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Critical transitions in early embryonic aortic arch patterning and hemodynamics.

ABSTRACT: Transformation from the bilaterally symmetric embryonic aortic arches to the mature great vessels is a complex morphogenetic process, requiring both vasculogenic and angiogenic mechanisms. Early aortic arch development occurs simultaneously with rapid changes in pulsatile blood flow, ventricular function, and downstream impedance in both invertebrate and vertebrate species. These dynamic biomechanical environmental landscapes provide critical epigenetic cues for vascular growth and remodeling. In our previous work, we examined hemodynamic loading and aortic arch growth in the chick embryo at Hamburger-Hamilton stages 18 and 24. We provided the first quantitative correlation between wall shear stress (WSS) and aortic arch diameter in the developing embryo, and observed that these two stages contained different aortic arch patterns with no inter-embryo variation. In the present study, we investigate these biomechanical events in the intermediate stage 21 to determine insights into this critical transition. We performed fluorescent dye microinjections to identify aortic arch patterns and measured diameters using both injection recordings and high-resolution optical coherence tomography. Flow and WSS were quantified with 3D computational fluid dynamics (CFD). Dye injections revealed that the transition in aortic arch pattern is not a uniform process and multiple configurations were documented at stage 21. CFD analysis showed that WSS is substantially elevated compared to both the previous (stage 18) and subsequent (stage 24) developmental time-points. These results demonstrate that acute increases in WSS are followed by a period of vascular remodeling to restore normative hemodynamic loading. Fluctuations in blood flow are one possible mechanism that impacts the timing of events such as aortic arch regression and generation, leading to the variable configurations at stage 21. Aortic arch variations noted during normal rapid vascular remodeling at stage 21 identify a temporal window of increased vulnerability to aberrant aortic arch morphogenesis with the potential for profound effects on subsequent cardiovascular morphogenesis.

SUBMITTER: Kowalski WJ

PROVIDER: S-EPMC3605337 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Critical transitions in early embryonic aortic arch patterning and hemodynamics.

Kowalski William J WJ Dur Onur O Wang Yajuan Y Patrick Michael J MJ Tinney Joseph P JP Keller Bradley B BB Pekkan Kerem K

PloS one 20130321 3

Transformation from the bilaterally symmetric embryonic aortic arches to the mature great vessels is a complex morphogenetic process, requiring both vasculogenic and angiogenic mechanisms. Early aortic arch development occurs simultaneously with rapid changes in pulsatile blood flow, ventricular function, and downstream impedance in both invertebrate and vertebrate species. These dynamic biomechanical environmental landscapes provide critical epigenetic cues for vascular growth and remodeling. I ...[more]

PMID: 23555940

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Project description:All embryonic and fetal amniotes possess a ductus(i) arteriosus(i) that allows blood to bypass the pulmonary circulation and the non-functional lungs. The central hemodynamic of embryonic reptiles are unique, given the additional systemic aorta that allows pulmonary circulatory bypass, the left aorta (LAo). The LAo exits in the right ventricle or 'pulmonary side' of reptilian hearts in both embryos and adults, but its functional significance in ovo is unknown. This study investigated the role of the LAo in embryonic American alligators by surgically occluding the LAo and measuring oxygen consumption and, in addition, measured hemodynamic responses to hypoxia in embryonic alligators. We measured systemic cardiac output and primary chorioallantoic membrane (CAM) artery blood flow for normoxic and hypoxic-incubated (10% O(2)) American alligator embryos (Alligator mississippiensis). Chronic blood flow (1-124 h) in the primary CAM artery for hypoxic-incubated embryos (92 ± 26 ml min(-1) kg(-1)) was elevated when compared with normoxic-incubated embryos (29 ± 14 ml min(-1) kg(-1), N = 6; P = 0.039). For hypoxic-incubated embryos, acute LAo blood flow (49.6 ± 24.4 ml min(-1) kg(-1)) was equivalent to the combined flow of the three systemic great vessels that arise from the left ventricle, the right aorta, common carotid and subclavian arteries (43.6 ± 21.5 ml min(-1) kg(-1), N = 5). Similarly, for normoxic-incubated embryos, LAo blood flow (27.3 ± 6.6 ml min(-1) kg(-1)) did not statistically differ from the other three vessels (18.4 ± 4.9 ml min(-1) kg(-1), N = 5). This study contains the first direct test of LAo function and the first measurements of blood flow in an embryonic reptile. These data support the hypotheses that embryonic alligators utilize the LAo to divert a significant amount of right ventricular blood into the systemic circulation, and that CAM blood flow increases following chronic hypoxic conditions. However, surgical occlusion of the LAo did not affect egg V(O) ? supporting the hypothesis that the LAo of reptiles is not critical to maintain in ovo oxygen consumption.

Dataset Information

Critical transitions in early embryonic aortic arch patterning and hemodynamics.

Publications

Critical transitions in early embryonic aortic arch patterning and hemodynamics.

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