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Spindle-localized F-actin regulates polar MTOC organization and the fidelity of meiotic spindle formation

Author

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  • Edgar J. Soto-Moreno

    (University of Missouri)

  • Nourhan N. Ali

    (University of Missouri)

  • Florian Küllmer

    (Institut für Organische Chemie und Makromolekulare Chemie)

  • Veselin Nasufovic

    (Institut für Organische Chemie und Makromolekulare Chemie)

  • Michaela Frolikova

    (Institute of Biotechnology of the Czech Academy of Sciences, BIOCEV)

  • Olga Tepla

    (Institute of Biotechnology of the Czech Academy of Sciences, BIOCEV
    Charles University and General University Hospital in Prague)

  • Jaromir Masata

    (Charles University and General University Hospital in Prague)

  • Dirk Trauner

    (University of Pennsylvania)

  • Amanda A. Patterson

    (University of Missouri)

  • Hans-Dieter Arndt

    (Institut für Organische Chemie und Makromolekulare Chemie)

  • Katerina Komrskova

    (Institute of Biotechnology of the Czech Academy of Sciences, BIOCEV
    Charles University)

  • Magdalena Zernicka-Goetz

    (California Institute of Technology)

  • David M. Glover

    (California Institute of Technology)

  • Ahmed Z. Balboula

    (University of Missouri)

Abstract

Mammalian oocytes are notoriously prone to chromosome segregation errors leading to aneuploidy. The spindle provides the machinery for accurate chromosome segregation during cell division. Mammalian oocytes lack centrioles and, therefore, mouse meiotic spindle relies on the organization of numerous acentriolar microtubule organizing centers into two poles (polar microtubule organizing centers, pMTOCs). The traditional view is that, in mammalian oocytes, microtubules are the sole cytoskeletal component responsible for regulating pMTOC organization and spindle assembly. We identify a previously unrecognized F-actin pool that surrounds pMTOCs, forming F-actin cage-like structure. We demonstrate that F-actin localization on the spindle depends on unconventional myosins X and VIIb. Selective disruption of spindle-localized F-actin, using myosin X/VIIb knockdown oocytes or photoswitchable Optojasp-1, perturbs pMTOC organization, leading to unfocused spindle poles and chromosome missegregation. Here, we unveil an important function of spindle-localized F-actin in regulating pMTOC organization, a critical process for ensuring the fidelity of meiotic spindle formation and proper chromosome segregation.

Suggested Citation

  • Edgar J. Soto-Moreno & Nourhan N. Ali & Florian Küllmer & Veselin Nasufovic & Michaela Frolikova & Olga Tepla & Jaromir Masata & Dirk Trauner & Amanda A. Patterson & Hans-Dieter Arndt & Katerina Komrs, 2025. "Spindle-localized F-actin regulates polar MTOC organization and the fidelity of meiotic spindle formation," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-63586-w
    DOI: 10.1038/s41467-025-63586-w
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    References listed on IDEAS

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    1. Margot E. Quinlan & John E. Heuser & Eugen Kerkhoff & R. Dyche Mullins, 2005. "Drosophila Spire is an actin nucleation factor," Nature, Nature, vol. 433(7024), pages 382-388, January.
    2. Dean Clift & Melina Schuh, 2015. "A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    3. Johannes Roeles & Georgios Tsiavaliaris, 2019. "Actin-microtubule interplay coordinates spindle assembly in human oocytes," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
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    5. Dalileh Nabi & Hauke Drechsler & Johannes Pschirer & Franz Korn & Nadine Schuler & Stefan Diez & Rolf Jessberger & Mariola Chacón, 2021. "CENP-V is required for proper chromosome segregation through interaction with spindle microtubules in mouse oocytes," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
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