Home LiteratureArticle Details
PMID: 22894908 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Genome wide identification of promoter binding sites for H4K12ac in human sperm and its relevance for early embryonic development.

Epigenetics ·Vol. 7 ·No. 9 ·2012-09-00 ·Pages 1057-70

Paradowska AS, Miller D, Spiess AN, Vieweg M, Cerna M, Dvorakova-Hortova K, Bartkuhn M, Schuppe HC, Weidner W, Steger K

Abstract

Sperm chromatin reveals two characteristic features in that protamines are the predominant nuclear proteins and remaining histones are highly acetylated. Histone H4 acetylated at lysine 12 (H4K12ac) is localized in the post-acrosomal region, while protamine-1 is present within the whole nucleus. Chromatin immunoprecipitation in combination with promoter array analysis allowed genome-wide identification of H4K12ac binding sites. Previously, we reported enrichment of H4K12ac at CTCF binding sites and promoters of genes involved in developmental processes. Here, we demonstrate that H4K12ac is enriched predominantly between ± 2 kb from the transcription start site. In addition, we identified developmentally relevant H4K12ac-associated promoters with high expression levels of their transcripts stored in mature sperm. The highest expressed mRNA codes for testis-specific PHD finger protein-7 (PHF7), suggesting an activating role of H4K12ac in the regulatory elements of this gene. H4K12ac-associated genes revealed a weak correlation with genes expressed at 4-cell stage human embryos, while 23 H4K12ac-associated genes were activated in 8-cell embryo and 39 in the blastocyst. Genes activated in 4-cell embryos are involved in gene expression, histone fold and DNA-dependent transcription, while genes expressed in the blastocyst were classified as involved in developmental processes. Immunofluorescence staining detected H4K12ac from the murine male pronucleus to early stages of embryogenesis. Aberrant histone acetylation within developmentally important gene promoters in infertile men may reflect insufficient sperm chromatin compaction, which may result in inappropriate transfer of epigenetic information to the oocyte.

