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      Modeling hematopoietic disorders in zebrafish

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          ABSTRACT

          Zebrafish offer a powerful vertebrate model for studies of development and disease. The major advantages of this model include the possibilities of conducting reverse and forward genetic screens and of observing cellular processes by in vivo imaging of single cells. Moreover, pathways regulating blood development are highly conserved between zebrafish and mammals, and several discoveries made in fish were later translated to murine and human models. This review and accompanying poster provide an overview of zebrafish hematopoiesis and discuss the existing zebrafish models of blood disorders, such as myeloid and lymphoid malignancies, bone marrow failure syndromes and immunodeficiencies, with a focus on how these models were generated and how they can be applied for translational research.

          Abstract

          Summary: This At A Glance article and poster summarize the last 20 years of research in zebrafish models for hematopoietic disorders, highlighting how these models were created and are being applied for translational research.

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          The zebrafish reference genome sequence and its relationship to the human genome.

          Kerstin Howe, Matthew D. Clark, Carlos F Torroja … (2013)
          Zebrafish have become a popular organism for the study of vertebrate gene function. The virtually transparent embryos of this species, and the ability to accelerate genetic studies by gene knockdown or overexpression, have led to the widespread use of zebrafish in the detailed investigation of vertebrate gene function and increasingly, the study of human genetic disease. However, for effective modelling of human genetic disease it is important to understand the extent to which zebrafish genes and gene structures are related to orthologous human genes. To examine this, we generated a high-quality sequence assembly of the zebrafish genome, made up of an overlapping set of completely sequenced large-insert clones that were ordered and oriented using a high-resolution high-density meiotic map. Detailed automatic and manual annotation provides evidence of more than 26,000 protein-coding genes, the largest gene set of any vertebrate so far sequenced. Comparison to the human reference genome shows that approximately 70% of human genes have at least one obvious zebrafish orthologue. In addition, the high quality of this genome assembly provides a clearer understanding of key genomic features such as a unique repeat content, a scarcity of pseudogenes, an enrichment of zebrafish-specific genes on chromosome 4 and chromosomal regions that influence sex determination.
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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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              In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium.

              Jean-Charles Boisset, Wiggert A. van Cappellen, Charlotte Andrieu-Soler … (2010)
              Haematopoietic stem cells (HSCs), responsible for blood production in the adult mouse, are first detected in the dorsal aorta starting at embryonic day 10.5 (E10.5). Immunohistological analysis of fixed embryo sections has revealed the presence of haematopoietic cell clusters attached to the aortic endothelium where HSCs might localize. The origin of HSCs has long been controversial and several candidates of the direct HSC precursors have been proposed (for review see ref. 7), including a specialized endothelial cell population with a haemogenic potential. Such cells have been described both in vitro in the embryonic stem cell (ESC) culture system and retrospectively in vivo by endothelial lineage tracing and conditional deletion experiments. Whether the transition from haemogenic endothelium to HSC actually occurs in the mouse embryonic aorta is still unclear and requires direct and real-time in vivo observation. To address this issue we used time-lapse confocal imaging and a new dissection procedure to visualize the deeply located aorta. Here we show the dynamic de novo emergence of phenotypically defined HSCs (Sca1(+), c-kit(+), CD41(+)) directly from ventral aortic haemogenic endothelial cells.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Dis Model Mech
                Journal ID (iso-abbrev): Dis Model Mech
                Journal ID (publisher-id): DMM
                Journal ID (hwp): dmm
                Title: Disease Models & Mechanisms
                Publisher: The Company of Biologists Ltd
                ISSN (Print): 1754-8403
                ISSN (Electronic): 1754-8411
                Publication date (Print, pub): 1 September 2019
                Publication date (Electronic): 6 September 2019
                Publication date PMC-release: 6 September 2019
                Volume: 12
                Issue: 9
                Electronic Location Identifier: dmm040360
                Affiliations
                [1 ]Department of Biomedicine, University of Basel and University Hospital Basel , Basel 4031, Switzerland
                [2 ]Division of Hematology, University of Basel and University Hospital Basel , Basel 4031, Switzerland
                Author notes
                [*]

                These authors contributed equally to this work

                [‡ ]Author for correspondence ( martina.konantz@ 123456unibas.ch )
                Author information
                http://orcid.org/0000-0002-4319-3119
                http://orcid.org/0000-0001-5442-2805
                Article
                Publisher ID: DMM040360
                DOI: 10.1242/dmm.040360
                PMC ID: 6765189
                PubMed ID: 31519693
                SO-VID: b824f128-14b6-4902-87e0-200f81e94550
                Copyright © © 2019. Published by The Company of Biologists Ltd
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                Funding
                Funded by: Swiss National Science Foundation, http://dx.doi.org/10.13039/501100001711;
                Award ID: 310030_149735
                Award ID: 310030_179239
                Funded by: University of Basel, http://dx.doi.org/10.13039/100008375;
                Categories
                Subject: Zebra
                Subject: At A Glance

                ScienceOpen disciplines: Molecular medicine
                Keywords: disease models,hematopoiesis,blood disorders,leukemia,immunodeficiency,bone marrow failure syndrome
                Data availability:
                ScienceOpen disciplines: Molecular medicine
                Keywords: disease models, hematopoiesis, blood disorders, leukemia, immunodeficiency, bone marrow failure syndrome

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