IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-27172-0.html
   My bibliography  Save this article

Cell-fate transition and determination analysis of mouse male germ cells throughout development

Author

Listed:
  • Jiexiang Zhao

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Ping Lu

    (Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking University
    Biomedical Pioneering Innovation Center, Ministry of Education Key Laboratory of Cell Proliferation and Differentiation)

  • Cong Wan

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Yaping Huang

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Manman Cui

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Xinyan Yang

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Yuqiong Hu

    (Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking University
    Biomedical Pioneering Innovation Center, Ministry of Education Key Laboratory of Cell Proliferation and Differentiation)

  • Yi Zheng

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Ji Dong

    (Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking University
    Biomedical Pioneering Innovation Center, Ministry of Education Key Laboratory of Cell Proliferation and Differentiation)

  • Mei Wang

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Shu Zhang

    (Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking University
    Biomedical Pioneering Innovation Center, Ministry of Education Key Laboratory of Cell Proliferation and Differentiation)

  • Zhaoting Liu

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Shuhui Bian

    (Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking University
    Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University)

  • Xiaoman Wang

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Rui Wang

    (Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking University
    Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University)

  • Shaofang Ren

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Dazhuang Wang

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Zhaokai Yao

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University)

  • Gang Chang

    (Shenzhen University Health Science Center)

  • Fuchou Tang

    (Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking University
    Biomedical Pioneering Innovation Center, Ministry of Education Key Laboratory of Cell Proliferation and Differentiation
    Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University)

  • Xiao-Yang Zhao

    (State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University
    Guangdong Key Laboratory of Construction and Detection in Tissue Engineering, Southern Medical University
    Guangzhou Regenerative Medicine and Health Guangdong Laboratory (GRMH-GDL))

