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      Cell cycle dynamics and complement expression distinguishes mature haematopoietic subsets arising from hemogenic endothelium

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          ABSTRACT

          The emergence of haematopoietic stem and progenitor cells (HSPCs) from hemogenic endothelium results in the formation of sizeable HSPC clusters attached to the vascular wall. We evaluate the cell cycle and proliferation of HSPCs involved in cluster formation, as well as the molecular signatures from their initial appearance to the point when cluster cells are capable of adult engraftment (definitive HSCs). We uncover a non-clonal origin of HSPC clusters with differing cell cycle, migration, and cell signaling attributes. In addition, we find that the complement cascade is highly enriched in mature HSPC clusters, possibly delineating a new role for this pathway in engraftment.

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          Hematopoietic stem cells derive directly from aortic endothelium during development

          Julien Y. Bertrand, Neil Chi, Buyung Santoso … (2010)
          A major goal of regenerative medicine is to instruct formation of multipotent, tissue-specific stem cells from induced pluripotent stem cells (iPSCs) for cell replacement therapies. Generation of hematopoietic stem cells (HSCs) from iPSCs or embryonic stem cells (ESCs) is not currently possible, however, necessitating a better understanding of how HSCs normally arise during embryonic development. We previously showed that hematopoiesis occurs through four distinct waves during zebrafish development, with HSCs arising in the final wave in close association with the dorsal aorta. Recent reports have suggested that murine HSCs derive from hemogenic endothelial cells (ECs) lining the aortic floor1,2. Additional in vitro studies have similarly suggested that the hematopoietic progeny of ESCs arise through intermediates with endothelial potential3,4. In this report, we have utilized the unique strengths of the zebrafish embryo to image directly the birth of HSCs from the ventral wall of the dorsal aorta. Utilizing combinations of fluorescent reporter transgenes, confocal timelapse microscopy and flow cytometry, we have identified and isolated the stepwise intermediates as aortic hemogenic endothelium transitions to nascent HSCs. Finally, using a permanent lineage tracing strategy, we demonstrate that the HSCs generated from hemogenic endothelium are the lineal founders of the adult hematopoietic system.
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            Blood stem cells emerge from aortic endothelium by a novel type of cell transition.

            Karima Kissa, Philippe Herbomel (2010)
            The ontogeny of haematopoietic stem cells (HSCs) during embryonic development is still highly debated, especially their possible lineage relationship to vascular endothelial cells. The first anatomical site from which cells with long-term HSC potential have been isolated is the aorta-gonad-mesonephros (AGM), more specifically the vicinity of the dorsal aortic floor. But although some authors have presented evidence that HSCs may arise directly from the aortic floor into the dorsal aortic lumen, others support the notion that HSCs first emerge within the underlying mesenchyme. Here we show by non-invasive, high-resolution imaging of live zebrafish embryos, that HSCs emerge directly from the aortic floor, through a stereotyped process that does not involve cell division but a strong bending then egress of single endothelial cells from the aortic ventral wall into the sub-aortic space, and their concomitant transformation into haematopoietic cells. The process is polarized not only in the dorso-ventral but also in the rostro-caudal versus medio-lateral direction, and depends on Runx1 expression: in Runx1-deficient embryos, the exit events are initially similar, but much rarer, and abort into violent death of the exiting cell. These results demonstrate that the aortic floor is haemogenic and that HSCs emerge from it into the sub-aortic space, not by asymmetric cell division but through a new type of cell behaviour, which we call an endothelial haematopoietic transition.
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              Definitive hematopoiesis is autonomously initiated by the AGM region.

              Alexander Medvinsky, Elaine Dzierzak (1996)
              The adult hematopoietic system of mammals is a dynamic hierarchy of cells with the hematopoietic stem cell at its foundation. During embryonic development, the source and expansion potential of this cell remain unclear. Two sites of hematopoietic activity, the yolk sac and aorta-gonad-mesonephros (AGM) region, function in mouse ontogeny at the pre-liver stage of hematopoiesis. However, cellular interchange between these tissues obscures the embryonic site of hematopoietic stem cell generation. Here we present the results of a novel in vitro organ culture system demonstrating that, at day 10 in gestation, hematopoietic stem cells initiate autonomously and exclusively within the AGM region. Furthermore, we provide evidence for the in vitro expansion of hematopoietic stem cells within the AGM region. These results strongly suggest that the AGM region is the source of the definitive adult hematopoietic system, which subsequently colonizes the liver.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Cell Cycle
                Journal ID (iso-abbrev): Cell Cycle
                Journal ID (publisher-id): KCCY
                Journal ID (publisher-id): kccy20
                Title: Cell Cycle
                Publisher: Taylor & Francis
                ISSN (Print): 1538-4101
                ISSN (Electronic): 1551-4005
                Publication date Collection: 2017
                Publication date (Electronic): 18 August 2017
                Publication date PMC-release: 18 August 2017
                Volume: 16
                Issue: 19
                Pages: 1835-1847
                Affiliations
                [a ]Cardiovascular Research Institute, University of California San Francisco , San Francisco, CA, USA
                [b ]Department of Pediatrics, Division of Neonatology, University of California San Francisco School of Medicine , San Francisco, CA, USA
                [c ]Department of Laboratory of Medicine, University of California San Francisco, School of Medicine , San Francisco, CA, USA
                Author notes
                CONTACT Ann C. Zovein ann.zovein@ 123456ucsf.edu , Cardiovascular Research Institute at UCSF , 555 Mission Bay Boulevard South, SCVRB 352X/MC: 3120, San Francisco, CA 94158–3120, USA

                Supplemental data for this article can be accessed on the publisher's website.

                Article
                Publisher ID: 1361569
                DOI: 10.1080/15384101.2017.1361569
                PMC ID: 5628647
                PubMed ID: 28820341
                SO-VID: 23e24cd6-3674-4253-8291-880b4e97071d
                Copyright © © 2017 The Author(s). Published with license by Taylor & Francis.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License ( http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.

                History
                Date received : 5 July 2017
                Date accepted : 25 July 2017
                Page count
                Figures: 7, Tables: 3, Equations: 0, References: 60, Pages: 13
                Categories
                Subject: Reports

                ScienceOpen disciplines: Cell biology
                Keywords: hematopoiesis,hematopoietic stem cells,hemogenic endothelium
                Data availability:
                ScienceOpen disciplines: Cell biology
                Keywords: hematopoiesis, hematopoietic stem cells, hemogenic endothelium

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