IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v9y2018i1d10.1038_s41467-018-04678-8.html
   My bibliography  Save this article

A novel atypical sperm centriole is functional during human fertilization

Author

Listed:
  • Emily L. Fishman

    (University of Toledo)

  • Kyoung Jo

    (University of Toledo)

  • Quynh P. H. Nguyen

    (University of Toronto)

  • Dong Kong

    (National Cancer Institute)

  • Rachel Royfman

    (University of Toledo)

  • Anthony R. Cekic

    (University of Toledo)

  • Sushil Khanal

    (University of Toledo)

  • Ann L. Miller

    (University of Michigan)

  • Calvin Simerly

    (University of Pittsburgh School of Medicine)

  • Gerald Schatten

    (University of Pittsburgh School of Medicine)

  • Jadranka Loncarek

    (National Cancer Institute)

  • Vito Mennella

    (University of Toronto)

  • Tomer Avidor-Reiss

    (University of Toledo)

Abstract

The inheritance of the centrosome during human fertilization remains mysterious. Here we show that the sperm centrosome contains, in addition to the known typical barrel-shaped centriole (the proximal centriole, PC), a surrounding matrix (pericentriolar material, PCM), and an atypical centriole (distal centriole, DC) composed of splayed microtubules surrounding previously undescribed rods of centriole luminal proteins. The sperm centrosome is remodeled by both reduction and enrichment of specific proteins and the formation of these rods during spermatogenesis. In vivo and in vitro investigations show that the flagellum-attached, atypical DC is capable of recruiting PCM, forming a daughter centriole, and localizing to the spindle pole during mitosis. Altogether, we show that the DC is compositionally and structurally remodeled into an atypical centriole, which functions as the zygote’s second centriole. These findings now provide novel avenues for diagnostics and therapeutic strategies for male infertility, and insights into early embryo developmental defects.

Suggested Citation

  • Emily L. Fishman & Kyoung Jo & Quynh P. H. Nguyen & Dong Kong & Rachel Royfman & Anthony R. Cekic & Sushil Khanal & Ann L. Miller & Calvin Simerly & Gerald Schatten & Jadranka Loncarek & Vito Mennella, 2018. "A novel atypical sperm centriole is functional during human fertilization," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-04678-8
    DOI: 10.1038/s41467-018-04678-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-018-04678-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-018-04678-8?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
    ---><---

    Citations

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


    Cited by:

    1. Xueguang Zhang & Gelin Huang & Ting Jiang & Lanlan Meng & Tongtong Li & Guohui Zhang & Nan Wu & Xinyi Chen & Bingwang Zhao & Nana Li & Sixian Wu & Junceng Guo & Rui Zheng & Zhiliang Ji & Zhigang Xu & , 2024. "CEP112 coordinates translational regulation of essential fertility genes during spermiogenesis through phase separation in humans and mice," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Sushil Khanal & Ankit Jaiswal & Rajanikanth Chowdanayaka & Nahshon Puente & Katerina Turner & Kebron Yeshitela Assefa & Mohamad Nawras & Ezekiel David Back & Abigail Royfman & James P. Burkett & Soon , 2024. "The evolution of centriole degradation in mouse sperm," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    3. Yuki Ono & Hiromitsu Shirasawa & Kazumasa Takahashi & Mayumi Goto & Takahiro Ono & Taichi Sakaguchi & Motonari Okabe & Takeo Hirakawa & Takuya Iwasawa & Akiko Fujishima & Tae Sugawara & Kenichi Makino, 2024. "Shape of the first mitotic spindles impacts multinucleation in human embryos," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Volodymyr Porokh & Drahomíra Kyjovská & Martina Martonová & Tereza Klenková & Pavel Otevřel & Soňa Kloudová & Zuzana Holubcová, 2024. "Zygotic spindle orientation defines cleavage pattern and nuclear status of human embryos," Nature Communications, Nature, vol. 15(1), pages 1-9, 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:9:y:2018:i:1:d:10.1038_s41467-018-04678-8. 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.

    We have no bibliographic references for this item. You can help adding them by using 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.