Embryonic origin of the adult hematopoietic system: advances and questions

SLAM Family Receptors Distinguish Hematopoietic Stem and Progenitor Cells and Reveal Endothelial Niches for Stem Cells

Kiel, M. J., Yilmaz, Ö. H., Iwashita, T., Yilmaz, O. H., Terhorst, C., & Morrison, S. J. (2005) · Cell · doi:10.1016/j.cell.2005.05.026 · Cited by 3,168

AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis.

Okuda, T., van Deursen, J., Hiebert, S. W., Grosveld, G., & Downing, J. R. (1996) · Cell · doi:10.1016/s0092-8674(00)80986-1 · Cited by 1,856

Differentiation of Embryonic Stem Cells to Clinically Relevant Populations: Lessons from Embryonic Development

Murry, C. E., & Keller, G. (2008) · Cell · doi:10.1016/j.cell.2008.02.008 · Cited by 1,729

Definitive Hematopoiesis Is Autonomously Initiated by the AGM Region

Medvinsky, A., & Dzierzak, E. (1996) · Cell · doi:10.1016/s0092-8674(00)80165-8 · Cited by 1,548

A common precursor for hematopoietic and endothelial cells

Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J. C., & Keller, G. (1998) · Development · doi:10.1242/dev.125.4.725 · Cited by 1,427

Targeted Deficiency or Cytosolic Truncation of the VE-cadherin Gene in Mice Impairs VEGF-Mediated Endothelial Survival and Angiogenesis

Carmeliet, P., Lampugnani, M.-G., Moons, L., Breviario, F., Compernolle, V., Bono, F., Balconi, G., Spagnuolo, R., Oosthuyse, B., Dewerchin, M., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)81010-7 · Cited by 1,283

Embryonic stem cell differentiation: emergence of a new era in biology and medicine

Keller, G. (2005) · Genes & Development · doi:10.1101/gad.1303605 · Cited by 1,151

Haematopoietic stem cells derive directly from aortic endothelium during development

Bertrand, J. Y., Chi, N. C., Santoso, B., Teng, S., Stainier, D. Y. R., & Traver, D. (2010) · Nature · doi:10.1038/nature08738 · Cited by 1,025

Ontogeny of the Haemopoietic System: Yolk Sac Origin of In Vivo and In Vitro Colony Forming Cells in the Developing Mouse Embryo*

Moore, M. A. S., & Metcalf, D. (1970) · British Journal of Haematology · doi:10.1111/j.1365-2141.1970.tb01443.x · Cited by 1,017

Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter

Chen, M. J., Yokomizo, T., Zeigler, B. M., Dzierzak, E., & Speck, N. A. (2009) · Nature · doi:10.1038/nature07619 · Cited by 1,013

Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse

Palis, J., Robertson, S., Kennedy, M., Wall, C., & Keller, G. (1999) · Development · doi:10.1242/dev.126.22.5073 · Cited by 965

Blood stem cells emerge from aortic endothelium by a novel type of cell transition

Kissa, K., & Herbomel, P. (2010) · Nature · doi:10.1038/nature08761 · Cited by 961

In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium

Boisset, J.-C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E., & Robin, C. (2010) · Nature · doi:10.1038/nature08764 · Cited by 917

Notch signaling is required for arterial-venous differentiation during embryonic vascular development

Lawson, N. D., Scheer, N., Pham, V. N., Kim, C.-H., Chitnis, A. B., Campos-Ortega, J. A., & Weinstein, B. M. (2001) · Development · doi:10.1242/dev.128.19.3675 · Cited by 915

Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis.

Ziche, M., Morbidelli, L., Choudhuri, R., Zhang, H. T., Donnini, S., Granger, H. J., & Bicknell, R. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119451 · Cited by 915

Development of hematopoietic stem cell activity in the mouse embryo

Müller, A. M., Medvinsky, A., Strouboulis, J., Grosveld, F., & Dzierzakt, E. (1994) · Immunity · doi:10.1016/1074-7613(94)90081-7 · Cited by 901

Angiogenesis: A Team Effort Coordinated by Notch

Phng, L.-K., & Gerhardt, H. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.01.015 · Cited by 832

Progressive lineage analysis by cell sorting and culture identifies FLK1+VEcadherin+ cells at a diverging point of endothelial and hemopoietic lineages

Nishikawa, S.-I., Nishikawa, S., Hirashima, M., Matsuyoshi, N., & Kodama, H. (1998) · Development · doi:10.1242/dev.125.9.1747 · Cited by 829

Multipotent Flk-1+ Cardiovascular Progenitor Cells Give Rise to the Cardiomyocyte, Endothelial, and Vascular Smooth Muscle Lineages

