Literature DB >> 24957527

Global characterization of the oocyte-to-embryo transition in Caenorhabditis elegans uncovers a novel mRNA clearance mechanism.

Marlon Stoeckius1, Dominic Grün1, Marieluise Kirchner2, Salah Ayoub1, Francesca Torti1, Fabio Piano3, Margareta Herzog1, Matthias Selbach2, Nikolaus Rajewsky4.   

Abstract

The oocyte-to-embryo transition (OET) is thought to be mainly driven by post-transcriptional gene regulation. However, expression of both RNAs and proteins during the OET has not been comprehensively assayed. Furthermore, specific molecular mechanisms that regulate gene expression during OET are largely unknown. Here, we quantify and analyze transcriptome-wide, expression of mRNAs and thousands of proteins in Caenorhabditis elegans oocytes, 1-cell, and 2-cell embryos. This represents a first comprehensive gene expression atlas during the OET in animals. We discovered a first wave of degradation in which thousands of mRNAs are cleared shortly after fertilization. Sequence analysis revealed a statistically highly significant presence of a polyC motif in the 3' untranslated regions of most of these degraded mRNAs. Transgenic reporter assays demonstrated that this polyC motif is required and sufficient for mRNA degradation after fertilization. We show that orthologs of human polyC-binding protein specifically bind this motif. Our data suggest a mechanism in which the polyC motif and binding partners direct degradation of maternal mRNAs. Our data also indicate that endogenous siRNAs but not miRNAs promote mRNA clearance during the OET.
© 2014 The Authors.

Entities:  

Keywords:  Caenorhabditis elegans; embryogenesis; maternal mRNA; oocyte‐to‐embryo transition; posttranscriptional gene regulation

Mesh:

Substances:

Year:  2014        PMID: 24957527      PMCID: PMC4195759          DOI: 10.15252/embj.201488769

Source DB:  PubMed          Journal:  EMBO J        ISSN: 0261-4189            Impact factor:   11.598


  71 in total

1.  The dynamics of gene products fluctuation during bovine pre-hatching development.

Authors:  Isabelle Gilbert; Sara Scantland; Eve-Lyne Sylvestre; Catherine Gravel; Isabelle Laflamme; Marc-André Sirard; Claude Robert
Journal:  Mol Reprod Dev       Date:  2009-08       Impact factor: 2.609

2.  A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics.

Authors:  Jürgen Cox; Ivan Matic; Maximiliane Hilger; Nagarjuna Nagaraj; Matthias Selbach; Jesper V Olsen; Matthias Mann
Journal:  Nat Protoc       Date:  2009       Impact factor: 13.491

3.  Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes.

Authors:  Oliver H Tam; Alexei A Aravin; Paula Stein; Angelique Girard; Elizabeth P Murchison; Sihem Cheloufi; Emily Hodges; Martin Anger; Ravi Sachidanandam; Richard M Schultz; Gregory J Hannon
Journal:  Nature       Date:  2008-04-10       Impact factor: 49.962

4.  Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes.

Authors:  Toshiaki Watanabe; Yasushi Totoki; Atsushi Toyoda; Masahiro Kaneda; Satomi Kuramochi-Miyagawa; Yayoi Obata; Hatsune Chiba; Yuji Kohara; Tomohiro Kono; Toru Nakano; M Azim Surani; Yoshiyuki Sakaki; Hiroyuki Sasaki
Journal:  Nature       Date:  2008-04-10       Impact factor: 49.962

5.  Cracking the egg: molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo.

Authors:  Alexei V Evsikov; Joel H Graber; J Michael Brockman; Ales Hampl; Andrea E Holbrook; Priyam Singh; John J Eppig; Davor Solter; Barbara B Knowles
Journal:  Genes Dev       Date:  2006-10-01       Impact factor: 11.361

6.  SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase.

Authors:  Wael Tadros; Aaron L Goldman; Tomas Babak; Fiona Menzies; Leah Vardy; Terry Orr-Weaver; Timothy R Hughes; J Timothy Westwood; Craig A Smibert; Howard D Lipshitz
Journal:  Dev Cell       Date:  2007-01       Impact factor: 12.270

7.  3' UTRs are the primary regulators of gene expression in the C. elegans germline.

