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Development of Hematopoietic Stem Cells in Zebrafish

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Zebrafish, Medaka, and Other Small Fishes

Abstract

Hematopoietic stem cells (HSCs) are a rare population of cells with the remarkable abilities to both self-renew and differentiate into all types of mature blood cells. Understanding of the developmental mechanisms of HSCs is of great importance to instruct and expand HSCs from pluripotent precursors, such as induced pluripotent stem cells (iPSCs). The zebrafish is a unique vertebrate model in which numerous elegant experimental approaches can be applied to the study of HSC development, including live-imaging, chemical and genetic screening, and genome editing. HSCs are specified from a shared vascular precursor, the angioblast, and arise directly from the ventral floor of the dorsal aorta. HSCs then migrate to a transient hematopoietic organ, the caudal hematopoietic tissue, where microenvironmental niche cells promote the expansion of HSCs prior to the colonization of the kidney, the final adult hematopoietic organ in zebrafish. Over the past decade, a number of intrinsic and extrinsic signaling molecules involved in the specification, maintenance, migration, and proliferation of HSCs have been identified in the zebrafish embryo. Importantly, despite evolutional divergence, the genetic programs governing HSC development are highly conserved among vertebrates, indicating that studies in zebrafish may be translated to regenerative medicine using human iPSCs. This chapter highlights the current knowledge and recent advances regarding the cellular origin and molecular regulation of HSC development in zebrafish.

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References

  • Beerman I, Luis TC, Singbrant S, Lo Celso C, Méndez-Ferrer S (2017) The evolving view of the hematopoietic stem cell niche. Exp Hematol 50:22e6

    Article  Google Scholar 

  • Bertrand JY, Giroux S, Golub R et al (2005) Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proc Natl Acad Sci U S A 102:134–139

    Article  CAS  PubMed  Google Scholar 

  • Bertrand JY, Kim AD, Violette EP, Stachura DL, Cisson JL, Traver D (2007) Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development 134:4147–4156

    Article  CAS  PubMed  Google Scholar 

  • Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D (2010) Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464:108–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaser BW, Moore JL, Hagedorn EJ et al (2017) CXCR1 remodels the vascular niche to promote hematopoietic stem and progenitor cell engraftment. J Exp Med 214:1011–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C (2010) In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464:116–120

    Article  CAS  PubMed  Google Scholar 

  • Bozkulak EC, Weinmaster G (2009) Selective use of ADAM10 and ADAM17 in activation of Notch1 signaling. Mol Cell Biol 29:5679–5695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradbury J (2004) Small fish, big science. PLoS Biol 2:E148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brou C, Logeat F, Gupta N et al (2000) A novel proteolytic cleavage involved in notch signaling: the role of the disintegrin-metalloprotease TACE. Mol Cell 5:207–216

    Article  CAS  PubMed  Google Scholar 

  • Brown LA, Rodaway AR, Schilling TF et al (2000) Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor Fli-1 in wild-type and mutant zebrafish embryos. Mech Dev 90:237–252

    Article  CAS  PubMed  Google Scholar 

  • Burns CE, DeBlasio T, Zhou Y, Zhang J, Zon L, Nimer SD (2002) Isolation and characterization of runxa and runxb, zebrafish members of the runt family of transcriptional regulators. Exp Hematol 30:1381–1389

    Article  CAS  PubMed  Google Scholar 

  • Burns CE, Traver D, Mayhall E, Shepard JL, Zon LI (2005) Hematopoietic stem cell fate is established by the notch-Runx pathway. Genes Dev 19:2331–2342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butko E, Distel M, Pouget C et al (2015) Gata2b is a restricted early regulator of hemogenic endothelium in the zebrafish embryo. Development 142:1050–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrd N, Becker S, Maye P et al (2002) Hedgehog is required for murine yolk sac angiogenesis. Development 129:361–372

    CAS  PubMed  Google Scholar 

  • Chen W, Casey Corliss D (2004) Three modules of zebrafish mind bomb work cooperatively to promote Delta ubiquitination and endocytosis. Dev Biol 267:361–373

