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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
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    Cited by:

    1. 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.
    2. 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.
    3. 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.

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