Direct laser manipulation reveals the mechanics of cell contacts in vivo
Significance The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to understand how cell-generated forces produce cell shape changes and how such forces transmit through a group of adhesive cells in vivo. In thi...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 5; pp. 1416 - 1421 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
United States
National Academy of Sciences
03.02.2015
National Acad Sciences |
Subjects | |
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Abstract | Significance The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to understand how cell-generated forces produce cell shape changes and how such forces transmit through a group of adhesive cells in vivo. In this context, we have developed an approach using laser manipulation to impose local forces on cell contacts in the early Drosophila embryo. Quantification of local and global shape changes using our approach can both provide direct measurements of the forces acting at cell contacts and delineate the time-dependent viscoelastic properties of the tissue. The latter provides an explicit relationship, the so-called constitutive law, between forces and deformations.
Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell–cell and cell–ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell–cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue. |
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AbstractList | Significance The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to understand how cell-generated forces produce cell shape changes and how such forces transmit through a group of adhesive cells in vivo. In this context, we have developed an approach using laser manipulation to impose local forces on cell contacts in the early Drosophila embryo. Quantification of local and global shape changes using our approach can both provide direct measurements of the forces acting at cell contacts and delineate the time-dependent viscoelastic properties of the tissue. The latter provides an explicit relationship, the so-called constitutive law, between forces and deformations.
Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell–cell and cell–ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell–cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue. Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell-cell and cell-ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell-cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue. The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to understand how cell-generated forces produce cell shape changes and how such forces transmit through a group of adhesive cells in vivo. In this context, we have developed an approach using laser manipulation to impose local forces on cell contacts in the early Drosophila embryo. Quantification of local and global shape changes using our approach can both provide direct measurements of the forces acting at cell contacts and delineate the time-dependent viscoelastic properties of the tissue. The latter provides an explicit relationship, the so-called constitutive law, between forces and deformations. Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell–cell and cell–ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell–cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue. Significance The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to understand how cell-generated forces produce cell shape changes and how such forces transmit through a group of adhesive cells in vivo. In this context, we have developed an approach using laser manipulation to impose local forces on cell contacts in the early Drosophila embryo. Quantification of local and global shape changes using our approach can both provide direct measurements of the forces acting at cell contacts and delineate the time-dependent viscoelastic properties of the tissue. The latter provides an explicit relationship, the so-called constitutive law, between forces and deformations. Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell–cell and cell–ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell–cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue. Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell–cell and cell–ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the earlyDrosophilaembryo. We show that optical trapping can efficiently deform cell–cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue. |
Author | Lenne, Pierre-François Blanc, Olivier Chardè, Claires Bambardekar, Kapil Clément, Raphaël |
Author_xml | – sequence: 1 givenname: Kapil surname: Bambardekar fullname: Bambardekar, Kapil – sequence: 2 givenname: Raphaël surname: Clément fullname: Clément, Raphaël – sequence: 3 givenname: Olivier surname: Blanc fullname: Blanc, Olivier – sequence: 4 givenname: Claires surname: Chardè fullname: Chardè, Claires – sequence: 5 givenname: Pierre-François surname: Lenne fullname: Lenne, Pierre-François |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25605934$$D View this record in MEDLINE/PubMed https://hal.science/hal-01428952$$DView record in HAL |
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ContentType | Journal Article |
Copyright | Volumes 1–89 and 106–112, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Feb 3, 2015 Distributed under a Creative Commons Attribution 4.0 International License |
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Keywords | optical tweezers tissue morphogenesis Myosin-II cell mechanics light-sheet microscopy |
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Notes | http://dx.doi.org/10.1073/pnas.1418732112 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PMCID: PMC4321260 Author contributions: P.-F.L. designed research; K.B., R.C., O.B., and C.C. performed research; R.C., O.B., and C.C. contributed new reagents/analytic tools; K.B., R.C., O.B., C.C., and P.-F.L. analyzed data; R.C. and P.-F.L. wrote the paper; O.B. and C.C. contributed new instrumentation; O.B. performed the initial experiments; and R.C. developed the model. 1K.B. and R.C. contributed equally to this work. Edited by Eric F. Wieschaus, Princeton University, Princeton, NJ, and approved December 22, 2014 (received for review October 1, 2014) |
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Snippet | Significance The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to... Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell–cell... Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell-cell... Significance The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to... The shaping of tissues and organs relies on the ability of cells to adhere together and deform in a coordinated manner. It is, therefore, key to understand how... |
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SubjectTerms | Animals Biological Sciences Cell Communication Cells Cellular Biology Cytoskeleton Drosophila - embryology Insects Lasers Life Sciences Optical Tweezers Tissues |
Title | Direct laser manipulation reveals the mechanics of cell contacts in vivo |
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