Strong intracellular signal inactivation produces sharper and more robust signaling from cell membrane to nucleus
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 an...
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creator | Ma, Jingwei Do, Myan Le Gros, Mark A Peskin, Charles S Larabell, Carolyn A Mori, Yoichiro Isaacson, Samuel A |
description | 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. |
doi_str_mv | 10.1371/journal.pcbi.1008356 |
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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. 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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. 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subjects | Active Transport, Cell Nucleus B-Lymphocytes - metabolism B-Lymphocytes - ultrastructure Biology and Life Sciences Boundary conditions Cartesian coordinates Cell activation Cell Membrane - metabolism Cell Membrane - ultrastructure Cell membranes Cell Nucleus - metabolism Cell Nucleus - ultrastructure Cell surface Cellular signal transduction Chemical reactions Computational Biology Computer Simulation Cubes Cyclic AMP Dirichlet problem Engineering and Technology Exact solutions Finite element method Humans Imaging, Three-Dimensional Inactivation Intracellular signalling Kinases Kinetics Lymphocytes Lymphocytes T Mathematical models Mathematics Medicine and Health Sciences Membranes Models, Biological Nuclear Envelope - metabolism Nuclear Envelope - ultrastructure Observations Organelles Physiological aspects Probability density functions Propagation Protein kinase Proteins Receptors Representations Robustness (mathematics) Signal Transduction - physiology Signaling Statistics Synaptogenesis T cell receptors T-cell receptor Tomography Tomography, X-Ray |
title | Strong intracellular signal inactivation produces sharper and more robust signaling from cell membrane to nucleus |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-23T03%3A52%3A58IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Strong%20intracellular%20signal%20inactivation%20produces%20sharper%20and%20more%20robust%20signaling%20from%20cell%20membrane%20to%20nucleus&rft.jtitle=PLoS%20computational%20biology&rft.au=Ma,%20Jingwei&rft.date=2020-11-16&rft.volume=16&rft.issue=11&rft.spage=e1008356&rft.epage=e1008356&rft.pages=e1008356-e1008356&rft.issn=1553-7358&rft.eissn=1553-7358&rft_id=info:doi/10.1371/journal.pcbi.1008356&rft_dat=%3Cgale_plos_%3EA643392376%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2479463834&rft_id=info:pmid/33196636&rft_galeid=A643392376&rft_doaj_id=oai_doaj_org_article_e684153658db454b9eee17439c2346d5&rfr_iscdi=true |