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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

Cardiac c-looping in chick embryo. (A–C) SEM images of embryonic chick hearts during c-looping (ventral view). (Reprinted from Shi et al., 2014 with permission of ASME.) The originally straight heart tube (HT) at HH10 in (A) bends ventrally and rotates rightward, transforming into a c-shaped tube at HH12 in (C). Note that artificial labels (red dots) along the ventral midline of the HT at HH10 move to the outer curvature of the HH12 heart. (A′–C′) Rotation of the HT is shown by the orientation of the elliptical lumen (red arrowheads) in OCT cross sections taken midway along the length of the HT [yellow dashed lines in (A–C)]. AIP, anterior intestinal portal; AT, atrium; CJ, cardiac jelly; CT, conotruncus; DM, dorsal mesocardium; EN, endocardium; IC, inner curvature; LU, lumen; MY, myocardium; OC, outer curvature; OV, omphalomesenteric vein; SPL, splanchnopleure; VE, ventricle. Scale bars: 200 μm. Yellow arrows indicate the annotated anatomic structures.
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Figure 1: Cardiac c-looping in chick embryo. (A–C) SEM images of embryonic chick hearts during c-looping (ventral view). (Reprinted from Shi et al., 2014 with permission of ASME.) The originally straight heart tube (HT) at HH10 in (A) bends ventrally and rotates rightward, transforming into a c-shaped tube at HH12 in (C). Note that artificial labels (red dots) along the ventral midline of the HT at HH10 move to the outer curvature of the HH12 heart. (A′–C′) Rotation of the HT is shown by the orientation of the elliptical lumen (red arrowheads) in OCT cross sections taken midway along the length of the HT [yellow dashed lines in (A–C)]. AIP, anterior intestinal portal; AT, atrium; CJ, cardiac jelly; CT, conotruncus; DM, dorsal mesocardium; EN, endocardium; IC, inner curvature; LU, lumen; MY, myocardium; OC, outer curvature; OV, omphalomesenteric vein; SPL, splanchnopleure; VE, ventricle. Scale bars: 200 μm. Yellow arrows indicate the annotated anatomic structures.

Mentions: When it is first created in the chick embryo at stage HH10 of Hamburger and Hamilton (1951), the heart is a relatively straight tube consisting of an outer layer of myocardium, a middle layer of matrix called cardiac jelly (CJ), and an inner layer of endocardium (Figures 1A,A′). The HT is connected caudally to the omphalomesenteric veins (OVs), cranially to the conotruncus (outflow tract), and dorsally to the dorsal mesocardium (DM), which attaches the entire length of the HT to the foregut. In addition, the splanchnopleuric membrane (SPL) presses against the ventral side of the HT and wraps around the caudal sides of the OVs at the anterior intestinal portal (AIP) (Männer, 2000; Taber, 2006).


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)

Cardiac c-looping in chick embryo. (A–C) SEM images of embryonic chick hearts during c-looping (ventral view). (Reprinted from Shi et al., 2014 with permission of ASME.) The originally straight heart tube (HT) at HH10 in (A) bends ventrally and rotates rightward, transforming into a c-shaped tube at HH12 in (C). Note that artificial labels (red dots) along the ventral midline of the HT at HH10 move to the outer curvature of the HH12 heart. (A′–C′) Rotation of the HT is shown by the orientation of the elliptical lumen (red arrowheads) in OCT cross sections taken midway along the length of the HT [yellow dashed lines in (A–C)]. AIP, anterior intestinal portal; AT, atrium; CJ, cardiac jelly; CT, conotruncus; DM, dorsal mesocardium; EN, endocardium; IC, inner curvature; LU, lumen; MY, myocardium; OC, outer curvature; OV, omphalomesenteric vein; SPL, splanchnopleure; VE, ventricle. Scale bars: 200 μm. Yellow arrows indicate the annotated anatomic structures.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Cardiac c-looping in chick embryo. (A–C) SEM images of embryonic chick hearts during c-looping (ventral view). (Reprinted from Shi et al., 2014 with permission of ASME.) The originally straight heart tube (HT) at HH10 in (A) bends ventrally and rotates rightward, transforming into a c-shaped tube at HH12 in (C). Note that artificial labels (red dots) along the ventral midline of the HT at HH10 move to the outer curvature of the HH12 heart. (A′–C′) Rotation of the HT is shown by the orientation of the elliptical lumen (red arrowheads) in OCT cross sections taken midway along the length of the HT [yellow dashed lines in (A–C)]. AIP, anterior intestinal portal; AT, atrium; CJ, cardiac jelly; CT, conotruncus; DM, dorsal mesocardium; EN, endocardium; IC, inner curvature; LU, lumen; MY, myocardium; OC, outer curvature; OV, omphalomesenteric vein; SPL, splanchnopleure; VE, ventricle. Scale bars: 200 μm. Yellow arrows indicate the annotated anatomic structures.
Mentions: When it is first created in the chick embryo at stage HH10 of Hamburger and Hamilton (1951), the heart is a relatively straight tube consisting of an outer layer of myocardium, a middle layer of matrix called cardiac jelly (CJ), and an inner layer of endocardium (Figures 1A,A′). The HT is connected caudally to the omphalomesenteric veins (OVs), cranially to the conotruncus (outflow tract), and dorsally to the dorsal mesocardium (DM), which attaches the entire length of the HT to the foregut. In addition, the splanchnopleuric membrane (SPL) presses against the ventral side of the HT and wraps around the caudal sides of the OVs at the anterior intestinal portal (AIP) (Männer, 2000; Taber, 2006).

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