Abstract

Mammalian male germ cell development is a stepwise cell-fate transition process; however, the full-term developmental profile of male germ cells remains undefined. Here, by interrogating the high-precision transcriptome atlas of 11,598 cells covering 28 critical time-points, we demonstrate that cell-fate transition from mitotic to post-mitotic primordial germ cells is accompanied by transcriptome-scale reconfiguration and a transitional cell state. Notch signaling pathway is essential for initiating mitotic arrest and the maintenance of male germ cells’ identities. Ablation of HELQ induces developmental arrest and abnormal transcriptome reprogramming of male germ cells, indicating the importance of cell cycle regulation for proper cell-fate transition. Finally, systematic human-mouse comparison reveals potential regulators whose deficiency contributed to human male infertility via mitotic arrest regulation. Collectively, our study provides an accurate and comprehensive transcriptome atlas of the male germline cycle and allows for an in-depth understanding of the cell-fate transition and determination underlying male germ cell development.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27172-0
    DOI: 10.1038/s41467-021-27172-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-27172-0
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-27172-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Chen Chen & Wenjun Ouyang & Vadim Grigura & Qing Zhou & Kay Carnes & Hyunjung Lim & Guang-Quan Zhao & Silvia Arber & Natasza Kurpios & Theresa L. Murphy & Alec M. Cheng & John A. Hassell & Varadaraj C, 2005. "ERM is required for transcriptional control of the spermatogonial stem cell niche," Nature, Nature, vol. 436(7053), pages 1030-1034, August.
    2. Qi-Long Ying & Jason Wray & Jennifer Nichols & Laura Batlle-Morera & Bradley Doble & James Woodgett & Philip Cohen & Austin Smith, 2008. "The ground state of embryonic stem cell self-renewal," Nature, Nature, vol. 453(7194), pages 519-523, May.
    3. Takuya Sato & Kumiko Katagiri & Tetsuhiro Yokonishi & Yoshinobu Kubota & Kimiko Inoue & Narumi Ogonuki & Shogo Matoba & Atsuo Ogura & Takehiko Ogawa, 2011. "In vitro production of fertile sperm from murine spermatogonial stem cell lines," Nature Communications, Nature, vol. 2(1), pages 1-7, September.
    4. Yasuhide Ohinata & Bernhard Payer & Dónal O'Carroll & Katia Ancelin & Yukiko Ono & Mitsue Sano & Sheila C. Barton & Tetyana Obukhanych & Michel Nussenzweig & Alexander Tarakhovsky & Mitinori Saitou & , 2005. "Blimp1 is a critical determinant of the germ cell lineage in mice," Nature, Nature, vol. 436(7048), pages 207-213, July.
    5. Kei-ichi Takata & Shelley Reh & Junya Tomida & Maria D. Person & Richard D. Wood, 2013. "Human DNA helicase HELQ participates in DNA interstrand crosslink tolerance with ATR and RAD51 paralogs," Nature Communications, Nature, vol. 4(1), pages 1-11, December.
    6. Fumio Nakaki & Katsuhiko Hayashi & Hiroshi Ohta & Kazuki Kurimoto & Yukihiro Yabuta & Mitinori Saitou, 2013. "Induction of mouse germ-cell fate by transcription factors in vitro," Nature, Nature, vol. 501(7466), pages 222-226, September.
    7. 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.
    8. Carrie A. Adelman & Rafal L. Lolo & Nicolai J. Birkbak & Olga Murina & Kenichiro Matsuzaki & Zuzana Horejsi & Kalindi Parmar & Valérie Borel & J. Mark Skehel & Gordon Stamp & Alan D’Andrea & Alessandr, 2013. "HELQ promotes RAD51 paralogue-dependent repair to avert germ cell loss and tumorigenesis," Nature, Nature, vol. 502(7471), pages 381-384, October.
    9. Baolin Liu & Chenwei Li & Ziyi Li & Dongfang Wang & Xianwen Ren & Zemin Zhang, 2020. "An entropy-based metric for assessing the purity of single cell populations," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Shengyong Yu & Chunhua Zhou & Jiangping He & Zhaokai Yao & Xingnan Huang & Bowen Rong & Hong Zhu & Shijie Wang & Shuyan Chen & Xialian Wang & Baomei Cai & Guoqing Zhao & Yuhan Chen & Lizhan Xiao & He , 2022. "BMP4 drives primed to naïve transition through PGC-like state," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Jessica D. Tischler & Hiroshi Tsuchida & Rosevalentine Bosire & Tommy T. Oda & Ana Park & Richard O. Adeyemi, 2024. "FLIP(C1orf112)-FIGNL1 complex regulates RAD51 chromatin association to promote viability after replication stress," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Miguel Angel Brieño-Enríquez & Mariela Faykoo-Martinez & Meagan Goben & Jennifer K. Grenier & Ashley McGrath & Alexandra M. Prado & Jacob Sinopoli & Kate Wagner & Patrick T. Walsh & Samia H. Lopa & Di, 2023. "Postnatal oogenesis leads to an exceptionally large ovarian reserve in naked mole-rats," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. J. A. Kamp & B. B. L. G. Lemmens & R. J. Romeijn & S. C. Changoer & R. Schendel & M. Tijsterman, 2021. "Helicase Q promotes homology-driven DNA double-strand break repair and prevents tandem duplications," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    5. Yanchuan Li & Huamei Li & Cheng Peng & Ge Meng & Yijun Lu & Honglin Liu & Li Cui & Huan Zhou & Zhu Xu & Lingyun Sun & Lihong Liu & Qing Xiong & Beicheng Sun & Shiping Jiao, 2024. "Unraveling the spatial organization and development of human thymocytes through integration of spatial transcriptomics and single-cell multi-omics profiling," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    6. Sina Schumacher & Max Fernkorn & Michelle Marten & Rui Chen & Yung Su Kim & Ivan Bedzhov & Christian Schröter, 2024. "Tissue-intrinsic beta-catenin signals antagonize Nodal-driven anterior visceral endoderm differentiation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Shiran Bar & Dan Vershkov & Gal Keshet & Elyad Lezmi & Naama Meller & Atilgan Yilmaz & Ofra Yanuka & Malka Nissim-Rafinia & Eran Meshorer & Talia Eldar-Geva & Nissim Benvenisty, 2021. "Identifying regulators of parental imprinting by CRISPR/Cas9 screening in haploid human embryonic stem cells," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    8. 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.
    9. Iqra Saani & Nitish Raj & Raja Sood & Shahbaz Ansari & Haider Abbas Mandviwala & Elisabet Sanchez & Stergios Boussios, 2023. "Clinical Challenges in the Management of Malignant Ovarian Germ Cell Tumours," IJERPH, MDPI, vol. 20(12), pages 1-16, June.
    10. Sean West & Sushil Kumar & Surinder K Batra & Hesham Ali & Dario Ghersi, 2019. "Uncovering and characterizing splice variants associated with survival in lung cancer patients," PLOS Computational Biology, Public Library of Science, vol. 15(10), pages 1-16, October.
    11. Yan Wang & Binbin Ma & Xiaoxu Liu & Ge Gao & Zhuanzhuan Che & Menghan Fan & Siyan Meng & Xiru Zhao & Rio Sugimura & Hua Cao & Zhongjun Zhou & Jing Xie & Chengqi Lin & Zhuojuan Luo, 2022. "ZFP281-BRCA2 prevents R-loop accumulation during DNA replication," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    12. David R. Ghasemi & Konstantin Okonechnikov & Anne Rademacher & Stephan Tirier & Kendra K. Maass & Hanna Schumacher & Piyush Joshi & Maxwell P. Gold & Julia Sundheimer & Britta Statz & Ahmet S. Rifaiog, 2024. "Compartments in medulloblastoma with extensive nodularity are connected through differentiation along the granular precursor lineage," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    13. Andrew Keniry & Natasha Jansz & Linden J. Gearing & Iromi Wanigasuriya & Joseph Chen & Christian M. Nefzger & Peter F. Hickey & Quentin Gouil & Joy Liu & Kelsey A. Breslin & Megan Iminitoff & Tamara B, 2022. "BAF complex-mediated chromatin relaxation is required for establishment of X chromosome inactivation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. F. Nadalin & M. J. Marzi & M. Pirra Piscazzi & P. Fuentes-Bravo & S. Procaccia & M. Climent & P. Bonetti & C. Rubolino & B. Giuliani & I. Papatheodorou & J. C. Marioni & F. Nicassio, 2024. "Multi-omic lineage tracing predicts the transcriptional, epigenetic and genetic determinants of cancer evolution," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    15. 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.
    16. 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.
    17. Le Tran Phuc Khoa & Wentao Yang & Mengrou Shan & Li Zhang & Fengbiao Mao & Bo Zhou & Qiang Li & Rebecca Malcore & Clair Harris & Lili Zhao & Rajesh C. Rao & Shigeki Iwase & Sundeep Kalantry & Stephani, 2024. "Quiescence enables unrestricted cell fate in naive embryonic stem cells," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    18. Lihu Gong & Xiuli Liu & Lianying Jiao & Xin Yang & Andrew Lemoff & Xin Liu, 2022. "CK2-mediated phosphorylation of SUZ12 promotes PRC2 function by stabilizing enzyme active site," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    19. 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.
    20. Gintautas Vainorius & Maria Novatchkova & Georg Michlits & Juliane Christina Baar & Cecilia Raupach & Joonsun Lee & Ramesh Yelagandula & Marius Wernig & Ulrich Elling, 2023. "Ascl1 and Ngn2 convert mouse embryonic stem cells to neurons via functionally distinct paths," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27172-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.