Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition

The oocyte-to-embryo transition marks the onset of development. The initial phase of this profound change from the differentiated oocyte to the totipotent embryo occurs in the absence of both transcription and mRNA degradation. Here we combine global polysome profiling, ribosome-footprint profiling,...

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Main Authors: Iva Kronja, Bingbing Yuan, Stephen W. Eichhorn, Kristina Dzeyk, Jeroen Krijgsveld, David P. Bartel, Terry L. Orr-Weaver
Format: Article
Language:English
Published: Elsevier 2014-06-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124714003775
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spelling doaj-5a500ff43cba459da50ecf4d9b280b892020-11-24T21:34:07ZengElsevierCell Reports2211-12472014-06-01751495150810.1016/j.celrep.2014.05.002Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo TransitionIva Kronja0Bingbing Yuan1Stephen W. Eichhorn2Kristina Dzeyk3Jeroen Krijgsveld4David P. Bartel5Terry L. Orr-Weaver6Whitehead Institute, Cambridge, MA 02142, USAWhitehead Institute, Cambridge, MA 02142, USAWhitehead Institute, Cambridge, MA 02142, USAEuropean Molecular Biology Laboratory, 69117 Heidelberg, GermanyEuropean Molecular Biology Laboratory, 69117 Heidelberg, GermanyWhitehead Institute, Cambridge, MA 02142, USAWhitehead Institute, Cambridge, MA 02142, USAThe oocyte-to-embryo transition marks the onset of development. The initial phase of this profound change from the differentiated oocyte to the totipotent embryo occurs in the absence of both transcription and mRNA degradation. Here we combine global polysome profiling, ribosome-footprint profiling, and quantitative mass spectrometry in a comprehensive approach to delineate the translational and proteomic changes that occur during this important transition in Drosophila. Our results show that PNG kinase is a critical regulator of the extensive changes in the translatome, acting uniquely at this developmental window. Analysis of the proteome in png mutants provided insights into the contributions of translation to changes in protein levels, revealing a compensatory dynamic between translation and protein turnover during proteome remodeling at the return to totipotency. The proteome changes additionally suggested regulators of meiosis and early embryogenesis, including the conserved H3K4 demethylase LID, which we demonstrated is required during this period despite transcriptional inactivity.http://www.sciencedirect.com/science/article/pii/S2211124714003775
collection DOAJ
language English
format Article
sources DOAJ
author Iva Kronja
Bingbing Yuan
Stephen W. Eichhorn
Kristina Dzeyk
Jeroen Krijgsveld
David P. Bartel
Terry L. Orr-Weaver
spellingShingle Iva Kronja
Bingbing Yuan
Stephen W. Eichhorn
Kristina Dzeyk
Jeroen Krijgsveld
David P. Bartel
Terry L. Orr-Weaver
Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition
Cell Reports
author_facet Iva Kronja
Bingbing Yuan
Stephen W. Eichhorn
Kristina Dzeyk
Jeroen Krijgsveld
David P. Bartel
Terry L. Orr-Weaver
author_sort Iva Kronja
title Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition
title_short Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition
title_full Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition
title_fullStr Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition
title_full_unstemmed Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition
title_sort widespread changes in the posttranscriptional landscape at the drosophila oocyte-to-embryo transition
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2014-06-01
description The oocyte-to-embryo transition marks the onset of development. The initial phase of this profound change from the differentiated oocyte to the totipotent embryo occurs in the absence of both transcription and mRNA degradation. Here we combine global polysome profiling, ribosome-footprint profiling, and quantitative mass spectrometry in a comprehensive approach to delineate the translational and proteomic changes that occur during this important transition in Drosophila. Our results show that PNG kinase is a critical regulator of the extensive changes in the translatome, acting uniquely at this developmental window. Analysis of the proteome in png mutants provided insights into the contributions of translation to changes in protein levels, revealing a compensatory dynamic between translation and protein turnover during proteome remodeling at the return to totipotency. The proteome changes additionally suggested regulators of meiosis and early embryogenesis, including the conserved H3K4 demethylase LID, which we demonstrated is required during this period despite transcriptional inactivity.
url http://www.sciencedirect.com/science/article/pii/S2211124714003775
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