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• W2061569492 abstract "Three recent Nature papers use time-lapse confocal imaging to visualize the birth of blood cells from the aortic endothelium. Two studies (Bertrand et al., 2010Bertrand J.Y. Chi N.C. Santoso B. Teng S. Stainier D.Y. Traver D. Nature. 2010; 464: 108-111Crossref PubMed Scopus (722) Google Scholar, Kissa and Herbomel, 2010Kissa K. Herbomel P. Nature. 2010; 464: 112-115Crossref PubMed Scopus (674) Google Scholar) utilize the zebrafish embryo, while the third (Boisset et al., 2010Boisset J.C. van Cappellen W. Andrieu-Soler C. Galjart N. Dzierzak E. Robin C. Nature. 2010; 464: 116-120Crossref PubMed Scopus (643) Google Scholar) develops a novel technique to image the mouse aorta. Three recent Nature papers use time-lapse confocal imaging to visualize the birth of blood cells from the aortic endothelium. Two studies (Bertrand et al., 2010Bertrand J.Y. Chi N.C. Santoso B. Teng S. Stainier D.Y. Traver D. Nature. 2010; 464: 108-111Crossref PubMed Scopus (722) Google Scholar, Kissa and Herbomel, 2010Kissa K. Herbomel P. Nature. 2010; 464: 112-115Crossref PubMed Scopus (674) Google Scholar) utilize the zebrafish embryo, while the third (Boisset et al., 2010Boisset J.C. van Cappellen W. Andrieu-Soler C. Galjart N. Dzierzak E. Robin C. Nature. 2010; 464: 116-120Crossref PubMed Scopus (643) Google Scholar) develops a novel technique to image the mouse aorta. Almost a century ago, through careful observation of fixed specimens, histologists proposed that blood cells differentiate from a specialized population of endothelial cells in vertebrate embryos. For example, in 1916, H.E. Jordan wrote, “In searching through the 10 mm pig embryo …, my attention was arrested by the presence of peculiar cell clusters in the aorta. Brief attention has been called to these also by Emmel. He describes them for pig embryos … and in rabbit and mouse; and I have seen them also in mongoose and turtle embryos. Their occurrence would seem to be quite general in young vertebrate embryos. It is from a study of these clusters that I believe the most cogent evidence accrues of intrasomatic hemogenic capacity of young endothelium.” Volumes of data have supported these original observations by histologists and furthermore have begun to describe how these “peculiar cell clusters” form (reviewed in Jaffredo et al., 2005Jaffredo T. Nottingham W. Liddiard K. Bollerot K. Pouget C. de Bruijn M. Exp. Hematol. 2005; 33: 1029-1040Abstract Full Text Full Text PDF PubMed Scopus (102) Google Scholar). Major findings over the last 15 years include identification of a region of the vertebrate embryo containing the dorsal aorta as the site where hematopoietic stem cells (HSCs) are first and autonomously generated. Experiments in avian embryos showed that endothelial cells labeled with vital dyes gave rise to labeled clusters, and in the mouse the transcription factor Runx1 was identified as a marker of the hemogenic endothelium and was shown to be required for the formation of the clusters. More widespread acceptance of an endothelial origin of blood occurred after time-lapse photography showed a subset of endothelial cells undergoing a direct transition into blood cells during in vitro culture (Eilken et al., 2009Eilken H.M. Nishikawa S. Schroeder T. Nature. 2009; 457: 896-900Crossref PubMed Scopus (466) Google Scholar). Indications that the same process happens in vivo were provided by lineage tracing experiments in the mouse, where it was shown that almost all adult HSCs are derived from a cell that at one time had expressed vascular endothelial (VE) cadherin, a marker associated with endothelial cells (Chen et al., 2009Chen M.J. Yokomizo T. Zeigler B.M. Dzierzak E. Speck N.A. Nature. 