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Shielding of actin by the endoplasmic reticulum impacts nuclear positioning

Author

Listed:
  • Cátia Silva Janota

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa)

  • Andreia Pinto

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Royal Brompton Hospital and Harefield NHS Foundation Trust)

  • Anna Pezzarossa

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Champalimaud Foundation, Champalimaud Centre for the Unknown)

  • Pedro Machado

    (Electron Microscopy Core Facility (EMCF), European Molecular Biology Laboratory
    Centre for Ultrastructural Imaging, King’s College London)

  • Judite Costa

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa)

  • Pedro Campinho

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Champalimaud Foundation, Champalimaud Centre for the Unknown)

  • Cláudio A. Franco

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Instituto de Histologia e Biologia do Desenvolvimento, Faculdade de Medicina, Universidade de Lisboa)

  • Edgar R. Gomes

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Instituto de Histologia e Biologia do Desenvolvimento, Faculdade de Medicina, Universidade de Lisboa)

Abstract

Nuclear position is central to cell polarization, and its disruption is associated with various pathologies. The nucleus is moved away from the leading edge of migrating cells through its connection to moving dorsal actin cables, and the absence of connections to immobile ventral stress fibers. It is unclear how these asymmetric nucleo-cytoskeleton connections are established. Here, using an in vitro wound assay, we find that remodeling of endoplasmic reticulum (ER) impacts nuclear positioning through the formation of a barrier that shields immobile ventral stress fibers. The remodeling of ER and perinuclear ER accumulation is mediated by the ER shaping protein Climp-63. Furthermore, ectopic recruitment of the ER to stress fibers restores nuclear positioning in the absence of Climp-63. Our findings suggest that the ER mediates asymmetric nucleo-cytoskeleton connections to position the nucleus.

Suggested Citation

  • Cátia Silva Janota & Andreia Pinto & Anna Pezzarossa & Pedro Machado & Judite Costa & Pedro Campinho & Cláudio A. Franco & Edgar R. Gomes, 2022. "Shielding of actin by the endoplasmic reticulum impacts nuclear positioning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30388-3
    DOI: 10.1038/s41467-022-30388-3
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    References listed on IDEAS

    as
    1. Pengli Zheng & Christopher J. Obara & Ewa Szczesna & Jonathon Nixon-Abell & Kishore K. Mahalingan & Antonina Roll-Mecak & Jennifer Lippincott-Schwartz & Craig Blackstone, 2022. "ER proteins decipher the tubulin code to regulate organelle distribution," Nature, Nature, vol. 601(7891), pages 132-138, January.
    2. Alex M. Valm & Sarah Cohen & Wesley R. Legant & Justin Melunis & Uri Hershberg & Eric Wait & Andrew R. Cohen & Michael W. Davidson & Eric Betzig & Jennifer Lippincott-Schwartz, 2017. "Applying systems-level spectral imaging and analysis to reveal the organelle interactome," Nature, Nature, vol. 546(7656), pages 162-167, June.
    3. Francesca Bottanelli & Emil B. Kromann & Edward S. Allgeyer & Roman S. Erdmann & Stephanie Wood Baguley & George Sirinakis & Alanna Schepartz & David Baddeley & Derek K. Toomre & James E. Rothman & Jo, 2016. "Two-colour live-cell nanoscale imaging of intracellular targets," Nature Communications, Nature, vol. 7(1), pages 1-5, April.
    4. Thomas Metzger & Vincent Gache & Mu Xu & Bruno Cadot & Eric S. Folker & Brian E. Richardson & Edgar R. Gomes & Mary K. Baylies, 2012. "MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function," Nature, Nature, vol. 484(7392), pages 120-124, April.
    5. Jörg Renkawitz & Aglaja Kopf & Julian Stopp & Ingrid Vries & Meghan K. Driscoll & Jack Merrin & Robert Hauschild & Erik S. Welf & Gaudenz Danuser & Reto Fiolka & Michael Sixt, 2019. "Nuclear positioning facilitates amoeboid migration along the path of least resistance," Nature, Nature, vol. 568(7753), pages 546-550, April.
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