Myosin-based contraction is not necessary for cardiac c-looping in the chick embryo

Rémond, Mathieu C.; Fee, Judy A.; Elson, Elliot L.; Taber, Larry A.

doi:10.1007/s00429-006-0094-0

Cited by 25 publications

(49 citation statements)

References 44 publications

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“…The first observation is consistent with recent evidence showing that c-looping does not require contraction (Rémond et al, 2006). Recently, Latacha et al (2005) suggested that actin polymerization drives the bending component of c-looping.…”

Section: Increased Heart Stiffness Is Caused By Cytoskeletal Contractionsupporting

confidence: 87%

“…In embryos cultured with the SPL intact, looping was unaffected by exposure to the drug (Fig. 5A-C), corroborating recent evidence from our laboratory that nonmuscle myosin II is not necessary for normal c-looping (Rémond et al, 2006). In hearts where the SPL was removed, however, exposure to Y-27632 resulted in ventral (and some rightward) bending, but little or no rotation (Fig.…”

Section: Asymmetric Cytoskeletal Contraction Drives Delayed Cardiac Tsupporting

confidence: 87%

“…As shown by Latacha et al [2005], the presence of extracardiac tissue requires a higher drug concentration to obtain the effects seen in isolated hearts. We have also confirmed that cytoskeletal architecture remains unaffected at this concentration [Rémond et al, 2006]). Torsion was visualized through the motions of fluorescent labels in the myocardium.…”

Section: Asymmetric Cytoskeletal Contraction Drives Delayed Cardiac Tsupporting

confidence: 74%

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Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads

Nerurkar

Ramasubramanian

Taber

2006

Developmental Dynamics

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The biophysical mechanisms that drive and regulate cardiac looping are not well understood, but mechanical forces likely play a central role. Previous studies have shown that cardiac torsion, which defines left-right directionality, is caused largely by forces exerted on the heart tube by a membrane called the splanchnopleure (SPL). Here we show that, when the SPL is removed from the embryonic chick heart, torsion is initially suppressed. Several hours later, however, normal torsion is restored. This delayed torsion coincides with increased myocardial stiffness, especially on the right side of the heart. Exposure to the myosin inhibitor Y-27632 suppressed both responses, suggesting that the delayed torsion is caused by an abnormal cytoskeletal contraction. This hypothesis is supported further by computational modeling. These results suggest that the looping embryonic heart has the ability to adapt to changes in the mechanical environment, which may play a regulatory role during morphogenesis.

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Section: Increased Heart Stiffness Is Caused By Cytoskeletal Contractionsupporting

confidence: 87%

Section: Asymmetric Cytoskeletal Contraction Drives Delayed Cardiac Tsupporting

confidence: 87%

Section: Asymmetric Cytoskeletal Contraction Drives Delayed Cardiac Tsupporting

confidence: 74%

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Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads

Nerurkar

Ramasubramanian

Taber

2006

Developmental Dynamics

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“…They concluded, however, that the observed heart and foregut defects were not due to a lack of contractility, as treatment with the myosin light chain kinase (MLCK) inhibitor ML-9 did not reproduce the observed abnormalities. Previous work in our laboratory, however, has shown that the similar but more specific MLCK inhibitor ML-7 (Bain et al, 2003) did not significantly reduce either myosin regulatory light chain phosphorylation or tissue stiffness in looping chick hearts (Rémond et al, 2006). It is thus possible that ML-9 did not completely suppress cytoskeletal contraction, and that cardia bifida produced by treatment with Y27632 was (at least in part) due to attenuated contraction.…”

