Fate Mapping Embryonic Blood in Zebrafish: Multi- and Unipotential Lineages Are Segregated at Gastrulation

Warga, Rachel M.; Kane, Donald A.; Ho, Ruoya

doi:10.1016/j.devcel.2009.04.007

Cited by 73 publications

(84 citation statements)

References 60 publications

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“…This postulate is strongly supported by recent fate-mapping studies in the zebrafish embryo. 43 In our model, fish primitive macrophages are more similar to the primitive macrophage lineage in the murine yolk sac, which has been demonstrated to be unipotent. 28 Because EMPs arise normally in HSC-deficient mindbomb mutants, we have been able to monitor their differentiation potential in the absence of confounding HSC-derived progeny.…”

Section: Discussionmentioning

confidence: 89%

Notch signaling distinguishes 2 waves of definitive hematopoiesis in the zebrafish embryo

Bertrand¹,

Cisson²,

Stachura³

et al. 2010

Blood

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Recent studies have revealed that definitive hematopoiesis in vertebrates initiates through the formation of a non-selfrenewing progenitor with limited multilineage differentiation potential termed the erythromyeloid progenitor (EMP). EMPs are specified before hematopoietic stem cells (HSCs), which self-renew and are capable of forming all mature adult blood lineages including lymphoid cells. Despite their differences, EMPs and HSCs share many phenotypic traits, making precise study of their respective functions difficult. Here, we examine whether embryonic specification of EMPs requires Notch signaling as has been shown for HSCs. In mindbomb mutants, which lack functional Notch ligands, we show that EMPs are specified normally: we detect no significant differences in cell number, gene expression, or differentiation capacity between EMPs purified from wildtype (WT) or mindbomb mutant embryos. IntroductionIn adult vertebrates, constant replenishment of mature blood cells depends upon the existence of rare hematopoietic stem cells (HSCs). The 2 hallmarks of HSCs, multilineage differentiation capacity and long-term self-renewal potential, are sufficient to sustain hematopoiesis for life.In the mouse, embryonic HSCs emerge in close association with the major arteries of the conceptus: the vitelline arteries of the yolk sac (YS) 1-3 the dorsal aorta, 3-5 and the umbilical arteries of the placenta 6,7 between 9 and 12 days postcoitus (dpc). HSCs subsequently migrate to the fetal liver and spleen before seeding the bone marrow, 8,9 which is the main site of mammalian hematopoiesis during adulthood. Lineage tracing of embryonic HSCs showed contribution to the adult hematopoietic system, 10 although additional subsequent sources of HSCs could not be ruled out as contributors to the adult HSC pool. Importantly, recent studies have implicated hemogenic endothelium from the midgestation embryo as the original source of HSCs. 11,12 Similar to mammals, zebrafish possess shifting sites of hematopoiesis during embryonic development, with HSCs first appearing along the dorsal aorta between 26 and 28 hours postfertilization (hpf). [13][14][15][16] Nascent HSCs migrate from this analog of the mammalian aorta-gonads-mesonephros (AGM) region to seed the caudal hematopoietic tissues, which serve a role similar to that of the mammalian fetal liver in transiently hosting multilineage hematopoiesis 16 until hematopoiesis transitions to the kidney, the major site of hematopoiesis in adult teleosts (reviewed in Stachura and Traver 17 ). Presumably, these migrations reflect the changing needs of HSCs to experience different signaling environments at different points in their maturation.A major challenge in the field of developmental hematopoiesis is to determine the molecular cues that instruct each hematopoietic wave from mesoderm. In both mammals and zebrafish, signaling through the Notch pathway is important in HSC specification. Notch is a single-pass transmembrane receptor, which, upon association with its ligands Delta or Jagged, un...

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Section: Discussionmentioning

confidence: 89%

Notch signaling distinguishes 2 waves of definitive hematopoiesis in the zebrafish embryo

Bertrand¹,

Cisson²,

Stachura³

et al. 2010

Blood

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“…1C). Taken together, a picture emerges of a graded dependence on Fgf signalling whereby ventricular fate is most dependent on Fgf, with atrial differentiation requiring less, and anterior blood/endothelium less still (Keegan et al, 2004;Warga et al, 2009) (Fig. 6A).…”

Section: Discussionmentioning

confidence: 99%

Fgf differentially controls cross-antagonism between cardiac and haemangioblast regulators

