Literature DB >> 23663777

Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos.

Lan Jiang1, Jing Zhang, Jing-Jing Wang, Lu Wang, Li Zhang, Guoqiang Li, Xiaodan Yang, Xin Ma, Xin Sun, Jun Cai, Jun Zhang, Xingxu Huang, Miao Yu, Xuegeng Wang, Feng Liu, Chung-I Wu, Chuan He, Bo Zhang, Weimin Ci, Jiang Liu.   

Abstract

5-methylcytosine is a major epigenetic modification that is sometimes called "the fifth nucleotide." However, our knowledge of how offspring inherit the DNA methylome from parents is limited. We generated nine single-base resolution DNA methylomes, including zebrafish gametes and early embryos. The oocyte methylome is significantly hypomethylated compared to sperm. Strikingly, the paternal DNA methylation pattern is maintained throughout early embryogenesis. The maternal DNA methylation pattern is maintained until the 16-cell stage. Then, the oocyte methylome is gradually discarded through cell division and is progressively reprogrammed to a pattern similar to that of the sperm methylome. The passive demethylation rate and the de novo methylation rate are similar in the maternal DNA. By the midblastula stage, the embryo's methylome is virtually identical to the sperm methylome. Moreover, inheritance of the sperm methylome facilitates the epigenetic regulation of embryogenesis. Therefore, besides DNA sequences, sperm DNA methylome is also inherited in zebrafish early embryos.
Copyright © 2013 Elsevier Inc. All rights reserved.

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Year:  2013        PMID: 23663777      PMCID: PMC4081501          DOI: 10.1016/j.cell.2013.04.041

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  45 in total

Review 1.  De novo DNA methylation: a germ cell perspective.

Authors:  Sébastien A Smallwood; Gavin Kelsey
Journal:  Trends Genet       Date:  2011-10-21       Impact factor: 11.639

Review 2.  Understanding transgenerational epigenetic inheritance via the gametes in mammals.

Authors:  Lucia Daxinger; Emma Whitelaw
Journal:  Nat Rev Genet       Date:  2012-01-31       Impact factor: 53.242

3.  Pull-down of 5-hydroxymethylcytosine DNA using JBP1-coated magnetic beads.

Authors:  Adam B Robertson; John Arne Dahl; Rune Ougland; Arne Klungland
Journal:  Nat Protoc       Date:  2012-01-26       Impact factor: 13.491

4.  Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos.

Authors:  Azusa Inoue; Yi Zhang
Journal:  Science       Date:  2011-09-22       Impact factor: 47.728

5.  Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates.

Authors:  Antoine Molaro; Emily Hodges; Fang Fang; Qiang Song; W Richard McCombie; Gregory J Hannon; Andrew D Smith
Journal:  Cell       Date:  2011-09-16       Impact factor: 41.582

6.  Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine.

Authors:  Khursheed Iqbal; Seung-Gi Jin; Gerd P Pfeifer; Piroska E Szabó
Journal:  Proc Natl Acad Sci U S A       Date:  2011-02-14       Impact factor: 11.205

7.  The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes.

Authors:  Tian-Peng Gu; Fan Guo; Hui Yang; Hai-Ping Wu; Gui-Fang Xu; Wei Liu; Zhi-Guo Xie; Linyu Shi; Xinyi He; Seung-gi Jin; Khursheed Iqbal; Yujiang Geno Shi; Zixin Deng; Piroska E Szabó; Gerd P Pfeifer; Jinsong Li; Guo-Liang Xu
Journal:  Nature       Date:  2011-09-04       Impact factor: 49.962

8.  Developmentally regulated piRNA clusters implicate MILI in transposon control.

Authors:  Alexei A Aravin; Ravi Sachidanandam; Angelique Girard; Katalin Fejes-Toth; Gregory J Hannon
Journal:  Science       Date:  2007-04-19       Impact factor: 47.728

9.  A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish.

Authors:  Saskia Houwing; Leonie M Kamminga; Eugene Berezikov; Daniela Cronembold; Angélique Girard; Hans van den Elst; Dmitri V Filippov; Heiko Blaser; Erez Raz; Cecilia B Moens; Ronald H A Plasterk; Gregory J Hannon; Bruce W Draper; René F Ketting
Journal:  Cell       Date:  2007-04-06       Impact factor: 41.582

10.  Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications.

Authors:  Felix Krueger; Simon R Andrews
Journal:  Bioinformatics       Date:  2011-04-14       Impact factor: 6.937

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  145 in total

1.  Presence of the Paternal Pronucleus Assists Embryo in Overcoming Cycloheximide Induced Abnormalities in Zygotic Mitosis.

Authors:  Michael A Ortega; Myungjun Ko; Joel Marh; Ariel Finberg; Marissa Oshiro; W Steven Ward
Journal:  J Cell Biochem       Date:  2016-01-21       Impact factor: 4.429

Review 2.  Zygotic genome activation during the maternal-to-zygotic transition.

Authors:  Miler T Lee; Ashley R Bonneau; Antonio J Giraldez
Journal:  Annu Rev Cell Dev Biol       Date:  2014-08-11       Impact factor: 13.827

3.  Development: Zebrafish early methylomes.

Authors:  Hannah Stower
Journal:  Nat Rev Genet       Date:  2013-05-29       Impact factor: 53.242

4.  Lessons from zebrafish on reprogramming the epigenetic code after fertilisation.

Authors:  Chris O'Neill
Journal:  Asian J Androl       Date:  2013-07-15       Impact factor: 3.285

Review 5.  The Epigenetic Consequences of Paternal Exposure to Environmental Contaminants and Reproductive Toxicants.

Authors:  Molly S Estill; Stephen A Krawetz
Journal:  Curr Environ Health Rep       Date:  2016-09

Review 6.  Epigenetic regulation of germ cells-remember or forget?

Authors:  Lijuan Feng; Xin Chen
Journal:  Curr Opin Genet Dev       Date:  2015-05-01       Impact factor: 5.578

Review 7.  Mechanisms regulating zygotic genome activation.

Authors:  Katharine N Schulz; Melissa M Harrison
Journal:  Nat Rev Genet       Date:  2019-04       Impact factor: 53.242

Review 8.  DNA Methylation in Basal Metazoans: Insights from Ctenophores.

Authors:  Emily C Dabe; Rachel S Sanford; Andrea B Kohn; Yelena Bobkova; Leonid L Moroz
Journal:  Integr Comp Biol       Date:  2015-07-14       Impact factor: 3.326

9.  Transcriptomic Changes in Zebrafish Embryos and Larvae Following Benzo[a]pyrene Exposure.

Authors:  Xiefan Fang; Jone Corrales; Cammi Thornton; Tracy Clerk; Brian E Scheffler; Kristine L Willett
Journal:  Toxicol Sci       Date:  2015-05-21       Impact factor: 4.849

10.  Programming and inheritance of parental DNA methylomes in mammals.

Authors:  Lu Wang; Jun Zhang; Jialei Duan; Xinxing Gao; Wei Zhu; Xingyu Lu; Lu Yang; Jing Zhang; Guoqiang Li; Weimin Ci; Wei Li; Qi Zhou; Neel Aluru; Fuchou Tang; Chuan He; Xingxu Huang; Jiang Liu
Journal:  Cell       Date:  2014-05-08       Impact factor: 41.582

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