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confidence: 81%

Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly

Varner

Taber

2012

Development

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SUMMARYThe heart is the first functioning organ to form during development. During gastrulation, the cardiac progenitors reside in the lateral plate mesoderm but maintain close contact with the underlying endoderm. In amniotes, these bilateral heart fields are initially organized as a pair of flat epithelia that move towards the embryonic midline and fuse above the anterior intestinal portal (AIP) to form the heart tube. This medial motion is typically attributed to active mesodermal migration over the underlying endoderm. In this model, the role of the endoderm is twofold: to serve as a mechanically passive substrate for the crawling mesoderm and to secrete various growth factors necessary for cardiac specification and differentiation. Here, using computational modeling and experiments on chick embryos, we present evidence supporting an active mechanical role for the endoderm during heart tube assembly. Label-tracking experiments suggest that active endodermal shortening around the AIP accounts for most of the heart field motion towards the midline. Results indicate that this shortening is driven by cytoskeletal contraction, as exposure to the myosin-II inhibitor blebbistatin arrested any shortening and also decreased both tissue stiffness (measured by microindentation) and mechanical tension (measured by cutting experiments). In addition, blebbistatin treatment often resulted in cardia bifida and abnormal foregut morphogenesis. Moreover, finite element simulations of our cutting experiments suggest that the endoderm (not the mesoderm) is the primary contractile tissue layer during this process. Taken together, these results indicate that contraction of the endoderm actively pulls the heart fields towards the embryonic midline, where they fuse to form the heart tube. KEY WORDS: Biomechanics, Chick embryo, Computational modeling, Endoderm, Heart development, MorphogenesisNot just inductive: a crucial mechanical role for the endoderm during heart tube assembly Victor D. Varner and Larry A. Taber* DEVELOPMENT of liquid culture media and incubated at 38°C in 95% O 2 and 5% CO 2 . This method prevents artifacts caused by fluid surface tension, which alter the mechanical stresses in the embryo (Voronov and Taber, 2002).In some experiments, embryos were cultured in 100 M (-)-blebbistatin (Sigma, St Louis, MO, USA) to broadly suppress any cytoskeletal contraction dependent on myosin II. The inhibitor could be washed out by rinsing the embryo several times in PBS and then continuing the culture with new blebbistatin-free media. Injection labeling and trackingTo measure tissue motion in both the endoderm and mesoderm around the AIP, small groups of cells (in both germ layers) were labeled at HH stage 7+/8-with the lipophilic fluorescent dye DiI (Molecular Probes, Eugene, OR, USA) mixed in a 20% sucrose solution. DiI injections were made using pulled glass micropipettes and a pneumatic pump (PicoPump PV830, World Precision Instruments). To label cardiogenic mesoderm, the tip of the injection pipette was first pierced thr...

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“…Moreover, the disruption of myosin-based tension generation with a ROCK inhibitor during the initial stages of heart looping disturbs morphogenesis in this system (Wei et al, 2002); however, tension inhibitors do not interfere with heart looping in chicks, so the conservation of this mechanism remains uncertain (Remond et al, 2006). In rats, the heart also alters its stiffness according to its developmental stage by changing the isoform ratios of the cytoskeletal protein titin, the elastic properties of which influence the physical compliance of heart tissue (Lahmers et al, 2004).…”

Section: Organogenesismentioning

confidence: 99%

Mechanical control of tissue and organ development

2010

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Many genes and molecules that drive tissue patterning during organogenesis and tissue regeneration have been discovered. Yet, we still lack a full understanding of how these chemical cues induce the formation of living tissues with their unique shapes and material properties. Here, we review work based on the convergence of physics, engineering and biology that suggests that mechanical forces generated by living cells are as crucial as genes and chemical signals for the control of embryological development, morphogenesis and tissue patterning. Key words: Cytoskeleton, Mechanical signaling, Morphogenesis, Pattern formation, Tension IntroductionWe now know many genes, morphogens and signaling molecules that govern tissue genesis. However, we do not fully understand how these chemical cues drive the formation of living tissues and organs with specialized forms and unique physical properties (e.g. rigidity, elastic recoil or viscoelasticity) required to pump blood, withstand repetitive movements or lift our bodies up against the force of gravity. A century ago, much of developmental control was explained in mechanical terms. In his classic treatise On Growth and Form, D'Arcy Thompson described how patterns are "diagrams of underlying forces" (Thompson, 1917). This is because a change in the three-dimensional (3D) shape of any structure, including living cells and tissues, must, at some level, result from the action of a force acting on a mass. Although this view was pushed aside by the advance of molecular biology, the relationship between physicality and developmental control is now coming into focus once again as a result of powerful new alliances between biologists, geneticists, engineers and physicists. This interdisciplinary approach has led to the discovery of fundamental links between mechanical forces, molecular biochemistry, gene expression and tissue patterning that drive embryogenesis and play a central role in morphogenesis and tissue maintenance throughout the life of an organism.In this article, we highlight some of the recent advances in this emerging field of mechanical biology. In particular, we focus on the role of mechanical forces that are generated in the contractile actin cytoskeleton of living cells and that act on the adhesions of these cells to neighboring cells and to the extracellular matrix (ECM). We describe how both traction forces exerted locally by single cells and more generalized forces (e.g. fluid shear, hydrostatic pressure) resulting from tension generated within the cytoskeletons of large groups of cells in tissues and organs are central to the control of tissue pattern formation during virtually all stages of embryogenesis.We also explore how mechanical signals are converted into changes in intracellular biochemistry and gene expression so that they influence fundamental mechanisms of cell fate determination and morphogenetic control that are also controlled by genes, soluble morphogens and chemical factors. Mechanical forces in early developmentThe shaping of the living embryo...

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Myosin-based contraction is not necessary for cardiac c-looping in the chick embryo

Cited by 25 publications

References 44 publications

Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads

Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads

Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly

Mechanical control of tissue and organ development

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