Abstract
Information about embryonic development of coronary endothelium is the main clue for the creation of new methods in tissue engineering for treatment of ischemic heart diseases. The purpose of the research was to describe human coronary vessels development on early stages of the prenatal ontogenesis. The first step in human coronary vessels development is the formation of endothelium de novo by transformation of some epicardial and, possibly, endocardial cells. The next step is the ingrowth of sinus venosus endothelium in subepicardium over ventricles and atria, which gives rise to the coronary vessels. Only after 7 days does the primitive coronary plexus of the heart communicate with aorta (third step). During this period, some subepicardial vessels invade myocardium and some intramyocardial vessels contact with the heart cavity. Such intercommunications could help in regulation of blood circulation in primitive coronary plexus before establishment of effective contacts between arterial and venous vessels—excess of blood could be discharged directly into the heart cavity. Additional population of CD34+ cells were revealed inside condensed mesenchyme of the conotruncus; it participates in the formation of vasa vasorum in the aorta. Epicardium and sinus venosus generate endothelium of coronary vessels by neovasculo- and angiogenesis, respectively. During a week after ingrowth of vessels from SV and before their ingrowth to the aorta, ventriculo-coronary communications could be found in the heart.
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References
Ansari, A., Anatomy and clinical significance of ventricular thebesian veins, Clin. Anat., 2001, vol. 14, no. 2, pp. 102–110.
Chen, H.I., Sharma, B., Akerberg, B.N., et al., The sinus venosus contributes to coronary vasculature through VEGF-C-stimulated angiogenesis, Development (Cambridge: England), 2014, vol. 141 no. 23, pp. 4500–4512.
Chen, H.I., Poduri, A., Numi, H., et al., VEGF-C and aortic cardiomyocytes guide coronary artery stem development, J. Clin. Invest., 2014, vol. 124, no. 11, pp. 4899–4914.
Combs, M.D., Braitsch, C.M., Lange, A.W., et al., NFATC1promotes epicardium-derived cell invasion into myocardium, Development (Cambridge, England), 2011, vol. 138, no. 9, pp. 1747–1757.
Conte, G. and Pellegrini, A., On the development of the coronary arteries in human embryos, stages 14–19, Anat. Embryol. (Berl.), 1984, vol. 169, no. 2, pp. 209–218.
Dettman, R.W., Denetclaw, W., Jr., Ordahl, C.P., and Bristow, J., Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart, Dev. Biol., 1998, vol. 193, no. 2, pp. 169–181.
Duran, C.M.G. and Gunning, A.J., The vascularization of the heart valves: a comparative study, Cardiovasc. Res., 1968, vol. 2, no. 3, pp. 290–296.
Gittenberger-de Groot, A.C., Vrancken Peeters, M.P., Mentink, M.M., Gourdie, R.G., and Poelmann, R.E., Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions, Circ. Res., 1998, vol. 82, no. 10, pp. 1043–1052.
Hutchins, G.M. and Moore, G.W., Development of the coronary arteries in the embryonic human heart, Circulation, 1988, vol. 77, no. 6, pp. 1250–1257.
Jankowska-Steifer, E., Madej, M., Niderla-Bielińska, J., et al., Vasculogenic and hematopoietic cellular progenitors are scattered within the prenatal mouse heart, Histochem. Cell Biol., 2015, vol. 143, no. 2, pp. 153–169.
Kulchitskii, K.I. and Romenskii, O.Yu., Sravnitel’naya anatomiya i evolyutsiya krovenosnykh sosudov serdtsa (Comparative Anatomy and Evolution of Blood Vessels of the Heart), Kyiv.: Zdorov’ya, 1985.
Lie-Venema, H., Eralp, I., Maas, S., Gittenberger-De Groot, A.C., Poelmann, R.E., and DeRuiter, M.C., Myocardial heterogeneity in permissiveness for epicardium-derived cells and endothelial precursor cells along the developing heart tube at the onset of coronary vascularization, The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology, 2005, vol. 282, no. 2, pp. 120–129.
Lie-Venema, H., Akker, N.M., Bax, N.A., et al., Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development, Sci. World J., 2007, vol. 7, pp. 1777–1798.
Mandarim-de-Lacerda, C.A., Development of the coronary arteries in staged human embryos (the Paris Embryological Collection revisited), An. Acad. Bras. Cienc., 1990, vol. 62, no. 1, pp. 79–84.