Kattman, S. J., Huber, T. L., & Keller, G. M. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.10.002 · Cited by 729

Of lineage and legacy: the development of mammalian hematopoietic stem cells

Dzierzak, E., & Speck, N. A. (2008) · Nature Immunology · doi:10.1038/ni1560 · Cited by 707

Haemangioblast commitment is initiated in the primitive streak of the mouse embryo

Huber, T. L., Kouskoff, V., Joerg Fehling, H., Palis, J., & Keller, G. (2004) · Nature · doi:10.1038/nature03122 · Cited by 698

Fate tracing reveals the endothelial origin of hematopoietic stem cells

Zovein, A. C., Hofmann, J. J., Lynch, M., French, W. J., Turlo, K. A., Yang, Y., Becker, M. S., Zanetta, L., Dejana, E., Gasson, J. C., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.09.018 · Cited by 691

Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity

You, L.-R., Lin, F.-J., Lee, C. T., DeMayo, F. J., Tsai, M.-J., & Tsai, S. Y. (2005) · Nature · doi:10.1038/nature03511 · Cited by 666

Cbfa2 is required for the formation of intra-aortic hematopoietic clusters

North, T., Gu, T.-L., Stacy, T., Wang, Q., Howard, L., Binder, M., Marín-Padilla, M., & Speck, N. A. (1999) · Development · doi:10.1242/dev.126.11.2563 · Cited by 662

The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage

Lancrin, C., Sroczynska, P., Stephenson, C., Allen, T., Kouskoff, V., & Lacaud, G. (2009) · Nature · doi:10.1038/nature07679 · Cited by 633

Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo

de Bruijn, M. F. T. R. (2000) · The EMBO Journal · doi:10.1093/emboj/19.11.2465 · Cited by 616

Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny

Jaffredo, T., Gautier, R., Eichmann, A., & Dieterlen-Lièvre, F. (1998) · Development · doi:10.1242/dev.125.22.4575 · Cited by 591

Runx1 Expression Marks Long-Term Repopulating Hematopoietic Stem Cells in the Midgestation Mouse Embryo

North, T. E., de Bruijn, M. F. T. R., Stacy, T., Talebian, L., Lind, E., Robin, C., Binder, M., Dzierzak, E., & Speck, N. A. (2002) · Immunity · doi:10.1016/s1074-7613(02)00296-0 · Cited by 583

The placenta is a niche for hematopoietic stem cells

Gekas, C., Dieterlen-Lièvre, F., Orkin, S. H., & Mikkola, H. K. A. (2005) · Developmental Cell · doi:10.1016/j.devcel.2004.12.016 · Cited by 570

Continuous single-cell imaging of blood generation from haemogenic endothelium

Eilken, H. M., Nishikawa, S.-I., & Schroeder, T. (2009) · Nature · doi:10.1038/nature07760 · Cited by 569

Lymphoid Potential, Probed before Circulation in Mouse, Is Restricted to Caudal Intraembryonic Splanchnopleura

Cumano, A., Dieterlen-Lievre, F., & Godin, I. (1996) · Cell · doi:10.1016/s0092-8674(00)80166-x · Cited by 569

Biomechanical forces promote embryonic haematopoiesis

Adamo, L., Naveiras, O., Wenzel, P. L., McKinney-Freeman, S., Mack, P. J., Gracia-Sancho, J., Suchy-Dicey, A., Yoshimoto, M., Lensch, M. W., Yoder, M. C., et al. (2009) · Nature · doi:10.1038/nature08073 · Cited by 534

Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development

Murayama, E., Kissa, K., Zapata, A., Mordelet, E., Briolat, V., Lin, H.-F., Handin, R. I., & Herbomel, P. (2006) · Immunity · doi:10.1016/j.immuni.2006.10.015 · Cited by 532

Aorta-associated CD34+ hematopoietic cells in the early human embryo

Tavian, M., Coulombel, L., Luton, D., Clemente, H., Dieterlen-Lievre, F., & Peault, B. (1996) · Blood · doi:10.1182/blood.v87.1.67.67 · Cited by 509

An early pre-liver intraembryonic source of CFU-S in the developing mouse

Medvinsky, A. L., Samoylina, N. L., Müller, A. M., & Dzierzak, E. A. (1993) · Nature · doi:10.1038/364064a0 · Cited by 508

Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures

Kennedy, M., D'Souza, S. L., Lynch-Kattman, M., Schwantz, S., & Keller, G. (2007) · Blood · doi:10.1182/blood-2006-09-047704 · Cited by 483