    Article  CAS  PubMed  Google Scholar 

  • Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA (2009) Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457:887–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheshier SH, Morrison SJ, Liao X, Weissman IL (1999) In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci U S A 96:3120–3125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin AJ, Chen JN, Weinberg ES (1997) Bone morphogenetic protein-4 expression characterizes inductive boundaries in organs of developing zebrafish. Dev Genes Evol 207:107–114

    Article  CAS  PubMed  Google Scholar 

  • Clements WK, Traver D (2013) Signalling pathways that control vertebrate haematopoietic stem cell specification. Nat Rev Immunol 13:336–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clements WK, Kim AD, Ong KG, Moore JC, Lawson ND, Traver D (2011) A somitic Wnt16/notch pathway specifies haematopoietic stem cells. Nature 474:220–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cortes M, Chen MJ, Stachura DL et al (2016) Developmental vitamin D availability impacts hematopoietic stem cell production. Cell Rep 17:458–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cumano A, Dieterlen-Lievre F, Godin I (1996) Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86:907–916

    Article  CAS  PubMed  Google Scholar 

  • Davidson AJ, Zon LI (2004) The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis. Oncogene 23:7233–7246

    Article  CAS  PubMed  Google Scholar 

  • Davis GE, Senger DR (2005) Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 97:1093–1107

    Article  CAS  PubMed  Google Scholar 

  • de Bruijn MF, Speck NA, Peeters MC, Dzierzak E (2000) Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 19:2465–2474

    Article  PubMed  PubMed Central  Google Scholar 

  • de Bruijn MF, Ma X, Robin C, Ottersbach K, Sanchez MJ, Dzierzak E (2002) Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 16:673–683

    Article  PubMed  Google Scholar 

  • de Jong JL, Zon LI (2005) Use of the zebrafish system to study primitive and definitive hematopoiesis. Annu Rev Genet 39:481–501

    Article  CAS  PubMed  Google Scholar 

  • de Pater E, Kaimakis P, Vink CS et al (2013) Gata2 is required for HSC generation and survival. J Exp Med 210:2843–2850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Detrich HW, Kieran MW, Chan FY et al (1995) Intraembryonic hematopoietic cell migration during vertebrate development. Proc Natl Acad Sci U S A 92:10713–10717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481:457–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dooley KA, Davidson AJ, Zon LI (2005) Zebrafish scl functions independently in hematopoietic and endothelial development. Dev Biol 277:522–536

    Article  CAS  PubMed  Google Scholar 

  • Dyer MA, Farrington SM, Mohn D, Munday JR, Baron MH (2001) Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 128:1717–1730

    CAS  PubMed  Google Scholar 

  • Dzierzak E, Medvinsky A (1995) Mouse embryonic hematopoiesis. Trends Genet 11:359–366

    Article  CAS  PubMed  Google Scholar 

  • Ehninger A, Trumpp A (2011) The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J Exp Med 208:421–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ema H, Nakauchi H (2000) Expansion of hematopoietic stem cells in the developing liver of a mouse embryo. Blood 95:2284–2288

    CAS  PubMed  Google Scholar 

  • Espín-Palazón R, Stachura DL, Campbell CA et al (2014) Proinflammatory signaling regulates hematopoietic stem cell emergence. Cell 159:1070–1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser ST, Ogawa M, Yu RT, Nishikawa S, Yoder MC (2002) Definitive hematopoietic commitment within the embryonic vascular endothelial-cadherin(+) population. Exp Hematol 30:1070–1078

    Article  CAS  PubMed  Google Scholar 

  • Gagnon JA, Valen E, Thyme SB et al (2014) Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS One 9:e98186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galloway JL, Zon LI (2003) Ontogeny of hematopoiesis: examining the emergence of hematopoietic cells in the vertebrate embryo. Curr Top Dev Biol 53:139–158

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Johnson KD, Chang YI et al (2013) Gata2 cis-element is required for hematopoietic stem cell generation in the mammalian embryo. J Exp Med 210:2833–2842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gekas C, Dieterlen-Lièvre F, Orkin SH, Mikkola HK (2005) The placenta is a niche for hematopoietic stem cells. Dev Cell 8:365–375

