5B interaction and released by CK2 phosphorylation.

Authors:  Yingfeng Deng; Robert H Singer; Wei Gu
Journal:  Genes Dev       Date:  2008-04-15       Impact factor: 11.361

8.  Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1.

Authors:  Irina A Vlasova; Nuzha M Tahoe; Danhua Fan; Ola Larsson; Bernd Rattenbacher; Julius R Sternjohn; Jayprakash Vasdewani; George Karypis; Cavan S Reilly; Peter B Bitterman; Paul R Bohjanen
Journal:  Mol Cell       Date:  2008-02-01       Impact factor: 17.970

9.  The RNA-binding protein CUGBP1 regulates stability of tumor necrosis factor mRNA in muscle cells: implications for myotonic dystrophy.

Authors:  Libin Zhang; Jerome E Lee; Jeffrey Wilusz; Carol J Wilusz
Journal:  J Biol Chem       Date:  2008-06-16       Impact factor: 5.157

10.  Identification of CUG-BP1/EDEN-BP target mRNAs in Xenopus tropicalis.

Authors:  Antoine Graindorge; Olivier Le Tonquèze; Raphaël Thuret; Nicolas Pollet; H Beverley Osborne; Yann Audic
Journal:  Nucleic Acids Res       Date:  2008-02-11       Impact factor: 16.971

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  13 in total

Review 1.  The multifaceted role of the embryonic gene Cripto-1 in cancer, stem cells and epithelial-mesenchymal transition.

Authors:  Malgorzata Klauzinska; Nadia P Castro; Maria Cristina Rangel; Benjamin T Spike; Peter C Gray; Daniel Bertolette; Frank Cuttitta; David Salomon
Journal:  Semin Cancer Biol       Date:  2014-08-19       Impact factor: 15.707

Review 2.  Controlling the Messenger: Regulated Translation of Maternal mRNAs in Xenopus laevis Development.

Authors:  Michael D Sheets; Catherine A Fox; Megan E Dowdle; Susanne Imboden Blaser; Andy Chung; Sookhee Park
Journal:  Adv Exp Med Biol       Date:  2017       Impact factor: 2.622

3.  Assaying NanoLuc Luciferase Activity from mRNA-Injected Xenopus Embryos.

Authors:  Michael D Sheets
Journal:  Methods Mol Biol       Date:  2019

4.  A single KH domain in Bicaudal-C links mRNA binding and translational repression functions to maternal development.

Authors:  Megan E Dowdle; Sookhee Park; Susanne Blaser Imboden; Catherine A Fox; Douglas W Houston; Michael D Sheets
Journal:  Development       Date:  2019-05-15       Impact factor: 6.868

5.  Systematic analysis of cis-elements in unstable mRNAs demonstrates that CUGBP1 is a key regulator of mRNA decay in muscle cells.

Authors:  Jerome E Lee; Ju Youn Lee; Jeffrey Wilusz; Bin Tian; Carol J Wilusz
Journal:  PLoS One       Date:  2010-06-21       Impact factor: 3.240

6.  Polyribosome analysis for investigating mRNA translation in Xenopus oocytes, eggs and embryos.

Authors:  M D Sheets; B Fritz; R S Hartley; Y Zhang
Journal:  Methods       Date:  2010-01-22       Impact factor: 3.608

7.  Determinants of RNA binding and translational repression by the Bicaudal-C regulatory protein.

Authors:  Yan Zhang; Sookhee Park; Susanne Blaser; Michael D Sheets
Journal:  J Biol Chem       Date:  2014-01-29       Impact factor: 5.157

8.  A gradient of maternal Bicaudal-C controls vertebrate embryogenesis via translational repression of mRNAs encoding cell fate regulators.

Authors:  Sookhee Park; Susanne Blaser; Melissa A Marchal; Douglas W Houston; Michael D Sheets
Journal:  Development       Date:  2016-01-25       Impact factor: 6.868

9.  An essential role for maternal control of Nodal signaling.

Authors:  Pooja Kumari; Patrick C Gilligan; Shimin Lim; Long Duc Tran; Sylke Winkler; Robin Philp; Karuna Sampath
Journal:  Elife       Date:  2013-09-10       Impact factor: 8.140

10.  Bicaudal-C spatially controls translation of vertebrate maternal mRNAs.

Authors:  Yan Zhang; Amy Cooke; Sookhee Park; Colin N Dewey; Marvin Wickens; Michael D Sheets
Journal:  RNA       Date:  2013-09-23       Impact factor: 4.942

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