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Cardiovascular Development Cardiovascular Development Handout for “Developmental Biology” Dawei W Dong Learning goals 1. explain the early development of the cardiac tube from visceral mesoderm ahead of the neural plate which is then folded beneath the pharynx of the head fold. 2. outline the fusion of the cardiac tube to form the simple linear heart, the segmentation and the loop formation with sinus venosus, atrium, ventricle, bulbus cordis, and truncus arteriosus. 3. show how septum formation in the primitive heart allows separate pumping of blood into the aortic and the pulmonary trunk. 4. describe the heart inlet separation through the incorporation of the sinus venosus and the pulmonary veins into the atrium. 5. understand the developmental process by which the conus cordis and truncus arteriosus are adapted to give the aortic and pulmonary trunk, i.e., the heart outlet separation. 6. describe the three periods of blood cell formation related to the yolk sac, the liver and the bone marrow. 7. define the three circulatory arcs of the heart to/from the body tissues, the yolk sac (vitelline) and the allantois (umbilical), describe their functions, and understand devel- opmental changes of the arterial and venous systems, in particular, the left and right symmetry breaking. 8. understand the changes of the circulation at birth. Quiz Please test yourself with the quizzes at the end. It does not cover everything, but should give you some hints at how well you have learned the subject. 1 Cardiovascular Development Dawei W Dong 1 Formation and folding of the cardiac tube The cardiac development is specified through BMP signalling originating from the under- lying hypoblast and endoderm. Inhibitory signals from the neural tube (Wnt) prevent the formation of cardiogenic fields in the posterior parts of the embryo. In the anterior portion of the embryo, on the contrary, hypoblast and endodermal cells within the developing foregut produce signalling molecules antagonizing the neural tube Wnt signalling, thus enable the cardiac development. The cardiac tube is horsedshoe-shaped and is established in the early gastrula from regions of haemangioblasts in the visceral mesoderm (the cardiogenic field) ahead of the embryo itself (Figure 1). As a result of the head fold, the developing heart ends up beneath the gut tube (Figure 2, 3), the posterior extensions of the tube become anterior and develop into the two ventral aortae, and the anterior of the cardiac tube becomes posterior and fuses with the vitelline veins (Figure 4). The two dorsal aortae form independently from clusters of angioblasts assembled on each side of the midline of the embryo, outside the cardiogenic field. They grow cranial-ventrally to meet the ventral aortae through aortic arches, while fuse caudally. Due to the lateral folding, the posterior portions of the two ventral aortae fuse to produce a single tube. The two ventral aortae connect the anterior end of the tube, the outlet of the heart; while the venous system connects the posterior end of the tube, the inlet of the heart. It is a simple linear pump. Figure 1: A. Dorsal view of a late presomite embryo after removal of the amnion. B. Transverse section to show the position of the blood islands in the lateral splanchnic (vis- ceral) mesoderm layer. C. Cephalocaudal section showing the position of the pericardial cavity and cardiogenic field (Sadler 2006). 2 Segmentation and loop formation of the heart The fused cardiac tube expands, some parts faster than others, resulting segmented tube with dilatations separated by indentations (Figure 4). In anterior-posterior order, the dilatations 2 Cardiovascular Development Dawei W Dong Figure 2: Sequential stages in the cranial-caudal folding of the embryo (Sadler 2006). are the truncus arteriosus, the bulbus cordis, the ventricle, the atrium, and the sinus venosus (Figure 5, 6). At first, the sinus venosus and the atrium are not enclosed within the pericardium cavity, but because the cardiac tube outgrows the pericardial cavity, and because the tube is fixed in the pericardium at both ends, the tube becomes U-shaped with the loop of U pointing ventrally, i.e., the “bulboventricular loop”, which draws the atrium and the sinus venosus into the pericardial cavity. Figure 3: The sagittal (left), frontal (center) and transverse (right) views of the scanning electron micrographs of the mouse embryo at gestation day 8. The cranial-caudal folding of the embryo (left and center): the heart (green) folds under the pharynx (pink). The lateral folding of the embryo (right): A: aortae (dorsal); G: gut tube; C: intraembryonic cavity (coelem); Sp: splanchnic (visceral) mesoderm; So: somatic (parietal) mesoderm. (http://www.med.unc.edu/embryo images/). Continued cardiac growth results in the atrium occupying a position dorsal and slightly rostral to the bulbus cordis and the ventricle and it expands toward the truncus arteriosus, 3 Cardiovascular Development Dawei W Dong which connects to the dorsal aortae through the aortic arches. At this time, the heart becomes S-shaped, with the sinus venosus and the atrium as the first loop of S and the ventricle and the bulbus cordis as the second loop of S. Figure 4: Stages in the formation of the heart from the cardiac tube stage to the devel- opment of an U-shaped structure (McGeady etal 2006). 