Literature DB >> 23978535

Cytoplasmic polyadenylation is a major mRNA regulator during oogenesis and egg activation in Drosophila.

Jun Cui1, Caroline V Sartain, Jeffrey A Pleiss, Mariana F Wolfner.   

Abstract

The GLD-2 class of poly(A) polymerases regulate the timing of translation of stored transcripts by elongating the poly(A) tails of target mRNAs in the cytoplasm. WISPY is a GLD-2 enzyme that acts in the Drosophila female germline and is required for the completion of the egg-to-embryo transition. Though a handful of WISPY target mRNAs have been identified during both oogenesis and early embryogenesis, it was unknown whether WISP simply regulated a small pool of patterning or cell cycle genes, or whether, instead, cytoplasmic polyadenylation was widespread during this developmental transition. To identify the full range of WISPY targets, we carried out microarray analysis to look for maternal mRNAs whose poly(A) tails fail to elongate in the absence of WISP function. We examined the polyadenylated portion of the maternal transcriptome in both stage 14 (mature) oocytes and in early embryos that had completed egg activation. Our analysis shows that the poly(A) tails of thousands of maternal mRNAs fail to elongate in wisp-deficient oocytes and embryos. Furthermore, we have identified specific classes of genes that are highly regulated in this manner at each stage. Our study shows that cytoplasmic polyadenylation is a major regulatory mechanism during oocyte maturation and egg activation.
© 2013 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Cytoplasmic polyadenylation; Egg activation; Egg-to-embryo transition; GLD2 family poly(A) polymerase; Oocyte maturation

Mesh:

Substances:

Year:  2013        PMID: 23978535      PMCID: PMC3821703          DOI: 10.1016/j.ydbio.2013.08.013

Source DB:  PubMed          Journal:  Dev Biol        ISSN: 0012-1606            Impact factor:   3.582


  47 in total

1.  Translational control of cyclin B1 mRNA during meiotic maturation: coordinated repression and cytoplasmic polyadenylation.

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Journal:  Dev Biol       Date:  2000-04-01       Impact factor: 3.582

2.  Analysis of poly(A) tail lengths by PCR: the PAT assay.

Authors:  F J Sallés; S Strickland
Journal:  Methods Mol Biol       Date:  1999

3.  Identification of a novel isoform of poly(A) polymerase, TPAP, specifically present in the cytoplasm of spermatogenic cells.

Authors:  S Kashiwabara; T Zhuang; K Yamagata; J Noguchi; A Fukamizu; T Baba
Journal:  Dev Biol       Date:  2000-12-01       Impact factor: 3.582

4.  Zinc requirement during meiosis I-meiosis II transition in mouse oocytes is independent of the MOS-MAPK pathway.

Authors:  Miranda L Bernhardt; Alison M Kim; Thomas V O'Halloran; Teresa K Woodruff
Journal:  Biol Reprod       Date:  2010-11-10       Impact factor: 4.285

5.  Mitotic cell-cycle progression is regulated by CPEB1 and CPEB4-dependent translational control.

Authors:  Isabel Novoa; Javier Gallego; Pedro G Ferreira; Raul Mendez
Journal:  Nat Cell Biol       Date:  2010-04-04       Impact factor: 28.824

6.  The hiiragi gene encodes a poly(A) polymerase, which controls the formation of the wing margin in Drosophila melanogaster.