Männer, J., Does the subepicardial mesenchyme contribute myocardioblasts to the myocardium of the chick embryo heart? a quail-chick chimera study tracing the fate of the epicardial primordium, Anat. Rec., 1999, vol. 255, no. 2, pp. 212–226.
Männer, J., Embryology of congenital ventriculo-coronary communications: a study on quail-chick chimeras, Cardiol. Young, 2000, vol. 10, no. 3, pp. 233–238.
Mikawa, T. and Fischman, D.A., Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels, Proc. Natl. Acad. Sci. U. S. A., 1992, vol. 89, no. 20, pp. 9504–9508.
Milgrom-Hoffman, M., Michailovici, I., Ferrara, N., Zelzer, E., and Tzahor, E., Endothelial cells regulate neural crest and second heart field morphogenesis, Biol. Open, 2014, vol. 3, no. 8, pp. 679–688.
Pérez-Pomares, J.-M., Carmona, R., González-Iriarte, M., et al., Origin of coronary endothelial cells from epicardial mesothelium in avian embryos, Int. J. Dev. Biol., 2002, vol. 46, no. 8, pp. 1005–1013.
Pérez-Pomares, J.M., Mironov, V., Guadix, J.A., et al., In vitro self-assembly of proepicardial cell aggregates: an embryonic vasculogenic model for vascular tissue engineering, Anat. Rec. Pt. A: Discov. Mol. Cell. Evol. Biol., 2006, vol. 288, no. 7, pp. 700–713.
Poelmann, R.E., Gittenberger-de Groot, A.C., Mentink, M.M., et al., Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras, Circ. Res., 1993, vol. 73, no. 3, pp. 559–568.
Ratajska, A., Czarnowska, E., Kołodzinska, A., Kluzek, W., and Leśniak, W., Vasculogenesis of the embryonic heart: origin of blood island-like structures, Anat. Rec. Pt. A: Discov. Mol. Cell. Evol. Biol., 2006, vol. 288, no. 3, pp. 223–232.
Ratajska, A., Czarnowska, E., Kołodzinska, A., et al., New morphological aspects of blood islands formation in the embryonic mouse hearts, Histochem. Cell Biol., 2009, vol. 131, no. 3, pp. 297–311.
Red-Horse, K., Ueno, H., Weissman, I.L., and Krasnow, M.A., Coronary arteries form by developmental reprogramming of venous cells, Nature, 2010, vol. 464, no. 7288, pp. 549–553.
Rusu, M.C., Poalelungi, C.V., Vrapciu, A.D., et al., Endocardial tip cells in the human embryo—facts and hypotheses, PLoS One, 2015, vol. 10, no. 1, p. 0115853.
Tian, X., Hu, T., He, L., Zhang, H., et al., Peritruncal coronary endothelial cells contribute to proximal coronary artery stems and their aortic orifices in the mouse heart, PLoS One, 2013a, vol. 8, no. 11, p. e80857.
Tian, X., Hu, T., Zhang, H., He, L., et al., Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries, Cell Res., 2013b, vol. 23, no. 9, pp. 1075–1090.
Tomanek, R.J., Ishii, Y., Holifield, J.S., et al., VEGF family members regulate myocardial tubulogenesis and coronary artery formation in the embryo, Circ. Res., 2006, vol. 98, no. 7, pp. 947–953.
Vrancken Peeters, M.P., Gittenberger-de Groot, A.C., Mentink, M.M., and Poelmann, R.E., Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial-mesenchymal transformation of the epicardium, Anat. Embryol., 1999, vol. 199, no. 4, pp. 367–378.
Waldo, K.L., Kumiski, D.H., and Kirby, M.L., Association of the cardiac neural crest with development of the coronary arteries in the chick embryo, Anat. Rec., 1994, vol. 239, no. 3, pp. 315–331.
Wu, B., Zhang, Z., Lui, W., et al., Endocardial cells form the coronary arteries by angiogenesis through myocardial- endocardial VEGF signaling, Cell, 2012, vol. 151, no. 5, pp. 1083–1096.
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Published in Russian in Ontogenez, 2016, Vol. 47, No. 6, pp. 373–385.
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Pototska, O.Y. Histological and immunocytochemical investigation of human coronary vessel development with anti-CD34 antibodies. Russ J Dev Biol 47, 348–358 (2016). https://doi.org/10.1134/S1062360416060047
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DOI: https://doi.org/10.1134/S1062360416060047