Hematopoietic Stem Cells Localize to the Endothelial Cell Layer in the Midgestation Mouse Aorta

de Bruijn, M. F. T. R., Ma, X., Robin, C., Ottersbach, K., Sanchez, M.-J., & Dzierzak, E. (2002) · Immunity · doi:10.1016/s1074-7613(02)00313-8 · Cited by 474

Notch1 but Not Notch2 Is Essential for Generating Hematopoietic Stem Cells from Endothelial Cells

Kumano, K., Chiba, S., Kunisato, A., Sata, M., Saito, T., Nakagami-Yamaguchi, E., Yamaguchi, T., Masuda, S., Shimizu, K., Takahashi, T., et al. (2003) · Immunity · doi:10.1016/s1074-7613(03)00117-1 · Cited by 469

Cell tracing shows the contribution of the yolk sac to adult haematopoiesis

Samokhvalov, I. M., Samokhvalova, N. I., & Nishikawa, S.-I. (2007) · Nature · doi:10.1038/nature05725 · Cited by 460

Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy.

Szilvassy, S. J., Humphries, R. K., Lansdorp, P. M., Eaves, A. C., & Eaves, C. J. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.22.8736 · Cited by 450

Hematopoietic Stem Cell Development Is Dependent on Blood Flow

North, T. E., Goessling, W., Peeters, M., Li, P., Ceol, C., Lord, A. M., Weber, G. J., Harris, J., Cutting, C. C., Huang, P., et al. (2009) · Cell · doi:10.1016/j.cell.2009.04.023 · Cited by 447

The Murine Placenta Contains Hematopoietic Stem Cells within the Vascular Labyrinth Region

Ottersbach, K., & Dzierzak, E. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.02.001 · Cited by 445

Studies on the origin of blood vessels and of red corpuscles as seen in the living blastoderm of the chick during the second day of incubation

Sabin, F. (1920) · Medical Entomology and Zoology · Cited by 444

Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver

Kumaravelu, P., Hook, L., Morrison, A. M., Ure, J., Zhao, S., Zuyev, S., Ansell, J., & Medvinsky, A. (2002) · Development · doi:10.1242/dev.129.21.4891 · Cited by 434

Ontogeny of the Hematopoietic System

Cumano, A., & Godin, I. (2007) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141538 · Cited by 434

Sox17 Dependence Distinguishes the Transcriptional Regulation of Fetal from Adult Hematopoietic Stem Cells

Kim, I., Saunders, T. L., & Morrison, S. J. (2007) · Cell · doi:10.1016/j.cell.2007.06.011 · Cited by 421

Characterization of Definitive Lymphohematopoietic Stem Cells in the Day 9 Murine Yolk Sac

Yoder, M. C., Hiatt, K., Dutt, P., Mukherjee, P., Bodine, D. M., & Orlic, D. (1997) · Immunity · doi:10.1016/s1074-7613(00)80355-6 · Cited by 419

The SCL gene specifies haemangioblast development from early mesoderm

Gering, M., Rodaway, A. R. F., Göttgens, B., Patient, R. K., & Green, A. R. (1998) · The EMBO Journal · doi:10.1093/emboj/17.14.4029 · Cited by 418

Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis

Pardanaud, L., Luton, D., Prigent, M., Bourcheix, L.-M., Catala, M., & Dieterlen-Lièvre, F. (1996) · Development · doi:10.1242/dev.122.5.1363 · Cited by 417

On the origin of haemopoietic stem cells in the avian embryo: an experimental approach

Dieterlen-Lievre, F. (1975) · Development · doi:10.1242/dev.33.3.607 · Cited by 403

The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo

Kinder, S. J., Tsang, T. E., Quinlan, G. A., Hadjantonakis, A.-K., Nagy, A., & Tam, P. P. L. (1999) · Development · doi:10.1242/dev.126.21.4691 · Cited by 403

Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2

Eichmann, A., Corbel, C., Nataf, V., Vaigot, P., Bréant, C., & Le Douarin, N. M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5141 · Cited by 401

Hematopoietic stem cell fate is established by the Notch-Runx pathway

Burns, C. E., Traver, D., Mayhall, E., Shepard, J. L., & Zon, L. I. (2005) · Genes & Development · doi:10.1101/gad.1337005 · Cited by 401

Para-aortic splanchnopleura from early mouse embryos contains B1a cell progenitors

Godin, I. E., Garcia-Porrero, J. A., Coutinho, A., Dieterlen-Lièvre, F., & Marcos, M. A. R. (1993) · Nature · doi:10.1038/364067a0 · Cited by 388

Fetal and Adult Hematopoietic Stem Cells Require β1 Integrin Function for Colonizing Fetal Liver, Spleen, and Bone Marrow

