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Bending and twisting the embryonic heart: a computational model for c-looping based on realistic geometry.

Shi Y, Yao J, Young JM, Fee JA, Perucchio R, Taber LA - Front Physiol (2014)

Bottom Line: The behavior of the model is in reasonable agreement with available experimental data from control and perturbed embryos, offering support for our hypothesis.The results also suggest, however, that several other mechanisms contribute secondarily to normal looping, and we speculate that these mechanisms play backup roles when looping is perturbed.Finally, some outstanding questions are discussed for future study.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, Washington University St. Louis, MO, USA.

ABSTRACT
The morphogenetic process of cardiac looping transforms the straight heart tube into a curved tube that resembles the shape of the future four-chambered heart. Although great progress has been made in identifying the molecular and genetic factors involved in looping, the physical mechanisms that drive this process have remained poorly understood. Recent work, however, has shed new light on this complicated problem. After briefly reviewing the current state of knowledge, we propose a relatively comprehensive hypothesis for the mechanics of the first phase of looping, termed c-looping, as the straight heart tube deforms into a c-shaped tube. According to this hypothesis, differential hypertrophic growth in the myocardium supplies the main forces that cause the heart tube to bend ventrally, while regional growth and cytoskeletal contraction in the omphalomesenteric veins (primitive atria) and compressive loads exerted by the splanchnopleuric membrane drive rightward torsion. A computational model based on realistic embryonic heart geometry is used to test the physical plausibility of this hypothesis. The behavior of the model is in reasonable agreement with available experimental data from control and perturbed embryos, offering support for our hypothesis. The results also suggest, however, that several other mechanisms contribute secondarily to normal looping, and we speculate that these mechanisms play backup roles when looping is perturbed. Finally, some outstanding questions are discussed for future study.

No MeSH data available.


Related in: MedlinePlus

Rotation of heart tube during c-looping. (A) Rotation angle α is defined as the angle between the long axis of the elliptical lumen and the embryonic dorsal-ventral axis in a cross section located at the middle of the heart tube (CJ, cardiac jelly; DM, dorsal mesocardium; MY, myocardium). (B) Plot of rotation angle given by baseline model and experimental measurements as function of developmental stage.
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Figure 5: Rotation of heart tube during c-looping. (A) Rotation angle α is defined as the angle between the long axis of the elliptical lumen and the embryonic dorsal-ventral axis in a cross section located at the middle of the heart tube (CJ, cardiac jelly; DM, dorsal mesocardium; MY, myocardium). (B) Plot of rotation angle given by baseline model and experimental measurements as function of developmental stage.

Mentions: To quantify torsion, we measured the rotation angle α of the HT in embryos cultured for 6 h from HH10- (Figure 5). The rotation angle increased as looping progressed, with most rotation occurring between HH10 (α = 18.0 ± 6.5 deg) and HH11 (α = 62.5 ± 10.8 deg; n = 5) (Figure 5B). The temporal plot of rotation angle given by our baseline model agrees with the experimental trend reasonably well (Figure 5B).


Bending and twisting the embryonic heart: a computational model for c-looping based on realistic geometry.

Shi Y, Yao J, Young JM, Fee JA, Perucchio R, Taber LA - Front Physiol (2014)

Rotation of heart tube during c-looping. (A) Rotation angle α is defined as the angle between the long axis of the elliptical lumen and the embryonic dorsal-ventral axis in a cross section located at the middle of the heart tube (CJ, cardiac jelly; DM, dorsal mesocardium; MY, myocardium). (B) Plot of rotation angle given by baseline model and experimental measurements as function of developmental stage.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4129494&req=5

Figure 5: Rotation of heart tube during c-looping. (A) Rotation angle α is defined as the angle between the long axis of the elliptical lumen and the embryonic dorsal-ventral axis in a cross section located at the middle of the heart tube (CJ, cardiac jelly; DM, dorsal mesocardium; MY, myocardium). (B) Plot of rotation angle given by baseline model and experimental measurements as function of developmental stage.
Mentions: To quantify torsion, we measured the rotation angle α of the HT in embryos cultured for 6 h from HH10- (Figure 5). The rotation angle increased as looping progressed, with most rotation occurring between HH10 (α = 18.0 ± 6.5 deg) and HH11 (α = 62.5 ± 10.8 deg; n = 5) (Figure 5B). The temporal plot of rotation angle given by our baseline model agrees with the experimental trend reasonably well (Figure 5B).

Bottom Line: The behavior of the model is in reasonable agreement with available experimental data from control and perturbed embryos, offering support for our hypothesis.The results also suggest, however, that several other mechanisms contribute secondarily to normal looping, and we speculate that these mechanisms play backup roles when looping is perturbed.Finally, some outstanding questions are discussed for future study.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, Washington University St. Louis, MO, USA.

ABSTRACT
The morphogenetic process of cardiac looping transforms the straight heart tube into a curved tube that resembles the shape of the future four-chambered heart. Although great progress has been made in identifying the molecular and genetic factors involved in looping, the physical mechanisms that drive this process have remained poorly understood. Recent work, however, has shed new light on this complicated problem. After briefly reviewing the current state of knowledge, we propose a relatively comprehensive hypothesis for the mechanics of the first phase of looping, termed c-looping, as the straight heart tube deforms into a c-shaped tube. According to this hypothesis, differential hypertrophic growth in the myocardium supplies the main forces that cause the heart tube to bend ventrally, while regional growth and cytoskeletal contraction in the omphalomesenteric veins (primitive atria) and compressive loads exerted by the splanchnopleuric membrane drive rightward torsion. A computational model based on realistic embryonic heart geometry is used to test the physical plausibility of this hypothesis. The behavior of the model is in reasonable agreement with available experimental data from control and perturbed embryos, offering support for our hypothesis. The results also suggest, however, that several other mechanisms contribute secondarily to normal looping, and we speculate that these mechanisms play backup roles when looping is perturbed. Finally, some outstanding questions are discussed for future study.

No MeSH data available.


Related in: MedlinePlus