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Staged developmental mapping and X chromosome transcriptional dynamics during mouse spermatogenesis

Author

Listed:
  • Christina Ernst

    (European Bioinformatics Institute, (EMBL-EBI), Wellcome Genome Campus
    University of Cambridge, Cancer Research UK Cambridge Institute, Robinson Way)

  • Nils Eling

    (European Bioinformatics Institute, (EMBL-EBI), Wellcome Genome Campus
    University of Cambridge, Cancer Research UK Cambridge Institute, Robinson Way)

  • Celia P. Martinez-Jimenez

    (University of Cambridge, Cancer Research UK Cambridge Institute, Robinson Way
    Wellcome Sanger Institute, Welcome Genome Campus)

  • John C. Marioni

    (European Bioinformatics Institute, (EMBL-EBI), Wellcome Genome Campus
    University of Cambridge, Cancer Research UK Cambridge Institute, Robinson Way
    Wellcome Sanger Institute, Welcome Genome Campus)

  • Duncan T. Odom

    (University of Cambridge, Cancer Research UK Cambridge Institute, Robinson Way
    German Cancer Research Center (DKFZ), Division Signaling and Functional Genomics)

Abstract

Male gametes are generated through a specialised differentiation pathway involving a series of developmental transitions that are poorly characterised at the molecular level. Here, we use droplet-based single-cell RNA-Sequencing to profile spermatogenesis in adult animals and at multiple stages during juvenile development. By exploiting the first wave of spermatogenesis, we both precisely stage germ cell development and enrich for rare somatic cell-types and spermatogonia. To capture the full complexity of spermatogenesis including cells that have low transcriptional activity, we apply a statistical tool that identifies previously uncharacterised populations of leptotene and zygotene spermatocytes. Focusing on post-meiotic events, we characterise the temporal dynamics of X chromosome re-activation and profile the associated chromatin state using CUT&RUN. This identifies a set of genes strongly repressed by H3K9me3 in spermatocytes, which then undergo extensive chromatin remodelling post-meiosis, thus acquiring an active chromatin state and spermatid-specific expression.

Suggested Citation

  • Christina Ernst & Nils Eling & Celia P. Martinez-Jimenez & John C. Marioni & Duncan T. Odom, 2019. "Staged developmental mapping and X chromosome transcriptional dynamics during mouse spermatogenesis," Nature Communications, Nature, vol. 10(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09182-1
    DOI: 10.1038/s41467-019-09182-1
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    Cited by:

    1. Saori Yoshimura & Ryuki Shimada & Koji Kikuchi & Soichiro Kawagoe & Hironori Abe & Sakie Iisaka & Sayoko Fujimura & Kei-ichiro Yasunaga & Shingo Usuki & Naoki Tani & Takashi Ohba & Eiji Kondoh & Tomoh, 2024. "Atypical heat shock transcription factor HSF5 is critical for male meiotic prophase under non-stress conditions," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    2. Emily G. Kaye & Kavyashree Basavaraju & Geoffrey M. Nelson & Helena D. Zomer & Debarun Roy & Irene Infancy Joseph & Reza Rajabi-Toustani & Huanyu Qiao & Karen Adelman & Prabhakara P. Reddi, 2024. "RNA polymerase II pausing is essential during spermatogenesis for appropriate gene expression and completion of meiosis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Jasper Panten & Tobias Heinen & Christina Ernst & Nils Eling & Rebecca E. Wagner & Maja Satorius & John C. Marioni & Oliver Stegle & Duncan T. Odom, 2024. "The dynamic genetic determinants of increased transcriptional divergence in spermatids," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Hironori Abe & Yu-Han Yeh & Yasuhisa Munakata & Kei-Ichiro Ishiguro & Paul R. Andreassen & Satoshi H. Namekawa, 2022. "Active DNA damage response signaling initiates and maintains meiotic sex chromosome inactivation," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Shixuan Liu & Camille Ezran & Michael F. Z. Wang & Zhengda Li & Kyle Awayan & Jonathan Z. Long & Iwijn De Vlaminck & Sheng Wang & Jacques Epelbaum & Christin S. Kuo & Jérémy Terrien & Mark A. Krasnow , 2024. "An organism-wide atlas of hormonal signaling based on the mouse lemur single-cell transcriptome," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    6. Moïra Rossitto & Stephanie Déjardin & Chris M. Rands & Stephanie Gras & Roberta Migale & Mahmoud-Reza Rafiee & Yasmine Neirijnck & Alain Pruvost & Anvi Laetitia Nguyen & Guillaume Bossis & Florence Ca, 2022. "TRIM28-dependent SUMOylation protects the adult ovary from activation of the testicular pathway," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Shuwen He & John P. Gillies & Juliana L. Zang & Carmen M. Córdoba-Beldad & Io Yamamoto & Yasuhiro Fujiwara & Julie Grantham & Morgan E. DeSantis & Hiroki Shibuya, 2023. "Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Debashish U. Menon & Oleksandr Kirsanov & Christopher B. Geyer & Terry Magnuson, 2021. "Mammalian SWI/SNF chromatin remodeler is essential for reductional meiosis in males," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    9. Jiexiang Zhao & Ping Lu & Cong Wan & Yaping Huang & Manman Cui & Xinyan Yang & Yuqiong Hu & Yi Zheng & Ji Dong & Mei Wang & Shu Zhang & Zhaoting Liu & Shuhui Bian & Xiaoman Wang & Rui Wang & Shaofang , 2021. "Cell-fate transition and determination analysis of mouse male germ cells throughout development," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    10. Wu Zuo & Guangming Chen & Zhimei Gao & Shuai Li & Yanyan Chen & Chenhui Huang & Juan Chen & Zhengjun Chen & Ming Lei & Qian Bian, 2021. "Stage-resolved Hi-C analyses reveal meiotic chromosome organizational features influencing homolog alignment," Nature Communications, Nature, vol. 12(1), pages 1-20, December.

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