Potocnik, A. J., Brakebusch, C., & Fässler, R. (2000) · Immunity · doi:10.1016/s1074-7613(00)80216-2 · Cited by 379

Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells

Zhang, C. C., Kaba, M., Ge, G., Xie, K., Tong, W., Hug, C., & Lodish, H. F. (2006) · Nature Medicine · doi:10.1038/nm1342 · Cited by 368

Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo

Mikkola, H. K. A., Fujiwara, Y., Schlaeger, T. M., Traver, D., & Orkin, S. H. (2003) · Blood · doi:10.1182/blood-2002-06-1699 · Cited by 356

In Vitro Generation of Lymphohematopoietic Cells from Endothelial Cells Purified from Murine Embryos

Nishikawa, S.-I., Nishikawa, S., Kawamoto, H., Yoshida, H., Kizumoto, M., Kataoka, H., & Katsura, Y. (1998) · Immunity · doi:10.1016/s1074-7613(00)80581-6 · Cited by 352

Intraembryonic, but Not Yolk Sac Hematopoietic Precursors, Isolated before Circulation, Provide Long-Term Multilineage Reconstitution

Cumano, A., Ferraz, J. C., Klaine, M., Di Santo, J. P., & Godin, I. (2001) · Immunity · doi:10.1016/s1074-7613(01)00190-x · Cited by 345

Differential Requirements for α4 Integrins during Fetal and Adult Hematopoiesis

Arroyo, A. G., Yang, J. T., Rayburn, H., & Hynes, R. O. (1996) · Cell · doi:10.1016/s0092-8674(00)81301-x · Cited by 335

CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo

Ferkowicz, M. J., Starr, M., Xie, X., Li, W., Johnson, S. A., Shelley, W. C., Morrison, P. R., & Yoder, M. C. (2003) · Development · doi:10.1242/dev.00632 · Cited by 333

Cellular mechanics and gene expression in blood vessels

Lehoux, S., & Tedgui, A. (2003) · Journal of Biomechanics · doi:10.1016/s0021-9290(02)00441-4 · Cited by 333

Impaired migration but not differentiation of haematopoietic stem cells in the absence of β1 integrins

Hirsch, E., Iglesias, A., Potocnik, A. J., Hartmann, U., & Fässler, R. (1996) · Nature · doi:10.1038/380171a0 · Cited by 332

Hedgehog Signaling Is Required for Adult Blood Stem Cell Formation in Zebrafish Embryos

Gering, M., & Patient, R. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.01.010 · Cited by 328

The Emergence of Hematopoietic Stem Cells Is Initiated in the Placental Vasculature in the Absence of Circulation

Rhodes, K. E., Gekas, C., Wang, Y., Lux, C. T., Francis, C. S., Chan, D. N., Conway, S., Orkin, S. H., Yoder, M. C., & Mikkola, H. K. A. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.01.001 · Cited by 325

A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula

Vogeli, K. M., Jin, S.-W., Martin, G. R., & Stainier, D. Y. R. (2006) · Nature · doi:10.1038/nature05045 · Cited by 319

GATA-2 Plays Two Functionally Distinct Roles during the Ontogeny of Hematopoietic Stem Cells

Ling, K.-W., Ottersbach, K., van Hamburg, J. P., Oziemlak, A., Tsai, F.-Y., Orkin, S. H., Ploemacher, R., Hendriks, R. W., & Dzierzak, E. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20031556 · Cited by 316

Characterization of the First Definitive Hematopoietic Stem Cells in the AGM and Liver of the Mouse Embryo

Sánchez, M.-J., Holmes, A., Miles, C., & Dzierzak, E. (1996) · Immunity · doi:10.1016/s1074-7613(00)80267-8 · Cited by 304

Vessel Patterning in the Embryo of the Zebrafish: Guidance by Notochord

Fouquet, B., Weinstein, B. M., Serluca, F. C., & Fishman, M. C. (1997) · Developmental Biology · doi:10.1006/dbio.1996.8495 · Cited by 300

Circulation is established in a stepwise pattern in the mammalian embryo

McGrath, K. E., Koniski, A. D., Malik, J., & Palis, J. (2003) · Blood · doi:10.1182/blood-2002-08-2531 · Cited by 293

Runx1 is required for zebrafish blood and vessel development and expression of a human RUNX1-CBF2T1 transgene advances a model for studies of leukemogenesis

Kalev-Zylinska, M. L., Horsfield, J. A., Flores, M. V. C., Postlethwait, J. H., Vitas, M. R., Baas, A. M., Crosier, P. S., & Crosier, K. E. (2002) · Development · doi:10.1242/dev.129.8.2015 · Cited by 289

