Liquid-crystal organization of liver tissue

Functional tissue architecture originates by self-assembly of distinct cell types, following tissue-specific rules of cell-cell interactions. In the liver, a structural model of the lobule was pioneered by Elias in 1949. This model, however, is in contrast with the apparent random 3D arrangement of...

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Main Authors: Hernán Morales-Navarrete, Hidenori Nonaka, André Scholich, Fabián Segovia-Miranda, Walter de Back, Kirstin Meyer, Roman L Bogorad, Victor Koteliansky, Lutz Brusch, Yannis Kalaidzidis, Frank Jülicher, Benjamin M Friedrich, Marino Zerial
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/44860
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author Hernán Morales-Navarrete
Hidenori Nonaka
André Scholich
Fabián Segovia-Miranda
Walter de Back
Kirstin Meyer
Roman L Bogorad
Victor Koteliansky
Lutz Brusch
Yannis Kalaidzidis
Frank Jülicher
Benjamin M Friedrich
Marino Zerial
author_facet Hernán Morales-Navarrete
Hidenori Nonaka
André Scholich
Fabián Segovia-Miranda
Walter de Back
Kirstin Meyer
Roman L Bogorad
Victor Koteliansky
Lutz Brusch
Yannis Kalaidzidis
Frank Jülicher
Benjamin M Friedrich
Marino Zerial
author_sort Hernán Morales-Navarrete
collection DOAJ
description Functional tissue architecture originates by self-assembly of distinct cell types, following tissue-specific rules of cell-cell interactions. In the liver, a structural model of the lobule was pioneered by Elias in 1949. This model, however, is in contrast with the apparent random 3D arrangement of hepatocytes. Since then, no significant progress has been made to derive the organizing principles of liver tissue. To solve this outstanding problem, we computationally reconstructed 3D tissue geometry from microscopy images of mouse liver tissue and analyzed it applying soft-condensed-matter-physics concepts. Surprisingly, analysis of the spatial organization of cell polarity revealed that hepatocytes are not randomly oriented but follow a long-range liquid-crystal order. This does not depend exclusively on hepatocytes receiving instructive signals by endothelial cells, since silencing Integrin-β1 disrupted both liquid-crystal order and organization of the sinusoidal network. Our results suggest that bi-directional communication between hepatocytes and sinusoids underlies the self-organization of liver tissue.
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spelling doaj.art-33e29e9f287b4b73becdf7cfdc1d6f672022-12-22T03:24:36ZengeLife Sciences Publications LtdeLife2050-084X2019-06-01810.7554/eLife.44860Liquid-crystal organization of liver tissueHernán Morales-Navarrete0https://orcid.org/0000-0002-9578-2556Hidenori Nonaka1André Scholich2https://orcid.org/0000-0002-9393-5459Fabián Segovia-Miranda3https://orcid.org/0000-0003-1546-0475Walter de Back4https://orcid.org/0000-0003-4641-8472Kirstin Meyer5Roman L Bogorad6Victor Koteliansky7Lutz Brusch8https://orcid.org/0000-0003-0137-5106Yannis Kalaidzidis9Frank Jülicher10https://orcid.org/0000-0003-4731-9185Benjamin M Friedrich11https://orcid.org/0000-0002-9742-6555Marino Zerial12https://orcid.org/0000-0002-7490-4235Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMax Planck Institute for the Physics of Complex Systems, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyInstitute for Medical Informatics and Biometry, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Centre for Information Services and High Performance Computing, Technische Universität Dresden, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, United StatesSkolkovo Institute of Science and Technology, Skolkovo, Russia; Department of Chemistry, MV Lomonosov Moscow State University, Moscow, RussiaCentre for Information Services and High Performance Computing, Technische Universität Dresden, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMax Planck Institute for the Physics of Complex Systems, Dresden, Germany; Cluster of Excellence Physics of Life, TU Dresden, Dresden, GermanyCluster of Excellence Physics of Life, TU Dresden, Dresden, Germany; Center for Advancing Electronics Dresden, Technische Universität Dresden, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Cluster of Excellence Physics of Life, TU Dresden, Dresden, GermanyFunctional tissue architecture originates by self-assembly of distinct cell types, following tissue-specific rules of cell-cell interactions. In the liver, a structural model of the lobule was pioneered by Elias in 1949. This model, however, is in contrast with the apparent random 3D arrangement of hepatocytes. Since then, no significant progress has been made to derive the organizing principles of liver tissue. To solve this outstanding problem, we computationally reconstructed 3D tissue geometry from microscopy images of mouse liver tissue and analyzed it applying soft-condensed-matter-physics concepts. Surprisingly, analysis of the spatial organization of cell polarity revealed that hepatocytes are not randomly oriented but follow a long-range liquid-crystal order. This does not depend exclusively on hepatocytes receiving instructive signals by endothelial cells, since silencing Integrin-β1 disrupted both liquid-crystal order and organization of the sinusoidal network. Our results suggest that bi-directional communication between hepatocytes and sinusoids underlies the self-organization of liver tissue.https://elifesciences.org/articles/44860liquid crystal order3D tissue organizationlivercell polarity
spellingShingle Hernán Morales-Navarrete
Hidenori Nonaka
André Scholich
Fabián Segovia-Miranda
Walter de Back
Kirstin Meyer
Roman L Bogorad
Victor Koteliansky
Lutz Brusch
Yannis Kalaidzidis
Frank Jülicher
Benjamin M Friedrich
Marino Zerial
Liquid-crystal organization of liver tissue
eLife
liquid crystal order
3D tissue organization
liver
cell polarity
title Liquid-crystal organization of liver tissue
title_full Liquid-crystal organization of liver tissue
title_fullStr Liquid-crystal organization of liver tissue
title_full_unstemmed Liquid-crystal organization of liver tissue
title_short Liquid-crystal organization of liver tissue
title_sort liquid crystal organization of liver tissue
topic liquid crystal order
3D tissue organization
liver
cell polarity
url https://elifesciences.org/articles/44860
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AT walterdeback liquidcrystalorganizationoflivertissue
AT kirstinmeyer liquidcrystalorganizationoflivertissue
AT romanlbogorad liquidcrystalorganizationoflivertissue
AT victorkoteliansky liquidcrystalorganizationoflivertissue
AT lutzbrusch liquidcrystalorganizationoflivertissue
AT yanniskalaidzidis liquidcrystalorganizationoflivertissue
AT frankjulicher liquidcrystalorganizationoflivertissue
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