XB-ART-53997
Genome Res
August 1, 2016;
26
(8):
1034-46.
Sperm is epigenetically programmed to regulate gene transcription in embryos.
Teperek M
,
Simeone A
,
Gaggioli V
,
Miyamoto K
,
Allen GE
,
Erkek S
,
Kwon T
,
Marcotte EM
,
Zegerman P
,
Bradshaw CR
,
Peters AH
,
Gurdon JB
,
Jullien J
.
Abstract
For a long time, it has been assumed that the only role of
sperm at fertilization is to introduce the male genome into the
egg. Recently, ideas have emerged that the epigenetic state of the
sperm nucleus could influence transcription in the
embryo. However, conflicting reports have challenged the existence of epigenetic marks on
sperm genes, and there are no functional tests supporting the role of
sperm epigenetic marking on embryonic gene expression. Here, we show that
sperm is epigenetically programmed to regulate embryonic gene expression. By comparing the development of
sperm- and
spermatid-derived frog embryos, we show that the programming of
sperm for successful development relates to its ability to regulate transcription of a set of developmentally important genes. During
spermatid maturation into
sperm, these genes lose H3K4me2/3 and retain H3K27me3 marks. Experimental removal of these epigenetic marks at fertilization de-regulates gene expression in the resulting embryos in a paternal chromatin-dependent manner. This demonstrates that epigenetic instructions delivered by the
sperm at fertilization are required for correct regulation of gene expression in the future embryos. The epigenetic mechanisms of developmental programming revealed here are likely to relate to the mechanisms involved in transgenerational transmission of acquired traits. Understanding how parental experience can influence development of the progeny has broad potential for improving human health.
PubMed ID:
27034506
PMC ID:
PMC4971762
Article link:
Grant support:
[+]
Species referenced:
Xenopus laevis
Antibodies:
H3f3a Ab24
H3f3a Ab27
GEO Series:
GSE75164:
Xenbase,
NCBI
References [+] :
Brykczynska,
Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa.
2010,
Pubmed
Brykczynska,
Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa.
2010,
Pubmed
Bui,
Essential role of paternal chromatin in the regulation of transcriptional activity during mouse preimplantation development.
2010,
Pubmed
Carone,
High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm.
2014,
Pubmed
El-Khoury,
Assessing cellular and circulating miRNA recovery: the impact of the RNA isolation method and the quantity of input material.
2016,
Pubmed
Erkek,
Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa.
2013,
Pubmed
GURDON,
Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei.
1958,
Pubmed
,
Xenbase
Gaggioli,
DNA topoisomerase IIα controls replication origin cluster licensing and firing time in Xenopus egg extracts.
2013,
Pubmed
,
Xenbase
Gaucher,
From meiosis to postmeiotic events: the secrets of histone disappearance.
2010,
Pubmed
Gurdon,
Injected nuclei in frog oocytes: fate, enlargement, and chromatin dispersal.
1977,
Pubmed
,
Xenbase
Hammoud,
Distinctive chromatin in human sperm packages genes for embryo development.
2009,
Pubmed
Hisano,
Genome-wide chromatin analysis in mature mouse and human spermatozoa.
2013,
Pubmed
Hutchison,
DNA replication and cell cycle control in Xenopus egg extracts.
1990,
Pubmed
,
Xenbase
Ihara,
Paternal poly (ADP-ribose) metabolism modulates retention of inheritable sperm histones and early embryonic gene expression.
2014,
Pubmed
Kimura,
Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring.
1995,
Pubmed
Kishigami,
Similar time restriction for intracytoplasmic sperm injection and round spermatid injection into activated oocytes for efficient offspring production.
2004,
Pubmed
Labit,
A simple and optimized method of producing silanized surfaces for FISH and replication mapping on combed DNA fibers.
2009,
Pubmed
,
Xenbase
Lee,
Embryonic dorsal-ventral signaling: secreted frizzled-related proteins as inhibitors of tolloid proteinases.
2006,
Pubmed
,
Xenbase
Lemaitre,
Mitotic remodeling of the replicon and chromosome structure.
2005,
Pubmed
,
Xenbase
Narbonne,
Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
2011,
Pubmed
,
Xenbase
Paradowska,
Genome wide identification of promoter binding sites for H4K12ac in human sperm and its relevance for early embryonic development.
2012,
Pubmed
Risley,
H1 histone variants in Xenopus laevis.
1981,
Pubmed
,
Xenbase
Samans,
Uniformity of nucleosome preservation pattern in Mammalian sperm and its connection to repetitive DNA elements.
2014,
Pubmed
Siklenka,
Disruption of histone methylation in developing sperm impairs offspring health transgenerationally.
2015,
Pubmed
Smith,
Xenopus laevis transgenesis by sperm nuclear injection.
2007,
Pubmed
,
Xenbase
Suri,
Inhibition of mesodermal fate by Xenopus HNF3beta/FoxA2.
2003,
Pubmed
,
Xenbase
Suzuki,
Comparison of the RNA polymerase I-, II- and III-dependent transcript levels between nuclear transfer and in vitro fertilized embryos at the blastocyst stage.
2007,
Pubmed
Vassena,
Tough beginnings: alterations in the transcriptome of cloned embryos during the first two cell cycles.
2007,
Pubmed
Weidgang,
TBX3 Directs Cell-Fate Decision toward Mesendoderm.
2013,
Pubmed
,
Xenbase
Wu,
Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm.
2011,
Pubmed
Yasuoka,
Occupancy of tissue-specific cis-regulatory modules by Otx2 and TLE/Groucho for embryonic head specification.
2014,
Pubmed
,
Xenbase
Zheng,
rRNA genes are not fully activated in mouse somatic cell nuclear transfer embryos.
2012,
Pubmed
Ziyyat,
Differential gene expression in pre-implantation embryos from mouse oocytes injected with round spermatids or spermatozoa.
2001,
Pubmed