Extensive Hematopoietic Stem Cell Generation in the AGM Region via Maturation of VE-Cadherin+CD45+ Pre-Definitive HSCs

Taoudi, S., Gonneau, C., Moore, K., Sheridan, J. M., Blackburn, C. C., Taylor, E., & Medvinsky, A. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.06.004 · Cited by 289

Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin

Bertrand, J. Y., Giroux, S., Golub, R., Klaine, M., Jalil, A., Boucontet, L., Godin, I., & Cumano, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402270102 · Cited by 283

Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential

Yoshimoto, M., Montecino-Rodriguez, E., Ferkowicz, M. J., Porayette, P., Shelley, W. C., Conway, S. J., Dorshkind, K., & Yoder, M. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015841108 · Cited by 282

RBPjκ-dependent Notch function regulates Gata2 and is essential for the formation of intra-embryonic hematopoietic cells

Robert-Moreno, A., Espinosa, L., de la Pompa, J. L., & Bigas, A. (2005) · Development · doi:10.1242/dev.01660 · Cited by 278

All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac

Lux, C. T., Yoshimoto, M., McGrath, K., Conway, S. J., Palis, J., & Yoder, M. C. (2008) · Blood · doi:10.1182/blood-2007-08-107086 · Cited by 273

Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos

Yokomizo, T., & Dzierzak, E. (2010) · Development · doi:10.1242/dev.051094 · Cited by 270

VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus

Cleaver, O., & Krieg, P. A. (1998) · Development · doi:10.1242/dev.125.19.3905 · Cited by 260

Haploinsufficiency of AML1 Affects the Temporal and Spatial Generation of Hematopoietic Stem Cells in the Mouse Embryo

Cai, Z., de Bruijn, M., Ma, X., Dortland, B., Luteijn, T., Downing, J. R., & Dzierzak, E. (2000) · Immunity · doi:10.1016/s1074-7613(00)00042-x · Cited by 254

Runx1-mediated hematopoietic stem-cell emergence is controlled by a Gata/Ets/SCL-regulated enhancer

Nottingham, W. T., Jarratt, A., Burgess, M., Speck, C. L., Cheng, J.-F., Prabhakar, S., Rubin, E. M., Li, P.-S., Sloane-Stanley, J., Kong-a-San, J., et al. (2007) · Blood · doi:10.1182/blood-2007-07-100883 · Cited by 249

In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus

Yoder, M. C., Hiatt, K., & Mukherjee, P. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6776 · Cited by 244

Clonal Analysis of Mouse Development Reveals a Polyclonal Origin for Yolk Sac Blood Islands

Ueno, H., & Weissman, I. L. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.08.001 · Cited by 242

The homeodomain protein Meis1 is essential for definitive hematopoiesis and vascular patterning in the mouse embryo

Azcoitia, V., Aracil, M., Martínez-A, C., & Torres, M. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.01.004 · Cited by 240

A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development

Hadland, B. K., Huppert, S. S., Kanungo, J., Xue, Y., Jiang, R., Gridley, T., Conlon, R. A., Cheng, A. M., Kopan, R., & Longmore, G. D. (2004) · Blood · doi:10.1182/blood-2004-03-1224 · Cited by 240

The Human Embryo, but Not Its Yolk Sac, Generates Lympho-Myeloid Stem Cells

Tavian, M., Robin, C., Coulombel, L., & Péault, B. (2001) · Immunity · doi:10.1016/s1074-7613(01)00193-5 · Cited by 231

Blood island formation: longstanding observations and modern interpretations

Ferkowicz, M. J., & Yoder, M. C. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2005.06.006 · Cited by 230

Distinct Origins of Adult and Embryonic Blood in Xenopus

Ciau-Uitz, A., Walmsley, M., & Patient, R. (2000) · Cell · doi:10.1016/s0092-8674(00)00067-2 · Cited by 228

Human Placenta Is a Potent Hematopoietic Niche Containing Hematopoietic Stem and Progenitor Cells throughout Development

Robin, C., Bollerot, K., Mendes, S., Haak, E., Crisan, M., Cerisoli, F., Lauw, I., Kaimakis, P., Jorna, R., Vermeulen, M., et al. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.08.020 · Cited by 228

The hematopoietic stem cell and its niche: a comparative view

Martinez-Agosto, J. A., Mikkola, H. K. A., Hartenstein, V., & Banerjee, U. (2007) · Genes & Development · doi:10.1101/gad.1602607 · Cited by 225

CD41+ cmyb+ precursors colonize the zebrafish pronephros by a novel migration route to initiate adult hematopoiesis