    Article  CAS  PubMed  Google Scholar 

  • Genthe JR, Clements WK (2017) R-spondin 1 is required for specification of hematopoietic stem cells through Wnt16 and Vegfa signaling pathways. Development 144:590–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gering M, Patient R (2005) Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Dev Cell 8:389–400

    Article  CAS  PubMed  Google Scholar 

  • Godin I, Cumano A (2002) The hare and the tortoise: an embryonic haematopoietic race. Nat Rev Immunol 2:593–604

    Article  CAS  PubMed  Google Scholar 

  • Goessling W, North TE, Loewer S et al (2009) Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 136:1136–1147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grainger S, Richter J, Palazón RE et al (2016) Wnt9a is required for the aortic amplification of nascent hematopoietic stem cells. Cell Rep 17:1595–1606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadland BK, Huppert SS, Kanungo J et al (2004) A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. Blood 104:3097–3105

    Article  CAS  PubMed  Google Scholar 

  • He Q, Zhang C, Wang L et al (2015) Inflammatory signaling regulates hematopoietic stem and progenitor cell emergence in vertebrates. Blood 125:1098–1106

    Article  CAS  PubMed  Google Scholar 

  • Heissig B, Hattori K, Friedrich M, Rafii S, Werb Z (2003) Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases. Curr Opin Hematol 10:136–141

    Article  CAS  PubMed  Google Scholar 

  • Henninger J, Santoso B, Hans S et al (2017) Clonal fate mapping quantifies the number of haematopoietic stem cells that arise during development. Nat Cell Biol 19:17–27

    Article  CAS  PubMed  Google Scholar 

  • Hisano Y, Sakuma T, Nakade S et al (2015) Precise in-frame integration of exogenous DNA mediated by CRISPR/Cas9 system in zebrafish. Sci Rep 5:8841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoggatt J, Kfoury Y, Scadden DT (2016) Hematopoietic stem cell niche in health and disease. Annu Rev Pathol 11:555–581

    Article  CAS  PubMed  Google Scholar 

  • Hsia N, Zon LI (2005) Transcriptional regulation of hematopoietic stem cell development in zebrafish. Exp Hematol 33:1007–1014

    Article  CAS  PubMed  Google Scholar 

  • Itoh M, Kim CH, Palardy G et al (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of notch signaling by Delta. Dev Cell 4:67–82

    Article  CAS  PubMed  Google Scholar 

  • Jao LE, Wente SR, Chen W (2013) Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A 110:13904–13909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132:5199–5209

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Xu J, Wen Z (2007) Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development. Blood 109:5208–5214

    Article  CAS  PubMed  Google Scholar 

  • Jing L, Tamplin OJ, Chen MJ et al (2015) Adenosine signaling promotes hematopoietic stem and progenitor cell emergence. J Exp Med 212:649–663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson KD, Hsu AP, Ryu MJ et al (2012) Cis-element mutated in GATA2-dependent immunodeficiency governs hematopoiesis and vascular integrity. J Clin Invest 122:3692–3704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalev-Zylinska ML, Horsfield JA, Flores MV et al (2002) Runx1 is required for zebrafish blood and vessel development and expression of a human RUNX1-CBF2T1 transgene advances a model for studies of leukemogenesis. Development 129:2015–2030

    CAS  PubMed  Google Scholar 

  • Kawahara A, Hisano Y, Ota S, Taimatsu K (2016) Site-specific integration of exogenous genes using genome editing technologies in zebrafish. Int J Mol Sci 17:727

    Article  CAS  PubMed Central  Google Scholar 

  • Khan JA, Mendelson A, Kunisaki Y et al (2016) Fetal liver hematopoietic stem cell niches associate with portal vessels. Science 351:176–180

    Article  CAS  PubMed  Google Scholar 

  • Kim AD, Melick CH, Clements WK et al (2014) Discrete notch signaling requirements in the specification of hematopoietic stem cells. EMBO J 33:2363–2373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kissa K, Herbomel P (2010) Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464:112–115