Authors:  T Murata; H Nagaso; S Kashiwabara ; T Baba; H Okano; K K Yokoyama
Journal:  Dev Biol       Date:  2001-05-01       Impact factor: 3.582

7.  The poly(A) polymerase GLD2 is required for spermatogenesis in Drosophila melanogaster.

Authors:  Caroline V Sartain; Jun Cui; Richard P Meisel; Mariana F Wolfner
Journal:  Development       Date:  2011-04       Impact factor: 6.868

8.  GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program.

Authors:  Kyung Won Kim; Tracy L Wilson; Judith Kimble
Journal:  Proc Natl Acad Sci U S A       Date:  2010-09-20       Impact factor: 11.205

9.  Zinc sparks are triggered by fertilization and facilitate cell cycle resumption in mammalian eggs.

Authors:  Alison M Kim; Miranda L Bernhardt; Betty Y Kong; Richard W Ahn; Stefan Vogt; Teresa K Woodruff; Thomas V O'Halloran
Journal:  ACS Chem Biol       Date:  2011-04-28       Impact factor: 5.100

10.  Protein phosphorylation changes reveal new candidates in the regulation of egg activation and early embryogenesis in D. melanogaster.

Authors:  Amber R Krauchunas; Vanessa L Horner; Mariana F Wolfner
Journal:  Dev Biol       Date:  2012-07-31       Impact factor: 3.582

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  34 in total

1.  Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition.

Authors:  Iva Kronja; Zachary J Whitfield; Bingbing Yuan; Kristina Dzeyk; Joanna Kirkpatrick; Jeroen Krijgsveld; Terry L Orr-Weaver
Journal:  Proc Natl Acad Sci U S A       Date:  2014-10-27       Impact factor: 11.205

Review 2.  Translational Control during Developmental Transitions.

Authors:  Felipe Karam Teixeira; Ruth Lehmann
Journal:  Cold Spring Harb Perspect Biol       Date:  2019-06-03       Impact factor: 10.005

Review 3.  A tale of non-canonical tails: gene regulation by post-transcriptional RNA tailing.

Authors:  Sha Yu; V Narry Kim
Journal:  Nat Rev Mol Cell Biol       Date:  2020-06-01       Impact factor: 94.444

4.  mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos.

Authors:  Stephen W Eichhorn; Alexander O Subtelny; Iva Kronja; Jamie C Kwasnieski; Terry L Orr-Weaver; David P Bartel
Journal:  Elife       Date:  2016-07-30       Impact factor: 8.140

Review 5.  Subcellular Specialization and Organelle Behavior in Germ Cells.

Authors:  Yukiko M Yamashita
Journal:  Genetics       Date:  2018-01       Impact factor: 4.562

6.  Adenylation of maternally inherited microRNAs by Wispy.

Authors:  Mihye Lee; Yeon Choi; Kijun Kim; Hua Jin; Jaechul Lim; Tuan Anh Nguyen; Jihye Yang; Minsun Jeong; Antonio J Giraldez; Hui Yang; Dinshaw J Patel; V Narry Kim
Journal:  Mol Cell       Date:  2014-11-13       Impact factor: 17.970

7.  Structural basis for the activation of the C. elegans noncanonical cytoplasmic poly(A)-polymerase GLD-2 by GLD-3.

Authors:  Katharina Nakel; Fabien Bonneau; Christian R Eckmann; Elena Conti
Journal:  Proc Natl Acad Sci U S A       Date:  2015-06-29       Impact factor: 11.205

Review 8.  Post-transcriptional regulation of early embryogenesis.

Authors:  Timothy T Weil
Journal:  F1000Prime Rep       Date:  2015-03-03

9.  Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in Arabidopsis thaliana.

Authors:  Christian Kappel; Gerda Trost; Hjördis Czesnick; Anna Ramming; Benjamin Kolbe; Son Lang Vi; Cláudia Bispo; Jörg D Becker; Cornelia de Moor; Michael Lenhard
Journal:  PLoS Genet       Date:  2015-08-25       Impact factor: 5.917

10.  Single-cell RNA-Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation.

Authors:  Yuanlin He; Qiuzhen Chen; Juncheng Dai; Yiqiang Cui; Chi Zhang; Xidong Wen; Jiazhao Li; Yue Xiao; Xiaoxu Peng; Mingxi Liu; Bin Shen; Jiahao Sha; Zhibin Hu; Jing Li; Wenjie Shu
Journal:  Aging Cell       Date:  2021-06-26       Impact factor: 9.304

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