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Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L

Author

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  • Déborah Bourc'his

    (College of Physicians and Surgeons of Columbia University)

  • Timothy H. Bestor

    (College of Physicians and Surgeons of Columbia University)

Abstract

Mammalian genomes employ heritable cytosine methylation in the long-term silencing of retrotransposons and genes subject to genomic imprinting and X chromosome inactivation. Little is known of the mechanisms that direct cytosine methylation to specific sequences. Here we show that DNA methyltransferase 3-like (Dnmt3L (ref. 1)) is expressed in testes during a brief perinatal period in the non-dividing precursors of spermatogonial stem cells at a stage where retrotransposons undergo de novo methylation. Deletion of the Dnmt3L gene prevented the de novo methylation of both long-terminal-repeat (LTR) and non-LTR retrotransposons, which were transcribed at high levels in spermatogonia and spermatocytes. Loss of Dnmt3L from early germ cells also caused meiotic failure in spermatocytes, which do not express Dnmt3L. Whereas dispersed repeated sequences were demethylated in mutant germ cells, tandem repeats in pericentric regions were methylated normally. This result indicates that the Dnmt3L protein might have a function in the de novo methylation of dispersed repeated sequences in a premeiotic genome scanning process that occurs in male germ cells at about the time of birth.

Suggested Citation

  • Déborah Bourc'his & Timothy H. Bestor, 2004. "Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L," Nature, Nature, vol. 431(7004), pages 96-99, September.
  • Handle: RePEc:nat:nature:v:431:y:2004:i:7004:d:10.1038_nature02886
    DOI: 10.1038/nature02886
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    Cited by:

    1. Ahmad Luqman-Fatah & Yuzo Watanabe & Kazuko Uno & Fuyuki Ishikawa & John V. Moran & Tomoichiro Miyoshi, 2023. "The interferon stimulated gene-encoded protein HELZ2 inhibits human LINE-1 retrotransposition and LINE-1 RNA-mediated type I interferon induction," Nature Communications, Nature, vol. 14(1), pages 1-26, December.
    2. Linfeng Gao & Yiran Guo & Mahamaya Biswal & Jiuwei Lu & Jiekai Yin & Jian Fang & Xinyi Chen & Zengyu Shao & Mengjiang Huang & Yinsheng Wang & Gang Greg Wang & Jikui Song, 2022. "Structure of DNMT3B homo-oligomer reveals vulnerability to impairment by ICF mutations," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Ariane Lismer & Sarah Kimmins, 2023. "Emerging evidence that the mammalian sperm epigenome serves as a template for embryo development," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    4. Zhengyi Zhen & Yu Chen & Haiyan Wang & Huanyin Tang & Haiping Zhang & Haipeng Liu & Ying Jiang & Zhiyong Mao, 2023. "Nuclear cGAS restricts L1 retrotransposition by promoting TRIM41-mediated ORF2p ubiquitination and degradation," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Jiuwei Lu & Yiran Guo & Jiekai Yin & Jianbin Chen & Yinsheng Wang & Gang Greg Wang & Jikui Song, 2024. "Structure-guided functional suppression of AML-associated DNMT3A hotspot mutations," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Julia Arand & David Spieler & Tommy Karius & Miguel R Branco & Daniela Meilinger & Alexander Meissner & Thomas Jenuwein & Guoliang Xu & Heinrich Leonhardt & Verena Wolf & Jörn Walter, 2012. "In Vivo Control of CpG and Non-CpG DNA Methylation by DNA Methyltransferases," PLOS Genetics, Public Library of Science, vol. 8(6), pages 1-11, June.
    7. Patricia Gerdes & Sue Mei Lim & Adam D. Ewing & Michael R. Larcombe & Dorothy Chan & Francisco J. Sanchez-Luque & Lucinda Walker & Alexander L. Carleton & Cini James & Anja S. Knaupp & Patricia E. Car, 2022. "Retrotransposon instability dominates the acquired mutation landscape of mouse induced pluripotent stem cells," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Shubha P. Kale & Lakisha Moore & Prescott L. Deininger & Astrid M. Roy-Engel, 2005. "Heavy Metals Stimulate Human LINE-1 Retrotransposition," IJERPH, MDPI, vol. 2(1), pages 1-10, April.
    9. Anthony V Furano & Charlie E Jones & Vipul Periwal & Kathryn E Callahan & Jean-Claude Walser & Pamela R Cook, 2020. "Cryptic genetic variation enhances primate L1 retrotransposon survival by enlarging the functional coiled coil sequence space of ORF1p," PLOS Genetics, Public Library of Science, vol. 16(8), pages 1-19, August.
    10. Pascal Giehr & Charalampos Kyriakopoulos & Gabriella Ficz & Verena Wolf & Jörn Walter, 2016. "The Influence of Hydroxylation on Maintaining CpG Methylation Patterns: A Hidden Markov Model Approach," PLOS Computational Biology, Public Library of Science, vol. 12(5), pages 1-16, May.

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