Bertrand, J. Y., Kim, A. D., Teng, S., & Traver, D. (2008) · Development · doi:10.1242/dev.015297 · Cited by 214

Functional identification of the hematopoietic stem cell niche in the ventral domain of the embryonic dorsal aorta

Taoudi, S., & Medvinsky, A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700984104 · Cited by 213

Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1

Robert‐Moreno, À., Guiu, J., Ruiz‐Herguido, C., López, M. E., Inglés‐Esteve, J., Riera, L., Tipping, A., Enver, T., Dzierzak, E., Gridley, T., et al. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.113 · Cited by 207

α4 Integrins Regulate the Proliferation/Differentiation Balance of Multilineage Hematopoietic Progenitors In Vivo

Arroyo, A. G., Yang, J. T., Rayburn, H., & Hynes, R. O. (1999) · Immunity · doi:10.1016/s1074-7613(00)80131-4 · Cited by 197

Hematopoietic development in the zebrafish

Paik, E. J., & Zon, L. I. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.093042ep · Cited by 181

The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential

Zeigler, B. M., Sugiyama, D., Chen, M., Guo, Y., Downs, K. M., & Speck, N. A. (2006) · Development · doi:10.1242/dev.02596 · Cited by 178

Requirement of Runx1/AML1/PEBP2αB for the generation of haematopoietic cells from endothelial cells

Yokomizo, T., Ogawa, M., Osato, M., Kanno, T., Yoshida, H., Fujimoto, T., Fraser, S., Nishikawa, S., Okada, H., Satake, M., et al. (2001) · Genes to Cells · doi:10.1046/j.1365-2443.2001.00393.x · Cited by 176

Mouse placenta is a major hematopoietic organ

Alvarez-Silva, M., Belo-Diabangouaya, P., Salaün, J., & Dieterlen-Lièvre, F. (2003) · Development · doi:10.1242/dev.00755 · Cited by 175

Live imaging of Runx1 expression in the dorsal aorta tracks the emergence of blood progenitors from endothelial cells

Lam, E. Y. N., Hall, C. J., Crosier, P. S., Crosier, K. E., & Flores, M. V. (2010) · Blood · doi:10.1182/blood-2010-01-264382 · Cited by 173

Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk

Pouget, C., Gautier, R., Teillet, M.-A., & Jaffredo, T. (2006) · Development · doi:10.1242/dev.02269 · Cited by 171

HGF/SF: a potent cytokine for mammary growth, morphogenesis and development

Niranjan, B., Buluwela, L., Yant, J., Perusinghe, N., Atherton, A., Phippard, D., Dale, T., Gusterson, B., & Kamalati, T. (1995) · Development · doi:10.1242/dev.121.9.2897 · Cited by 170

An Unexpected Role for IL-3 in the Embryonic Development of Hematopoietic Stem Cells

Robin, C., Ottersbach, K., Durand, C., Peeters, M., Vanes, L., Tybulewicz, V., & Dzierzak, E. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.07.002 · Cited by 161

Blood-borne seeding by hematopoietic and endothelial precursors from the allantois

Caprioli, A., Jaffredo, T., Gautier, R., Dubourg, C., & Dieterlen-Lièvre, F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.4.1641 · Cited by 161

Hedgehog and Bmp Polarize Hematopoietic Stem Cell Emergence in the Zebrafish Dorsal Aorta

Wilkinson, R. N., Pouget, C., Gering, M., Russell, A. J., Davies, S. G., Kimelman, D., & Patient, R. K. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.04.014 · Cited by 155

Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells

Durand, C., Robin, C., Bollérot, K., Baron, M. H., Ottersbach, K., & Dzierzak, E. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706923105 · Cited by 153

Zebrafish blood stem cells

Chen, A. T., & Zon, L. I. (2009) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22251 · Cited by 151

Zebrafish scl functions independently in hematopoietic and endothelial development

Dooley, K. A., Davidson, A. J., & Zon, L. I. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.09.004 · Cited by 149

Initiation of Murine Embryonic Erythropoiesis: A Spatial Analysis

Silver, L., & Palis, J. (1997) · Blood · doi:10.1182/blood.v89.4.1154 · Cited by 147

Progressive divergence of definitive haematopoietic stem cells from the endothelial compartment does not depend on contact with the foetal liver

Taoudi, S., Morrison, A. M., Inoue, H., Gribi, R., Ure, J., & Medvinsky, A. (2005) · Development · doi:10.1242/dev.01974 · Cited by 145

Polarized expression of bone morphogenetic protein-4 in the human aorta-gonad-mesonephros region