MeSH Terms
Acetylation Animals Binding Sites Blastocyst/metabolism Chromatin/genetics,metabolism Embryonic Development/genetics Epigenesis, Genetic Female Gene Expression Regulation, Developmental Genes, Developmental Genome, Human Histones/metabolism Humans Male Membrane Proteins/genetics,metabolism Mice Mice, Inbred C57BL Promoter Regions, Genetic Protein Processing, Post-Translational RNA, Messenger/biosynthesis Spermatozoa/metabolism Transcription Factors/genetics,metabolism
Chemicals
Chromatin Histones Membrane Proteins PHF7 protein, human RNA, Messenger Transcription Factors
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Paradowska Agnieszka S
Department of Urology, Pediatric Urology and Andrology, Justus Liebig University of Giessen, Giessen, Germany. [email protected]
Miller David
Spiess Andrej-Nikolai
Vieweg Markus
Cerna Martina
Dvorakova-Hortova Katerina
Bartkuhn Marek
Schuppe Hans-Christian
Weidner Wolfgang
Steger Klaus
References (30)
30 references, click to expand
  1. Chromatin remodelling and epigenetic features of germ cells.
    Nature. 2005 Mar 31;434(7033):583-9 PMID: 15800613
  2. Human sperm chromatin stabilization: a proposed model including zinc bridges.
    Mol Hum Reprod. 2010 Jan;16(1):23-9 PMID: 19933313
  3. The role of sperm proteasomes during sperm aster formation and early zygote development: implications for fertilization failure in humans.
    Hum Reprod. 2008 Mar;23(3):573-80 PMID: 18089554
  4. A suite of novel human spermatozoal RNAs.
    J Androl. 2005 Jan-Feb;26(1):70-4 PMID: 15611569
  5. The many faces of histone lysine methylation.
    Curr Opin Cell Biol. 2002 Jun;14(3):286-98 PMID: 12067650
  6. Presence of histone H3 acetylated at lysine 9 in male germ cells and its distribution pattern in the genome of human spermatozoa.
    Reprod Fertil Dev. 2011;23(8):997-1011 PMID: 22127005
  7. Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs.
    Hum Mol Genet. 2007 Apr 1;16(7):763-73 PMID: 17327269
  8. Sperm-derived histones contribute to zygotic chromatin in humans.
    BMC Dev Biol. 2008 Mar 31;8:34 PMID: 18377649
  9. Analyzing ChIP-chip data using bioconductor.
    PLoS Comput Biol. 2008 Nov;4(11):e1000227 PMID: 19043553
  10. A possible role for sperm RNA in early embryo development.
    Theriogenology. 2007 Sep 1;68 Suppl 1:S147-55 PMID: 17583784
  11. Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences.
    Genome Res. 2009 Aug;19(8):1338-49 PMID: 19584098
  12. Distinct but overlapping roles of histone acetylase PCAF and of the closely related PCAF-B/GCN5 in mouse embryogenesis.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11303-6 PMID: 11027331
  13. Paternal effects on early embryogenesis.
    J Exp Clin Assist Reprod. 2008 May 16;5:2 PMID: 18485208
  14. The human sperm epigenome and its potential role in embryonic development.
    Mol Hum Reprod. 2010 Jan;16(1):37-47 PMID: 19906823
  15. Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation.
    Genes Dev. 2001 Aug 15;15(16):2069-82 PMID: 11511539
  16. Transcriptome profiling of human pre-implantation development.
    PLoS One. 2009 Nov 16;4(11):e7844 PMID: 19924284
  17. Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin.
    Dev Biol. 2006 Oct 15;298(2):458-69 PMID: 16887113
  18. Dynamic reprogramming of DNA methylation in the early mouse embryo.
    Dev Biol. 2002 Jan 1;241(1):172-82 PMID: 11784103
  19. Infertility with defective spermiogenesis in mice lacking AF5q31, the target of chromosomal translocation in human infant leukemia.
    Mol Cell Biol. 2005 Aug;25(15):6834-45 PMID: 16024815
  20. Genome-wide analysis of Polycomb targets in Drosophila melanogaster.
    Nat Genet. 2006 Jun;38(6):700-5 PMID: 16732288
  21. Towards a better understanding of RNA carriage by ejaculate spermatozoa.
    Hum Reprod Update. 2006 Nov-Dec;12(6):757-67 PMID: 16882702
  22. Spermatozoal RNA profiles of normal fertile men.
    Lancet. 2002 Sep 7;360(9335):772-7 PMID: 12241836
  23. Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro fertilization.
    Biol Reprod. 2006 Sep;75(3):442-51 PMID: 16775225
  24. Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos.
    Development. 1997 Nov;124(22):4615-25 PMID: 9409678
  25. Distinctive chromatin in human sperm packages genes for embryo development.
    Nature. 2009 Jul 23;460(7254):473-8 PMID: 19525931
  26. Zinc-induced secondary structure transitions in human sperm protamines.
    J Biol Chem. 1990 Nov 25;265(33):20667-72 PMID: 2243113
  27. Integrating quantitative information from ChIP-chip experiments into motif finding.
    Biostatistics. 2008 Jan;9(1):51-65 PMID: 17533175
  28. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa.
    Nat Struct Mol Biol. 2010 Jun;17(6):679-87 PMID: 20473313
  29. Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote.
    Mech Dev. 2005 Sep;122(9):1008-22 PMID: 15922569
  30. The interaction of modified histones with the bromodomain testis-specific (BRDT) gene and its mRNA level in sperm of fertile donors and subfertile men.
    Reproduction. 2010 Sep;140(3):435-43 PMID: 20538714
Article Info
Journal
Epigenetics
Abbr.
Epigenetics
ISSN
1559-2308
Published
2012-09-00
Epub
2012-00-16
Pages
1057-70
Language
English
Region
United States
NLM ID
101265293
PMCID
PMC3466190
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BBS/B/04900 · United Kingdom
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]