The endoderm and myocardium join forces to drive early heart tube assembly

Aleksandrova, Anastasiia; Czirók, András; Kosa, Edina; Galkin, A. Yu.; Cheuvront, Tracey; Rongish, Brenda J.

doi:10.1016/j.ydbio.2015.04.016

Cited by 35 publications

(52 citation statements)

References 35 publications

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“…Earlier studies in chick suggested that myocardial cells have little ability to migrate, and that endoderm movement drives their migration (Cui et al, 2009;Varner and Taber, 2012). However, a new study showed that chick myocardial cells instead exhibit active displacement and autonomous ventral movement, and that these changes are independent of the endoderm (Aleksandrova et al, 2015). It is thus possible that the ventral movement of these cells in chick is similar to the myocardial subduction we observed in zebrafish.…”

Section: Myocardial Cells Engage In Subduction During Their Medial MImentioning

confidence: 62%

Endoderm convergence controls subduction of the myocardial precursors during heart-tube formation

Ding

Xie

et al. 2015

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Coordination between the endoderm and adjacent cardiac mesoderm is crucial for heart development. We previously showed that myocardial migration is promoted by convergent movement of the endoderm, which itself is controlled by the S1pr2/Gα 13 signaling pathway, but it remains unclear how the movements of the two tissues is coordinated. Here, we image live and fixed embryos to follow these movements, revealing previously unappreciated details of strikingly complex and dynamic associations between the endoderm and myocardial precursors. We found that during segmentation the endoderm underwent three distinct phases of movement relative to the midline: rapid convergence, little convergence and slight expansion. During these periods, the myocardial cells exhibited different stage-dependent migratory modes: co-migration with the endoderm, movement from the dorsal to the ventral side of the endoderm (subduction) and migration independent of endoderm convergence. We also found that defects in S1pr2/Gα 13 -mediated endodermal convergence affected all three modes of myocardial cell migration, probably due to the disruption of fibronectin assembly around the myocardial cells and consequent disorganization of the myocardial epithelium. Moreover, we found that additional cell types within the anterior lateral plate mesoderm (ALPM) also underwent subduction, and that this movement likewise depended on endoderm convergence. Our study delineates for the first time the details of the intricate interplay between the endoderm and ALPM during embryogenesis, highlighting why endoderm movement is essential for heart development, and thus potential underpinnings of congenital heart disease.

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Section: Myocardial Cells Engage In Subduction During Their Medial MImentioning

confidence: 62%

Endoderm convergence controls subduction of the myocardial precursors during heart-tube formation

Ding

Xie

et al. 2015

Development

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“…regression of the anterior intestinal portal) ( Fig. 2A) (Aleksandrova et al, 2015a;Varner and Taber, 2012). Time-lapse recordings show that as the myocardial progenitor fields approach the midline, the cells autonomously exert mechanical stresses within the tissue (Aleksandrova et al, 2015a).…”

Section: Tissue-scale Motion During Amniote Organogenesis Heart Formamentioning

confidence: 99%

“…Inevitably, cell fatemapping studies in which only cell motion is tracked cannot reveal large-scale composite tissue motion, much less the actual degree of cell-autonomous motility. This is primarily because conventional cell motion tracking studies do not employ the wide mesoscale vantage point needed to unravel large-scale tissue deformations spanning multiple germ layers (Aleksandrova et al, 2015a), and because standard image processing algorithms do not quantify either cellular versus tissue motion or the overall motion of the tissue environment, i.e. cells plus their filamentous ECM scaffold (Zamir et al, 2005).…”

Section: Tissue-scale Motion Includes Ecm Dynamicsmentioning

confidence: 99%

“…Computational tools allow the determination of cell-autonomous motility independent of large tissue-scale displacements. Accordingly, ECM dynamics can be quantified, not only during early embryogenesis Zamir et al, 2006Zamir et al, , 2008 but also during organogenesis (Aleksandrova et al, 2015a(Aleksandrova et al, , 2012, as discussed further below.…”

Section: Box 1 Extracting Tissue Motion From Image Sequencesmentioning

confidence: 99%

“…with their surrounding ECM). Thus, the movements of both the endocardial and myocardial precursors are due mainly to large-scale tissue deformation, and not classically defined cell migration (Aleksandrova et al, 2015a). …”

Section: Tissue-scale Motion During Amniote Organogenesis Heart Formamentioning

confidence: 99%

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Extracellular matrix motion and early morphogenesis

et al. 2016

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For over a century, embryologists who studied cellular motion in early amniotes generally assumed that morphogenetic movement reflected migration relative to a static extracellular matrix (ECM) scaffold. However, as we discuss in this Review, recent investigations reveal that the ECM is also moving during morphogenesis. Time-lapse studies show how convective tissue displacement patterns, as visualized by ECM markers, contribute to morphogenesis and organogenesis. Computational image analysis distinguishes between cell-autonomous (active) displacements and convection caused by large-scale (composite) tissue movements. Modern quantification of large-scale 'total' cellular motion and the accompanying ECM motion in the embryo demonstrates that a dynamic ECM is required for generation of the emergent motion patterns that drive amniote morphogenesis.

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Guiding Cell Network Assembly using Shape‐Morphing Hydrogels

et al. 2020

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Forces and relative movement between cells and extracellular matrix (ECM) are crucial to the self‐organization of tissues during development. However, the spatial range over which these dynamics can be controlled in engineering approaches is limited, impeding progress toward the construction of large, structurally mature tissues. Herein, shape‐morphing materials called “kinomorphs” that rationally control the shape and size of multicellular networks are described. Kinomorphs are sheets of ECM that change their shape, size, and density depending on patterns of cell contractility within them. It is shown that these changes can manipulate structure‐forming behaviors of epithelial cells in many spatial locations at once. Kinomorphs are built using a new photolithographic technology to pattern single cells into ECM sheets that are >10× larger than previously described. These patterns are designed to partially mimic the branch geometry of the embryonic kidney epithelial network. Origami‐inspired simulations are then used to predict changes in kinomorph shapes. Last, kinomorph dynamics are shown to provide a centimeter‐scale program that sets specific spatial locations in which ≈50 µm‐diameter epithelial tubules form by cell coalescence and structural maturation. The kinomorphs may significantly advance organ‐scale tissue construction by extending the spatial range of cell self‐organization in emerging model systems such as organoids.

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The endoderm and myocardium join forces to drive early heart tube assembly

Cited by 35 publications

References 35 publications

Endoderm convergence controls subduction of the myocardial precursors during heart-tube formation

Endoderm convergence controls subduction of the myocardial precursors during heart-tube formation

Extracellular matrix motion and early morphogenesis

Guiding Cell Network Assembly using Shape‐Morphing Hydrogels

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