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Actin polymerisation and crosslinking drive left-right asymmetry in single cell and cell collectives

Author

Listed:
  • Yee Han Tee

    (National University of Singapore)

  • Wei Jia Goh

    (National University of Singapore)

  • Xianbin Yong

    (National University of Singapore)

  • Hui Ting Ong

    (National University of Singapore)

  • Jinrong Hu

    (National University of Singapore)

  • Ignacius Yan Yun Tay

    (National University of Singapore)

  • Shidong Shi

    (National University of Singapore)

  • Salma Jalal

    (National University of Singapore)

  • Samuel F. H. Barnett

    (National University of Singapore)

  • Pakorn Kanchanawong

    (National University of Singapore
    National University of Singapore)

  • Wenmao Huang

    (National University of Singapore)

  • Jie Yan

    (National University of Singapore
    National University of Singapore)

  • Yong Ann Ben Lim

    (National University of Singapore)

  • Visalatchi Thiagarajan

    (National University of Singapore)

  • Alex Mogilner

    (New York University
    New York University)

  • Alexander D. Bershadsky

    (National University of Singapore
    Weizmann Institute of Science)

Abstract

Deviations from mirror symmetry in the development of bilateral organisms are common but the mechanisms of initial symmetry breaking are insufficiently understood. The actin cytoskeleton of individual cells self-organises in a chiral manner, but the molecular players involved remain essentially unidentified and the relationship between chirality of an individual cell and cell collectives is unclear. Here, we analysed self-organisation of the chiral actin cytoskeleton in individual cells on circular or elliptical patterns, and collective cell alignment in confined microcultures. Screening based on deep-learning analysis of actin patterns identified actin polymerisation regulators, depletion of which suppresses chirality (mDia1) or reverses chirality direction (profilin1 and CapZβ). The reversed chirality is mDia1-independent but requires the function of actin-crosslinker α−actinin1. A robust correlation between the effects of a variety of actin assembly regulators on chirality of individual cells and cell collectives is revealed. Thus, actin-driven cell chirality may underlie tissue and organ asymmetry.

Suggested Citation

  • Yee Han Tee & Wei Jia Goh & Xianbin Yong & Hui Ting Ong & Jinrong Hu & Ignacius Yan Yun Tay & Shidong Shi & Salma Jalal & Samuel F. H. Barnett & Pakorn Kanchanawong & Wenmao Huang & Jie Yan & Yong Ann, 2023. "Actin polymerisation and crosslinking drive left-right asymmetry in single cell and cell collectives," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35918-1
    DOI: 10.1038/s41467-023-35918-1
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    References listed on IDEAS

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    1. Miao Yu & Xin Yuan & Chen Lu & Shimin Le & Ryo Kawamura & Artem K. Efremov & Zhihai Zhao & Michael M. Kozlov & Michael Sheetz & Alexander Bershadsky & Jie Yan, 2017. "mDia1 senses both force and torque during F-actin filament polymerization," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    2. Thuan Beng Saw & Amin Doostmohammadi & Vincent Nier & Leyla Kocgozlu & Sumesh Thampi & Yusuke Toyama & Philippe Marcq & Chwee Teck Lim & Julia M. Yeomans & Benoit Ladoux, 2017. "Topological defects in epithelia govern cell death and extrusion," Nature, Nature, vol. 544(7649), pages 212-216, April.
    3. Shunya Hozumi & Reo Maeda & Kiichiro Taniguchi & Maiko Kanai & Syuichi Shirakabe & Takeshi Sasamura & Pauline Spéder & Stéphane Noselli & Toshiro Aigaki & Ryutaro Murakami & Kenji Matsuno, 2006. "An unconventional myosin in Drosophila reverses the default handedness in visceral organs," Nature, Nature, vol. 440(7085), pages 798-802, April.
    4. Pauline Spéder & Géza Ádám & Stéphane Noselli, 2006. "Type ID unconventional myosin controls left–right asymmetry in Drosophila," Nature, Nature, vol. 440(7085), pages 803-807, April.
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