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

Fabrizio A. Pennacchio, Alessandro Poli, Francesca Michela Pramotton, Stefania Lavore, Ilaria Rancati, Mario Cinquanta, Daan Vorselen, Elisabetta Prina, Orso Maria Romano, Aldo Ferrari, Matthieu Piel, Marco Cosentino Lagomarsino and Paolo Maiuri ()
Additional contact information
Fabrizio A. Pennacchio: IFOM ETS—The AIRC Institute of Molecular Oncology
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
Marco Cosentino Lagomarsino: IFOM ETS—The AIRC Institute of Molecular Oncology
Paolo Maiuri: IFOM ETS—The AIRC Institute of Molecular Oncology

Nature Communications, 2024, vol. 15, issue 1, 1-10

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-45168-4

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