Myocardium-derived angiopoietin-1 is essential for coronary vein formation in the developing heart

Yoh Arita, Yoshikazu Nakaoka (), Taichi Matsunaga, Hiroyasu Kidoya, Kohei Yamamizu, Yuichiro Arima, Takahiro Kataoka-Hashimoto, Kuniyasu Ikeoka, Taku Yasui, Takeshi Masaki, Kaori Yamamoto, Kaori Higuchi, Jin-Sung Park, Manabu Shirai, Koichi Nishiyama, Hiroyuki Yamagishi, Kinya Otsu, Hiroki Kurihara, Takashi Minami, Keiko Yamauchi-Takihara, Gou Y. Koh, Naoki Mochizuki, Nobuyuki Takakura, Yasushi Sakata, Jun K. Yamashita and Issei Komuro
Additional contact information
Yoh Arita: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Yoshikazu Nakaoka: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Taichi Matsunaga: Laboratory of Stem Cell Differentiation, Center for iPS Cell Research and Application (CiRA), Kyoto University, 53, Shogoin-Kawahara-cho
Hiroyasu Kidoya: Research Institute for Microbial Diseases, Osaka University, 3-1, Yamadaoka
Kohei Yamamizu: Laboratory of Stem Cell Differentiation, Center for iPS Cell Research and Application (CiRA), Kyoto University, 53, Shogoin-Kawahara-cho
Yuichiro Arima: Graduate School of Medicine, University of Tokyo, 7-3-1, Hongo
Takahiro Kataoka-Hashimoto: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Kuniyasu Ikeoka: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Taku Yasui: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Takeshi Masaki: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Kaori Yamamoto: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Kaori Higuchi: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Jin-Sung Park: National Research Laboratory of Vascular Biology and Stem Cells, Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST), 373-1
Manabu Shirai: National Cerebral and Cardiovascular Center Research Institute, 5-7-1, Fujishirodai
Koichi Nishiyama: Graduate School of Medicine, University of Tokyo, 7-3-1, Hongo
Hiroyuki Yamagishi: Keio University School of Medicine, 35, Shinano-machi
Kinya Otsu: King’s College London, 25, Coldharbour Lane
Hiroki Kurihara: Graduate School of Medicine, University of Tokyo, 7-3-1, Hongo
Takashi Minami: Laboratory for Vascular Biology, Research Center for Advanced Science and Technology, University of Tokyo, 4-6-4, Komaba
Keiko Yamauchi-Takihara: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Gou Y. Koh: National Research Laboratory of Vascular Biology and Stem Cells, Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST), 373-1
Naoki Mochizuki: JST-CREST, National Cerebral and Cardiovascular Center Research Institute, 5-7-1, Fujishirodai
Nobuyuki Takakura: Research Institute for Microbial Diseases, Osaka University, 3-1, Yamadaoka
Yasushi Sakata: Osaka University Graduate School of Medicine, 2-2, Yamadaoka
Jun K. Yamashita: Laboratory of Stem Cell Differentiation, Center for iPS Cell Research and Application (CiRA), Kyoto University, 53, Shogoin-Kawahara-cho
Issei Komuro: Graduate School of Medicine, University of Tokyo, 7-3-1, Hongo

Nature Communications, 2014, vol. 5, issue 1, 1-14

Abstract: Abstract The origin and developmental mechanisms underlying coronary vessels are not fully elucidated. Here we show that myocardium-derived angiopoietin-1 (Ang1) is essential for coronary vein formation in the developing heart. Cardiomyocyte-specific Ang1 deletion results in defective formation of the subepicardial coronary veins, but had no significant effect on the formation of intramyocardial coronary arteries. The endothelial cells (ECs) of the sinus venosus (SV) are heterogeneous population, composed of APJ-positive and APJ-negative ECs. Among these, the APJ-negative ECs migrate from the SV into the atrial and ventricular myocardium in Ang1-dependent manner. In addition, Ang1 may positively regulate venous differentiation of the subepicardial APJ-negative ECs in the heart. Consistently, in vitro experiments show that Ang1 indeed promotes venous differentiation of the immature ECs. Collectively, our results indicate that myocardial Ang1 positively regulates coronary vein formation presumably by promoting the proliferation, migration and differentiation of immature ECs derived from the SV.

Date: 2014
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DOI: 10.1038/ncomms5552

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