Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa

被引:517
作者
Brykczynska, Urszula [1 ]
Hisano, Mizue [1 ]
Erkek, Serap [1 ]
Ramos, Liliana [2 ]
Oakeley, Edward J. [1 ]
Roloff, Tim C. [1 ]
Beisel, Christian [3 ]
Schuebeler, Dirk [1 ]
Stadler, Michael B. [1 ]
Peters, Antoine H. F. M. [1 ]
机构
[1] Friedrich Miescher Inst Biomed Res, Basel, Switzerland
[2] Radboud Univ Nijmegen, Med Ctr, Dept Obstet & Gynaecol, Fertil Lab, NL-6525 ED Nijmegen, Netherlands
[3] Swiss Fed Inst Technol, Dept Biosyst Sci & Engn, Basel, Switzerland
基金
日本学术振兴会; 瑞士国家科学基金会;
关键词
EMBRYONIC STEM-CELLS; ZYGOTIC GENE ACTIVATION; SPERM CHROMATIN; TRANSCRIPTIONAL REPRESSION; LYSINE-27; METHYLATION; EPIGENETIC MEMORY; DNA METHYLATION; MALE GERMLINE; GENOME; FATE;
D O I
10.1038/nsmb.1821
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
In higher eukaryotes, histone methylation is involved in maintaining cellular identity during somatic development. As most nucleosomes are replaced by protamines during spermatogenesis, it is unclear whether histone modifications function in paternal transmission of epigenetic information. Here we show that two modifications important for Trithorax-and Polycomb-mediated gene regulation have methylation-specific distributions at regulatory regions in human spermatozoa. Histone H3 Lys4 dimethylation (H3K4me2) marks genes that are relevant in spermatogenesis and cellular homeostasis. In contrast, histone H3 Lys27 trimethylation (H3K27me3) marks developmental regulators in sperm, as in somatic cells. However, nucleosomes are only moderately retained at regulatory regions in human sperm. Nonetheless, genes with extensive H3K27me3 coverage around transcriptional start sites in particular tend not to be expressed during male and female gametogenesis or in preimplantation embryos. Promoters of orthologous genes are similarly modified in mouse spermatozoa. These data are compatible with a role for Polycomb in repressing somatic determinants across generations, potentially in a variegating manner.
引用
收藏
页码:679 / U47
页数:10
相关论文
共 60 条
[21]   Distinctive chromatin in human sperm packages genes for embryo development [J].
Hammoud, Saher Sue ;
Nix, David A. ;
Zhang, Haiying ;
Purwar, Jahnvi ;
Carrell, Douglas T. ;
Cairns, Bradley R. .
NATURE, 2009, 460 (7254) :473-U47
[22]   A model for transmission of the H3K27me3 epigenetic mark [J].
Hansen, Klaus H. ;
Bracken, Adrian P. ;
Pasini, Diego ;
Dietrich, Nikolaj ;
Gehani, Simmi S. ;
Monrad, Astrid ;
Rappsilber, Juri ;
Lerdrup, Mads ;
Helin, Kristian .
NATURE CELL BIOLOGY, 2008, 10 (11) :1291-U89
[23]   Mechanisms of disease: Nuclear transplantation, embryonic stem cells, and the potential for cell therapy [J].
Hochedlinger, K ;
Jaenisch, R .
NEW ENGLAND JOURNAL OF MEDICINE, 2003, 349 (03) :275-286
[24]   Mechanisms of transcriptional repression by histone lysine methylation [J].
Hublitz, Philip ;
Albert, Mareike ;
Peters, Antoine H. F. M. .
INTERNATIONAL JOURNAL OF DEVELOPMENTAL BIOLOGY, 2009, 53 (2-3) :335-354
[25]   Transcriptional repression and DNA hypermethylation of a small set of ES cell marker genes in male germline stem cells [J].
Imamura, Masanori ;
Miura, Kyoko ;
Iwabuchi, Kumiko ;
Ichisaka, Tomoko ;
Nakagawa, Masato ;
Lee, Jiyoung ;
Kanatsu-Shinohara, Mito ;
Shinohara, Takashi ;
Yamanaka, Shinya .
BMC DEVELOPMENTAL BIOLOGY, 2006, 6
[26]   Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting [J].
Kaneda, M ;
Okano, M ;
Hata, K ;
Sado, T ;
Tsujimoto, N ;
Li, E ;
Sasaki, H .
NATURE, 2004, 429 (6994) :900-903
[27]   A C. elegans LSD1 Demethylase Contributes to Germline Immortality by Reprogramming Epigenetic Memory [J].
Katz, David J. ;
Edwards, T. Matthew ;
Reinke, Valerie ;
Kelly, William G. .
CELL, 2009, 137 (02) :308-320
[28]   High-frequency generation of viable mice from engineered bi-maternal embryos [J].
Kawahara, Manabu ;
Wu, Qiong ;
Takahashi, Nozomi ;
Morita, Shinnosuke ;
Yamada, Kaori ;
Ito, Mitsuteru ;
Ferguson-Smith, Anne C. ;
Kono, Tomohiro .
NATURE BIOTECHNOLOGY, 2007, 25 (09) :1045-1050
[29]   Genomewide Analysis of PRC1 and PRC2 Occupancy Identifies Two Classes of Bivalent Domains [J].
Ku, Manching ;
Koche, Richard P. ;
Rheinbay, Esther ;
Mendenhall, Eric M. ;
Endoh, Mitsuhiro ;
Mikkelsen, Tarjei S. ;
Presser, Aviva ;
Nusbaum, Chad ;
Xie, Xiaohui ;
Chi, Andrew S. ;
Adli, Mazhar ;
Kasif, Simon ;
Ptaszek, Leon M. ;
Cowan, Chad A. ;
Lander, Eric S. ;
Koseki, Haruhiko ;
Bernstein, Bradley E. .
PLOS GENETICS, 2008, 4 (10)
[30]   Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein [J].
Kuzmichev, A ;
Nishioka, K ;
Erdjument-Bromage, H ;
Tempst, P ;
Reinberg, D .
GENES & DEVELOPMENT, 2002, 16 (22) :2893-2905