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N2FXm, a method for joint nuclear and cytoplasmic volume measurements, unravels the osmo-mechanical regulation of nuclear volume in mammalian cells

Author

Listed:
  • Fabrizio A. Pennacchio

    (IFOM ETS—The AIRC Institute of Molecular Oncology
    ETH Zurich)

  • Alessandro Poli

    (IFOM ETS—The AIRC Institute of Molecular Oncology)

  • Francesca Michela Pramotton

    (ETH Zurich)

  • Stefania Lavore

    (IFOM ETS—The AIRC Institute of Molecular Oncology)

  • Ilaria Rancati

    (IFOM ETS—The AIRC Institute of Molecular Oncology)

  • Mario Cinquanta

    (IFOM ETS—The AIRC Institute of Molecular Oncology)

  • Daan Vorselen

    (University of Washington)

  • Elisabetta Prina

    (IFOM ETS—The AIRC Institute of Molecular Oncology)

  • Orso Maria Romano

    (IFOM ETS—The AIRC Institute of Molecular Oncology)

  • Aldo Ferrari

    (ETH Zurich)

  • Matthieu Piel

    (Institut Curie, PSL Research University, CNRS, UMR 144
    Institut Pierre-Gilles de Gennes, PSL Research University)

  • Marco Cosentino Lagomarsino

    (IFOM ETS—The AIRC Institute of Molecular Oncology
    Università degli Studi di Milano, and I.N.F.N.)

  • Paolo Maiuri

    (IFOM ETS—The AIRC Institute of Molecular Oncology
    Università degli Studi di Napoli Federico II)

Abstract

In eukaryotes, cytoplasmic and nuclear volumes are tightly regulated to ensure proper cell homeostasis. However, current methods to measure cytoplasmic and nuclear volumes, including confocal 3D reconstruction, have limitations, such as relying on two-dimensional projections or poor vertical resolution. Here, to overcome these limitations, we describe a method, N2FXm, to jointly measure cytoplasmic and nuclear volumes in single cultured adhering human cells, in real time, and across cell cycles. We find that this method accurately provides joint size over dynamic measurements and at different time resolutions. Moreover, by combining several experimental perturbations and analyzing a mathematical model including osmotic effects and tension, we show that N2FXm can give relevant insights on how mechanical forces exerted by the cytoskeleton on the nuclear envelope can affect the growth of nucleus volume by biasing nuclear import. Our method, by allowing for accurate joint nuclear and cytoplasmic volume dynamic measurements at different time resolutions, highlights the non-constancy of the nucleus/cytoplasm ratio along the cell cycle.

Suggested Citation

  • Fabrizio A. Pennacchio & Alessandro Poli & Francesca Michela Pramotton & Stefania Lavore & Ilaria Rancati & Mario Cinquanta & Daan Vorselen & Elisabetta Prina & Orso Maria Romano & Aldo Ferrari & Matt, 2024. "N2FXm, a method for joint nuclear and cytoplasmic volume measurements, unravels the osmo-mechanical regulation of nuclear volume in mammalian cells," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45168-4
    DOI: 10.1038/s41467-024-45168-4
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    References listed on IDEAS

    as
    1. Alessandro Poli & Fabrizio A. Pennacchio & Andrea Ghisleni & Mariagrazia Gennaro & Margaux Lecacheur & Paulina Nastały & Michele Crestani & Francesca M. Pramotton & Fabio Iannelli & Galina Beznusenko , 2023. "PIP4K2B is mechanoresponsive and controls heterochromatin-driven nuclear softening through UHRF1," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Daan Vorselen & Yifan Wang & Miguel M. Jesus & Pavak K. Shah & Matthew J. Footer & Morgan Huse & Wei Cai & Julie A. Theriot, 2020. "Microparticle traction force microscopy reveals subcellular force exertion patterns in immune cell–target interactions," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    3. Clotilde Cadart & Sylvain Monnier & Jacopo Grilli & Pablo J. Sáez & Nishit Srivastava & Rafaele Attia & Emmanuel Terriac & Buzz Baum & Marco Cosentino-Lagomarsino & Matthieu Piel, 2018. "Size control in mammalian cells involves modulation of both growth rate and cell cycle duration," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    4. Kazunori Kume & Helena Cantwell & Alana Burrell & Paul Nurse, 2019. "Nuclear membrane protein Lem2 regulates nuclear size through membrane flow," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
    5. Anthony P. Schuller & Matthias Wojtynek & David Mankus & Meltem Tatli & Rafael Kronenberg-Tenga & Saroj G. Regmi & Phat V. Dip & Abigail K. R. Lytton-Jean & Edward J. Brignole & Mary Dasso & Karsten W, 2021. "The cellular environment shapes the nuclear pore complex architecture," Nature, Nature, vol. 598(7882), pages 667-671, October.
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