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi I, Kobayashi-Sun J, Kim AD et al (2014) Jam1a-Jam2a interactions regulate haematopoietic stem cell fate through notch signalling. Nature 512:319–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konantz M, Alghisi E, Müller JS et al (2016) Evi1 regulates notch activation to induce zebrafish hematopoietic stem cell emergence. EMBO J 35:2315–2331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kopan R, Ilagan MX (2009) The canonical notch signaling pathway: unfolding the activation mechanism. Cell 137:216–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krebs LT, Xue Y, Norton CR et al (2000) Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14:1343–1352

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kwan W, Cortes M, Frost I et al (2016) The central nervous system regulates embryonic HSPC production via stress-responsive glucocorticoid receptor signaling. Cell Stem Cell 19:370–382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lapidot T, Dar A, Kollet O (2005) How do stem cells find their way home? Blood 106:1901–1910

    Article  CAS  PubMed  Google Scholar 

  • Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307–318

    Article  CAS  PubMed  Google Scholar 

  • Lawson ND, Vogel AM, Weinstein BM (2002) Sonic hedgehog and vascular endothelial growth factor act upstream of the notch pathway during arterial endothelial differentiation. Dev Cell 3:127–136

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Manegold JE, Kim AD et al (2014) FGF signalling specifies haematopoietic stem cells through its regulation of somitic notch signalling. Nat Commun 5:5583

    Article  CAS  PubMed  Google Scholar 

  • Lessard J, Faubert A, Sauvageau G (2004) Genetic programs regulating HSC specification, maintenance and expansion. Oncogene 23:7199–7209

    Article  CAS  PubMed  Google Scholar 

  • Leung A, Ciau-Uitz A, Pinheiro P et al (2013) Uncoupling VEGFA functions in arteriogenesis and hematopoietic stem cell specification. Dev Cell 24:144–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Esain V, Teng L et al (2014) Inflammatory signaling regulates embryonic hematopoietic stem and progenitor cell production. Genes Dev 28:2597–2612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao EC, Paw BH, Oates AC, Pratt SJ, Postlethwait JH, Zon LI (1998) SCL/Tal-1 transcription factor acts downstream of cloche to specify hematopoietic and vascular progenitors in zebrafish. Genes Dev 12:621–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim KC, Hosoya T, Brandt W et al (2012) Conditional Gata2 inactivation results in HSC loss and lymphatic mispatterning. J Clin Invest 122:3705–3717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lizama CO, Hawkins JS, Schmitt CE et al (2015) Repression of arterial genes in hemogenic endothelium is sufficient for haematopoietic fate acquisition. Nat Commun 6:7739

    Article  PubMed  Google Scholar 

  • Luis TC, Weerkamp F, Naber BA et al (2009) Wnt3a deficiency irreversibly impairs hematopoietic stem cell self-renewal and leads to defects in progenitor cell differentiation. Blood 113:546–554

    Article  CAS  PubMed  Google Scholar 

  • Mahony CB, Fish RJ, Pasche C, Bertrand JY (2016) tfec controls the hematopoietic stem cell vascular niche during zebrafish embryogenesis. Blood 128:1336–1345

    Article  CAS  PubMed  Google Scholar 

  • Maye P, Becker S, Kasameyer E, Byrd N, Grabel L (2000) Indian hedgehog signaling in extraembryonic endoderm and ectoderm differentiation in ES embryoid bodies. Mech Dev 94:117–132

    Article  CAS  PubMed  Google Scholar 

  • McGrath KE, Frame JM, Fromm GJ et al (2011) A transient definitive erythroid lineage with unique regulation of the β-globin locus in the mammalian embryo. Blood 117:4600–4608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medvinsky A, Dzierzak E (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86:897–906

    Article  CAS  PubMed  Google Scholar 

  • Moncada S, Higgs EA (2006) Nitric oxide and the vascular endothelium. Handb Exp Pharmacol 176:213–254

    Article  Google Scholar 

  • Monteiro R, Pinheiro P, Joseph N et al (2016) Transforming growth factor β drives Hemogenic endothelium programming and the transition to hematopoietic stem cells. Dev Cell 38:358–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller AM, Medvinsky A, Strouboulis J, Grosveld F, Dzierzak E (1994) Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1:291–301