Marshall, C. J., Kinnon, C., & Thrasher, A. J. (2000) · Blood · doi:10.1182/blood.v96.4.1591.h8001591_1591_1593 · Cited by 143

The wall of the chick embryo aorta harbours M-CFC, G-CFC, GM-CFC and BFU-E

Cormier, F., & Dieterlen‐Lièvre, F. (1988) · Development · doi:10.1242/dev.102.2.279 · Cited by 141

The Glycoprotein IIb Molecule Is Expressed on Early Murine Hematopoietic Progenitors and Regulates Their Numbers in Sites of Hematopoiesis

Emambokus, N. R., & Frampton, J. (2003) · Immunity · doi:10.1016/s1074-7613(03)00173-0 · Cited by 135

Vascularization in the murine allantois occurs by vasculogenesis without accompanying erythropoiesis

Downs, K. M., Gifford, S. M., Blahnik, M., & Gardner, R. L. (1998) · Development · doi:10.1242/dev.125.22.4507 · Cited by 124

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

Bertrand, J. Y., Schwedler, J. L., Stachura, D. L., & Traver, D. J. (2010) · Blood · doi:10.1182/blood-2009-09-244590 · Cited by 123

Hematopoietic potential of the pre-fusion allantois

Corbel, C., Salaün, J., Diabangouaya, P., & Dieterlen‐Lièvre, F. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.08.069 · Cited by 113

Ventral embryonic tissues and Hedgehog proteins induce early AGM hematopoietic stem cell development

Peeters, M. C. E., Ottersbach, K., Bollérot, K., Orelio, C. C., Bruijn, M. F. T. R. D., Wijgerde, M., & Dzierzak, E. A. (2009) · Development · doi:10.1242/dev.034728 · Cited by 113

CD144 (VE-cadherin) is transiently expressed by fetal liver hematopoietic stem cells

Kim, I., Yilmaz, Ö. H., & Morrison, S. J. (2005) · Blood · doi:10.1182/blood-2004-12-4960 · Cited by 111

Definitive hematopoietic commitment within the embryonic vascular endothelial-cadherin+ population

Fraser, S. T., Ogawa, M., Yu, R. T., Nishikawa, S., Yöder, M. C., & Nishikawa, S.-I. (2002) · Experimental Hematology · doi:10.1016/s0301-472x(02)00887-1 · Cited by 107

Hemopoietic stem cells in murine embryonic yolk sac and peripheral blood.

Toles, J. F., Chui, D. H. K., Belbeck, L. W., Starr, E., & Barker, J. E. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.19.7456 · Cited by 105

AML1/Runx1 rescues Notch1-null mutation-induced deficiency of para-aortic splanchnopleural hematopoiesis

Nakagawa, M. M., Ichikawa, M., Kumano, K., Goyama, S., Kawazu, M., Asai, T., Ogawa, S., Kurokawa, M., & Chiba, S. (2006) · Blood · doi:10.1182/blood-2006-04-019570 · Cited by 96

HoxA3 is an apical regulator of haemogenic endothelium

Iacovino, M., Chong, D. C., Szatmári, I., Hartweck, L. M., Rux, D. R., Caprioli, A., Cleaver, O. B., & Kyba, M. (2010) · Nature Cell Biology · doi:10.1038/ncb2137 · Cited by 88

Endothelial Cells in the Early Murine Yolk Sac Give Rise to CD41-expressing Hematopoietic Cells

Li, W., Ferkowicz, M. J., Johnson, S. A., Shelley, W. C., & Yöder, M. C. (2005) · Stem Cells and Development · doi:10.1089/scd.2005.14.44 · Cited by 87

Vascular remodeling of the vitelline artery initiates extravascular emergence of hematopoietic clusters

Zovein, A. C., Turlo, K. A., Ponec, R. M., Lynch, M. R., Chen, K. C., Hofmann, J. J., Cox, T. C., Gasson, J. C., & Iruela‐Arispe, M. L. (2010) · Blood · doi:10.1182/blood-2010-04-279497 · Cited by 87

Hematopoietic stem cell emergence in the conceptus and the role of Runx1

Swiers, G., Bruijn, M. F. T. R. D., & Speck, N. A. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.103106gs · Cited by 85

Hematopoietic cell development in the zebrafish embryo

Bertrand, J. Y., & Traver, D. J. (2009) · Current Opinion in Hematology · doi:10.1097/moh.0b013e32832c05e4 · Cited by 81

Development of day-8 colony-forming unit-spleen hematopoietic progenitors during early murine embryogenesis: spatial and temporal mapping