Authors:  Christopher Merritt; Dominique Rasoloson; Darae Ko; Geraldine Seydoux
Journal:  Curr Biol       Date:  2008-09-25       Impact factor: 10.834

8.  Single-copy insertion of transgenes in Caenorhabditis elegans.

Authors:  Christian Frøkjaer-Jensen; M Wayne Davis; Christopher E Hopkins; Blake J Newman; Jason M Thummel; Søren-Peter Olesen; Morten Grunnet; Erik M Jorgensen
Journal:  Nat Genet       Date:  2008-10-26       Impact factor: 38.330

9.  Most Caenorhabditis elegans microRNAs are individually not essential for development or viability.

Authors:  Eric A Miska; Ezequiel Alvarez-Saavedra; Allison L Abbott; Nelson C Lau; Andrew B Hellman; Shannon M McGonagle; David P Bartel; Victor R Ambros; H Robert Horvitz
Journal:  PLoS Genet       Date:  2007-12       Impact factor: 5.917

Review 10.  Translational control by cytoplasmic polyadenylation in Xenopus oocytes.

Authors:  Helois E Radford; Hedda A Meijer; Cornelia H de Moor
Journal:  Biochim Biophys Acta       Date:  2008-02-14
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  33 in total

1.  In Vivo Interaction Proteomics in Caenorhabditis elegans Embryos Provides New Insights into P Granule Dynamics.

Authors:  Jia-Xuan Chen; Patricia G Cipriani; Desirea Mecenas; Jolanta Polanowska; Fabio Piano; Kristin C Gunsalus; Matthias Selbach
Journal:  Mol Cell Proteomics       Date:  2016-02-24       Impact factor: 5.911

2.  Contribution of transcription to animal early development.

Authors:  Jianbin Wang; Richard E Davis
Journal:  Transcription       Date:  2014

Review 3.  Competition between target sites of regulators shapes post-transcriptional gene regulation.

Authors:  Marvin Jens; Nikolaus Rajewsky
Journal:  Nat Rev Genet       Date:  2014-12-09       Impact factor: 53.242

4.  "Father knows best?".

Authors:  Ashley T Neff; Jianbin Wang; Richard E Davis
Journal:  EMBO J       Date:  2014-07-24       Impact factor: 11.598

5.  Paternal RNA contributions in the Caenorhabditis elegans zygote.

Authors:  Marlon Stoeckius; Dominic Grün; Nikolaus Rajewsky
Journal:  EMBO J       Date:  2014-06-03       Impact factor: 11.598

Review 6.  Fishing forward and reverse: Advances in zebrafish phenomics.

Authors:  Ricardo Fuentes; Joaquín Letelier; Benjamin Tajer; Leonardo E Valdivia; Mary C Mullins
Journal:  Mech Dev       Date:  2018-08-18       Impact factor: 1.882

7.  A Massively Parallel Reporter Assay of 3' UTR Sequences Identifies In Vivo Rules for mRNA Degradation.

Authors:  Michal Rabani; Lindsey Pieper; Guo-Liang Chew; Alexander F Schier
Journal:  Mol Cell       Date:  2017-12-07       Impact factor: 17.970

Review 8.  The Maternal-to-Zygotic Transition During Vertebrate Development: A Model for Reprogramming.

Authors:  Valeria Yartseva; Antonio J Giraldez
Journal:  Curr Top Dev Biol       Date:  2015-08-13       Impact factor: 4.897

Review 9.  Next-generation analysis of gene expression regulation--comparing the roles of synthesis and degradation.

Authors:  Joel McManus; Zhe Cheng; Christine Vogel
Journal:  Mol Biosyst       Date:  2015-10

10.  The transgenerational effects of heat stress in the nematode Caenorhabditis remanei are negative and rapidly eliminated under direct selection for increased stress resistance in larvae.

Authors:  Kristin L Sikkink; Catherine M Ituarte; Rose M Reynolds; William A Cresko; Patrick C Phillips
Journal:  Genomics       Date:  2014-10-02       Impact factor: 5.736

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