IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37370-7.html
   My bibliography  Save this article

Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity

Author

Listed:
  • Shuwen He

    (University of Gothenburg)

  • John P. Gillies

    (University of Michigan)

  • Juliana L. Zang

    (University of Michigan)

  • Carmen M. Córdoba-Beldad

    (University of Gothenburg)

  • Io Yamamoto

    (University of Gothenburg)

  • Yasuhiro Fujiwara

    (University of Tokyo)

  • Julie Grantham

    (University of Gothenburg)

  • Morgan E. DeSantis

    (University of Michigan)

  • Hiroki Shibuya

    (University of Gothenburg)

Abstract

Spindle formation in male meiosis relies on the canonical centrosome system, which is distinct from acentrosomal oocyte meiosis, but its specific regulatory mechanisms remain unknown. Herein, we report that DYNLRB2 (Dynein light chain roadblock-type-2) is a male meiosis-upregulated dynein light chain that is indispensable for spindle formation in meiosis I. In Dynlrb2 KO mouse testes, meiosis progression is arrested in metaphase I due to the formation of multipolar spindles with fragmented pericentriolar material (PCM). DYNLRB2 inhibits PCM fragmentation through two distinct pathways; suppressing premature centriole disengagement and targeting NuMA (nuclear mitotic apparatus) to spindle poles. The ubiquitously expressed mitotic counterpart, DYNLRB1, has similar roles in mitotic cells and maintains spindle bipolarity by targeting NuMA and suppressing centriole overduplication. Our work demonstrates that two distinct dynein complexes containing DYNLRB1 or DYNLRB2 are separately used in mitotic and meiotic spindle formations, respectively, and that both have NuMA as a common target.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37370-7
    DOI: 10.1038/s41467-023-37370-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37370-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37370-7?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. Shuhei Yoshida & Sui Nishiyama & Lisa Lister & Shu Hashimoto & Tappei Mishina & Aurélien Courtois & Hirohisa Kyogoku & Takaya Abe & Aki Shiraishi & Meenakshi Choudhary & Yoshiharu Nakaoka & Mary Herbe, 2020. "Prc1-rich kinetochores are required for error-free acentrosomal spindle bipolarization during meiosis I in mouse oocytes," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. In-Gyun Lee & Mara A. Olenick & Malgorzata Boczkowska & Clara Franzini-Armstrong & Erika L. F. Holzbaur & Roberto Dominguez, 2018. "A conserved interaction of the dynein light intermediate chain with dynein-dynactin effectors necessary for processivity," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Lukas C. Kapitein & Erwin J. G. Peterman & Benjamin H. Kwok & Jeffrey H. Kim & Tarun M. Kapoor & Christoph F. Schmidt, 2005. "The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks," Nature, Nature, vol. 435(7038), pages 114-118, May.
    4. Jihye Kim & Kei-ichiro Ishiguro & Aya Nambu & Bungo Akiyoshi & Shihori Yokobayashi & Ayano Kagami & Tadashi Ishiguro & Alberto M. Pendas & Naoki Takeda & Yogo Sakakibara & Tomoya S. Kitajima & Yuji Ta, 2015. "Meikin is a conserved regulator of meiosis-I-specific kinetochore function," Nature, Nature, vol. 517(7535), pages 466-471, January.
    5. 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.
    6. Menuka Karki & Neda Keyhaninejad & Charles B. Shuster, 2017. "Precocious centriole disengagement and centrosome fragmentation induced by mitotic delay," Nature Communications, Nature, vol. 8(1), pages 1-12, August.
    Full references (including those not matched with items on IDEAS)

    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. Jurica Matković & Subhadip Ghosh & Mateja Ćosić & Susana Eibes & Marin Barišić & Nenad Pavin & Iva M. Tolić, 2022. "Kinetochore- and chromosome-driven transition of microtubules into bundles promotes spindle assembly," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. 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.
    3. 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.
    4. 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.
    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. Ricardo Celestino & Morkos A Henen & José B Gama & Cátia Carvalho & Maxwell McCabe & Daniel J Barbosa & Alexandra Born & Parker J Nichols & Ana X Carvalho & Reto Gassmann & Beat Vögeli, 2019. "A transient helix in the disordered region of dynein light intermediate chain links the motor to structurally diverse adaptors for cargo transport," PLOS Biology, Public Library of Science, vol. 17(1), pages 1-33, January.
    8. 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.
    9. Lucia Cassella & Anne Ephrussi, 2022. "Subcellular spatial transcriptomics identifies three mechanistically different classes of localizing RNAs," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. 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.
    11. 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.
    12. Tal Keren-Kaplan & Amra Sarić & Saikat Ghosh & Chad D. Williamson & Rui Jia & Yan Li & Juan S. Bonifacino, 2022. "RUFY3 and RUFY4 are ARL8 effectors that promote coupling of endolysosomes to dynein-dynactin," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    13. 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.
    14. Ray, Krishanu, 2006. "How kinesins walk, assemble and transport: A birds-eye-view of some unresolved questions," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 372(1), pages 52-64.

    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:14:y:2023:i:1:d:10.1038_s41467-023-37370-7. 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.