    Article  PubMed  Google Scholar 

  • Mumm JS, Schroeter EH, Saxena MT et al (2000) A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Mol Cell 5:197–206

    Article  CAS  PubMed  Google Scholar 

  • Murayama E, Kissa K, Zapata A et al (2006) Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25:963–975

    Article  CAS  PubMed  Google Scholar 

  • Murry CE, Keller G (2008) Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132:661–680

    Article  CAS  PubMed  Google Scholar 

  • North TE, de Bruijn MF, Stacy T et al (2002) Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 16:661–672

    Article  CAS  PubMed  Google Scholar 

  • North TE, Goessling W, Walkley CR et al (2007) Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447:1007–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • North TE, Goessling W, Peeters M et al (2009) Hematopoietic stem cell development is dependent on blood flow. Cell 137:736–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ottersbach K, Dzierzak E (2005) The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell 8:377–387

    Article  CAS  PubMed  Google Scholar 

  • Palis J, Robertson S, Kennedy M, Wall C, Keller G (1999) Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126:5073–5084

    CAS  PubMed  Google Scholar 

  • Patterson LJ, Gering M, Patient R (2005) Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood 105:3502–3511

    Article  CAS  PubMed  Google Scholar 

  • Pouget C, Peterkin T, Simões FC, Lee Y, Traver D, Patient R (2014) FGF signalling restricts haematopoietic stem cell specification via modulation of the BMP pathway. Nat Commun 5:5588

    Article  CAS  PubMed  Google Scholar 

  • Qian F, Zhen F, Xu J, Huang M, Li W, Wen Z (2007) Distinct functions for different scl isoforms in zebrafish primitive and definitive hematopoiesis. PLoS Biol 5:e132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren X, Gomez GA, Zhang B, Lin S (2010) Scl isoforms act downstream of etsrp to specify angioblasts and definitive hematopoietic stem cells. Blood 115:5338–5346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richard C, Drevon C, Canto PY et al (2013) Endothelio-mesenchymal interaction controls runx1 expression and modulates the notch pathway to initiate aortic hematopoiesis. Dev Cell 24:600–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robert-Moreno A, Guiu J, Ruiz-Herguido C et al (2008) Impaired embryonic haematopoiesis yet normal arterial development in the absence of the notch ligand Jagged1. EMBO J 27:1886–1895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Herguido C, Guiu J, D’Altri T et al (2012) Hematopoietic stem cell development requires transient Wnt/β-catenin activity. J Exp Med 209:1457–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rybtsov S, Sobiesiak M, Taoudi S et al (2011) Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region. J Exp Med 208:1305–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samokhvalov IM, Samokhvalova NI, Nishikawa S (2007) Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446:1056–1061

    Article  CAS  PubMed  Google Scholar 

  • Sawamiphak S, Kontarakis Z, Stainier DY (2014) Interferon gamma signaling positively regulates hematopoietic stem cell emergence. Dev Cell 31:640–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah AN, Davey CF, Whitebirch AC, Miller AC, Moens CB (2015) Rapid reverse genetic screening using CRISPR in zebrafish. Nat Methods 12:535–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shepard JL, Zon LI (2000) Developmental derivation of embryonic and adult macrophages. Curr Opin Hematol 7:3–8

    Article  CAS  PubMed  Google Scholar 

  • Soma T, Yu JM, Dunbar CE (1996) Maintenance of murine long-term repopulating stem cells in ex vivo culture is affected by modulation of transforming growth factor-beta but not macrophage inflammatory protein-1 alpha activities. Blood 87:4561–4567

    CAS  PubMed  Google Scholar 

  • Soza-Ried C, Hess I, Netuschil N, Schorpp M, Boehm T (2010) Essential role of c-myb in definitive hematopoiesis is evolutionarily conserved. Proc Natl Acad Sci U S A 107:17304–17308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stamatoyannopoulos G (2005) Control of globin gene expression during development and erythroid differentiation. Exp Hematol 33:259–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25:977–988

