Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic Geometry

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 dri...

Full description

Bibliographic Details
Main Authors: Yunfei eShi, Jiang eYao, Jonathan M Young, Judy A Fee, Renato ePerucchio, Larry A Taber
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-08-01
Series:Frontiers in Physiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fphys.2014.00297/full
id doaj-05e6afb64bb045688bbae1dd08201ad1
record_format Article
spelling doaj-05e6afb64bb045688bbae1dd08201ad12020-11-24T23:48:06ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2014-08-01510.3389/fphys.2014.0029799230Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic GeometryYunfei eShi0Jiang eYao1Jonathan M Young2Judy A Fee3Renato ePerucchio4Larry A Taber5Washington UniversityDassault Systemes Simulia Corp.L-3 Applied TechnologiesWashington UniversityUniversity of RochesterWashington UniversityThe 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 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 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.http://journal.frontiersin.org/Journal/10.3389/fphys.2014.00297/fullBiomechanicsChick EmbryoMorphogenesisfinite-element modelingCardiac Looping
collection DOAJ
language English
format Article
sources DOAJ
author Yunfei eShi
Jiang eYao
Jonathan M Young
Judy A Fee
Renato ePerucchio
Larry A Taber
spellingShingle Yunfei eShi
Jiang eYao
Jonathan M Young
Judy A Fee
Renato ePerucchio
Larry A Taber
Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic Geometry
Frontiers in Physiology
Biomechanics
Chick Embryo
Morphogenesis
finite-element modeling
Cardiac Looping
author_facet Yunfei eShi
Jiang eYao
Jonathan M Young
Judy A Fee
Renato ePerucchio
Larry A Taber
author_sort Yunfei eShi
title Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic Geometry
title_short Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic Geometry
title_full Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic Geometry
title_fullStr Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic Geometry
title_full_unstemmed Bending and Twisting the Embryonic Heart: A Computational Model for C-Looping Based on Realistic Geometry
title_sort bending and twisting the embryonic heart: a computational model for c-looping based on realistic geometry
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2014-08-01
description 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 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 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.
topic Biomechanics
Chick Embryo
Morphogenesis
finite-element modeling
Cardiac Looping
url http://journal.frontiersin.org/Journal/10.3389/fphys.2014.00297/full
work_keys_str_mv AT yunfeieshi bendingandtwistingtheembryonicheartacomputationalmodelforcloopingbasedonrealisticgeometry
AT jiangeyao bendingandtwistingtheembryonicheartacomputationalmodelforcloopingbasedonrealisticgeometry
AT jonathanmyoung bendingandtwistingtheembryonicheartacomputationalmodelforcloopingbasedonrealisticgeometry
AT judyafee bendingandtwistingtheembryonicheartacomputationalmodelforcloopingbasedonrealisticgeometry
AT renatoeperucchio bendingandtwistingtheembryonicheartacomputationalmodelforcloopingbasedonrealisticgeometry
AT larryataber bendingandtwistingtheembryonicheartacomputationalmodelforcloopingbasedonrealisticgeometry
_version_ 1725487270684786688