2011

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SUMMARYFibroblast growth factor (Fgf) has been implicated in the control of heart size during development, although whether this is by controlling cell fate, survival or proliferation has not been clear. Here, we show that Fgf, without affecting survival or proliferation, acts during gastrulation to drive cardiac fate and restrict anterior haemangioblast fate in zebrafish embryos. The haemangioblast programme was thought to be activated before the cardiac programme and is repressive towards it, suggesting that activation by Fgf of the cardiac programme might be via suppression of the haemangioblast programme. However, we show that the cardiac regulator nkx2.5 can also repress the haemangioblast programme and, furthermore, that cardiac specification still requires Fgf signalling even when haemangioblast regulators are independently suppressed. We further show that nkx2.5 and the cloche candidate gene lycat are expressed during gastrulation and regulated by Fgf, and that nkx2.5 overexpression, together with loss of the lycat targets etsrp and scl can stably induce expansion of the heart. We conclude that Fgf controls cardiac and haemangioblast fates by the simultaneous regulation of haemangioblast and cardiac regulators. We propose that elevation of Fgf signalling in the anterior haemangioblast territory could have led to its recruitment into the heart field during evolution, increasing the size of the heart.

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“…Quantitative RT-PCR was performed as previously described (Xiong et al, 2006). Specific pairs of primers were referred to followings: 5'-AGACTGCTGTAAGGAGTGTCCTC-3' (chd forward), 5'-CCATGAAGTCCTCTATGCATTCCG-3' (chd reverse), 5'-CAGAGCTCACTTAGGGAAAGGCTC-3' (bmp2 forward), 5'-CCAATAGTCTAGTGATGGGCTCCTG-3' (bmp2 reverse), 5'-CCGGTCTGCTCAGTCCAGACC-3' (gata1 forward), 5'-GGAAAGGGCTACTGGACCAGAC-3' (gata1 reverse), 5'-GGA-CAGCCTCCTCCCTAAGGC-3' (ctn forward), 5'-CAGTTCTAGCT-GGTTGATGCGG-3' (ctn reverse), 5'-ATGGATGATGAAATTGCCG-CAC-3' (β-actin forward), 5'-ACCATCACCAGAGTCCATCACG-3' (β-actin reverse), 5'-TCAGACGAGAAGACGGAACA-3' (myod forward), 5'-CACGATGCTGGACAGACAAT-3' (myod reverse), 5'-GGGAC-CATTGTGGTCGACAG-3' (shha forward), 5'-GCTTGAGTTTACT-GACATCCC-3' (shha reverse), 5'-CCCGCGCGGAGCCGCC-GCTGC-3' (sox9b forward) and 5'-GCAGGTGCGGGTACTGG-TCCGC-3' (sox9b reverse) (Maves et al, 2007;Warga et al, 2009). …”

Section: Morpholinos Design and Microinjectionmentioning

confidence: 99%

Nusap1 is essential for neural crest cell migration in zebrafish

Nie

Wang

et al. 2010

Protein Cell

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Microtubules play important roles in mitotic spindle assembly and chromosome segregation to maintain normal cell cycle progression. A number of microtubule-associated proteins have been identified in epithelial and neural cell cultures; however, their physiological significance is not well characterized due to the lack of appropriate in vivo animal models. Nucleolar spindleassociated protein (NuSAP) is a microtubule-binding protein and is reported to be involved in mitosis by cell culture studies. In this report, we identified the zebrafish homologue of human NuSAP and investigated its expression profile and functions. Using in situ hybridization, we demonstrated that transcripts of zebrafish nusap1 are specifically expressed in the retina, forebrain, hindbrain and neural crest. When the in vivo expression of nusap1 was knocked down through antisense oligonucleotide morpholino technology, the morphants of nusap1 showed impaired morphogenesis in the trunk and yolk extension, implying the involvement of Nusap1 in cell migration. Mechanistic studies revealed that nusap1 morphants have an altered expression pattern of neural crest markers crestin and sox9b, but normal expression of blood vessel and notochord markers gata1 and shh. In addition, nusap1 mRNA injection caused serious apoptosis in retina and hindbrain tissue, and these phenotypes can be rescued by co-injection of morpholino against nusap1. These observations not only suggest a role for Nusap1 in connecting apoptosis with cell migration, but also provide strong evidences that Nusap1 is potentially involved in morphogenesis in vertebrates.

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Fate Mapping Embryonic Blood in Zebrafish: Multi- and Unipotential Lineages Are Segregated at Gastrulation

Cited by 73 publications

References 60 publications

Notch signaling distinguishes 2 waves of definitive hematopoiesis in the zebrafish embryo

Notch signaling distinguishes 2 waves of definitive hematopoiesis in the zebrafish embryo

Fgf differentially controls cross-antagonism between cardiac and haemangioblast regulators

Nusap1 is essential for neural crest cell migration in zebrafish

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