BREs Mediate Both Repression and Activation of oskar mRNA Translation and Act In trans

Brad Reveal; Nan Yan; Mark J. Snee; Chin I. Pai; Youme Gim; Paul M. Macdonald

doi:10.1016/j.devcel.2009.12.021

BREs Mediate Both Repression and Activation of oskar mRNA Translation and Act In trans

Brad Reveal, Nan Yan, Mark J. Snee, Chin I. Pai, Youme Gim, Paul M. Macdonald

Research output: Contribution to journal › Article › peer-review

37 Scopus citations

Abstract

Asymmetric positioning of proteins within cells is crucial for cell polarization and function. Deployment of Oskar protein at the posterior pole of the Drosophila oocyte relies on localization of the oskar mRNA, repression of its translation prior to localization, and finally activation of translation. Translational repression is mediated by BREs, regulatory elements positioned in two clusters near both ends of the oskar mRNA 3’ UTR. Here we show some BREs are bifunctional: both clusters of BREs contribute to translational repression, and the 3’ cluster has an additional role in release from BRE-dependent repression. Remarkably, both BRE functions can be provided in trans by an oskar mRNA with wild-type BREs that is itself unable to encode Oskar protein. Regulation in trans is likely enabled by assembly of oskar transcripts in cytoplasmic RNPs. Concentration of transcripts in such RNPs is common, and trans regulation of mRNAs may therefore be widespread.

Original language	English (US)
Pages (from-to)	496-502
Number of pages	7
Journal	Developmental cell
Volume	18
Issue number	3
DOIs	https://doi.org/10.1016/j.devcel.2009.12.021
State	Published - Mar 16 2010

Keywords

DEVBIO
RNA

ASJC Scopus subject areas

Molecular Biology
General Biochemistry, Genetics and Molecular Biology
Developmental Biology
Cell Biology

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10.1016/j.devcel.2009.12.021

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abstract = "Asymmetric positioning of proteins within cells is crucial for cell polarization and function. Deployment of Oskar protein at the posterior pole of the Drosophila oocyte relies on localization of the oskar mRNA, repression of its translation prior to localization, and finally activation of translation. Translational repression is mediated by BREs, regulatory elements positioned in two clusters near both ends of the oskar mRNA 3{\textquoteright} UTR. Here we show some BREs are bifunctional: both clusters of BREs contribute to translational repression, and the 3{\textquoteright} cluster has an additional role in release from BRE-dependent repression. Remarkably, both BRE functions can be provided in trans by an oskar mRNA with wild-type BREs that is itself unable to encode Oskar protein. Regulation in trans is likely enabled by assembly of oskar transcripts in cytoplasmic RNPs. Concentration of transcripts in such RNPs is common, and trans regulation of mRNAs may therefore be widespread.",

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author = "Brad Reveal and Nan Yan and Snee, {Mark J.} and Pai, {Chin I.} and Youme Gim and Macdonald, {Paul M.}",

note = "Funding Information: We thank Janice Fischer, Dave Stein, Robin Wharton, and members of the Macdonald lab for discussion and criticism of the manuscript, and Anne Ephrussi, Girish Deshpande, and the Bloomington and Harvard Medical School stock centers for fly stocks. This work was supported by NIH grant GM54409. Publisher Copyright: {\textcopyright} 2010 Elsevier Inc.",

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AU - Gim, Youme

AU - Macdonald, Paul M.

N1 - Funding Information: We thank Janice Fischer, Dave Stein, Robin Wharton, and members of the Macdonald lab for discussion and criticism of the manuscript, and Anne Ephrussi, Girish Deshpande, and the Bloomington and Harvard Medical School stock centers for fly stocks. This work was supported by NIH grant GM54409. Publisher Copyright: © 2010 Elsevier Inc.

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N2 - Asymmetric positioning of proteins within cells is crucial for cell polarization and function. Deployment of Oskar protein at the posterior pole of the Drosophila oocyte relies on localization of the oskar mRNA, repression of its translation prior to localization, and finally activation of translation. Translational repression is mediated by BREs, regulatory elements positioned in two clusters near both ends of the oskar mRNA 3’ UTR. Here we show some BREs are bifunctional: both clusters of BREs contribute to translational repression, and the 3’ cluster has an additional role in release from BRE-dependent repression. Remarkably, both BRE functions can be provided in trans by an oskar mRNA with wild-type BREs that is itself unable to encode Oskar protein. Regulation in trans is likely enabled by assembly of oskar transcripts in cytoplasmic RNPs. Concentration of transcripts in such RNPs is common, and trans regulation of mRNAs may therefore be widespread.

AB - Asymmetric positioning of proteins within cells is crucial for cell polarization and function. Deployment of Oskar protein at the posterior pole of the Drosophila oocyte relies on localization of the oskar mRNA, repression of its translation prior to localization, and finally activation of translation. Translational repression is mediated by BREs, regulatory elements positioned in two clusters near both ends of the oskar mRNA 3’ UTR. Here we show some BREs are bifunctional: both clusters of BREs contribute to translational repression, and the 3’ cluster has an additional role in release from BRE-dependent repression. Remarkably, both BRE functions can be provided in trans by an oskar mRNA with wild-type BREs that is itself unable to encode Oskar protein. Regulation in trans is likely enabled by assembly of oskar transcripts in cytoplasmic RNPs. Concentration of transcripts in such RNPs is common, and trans regulation of mRNAs may therefore be widespread.

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BREs Mediate Both Repression and Activation of oskar mRNA Translation and Act In trans

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