Caudal dorsal artery generates hematopoietic stem and progenitor cells via the endothelial-to-hematopoietic transition in zebrafish

Zhan, Yandong; Huang, Youkui; Chen, Jingying; Cao, Zigang; He, Jianbo; Zhang, Jingjing; Huang, Hai; Ruan, Hua; Luo, Lingfei; Li, Li

doi:10.1016/j.jgg.2018.02.010

Cited by 13 publications

(10 citation statements)

References 54 publications

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“…During vertebrate development, distinct hematopoietic cell types reside in particular anatomical locations at specific time points ( Stachura and Traver, 2016 ). For example, erythrocytes and thrombocytes travel rapidly in circulation ( Brönnimann et al, 2018 Khandekar et al, 2012 ); macrophages and dendritic cells can reside in the skin ( Zhan et al., 2018 ); neutrophils ubiquitously spread throughout circulation, epidermis, or congregating in stressed tissue ( Le Guyader et al, 2008 ); and T cells are abundant in the thymus ( Tian et al, 2017 ). To measure Prog+ and HSC contribution to T lymphocytes, we imaged mCherry fluorescence in the thymus in 5–16 dpf larvae ( Figure 3A ).…”

Section: Resultsmentioning

confidence: 99%

“…If transient embryonic progenitors can generate erythroid, myeloid, and lymphoid cells, what do HSCs contribute to embryonic/prenatal hematopoiesis? A difficulty in addressing this question is the spatially and temporally overlapping yet independent generation of HSCs and HSC-independent progenitors and their shared expression of several marker genes used for cell isolation ( Zhan et al, 2018 ; Tian et al, 2017 ; Stachura and Traver, 2016 ; Chen et al, 2011 ; Davidson and Zon, 2004 ). Consequently, higher resolution data on the distinct transcriptional landscapes of hematopoietic stem and progenitor cell (HSPC) subsets are needed in combination with functional assays to examine their endogenous function in development.…”

Section: Introductionmentioning

confidence: 99%

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Definitive hematopoietic stem cells minimally contribute to embryonic hematopoiesis

et al. 2021

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Hematopoietic stem cells (HSCs) are rare cells that arise in the embryo and sustain adult hematopoiesis. Although the functional potential of nascent HSCs is detectable by transplantation, their native contribution during development is unknown, in part due to the overlapping genesis and marker gene expression with other embryonic blood progenitors. Using single-cell transcriptomics, we define gene signatures that distinguish nascent HSCs from embryonic blood progenitors. Applying a lineage-tracing approach to selectively track HSC output in situ, we find significantly delayed lymphomyeloid contribution. An inducible HSC injury model demonstrates a negligible impact on larval lymphomyelopoiesis following HSC depletion. HSCs are not merely dormant at this developmental stage, as they showed robust regeneration after injury. Combined, our findings illuminate that nascent HSCs self-renew but display differentiation latency, while HSC-independent embryonic progenitors sustain developmental hematopoiesis. Understanding these differences could improve de novo generation and expansion of functional HSCs.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Definitive hematopoietic stem cells minimally contribute to embryonic hematopoiesis

et al. 2021

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“…It is important to note that more lineage-restricted definitive progenitors have been documented to arise via EHT events both before and concurrent with HSC emergence, and new transcriptomic and lineage-tracing data from zebrafish suggests that embryonic blood production primarily occurs from these cell types (with the HSC pool being drawn on later in adult life) [8]. These include lymphoid progenitors from the caudal DA in zebrafish [9,10], murine lympho-myeloid progenitors [11,12] and erythro-myeloid restricted progenitors (EMPs) in the zebrafish trunk [13] and from yolk sac arteries in mice [14]. A recent report even suggests that yolk-sac derived EMPs may produce endothelial cells that can incorporate back into the developing embryonic vasculature [15].…”

Section: The Endothelial Origin Of Hscs 21 Definitive Hematopoiesis In the Embryomentioning

confidence: 99%

Making Blood from the Vessel: Extrinsic and Environmental Cues Guiding the Endothelial-to-Hematopoietic Transition

Sugden

North

2021

Life

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It is increasingly recognized that specialized subsets of endothelial cells carry out unique functions in specific organs and regions of the vascular tree. Perhaps the most striking example of this specialization is the ability to contribute to the generation of the blood system, in which a distinct population of “hemogenic” endothelial cells in the embryo transforms irreversibly into hematopoietic stem and progenitor cells that produce circulating erythroid, myeloid and lymphoid cells for the lifetime of an animal. This review will focus on recent advances made in the zebrafish model organism uncovering the extrinsic and environmental factors that facilitate hemogenic commitment and the process of endothelial-to-hematopoietic transition that produces blood stem cells. We highlight in particular biomechanical influences of hemodynamic forces and the extracellular matrix, metabolic and sterile inflammatory cues present during this developmental stage, and outline new avenues opened by transcriptomic-based approaches to decipher cell–cell communication mechanisms as examples of key signals in the embryonic niche that regulate hematopoiesis.

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“…Zebrafish CHT is characterized as a unique hematopoietic organ with multiple biological functions ( 9 , 14 , 49 – 51 ). In this study, we used scRNA-seq, combined with functional assays, to reveal the global transcriptome landscape and cellular organization of developing CHT in zebrafish.…”

Section: Discussionmentioning

confidence: 99%

A single-cell resolution developmental atlas of hematopoietic stem and progenitor cell expansion in zebrafish

Xia

Kang

Xue

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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During vertebrate embryogenesis, fetal hematopoietic stem and progenitor cells (HSPCs) exhibit expansion and differentiation properties in a supportive hematopoietic niche. To profile the developmental landscape of fetal HSPCs and their local niche, here, using single-cell RNA-sequencing, we deciphered a dynamic atlas covering 28,777 cells and 9 major cell types (23 clusters) of zebrafish caudal hematopoietic tissue (CHT). We characterized four heterogeneous HSPCs with distinct lineage priming and metabolic gene signatures. Furthermore, we investigated the regulatory mechanism of CHT niche components for HSPC development, with a focus on the transcription factors and ligand–receptor networks involved in HSPC expansion. Importantly, we identified an endothelial cell-specific G protein–coupled receptor 182, followed by in vivo and in vitro functional validation of its evolutionally conserved role in supporting HSPC expansion in zebrafish and mice. Finally, comparison between zebrafish CHT and human fetal liver highlighted the conservation and divergence across evolution. These findings enhance our understanding of the regulatory mechanism underlying hematopoietic niche for HSPC expansion in vivo and provide insights into improving protocols for HSPC expansion in vitro.

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Caudal dorsal artery generates hematopoietic stem and progenitor cells via the endothelial-to-hematopoietic transition in zebrafish

Cited by 13 publications

References 54 publications

Definitive hematopoietic stem cells minimally contribute to embryonic hematopoiesis

Definitive hematopoietic stem cells minimally contribute to embryonic hematopoiesis

Making Blood from the Vessel: Extrinsic and Environmental Cues Guiding the Endothelial-to-Hematopoietic Transition

A single-cell resolution developmental atlas of hematopoietic stem and progenitor cell expansion in zebrafish

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