Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humans

Most circulating endothelial cells are apoptotic, but rare circulating endothelial colony-forming cells (C-ECFCs), also known as blood outgrowth endothelial cells, with proliferative and vasculogenic activity can be cultured; however, the origin and naive function of these C-ECFCs remains obscure. H...

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Main Authors: Yang Lin, Kimihiko Banno, Chang-Hyun Gil, Jered Myslinski, Takashi Hato, William C. Shelley, Hongyu Gao, Xiaoling Xuei, Yunlong Liu, David P. Basile, Momoko Yoshimoto, Nutan Prasain, Stefan P. Tarnawsky, Ralf H. Adams, Katsuhiko Naruse, Junko Yoshida, Michael P. Murphy, Kyoji Horie, Mervin C. Yoder
Format: Article
Language:English
Published: American Society for Clinical investigation 2023-03-01
Series:JCI Insight
Subjects:
Online Access:https://doi.org/10.1172/jci.insight.164781
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author Yang Lin
Kimihiko Banno
Chang-Hyun Gil
Jered Myslinski
Takashi Hato
William C. Shelley
Hongyu Gao
Xiaoling Xuei
Yunlong Liu
David P. Basile
Momoko Yoshimoto
Nutan Prasain
Stefan P. Tarnawsky
Ralf H. Adams
Katsuhiko Naruse
Junko Yoshida
Michael P. Murphy
Kyoji Horie
Mervin C. Yoder
author_facet Yang Lin
Kimihiko Banno
Chang-Hyun Gil
Jered Myslinski
Takashi Hato
William C. Shelley
Hongyu Gao
Xiaoling Xuei
Yunlong Liu
David P. Basile
Momoko Yoshimoto
Nutan Prasain
Stefan P. Tarnawsky
Ralf H. Adams
Katsuhiko Naruse
Junko Yoshida
Michael P. Murphy
Kyoji Horie
Mervin C. Yoder
author_sort Yang Lin
collection DOAJ
description Most circulating endothelial cells are apoptotic, but rare circulating endothelial colony-forming cells (C-ECFCs), also known as blood outgrowth endothelial cells, with proliferative and vasculogenic activity can be cultured; however, the origin and naive function of these C-ECFCs remains obscure. Herein, detailed lineage tracing revealed murine C-ECFCs emerged in the early postnatal period, displayed high vasculogenic potential with enriched frequency of clonal proliferative cells compared with tissue-resident ECFCs, and were not committed to or derived from the BM hematopoietic system but from tissue-resident ECFCs. In humans, C-ECFCs were present in the CD34bright cord blood mononuclear subset, possessed proliferative potential and in vivo vasculogenic function in a naive or cultured state, and displayed a single cell transcriptome sharing some umbilical venous endothelial cell features, such as a higher protein C receptor and extracellular matrix gene expression. This study provides an advance for the field by identifying the origin, naive function, and antigens to prospectively isolate C-ECFCs for translational studies.
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spelling doaj.art-51cd15f30c264e4c8c211f1f7ecdd59c2023-11-07T16:25:19ZengAmerican Society for Clinical investigationJCI Insight2379-37082023-03-0185Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humansYang LinKimihiko BannoChang-Hyun GilJered MyslinskiTakashi HatoWilliam C. ShelleyHongyu GaoXiaoling XueiYunlong LiuDavid P. BasileMomoko YoshimotoNutan PrasainStefan P. TarnawskyRalf H. AdamsKatsuhiko NaruseJunko YoshidaMichael P. MurphyKyoji HorieMervin C. YoderMost circulating endothelial cells are apoptotic, but rare circulating endothelial colony-forming cells (C-ECFCs), also known as blood outgrowth endothelial cells, with proliferative and vasculogenic activity can be cultured; however, the origin and naive function of these C-ECFCs remains obscure. Herein, detailed lineage tracing revealed murine C-ECFCs emerged in the early postnatal period, displayed high vasculogenic potential with enriched frequency of clonal proliferative cells compared with tissue-resident ECFCs, and were not committed to or derived from the BM hematopoietic system but from tissue-resident ECFCs. In humans, C-ECFCs were present in the CD34bright cord blood mononuclear subset, possessed proliferative potential and in vivo vasculogenic function in a naive or cultured state, and displayed a single cell transcriptome sharing some umbilical venous endothelial cell features, such as a higher protein C receptor and extracellular matrix gene expression. This study provides an advance for the field by identifying the origin, naive function, and antigens to prospectively isolate C-ECFCs for translational studies.https://doi.org/10.1172/jci.insight.164781Vascular biology
spellingShingle Yang Lin
Kimihiko Banno
Chang-Hyun Gil
Jered Myslinski
Takashi Hato
William C. Shelley
Hongyu Gao
Xiaoling Xuei
Yunlong Liu
David P. Basile
Momoko Yoshimoto
Nutan Prasain
Stefan P. Tarnawsky
Ralf H. Adams
Katsuhiko Naruse
Junko Yoshida
Michael P. Murphy
Kyoji Horie
Mervin C. Yoder
Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humans
JCI Insight
Vascular biology
title Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humans
title_full Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humans
title_fullStr Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humans
title_full_unstemmed Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humans
title_short Origin, prospective identification, and function of circulating endothelial colony-forming cells in mice and humans
title_sort origin prospective identification and function of circulating endothelial colony forming cells in mice and humans
topic Vascular biology
url https://doi.org/10.1172/jci.insight.164781
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