4 Cardiovascular Development Dawei W Dong Figure 5: Dorso-ventral and left lateral views of sequential stages in the segmentation and the S-shaped loop formation of the cardiac tube (McGeady etal 2006). Figure 6: The frontal (on the left) and side (on the right) view of the scanning electron micrographs of the mouse embryo at gestation day 9. The atrium (purple) is dorsal and slightly rostral to the ventricle (pink). (http://www.med.unc.edu/embryo images/). 3 Partitioning of the heart into four chambers To circulate blood to the body and the lungs separately, the developing heart is partitioned into four chambers (Figure 7, 10). The septum intermedium grows from endocardial cushions to divide the atrioventricular canal to left and right. The interventricular septum grows near the interventricular sulcus to divide the ventricle and the bulbus cordis into left and right ventricles. This division is not complete at first, leaving interventricular opening (foramen). The interventricular foramen is later closed by 5 Cardiovascular Development Dawei W Dong the membranous interventricular septum, developed from the endocardial cushion, in such a way that both ventricles open into the conus cordis, the remain of the bulbus cordis connecting with truncus arteriosus. Figure 7: Stages in the partitioning of the developing atrium and ventricle, leading to the formation of left and right atria and ventricles. The arrow in F indicates the allowed direction of blood flow through the foramen ovale (McGeady etal 2006). The septum primum divides the common atrium into right and left atria. Initially the foramen primum persists as an opening, but it eventually closes. Before it closes completely, programmed cell death results in the foramen secundum. A second membrane—the septum secundum arises from the dorsal right atrium and extends to the septum intermedium but does not reach. The resulting opening is the foramen ovale. Because the foramen secundum is stiffer than the foramen primum (also see Figure 8), when blood pressure is higher in the right atrium, the blood flows into the left atrium, but not the other way around. 6 Cardiovascular Development Dawei W Dong 4 Division of the heart inlet The two horns of the sinus vernosus, i.e., the inlets from the right and left veins, have very different ends in the development. The left horn eventually develops into the coronary sinus. The right horn is favoured and incorporated into the right atrium, and also forms part of the cranial and caudal vena cava (Figure 8). The pulmonary veins are incorporated into the left atrium. Figure 8: Incorporation of the right sinus horn and the pulmonary veins into the atrium at two stages of development (A, B). 1: Opening of right sinus horn into the atrium; 2: Opening of the pulmonary veins into the atrium; 3: Septum primum; 4: Foramen pri- mum; 5: Incorporated portion of right sinus horn; 6: Incorporated portion of pulmonary veins; 7: Right atrium; 8: Left atrium; 9: Opening to caudal vena cava; 10: Opening to cranial vena cava; 11: Septum secundum; 12: Foramen secundum; 13: Foramen ovale. Modified from Hyttel etal 2010. 7 Cardiovascular Development Dawei W Dong 5 Division of the heart outlet The conus cordis and the truncus arteriosus are divided by growing pair of cushions from their walls to form aorticopulmonary septum. The outlet rotates 180 degrees, such that the aortic trunk on the right at the top is linked down to the left ventricle and the pulmonary trunk on the left at the top is link down to the right ventricle (Figure 9, 10). Figure 9: Partitioning of the concus cordis and truncus arteriosus into the aortic and pul- monary truncks respectively, A and B. The spiral arrangement and the final relationship is also shown in C (McGeady etal 2006). 8 Cardiovascular Development Dawei W Dong Figure 10: The scanning electron micrographs of the mouse embryo: left, the frontal section of the heart (gestation day 10) shows that blood from the atrium (purple) passes to the ventricle (pink) by the atrioventricular canal (red arrow) and the beginnings of interatrial septum formation can be seen (A); right, the transverse section of the truncus arteriosus (gestation day 12) shows that cushions (green) formed within the truncus arteriosus will fuse to form the aortico-pulmonary septum separating the aortic (red) and pulmonary (blue) flows. (http://www.med.unc.edu/embryo images/). 6 Formation of blood cells The formation of blood cells, haematopoiesis, occurs in three overlapping periods (Figure 11): Figure 11: Three periods of blood cell formation.
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