2009; 457: 887-891Crossref PubMed Scopus (720) Google Scholar, Zovein et al., 2008Zovein A.C. Hofmann J.J. Lynch M. French W.J. Turlo K.A. Yang Y. Becker M.S. Zanetta L. Dejana E. Gasson J.C. et al.Cell Stem Cell. 2008; 3: 625-636Abstract Full Text Full Text PDF PubMed Scopus (508) Google Scholar). Furthermore, Runx1 was shown to be required within the VE-Cadherin-positive endothelium for HSC emergence, confirming that it is required for an endothelial-to-hematopoietic cell transition (Chen et al., 2009Chen M.J. Yokomizo T. Zeigler B.M. Dzierzak E. Speck N.A. Nature. 2009; 457: 887-891Crossref PubMed Scopus (720) Google Scholar). Altogether these data were consistent with the notion that hematopoietic cells (with perhaps the exception of a specialized embryonic lineage, primitive erythrocytes) are generated via an endothelial intermediate in a Runx1-dependent manner. Although the evidence for blood formation from endothelium was compelling, as the old adage goes, “seeing is believing,” and three recent Nature papers for the first time provide live imaging of this process. Kissa and Herbomel, 2010Kissa K. Herbomel P. Nature. 2010; 464: 112-115Crossref PubMed Scopus (674) Google Scholar and Bertrand et al., 2010Bertrand J.Y. Chi N.C. Santoso B. Teng S. Stainier D.Y. Traver D. Nature. 2010; 464: 108-111Crossref PubMed Scopus (722) Google Scholar made use of the transparent zebrafish embryo, which is particularly amenable to in vivo imaging. Using the kdrl promoter (kdrl encodes a receptor for vascular endothelial growth factor) to drive fluorescent reporter gene expression in the endothelial cells of transgenic fish, both groups directly demonstrated the transition of aortic endothelial cells into blood cells by using time-lapse confocal imaging. Confirmation that these were blood cells was provided by tracing the kdrl-GFP-positive cells to the fetal hematopoietic organs, the thymus and kidney marrow (Kissa and Herbomel, 2010Kissa K. Herbomel P. Nature. 2010; 464: 112-115Crossref PubMed Scopus (674) Google Scholar). Similarly, Bertrand et al., 2010Bertrand J.Y. Chi N.C. Santoso B. Teng S. Stainier D.Y. Traver D. Nature. 2010; 464: 108-111Crossref PubMed Scopus (722) Google Scholar showed that cells genetically marked by the activity of kdrl-Cre made up the large majority of kidney marrow cells in adult fish, consistent with what was previously demonstrated in mouse (Chen et al., 2009Chen M.J. Yokomizo T. Zeigler B.M. Dzierzak E. Speck N.A. Nature. 2009; 457: 887-891Crossref PubMed Scopus (720) Google Scholar, Zovein et al., 2008Zovein A.C. Hofmann J.J. Lynch M. French W.J. Turlo K.A. Yang Y. Becker M.S. Zanetta L. Dejana E. Gasson J.C. et al.Cell Stem Cell. 2008; 3: 625-636Abstract Full Text Full Text PDF PubMed Scopus (508) Google Scholar). The Kissa and Herbomel, 2010Kissa K. Herbomel P. Nature. 2010; 464: 112-115Crossref PubMed Scopus (674) Google Scholar paper took the analysis one step further, by detailing how an endothelial cell of the aorta can leave the vessel floor without disrupting vascular integrity. In a process that spanned several hours, cells with an endothelial morphology underwent contraction and bending, allowing the lateral neighbors to reach “underneath” and close the “gap” in the endothelium, before releasing all cellular contact and obtaining a rounded blood cell morphology. They aptly termed this process “endothelial hematopoietic transition” (EHT). This series of events has similarities with earlier observations in fixed sections of mammalian embryos, although there the direction of budding was into the lumen (Figure 1). Interestingly, during the peak of EHT events in zebrafish (40–52 hr postfertilization [h.p.f.]) the diameter of the dorsal aorta decreased, in line with this being a process in which endothelial cells undergo a direct transition into blood cells (Eilken et al., 2009Eilken H.M. Nishikawa S. Schroeder T. Nature. 