Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation
During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we charac...
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Published in | Nature communications Vol. 16; no. 1; pp. 6473 - 17 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
14.07.2025
Nature Publishing Group Nature Portfolio |
Subjects | |
Online Access | Get full text |
ISSN | 2041-1723 2041-1723 |
DOI | 10.1038/s41467-025-61702-4 |
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Abstract | During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during
Drosophila
gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously.
Cellular forces shaping cells and tissues during development are well understood, but their dynamic material properties less so. Here, the authors use Brillouin microscopy to map cell material properties in developing fruit fly embryos, revealing dynamic, fate-specific modulation. |
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AbstractList | During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during
Drosophila
gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously.
Cellular forces shaping cells and tissues during development are well understood, but their dynamic material properties less so. Here, the authors use Brillouin microscopy to map cell material properties in developing fruit fly embryos, revealing dynamic, fate-specific modulation. During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during Drosophila gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously.During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during Drosophila gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously. During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during Drosophila gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously.Cellular forces shaping cells and tissues during development are well understood, but their dynamic material properties less so. Here, the authors use Brillouin microscopy to map cell material properties in developing fruit fly embryos, revealing dynamic, fate-specific modulation. During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during Drosophila gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously. Abstract During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during Drosophila gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously. |
ArticleNumber | 6473 |
Author | Heriche, Jean-Karim Gomez, Juan Manuel Thayambath, Abhisha Bevilacqua, Carlo Belmonte, Julio M. Prevedel, Robert Leptin, Maria |
Author_xml | – sequence: 1 givenname: Juan Manuel orcidid: 0000-0002-3041-2503 surname: Gomez fullname: Gomez, Juan Manuel email: juan.elliff@embl.de organization: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL) – sequence: 2 givenname: Carlo orcidid: 0000-0001-9084-0641 surname: Bevilacqua fullname: Bevilacqua, Carlo organization: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL) – sequence: 3 givenname: Abhisha surname: Thayambath fullname: Thayambath, Abhisha organization: Quantitative and Computational Developmental Biology Cluster, North Carolina State University, Department of Physics, North Carolina State University – sequence: 4 givenname: Jean-Karim orcidid: 0000-0001-6867-9425 surname: Heriche fullname: Heriche, Jean-Karim organization: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL) – sequence: 5 givenname: Maria orcidid: 0000-0001-7097-348X surname: Leptin fullname: Leptin, Maria organization: Developmental Biology Unit, European Molecular Biology Laboratory (EMBL), Director’s research, European Molecular Biology Laboratory (EMBL), Institute of Genetics, University of Cologne – sequence: 6 givenname: Julio M. surname: Belmonte fullname: Belmonte, Julio M. organization: Quantitative and Computational Developmental Biology Cluster, North Carolina State University, Department of Physics, North Carolina State University – sequence: 7 givenname: Robert orcidid: 0000-0003-3366-4703 surname: Prevedel fullname: Prevedel, Robert email: prevedel@embl.de organization: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Developmental Biology Unit, European Molecular Biology Laboratory (EMBL), Epigenetics and Neurobiology Unit, European Molecular Biology Laboratory (EMBL), German Center for Lung Research (DZL) |
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Title | Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation |
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