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The SUN1-SPDYA interaction plays an essential role in meiosis prophase I

Author

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  • Yanyan Chen

    (Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yan Wang

    (Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Juan Chen

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine)

  • Wu Zuo

    (Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yong Fan

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine)

  • Sijia Huang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine)

  • Yongmei Liu

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine)

  • Guangming Chen

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine
    Huzhou University, Huzhou Central Hospital)

  • Qing Li

    (University of Chinese Academy of Sciences
    Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences)

  • Jinsong Li

    (University of Chinese Academy of Sciences
    Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences)

  • Jian Wu

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine)

  • Qian Bian

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine)

  • Chenhui Huang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine)

  • Ming Lei

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Institute of Precision Medicine
    Shanghai Jiao Tong University School of Medicine)

Abstract

Chromosomes pair and synapse with their homologous partners to segregate correctly at the first meiotic division. Association of telomeres with the LINC (Linker of Nucleoskeleton and Cytoskeleton) complex composed of SUN1 and KASH5 enables telomere-led chromosome movements and telomere bouquet formation, facilitating precise pairwise alignment of homologs. Here, we identify a direct interaction between SUN1 and Speedy A (SPDYA) and determine the crystal structure of human SUN1-SPDYA-CDK2 ternary complex. Analysis of meiosis prophase I process in SPDYA-binding-deficient SUN1 mutant mice reveals that the SUN1-SPDYA interaction is required for the telomere-LINC complex connection and the assembly of a ring-shaped telomere supramolecular architecture at the nuclear envelope, which is critical for efficient homologous pairing and synapsis. Overall, our results provide structural insights into meiotic telomere structure that is essential for meiotic prophase I progression.

Suggested Citation

  • Yanyan Chen & Yan Wang & Juan Chen & Wu Zuo & Yong Fan & Sijia Huang & Yongmei Liu & Guangming Chen & Qing Li & Jinsong Li & Jian Wu & Qian Bian & Chenhui Huang & Ming Lei, 2021. "The SUN1-SPDYA interaction plays an essential role in meiosis prophase I," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23550-w
    DOI: 10.1038/s41467-021-23550-w
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    Cited by:

    1. 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.
    2. Erik B. Faber & Luxin Sun & Jian Tang & Emily Roberts & Sornakala Ganeshkumar & Nan Wang & Damien Rasmussen & Abir Majumdar & Laura E. Hirsch & Kristen John & An Yang & Hira Khalid & Jon E. Hawkinson , 2023. "Development of allosteric and selective CDK2 inhibitors for contraception with negative cooperativity to cyclin binding," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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