2009; 457: 896-900Crossref PubMed Scopus (466) Google Scholar), as opposed to undergoing asymmetric divisions with one cell staying behind in the vascular wall. Although a few EHT events initiated in runx1 morphant zebrafish embryos, no hematopoietic cells were generated (consistent with many previous studies), and those that attempted to form met with a quick and violent death (see also Lancrin et al., 2009Lancrin C. Sroczynska P. Stephenson C. Allen T. Kouskoff V. Lacaud G. Nature. 2009; 457: 892-895Crossref PubMed Scopus (493) Google Scholar). So does a similar process take place in the mammalian embryo? The opaqueness of the mouse embryo and the deep location of the dorsal aorta have severely hampered direct imaging of this process. However, Boisset et al., 2010Boisset J.C. van Cappellen W. Andrieu-Soler C. Galjart N. Dzierzak E. Robin C. Nature. 2010; 464: 116-120Crossref PubMed Scopus (643) Google Scholar, taking a page from neurobiology, overcame this difficulty by preparing thick slices through the trunk of the 10.5 days postcoitus (d.p.c.) embryo for ex vivo time-lapse imaging. Using CD31-labeled Ly6A-GFP transgenic tissue slices (whereby the HSC marker Ly6A-GFP also marks a subset of the CD31+ cells in the endothelial cell wall), the authors witnessed round GFP+ cells budding from the aortic wall into the lumen. The hematopoietic nature of these emerging cells was verified by further analysis of c-kit and CD41 hematopoietic marker expression and by the absence of such events in Runx1 null embryos. Compared to zebrafish, hematopoietic cell emergence in the mouse aorta was rare, with just 1.7 events per cultured 10.5 d.p.c. embryo over the course of 15 hr (as opposed to 3 events/hr in zebrafish). Previous quantification of c-kit+ cells in the dorsal aorta of mouse embryos, however, identified hundreds of these cells in small and larger clusters (Chen et al., 2009Chen M.J. Yokomizo T. Zeigler B.M. Dzierzak E. Speck N.A. Nature. 2009; 457: 887-891Crossref PubMed Scopus (720) Google Scholar). In light of recent demonstrations that blood flow augments Runx1 expression and blood formation (Adamo et al., 2009Adamo L. Naveiras O. Wenzel P.L. McKinney-Freeman S. Mack P.J. Gracia-Sancho J. Suchy-Dicey A. Yoshimoto M. Lensch M.W. Yoder M.C. et al.Nature. 2009; 459: 1131-1135Crossref PubMed Scopus (396) Google Scholar, North et al., 2009North T.E. Goessling W. Peeters M. Li P. Ceol C. Lord A.M. Weber G.J. Harris J. Cutting C.C. Huang P. et al.Cell. 2009; 137: 736-748Abstract Full Text Full Text PDF PubMed Scopus (354) Google Scholar), the low number of events observed ex vivo may be due to the absence of flow in the culture system. How do we reconcile these data with the concept of the hemangioblast, described as a cell, likely of mesenchymal or mesodermal origin, that can give rise to both blood and endothelium? It would appear that development of HSCs from an aortic hemangioblast (although this cell so far has proven elusive) must occur in a linear fashion that involves an endothelial intermediate, similar to what was recently reported for embryonic stem (ES) cell-derived blood cells (Eilken et al., 2009Eilken H.M. Nishikawa S. Schroeder T. Nature. 2009; 457: 896-900Crossref PubMed Scopus (466) Google Scholar, Lancrin et al., 2009Lancrin C. Sroczynska P. Stephenson C. Allen T. Kouskoff V. Lacaud G. Nature. 2009; 457: 892-895Crossref PubMed Scopus (493) Google Scholar). The story is not yet over—we have much left to learn. For example, what signals initiate and determine the direction of the budding process? Does the budding process utilize the same molecules that mediate vascular sprouting? Why is it so localized, both temporally and spatially, in the embryo? Can the presence of Runx1 alone drive any endothelial cell to produce blood, and via what intermediates? And finally, can we put this knowledge to clinical use for producing blood ex vivo?" @default.
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• W2061569492 title "Visualizing Blood Cell Emergence from Aortic Endothelium" @default.
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