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Embryogenesis of the First Circulating Endothelial Cells

Cui, Cheng and Filla, Michael B. and Jones, Elizabeth A. V. and Lansford, Rusty and Cheuvront, Tracey and Al-Roubaie, Sarah and Rongish, Brenda J. and Little, Charles D. (2013) Embryogenesis of the First Circulating Endothelial Cells. PLoS ONE, 8 (5). Art. No. e60841. ISSN 1932-6203. PMCID PMC3667859. https://resolver.caltech.edu/CaltechAUTHORS:20130821-090748059

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Abstract

Prior to this study, the earliest appearance of circulating endothelial cells in warm-blooded animals was unknown. Time-lapse imaging of germ-line transformed Tie1-YFP reporter quail embryos combined with the endothelial marker antibody QH1 provides definitive evidence for the existence of circulating endothelial cells – from the very beginning of blood flow. Blood-smear counts of circulating cells from Tie1-YFP embryos showed that up to 30% of blood-borne cells are Tie1 positive; though cells expressing low levels of YFP were also positive for benzidine, a hemoglobin stain, suggesting that these cells were differentiating into erythroblasts. Electroporation-based time-lapse experiments, exclusively targeting the intra-embryonic mesoderm were combined with QH1 immunostaining. The latter antibody marks quail endothelial cells. Together the optical data provide conclusive evidence that endothelial cells can enter blood flow from vessels of the embryo proper, as well as from extra-embryonic areas. When Tie1-YFP positive cells and tissues are transplanted to wild type host embryos, fluorescent cells emigrate from such transplants and join host vessels; subsequently a few YFP cells are shed into circulation. These data establish that entering circulation is a commonplace activity of embryonic vascular endothelial cells. We conclude that in the class of vertebrates most closely related to mammals a normal component of primary vasculogenesis is production of endothelial cells that enter circulation from all vessels, both intra- and extra-embryonic.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pone.0060841DOIArticle
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0060841PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3667859/PubMed CentralArticle
ORCID:
AuthorORCID
Lansford, Rusty0000-0002-2159-3699
Additional Information:© 2013 Cui et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: May 14, 2012; Accepted: March 5, 2013; Published: May 30, 2013. This work was supported by the National Institutes of Health R01 grants HL085694 (BJR), HL068855 (CDL) (http://www.nih.gov/); the G. Harold & Leila Y. Mathers Charitable Foundation (BJR and CDL) (http://www.mathersfoundation.org/); a NSERC Discovery 342134 (EAVJ) (http://www.nserc-crsng.gc.ca); and an American Heart Assoc, postdoctoral fellowship (0620105Z) to CC (http://www.heart.org). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author Contributions: Conceived and designed the experiments: CC MBF EAVJ BJR CDL. Performed the experiments: CC MBF RL TC SA. Analyzed the data: CC MBF EAVJ RL TC SA BJR CDL. Contributed reagents/materials/ analysis tools: CC EAVJ RL BJR CDL. Wrote the paper: CC MBF EAVJ RL AR BJR CDL.
Funders:
Funding AgencyGrant Number
NIHHL085694
NIHHL068855
G. Harold & Leila Y. Mathers Charitable FoundationUNSPECIFIED
Natural Sciences and Engineering Research Council of Canada (NSERC)342134
American Heart Association0620105Z
Issue or Number:5
PubMed Central ID:PMC3667859
Record Number:CaltechAUTHORS:20130821-090748059
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130821-090748059
Official Citation:Cui C, Filla MB, Jones EAV, Lansford R, Cheuvront T, et al. (2013) Embryogenesis of the First Circulating Endothelial Cells. PLoS ONE 8(5): e60841. doi:10.1371/journal.pone.0060841
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:40749
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:21 Aug 2013 21:50
Last Modified:03 Oct 2019 05:42

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