Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Yuichiro Arima
Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Developmental Cardiology Laboratory, International Research Center for Medical Science, Kumamoto University, Kumamoto, Japan
Department of Molecular Pathophysiology, Institute of Advanced Medical Sciences, Nippon Medical School, Tokyo, Japan
Norihiro Okada
School of Pharmacy, Kitasato University, Tokyo, Japan
Katsumi Kose
Institute of Applied Physics, University of Tsukuba, Tsukuba, Japan
Shigehito Yamada
Congenital Anomaly Research Center, Kyoto University Graduate School of Medicine, Kyoto, Japan
Jun K Takeuchi
Molecular Craniofacial Embryology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, Japan
Kazuko Koshiba-Takeuchi
Faculty of Life Sciences, Department of Applied Biosciences, Toyo University, Gunma, Japan
Shigetomo Fukuhara
Department of Molecular Pathophysiology, Institute of Advanced Medical Sciences, Nippon Medical School, Tokyo, Japan
Sachiko Miyagawa-Tomita
Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Heart Center, Department of Pediatric Cardiology, Tokyo Women’s Medical University, Tokyo, Japan; Department of Animal Nursing Science, Yamazaki University of Animal Health Technology, Tokyo, Japan
Hiroki Kurihara
Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Coronary arteries are a critical part of the vascular system and provide nourishment to the heart. In humans, even minor defects in coronary arteries can be lethal, emphasizing their importance for survival. However, some teleosts survive without coronary arteries, suggesting that there may have been some evolutionary changes in the morphology and function of coronary arteries in the tetrapod lineage. Here, we propose that the true ventricular coronary arteries were newly established during amniote evolution through remodeling of the ancestral coronary vasculature. In mouse (Mus musculus) and Japanese quail (Coturnix japonica) embryos, the coronary arteries unique to amniotes are established by the reconstitution of transient vascular plexuses: aortic subepicardial vessels (ASVs) in the outflow tract and the primitive coronary plexus on the ventricle. In contrast, amphibians (Hyla japonica, Lithobates catesbeianus, Xenopus laevis, and Cynops pyrrhogaster) retain the ASV-like vasculature as truncal coronary arteries throughout their lives and have no primitive coronary plexus. The anatomy and development of zebrafish (Danio rerio) and chondrichthyans suggest that their hypobranchial arteries are ASV-like structures serving as the root of the coronary vasculature throughout their lives. Thus, the ventricular coronary artery of adult amniotes is a novel structure that has acquired a new remodeling process, while the ASVs, which occur transiently during embryonic development, are remnants of the ancestral coronary vessels. This evolutionary change may be related to the modification of branchial arteries, indicating considerable morphological changes underlying the physiological transition during amniote evolution.
