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Strong intracellular signal inactivation produces sharper and more robust signaling from cell membrane to nucleus

Jingwei Ma, Myan Do, Mark. A. Le Gros, Charles S. Peskin, Carolyn A. Larabell, Yoichiro Mori, View ORCID ProfileSamuel A. Isaacson
doi: https://doi.org/10.1101/2020.01.16.909333
Jingwei Ma
1Department of Mathematics and Statistics, Boston University
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Myan Do
2Department of Cellular and Molecular Medicine, University of California, San Diego Medical School
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Mark. A. Le Gros
3Department of Anatomy, University of California, San Francisco
4National Center for X-ray Tomography, Lawrence Berkeley National Lab
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Charles S. Peskin
5Courant Institute of Mathematical Sciences, New York University
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Carolyn A. Larabell
3Department of Anatomy, University of California, San Francisco
4National Center for X-ray Tomography, Lawrence Berkeley National Lab
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Yoichiro Mori
6Department of Mathematics, University of Pennsylvania
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Samuel A. Isaacson
1Department of Mathematics and Statistics, Boston University
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  • ORCID record for Samuel A. Isaacson
  • For correspondence: isaacson@math.bu.edu
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Abstract

For a chemical signal to propagate across a cell, it must navigate a tortuous environment involving a variety of organelle barriers. In this work we study mathematical models for a basic chemical signal, the arrival times at the nuclear membrane of proteins that are activated at the cell membrane and diffuse throughout the cytosol. Organelle surfaces within human B cells are reconstructed from soft X-ray tomographic images, and modeled as reflecting barriers to the molecules’ diffusion. We show that signal inactivation sharpens signals, reducing variability in the arrival time at the nuclear membrane. Inactivation can also compensate for an observed slowdown in signal propagation induced by the presence of organelle barriers, leading to arrival times at the nuclear membrane that are comparable to models in which the cytosol is treated as an open, empty region. In the limit of strong signal inactivation this is achieved by filtering out molecules that traverse non-geodesic paths.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Adds additional references and discussion. Updates spherical model simulations to use spheres with radii that more closely match those of the imaged B cells.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 12, 2020.
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Strong intracellular signal inactivation produces sharper and more robust signaling from cell membrane to nucleus
Jingwei Ma, Myan Do, Mark. A. Le Gros, Charles S. Peskin, Carolyn A. Larabell, Yoichiro Mori, Samuel A. Isaacson
bioRxiv 2020.01.16.909333; doi: https://doi.org/10.1101/2020.01.16.909333
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Strong intracellular signal inactivation produces sharper and more robust signaling from cell membrane to nucleus
Jingwei Ma, Myan Do, Mark. A. Le Gros, Charles S. Peskin, Carolyn A. Larabell, Yoichiro Mori, Samuel A. Isaacson
bioRxiv 2020.01.16.909333; doi: https://doi.org/10.1101/2020.01.16.909333

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