    Article  CAS  PubMed  Google Scholar 

  • Sumanas S, Lin S (2006) Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol 4:e10

    Article  CAS  PubMed  Google Scholar 

  • Sumanas S, Gomez G, Zhao Y, Park C, Choi K, Lin S (2008) Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 111:4500–4510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamplin OJ, Durand EM, Carr LA et al (2015) Hematopoietic stem cell arrival triggers dynamic remodeling of the perivascular niche. Cell 160:241–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taoudi S, Gonneau C, Moore K et al (2008) Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs. Cell Stem Cell 3:99–108

    Article  CAS  PubMed  Google Scholar 

  • Theodore LN, Hagedorn EJ, Cortes M et al (2017) Distinct roles for matrix Metalloproteinases 2 and 9 in embryonic hematopoietic stem cell emergence, migration, and niche colonization. Stem Cell Rep 8:1226–1241

    Article  CAS  Google Scholar 

  • Thompson MA, Ransom DG, Pratt SJ et al (1998) The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev Biol 197:248–269

    Article  CAS  PubMed  Google Scholar 

  • Tober J, Koniski A, McGrath KE et al (2007) The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood 109:1433–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai FY, Orkin SH (1997) Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 89:3636–3643

    CAS  PubMed  Google Scholar 

  • Tsai FY, Keller G, Kuo FC et al (1994) An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371:221–226

    Article  CAS  PubMed  Google Scholar 

  • Walkley CR, McArthur GA, Purton LE (2005) Cell division and hematopoietic stem cells: not always exhausting. Cell Cycle 4:893–896

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Zhang P, Wei Y, Gao Y, Patient R, Liu F (2011) A blood flow-dependent klf2a-NO signaling cascade is required for stabilization of hematopoietic stem cell programming in zebrafish embryos. Blood 118:4102–4110

    Article  CAS  PubMed  Google Scholar 

  • Warga RM, Kane DA, Ho RK (2009) Fate mapping embryonic blood in zebrafish: multi- and unipotential lineages are segregated at gastrulation. Dev Cell 16:744–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weissman IL (2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157–168

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson RN, Pouget C, Gering M et al (2009) Hedgehog and Bmp polarize hematopoietic stem cell emergence in the zebrafish dorsal aorta. Dev Cell 16:909–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamazaki S, Ema H, Karlsson G et al (2011) Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147:1146–1158

    Article  CAS  PubMed  Google Scholar 

  • Yoon MJ, Koo BK, Song R et al (2008) Mind bomb-1 is essential for intraembryonic hematopoiesis in the aortic endothelium and the subaortic patches. Mol Cell Biol 28:4794–4804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu VW, Scadden DT (2016) Heterogeneity of the bone marrow niche. Curr Opin Hematol 23:331–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Jin H, Li L, Qin FX, Wen Z (2011) cMyb regulates hematopoietic stem/progenitor cell mobilization during zebrafish hematopoiesis. Blood 118:4093–4101

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, He Q, Chen D et al (2015) G protein-coupled receptor 183 facilitates endothelial-to-hematopoietic transition via Notch1 inhibition. Cell Res 25:1093–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhen F, Lan Y, Yan B, Zhang W, Wen Z (2013) Hemogenic endothelium specification and hematopoietic stem cell maintenance employ distinct Scl isoforms. Development 140:3977–3985

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Zon LI (2002) Use of zebrafish models for the analysis of human disease. Curr Protoc Hum Genet Chapter 15: unit 15.13

    Google Scholar 

  • Zhu C, Smith T, McNulty J et al (2011) Evaluation and application of modularly assembled zinc-finger nucleases in zebrafish. Development 138:4555–4564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zovein AC, Hofmann JJ, Lynch M et al (2008) Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3:625–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Isao Kobayashi .

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Kobayashi, I. (2018). Development of Hematopoietic Stem Cells in Zebrafish. In: Hirata, H., Iida, A. (eds) Zebrafish, Medaka, and Other Small Fishes. Springer, Singapore. https://doi.org/10.1007/978-981-13-1879-5_3

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