Medvinskiĭ, A. L., Gan, O. I., Semenova, М. L., & Samoylina, N. L. (1996) · Blood · doi:10.1182/blood.v87.2.557.bloodjournal872557 · Cited by 79

Runx1 is involved in primitive erythropoiesis in the mouse

Yokomizo, T., Hasegawa, K., Ishitobi, H., Osato, M., Ema, M., Ito, Y., Yamamoto, M., & Takahashi, S. (2008) · Blood · doi:10.1182/blood-2007-05-091637 · Cited by 78

Nitric Oxide Is a Regulator of Hematopoietic Stem Cell Activity

Michurina, T. V., Krasnov, P. A., Balazs, A. B., Nakaya, N., Vasilieva, T. V., Ba, K., Khrushchov, N. G., Mulligan, R. C., & Enikolopov, G. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2004.05.030 · Cited by 75

“Hemogenic endothelium” of the embryonic aorta: Does it exist?

Smith, R. A., & Glomski, C. A. (1982) · Developmental & Comparative Immunology · doi:10.1016/s0145-305x(82)80019-0 · Cited by 71

Rac1 is essential for intraembryonic hematopoiesis and for the initial seeding of fetal liver with definitive hematopoietic progenitor cells

Ghiaur, G., Ferkowicz, M. J., Milsom, M. D., Bailey, J., Witte, D. P., Cancelas, J. A., Yöder, M. C., & Williams, D. A. (2007) · Blood · doi:10.1182/blood-2007-08-110114 · Cited by 69

Normal and Neoplastic Maturation of T-lineage LymphocytesPreprint

Weissman, I. L., Baird, S., Gardner, R. L., Papaioannou, V. E., & Raschke, W. C. (1977) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1977.041.01.005 · Cited by 65

Are Intra-Aortic Hemopoietic Cells Derived from Endothelial Cells During Ontogeny?

Dieterlen‐Lièvre, F., Pouget, C., Bollérot, K., & Jaffredo, T. (2006) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2006.02.005 · Cited by 63

αIIb Integrin Expression during Development of the Murine Hemopoietic System

Corbel, C., & Salaün, J. (2002) · Developmental Biology · doi:10.1006/dbio.2001.0553 · Cited by 62

Early Placental Ontogeny in the Mouse

Downs, K. M. (2002) · Placenta · doi:10.1053/plac.2001.0763 · Cited by 61

The transcriptionally active form of AML1 is required for hematopoietic rescue of the AML1-deficient embryonic para-aortic splanchnopleural (P-Sp) region

Goyama, S., Yamaguchi, Y., Imai, Y., Kawazu, M., Nakagawa, M. M., Asai, T., Kumano, K., Mitani, K., Ogawa, S., Chiba, S., et al. (2004) · Blood · doi:10.1182/blood-2004-04-1535 · Cited by 57

From mesoderm to blood islands: patterns of key molecules during yolk sac erythropoiesis

Minkó, K., Bollérot, K., Drevon, C., Hallais, M., & Jaffredo, T. (2003) · Gene Expression Patterns · doi:10.1016/s1567-133x(03)00053-x · Cited by 56

Genetic control of hematopoietic development in Xenopus and zebrafish

Ciau‐Uitz, A., Liu, F., & Patient, R. K. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.093055ac · Cited by 55

Tel1/ETV6 Specifies Blood Stem Cells through the Agency of VEGF Signaling

Ciau‐Uitz, A., Pinheiro, P., Gupta, R., Enver, T., & Patient, R. K. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.02.009 · Cited by 54

Novel roles for Notch, Wnt and Hedgehog in hematopoesis derived from human pluripotent stem cells

Cerdan, C., & Bhatia, M. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.103067cc · Cited by 54

Hey2 acts upstream of Notch in hematopoietic stem cell specification in zebrafish embryos

Rowlinson, J., & Gering, M. (2010) · Blood · doi:10.1182/blood-2009-11-252635 · Cited by 51

Flow-Mediated Signaling Modulates Endothelial Cell Phenotype

Garin, G., & Berk, B. C. (2006) · Endothelium · doi:10.1080/10623320601061599 · Cited by 46

Restoration of Runx1 Expression in the Tie2 Cell Compartment Rescues Definitive Hematopoietic Stem Cells and Extends Life of Runx1 Knockout Animals Until Birth

Liakhovitskaia, A., Gribi, R., Stamateris, E., Villain, G., Jaffredo, T., Wilkie, R., Gilchrist, D. S., Yang, J., Ure, J., & Medvinsky, A. (2009) · Stem Cells · doi:10.1002/stem.71 · Cited by 40

Distinct hemogenic potential of endothelial cells and CD41+ cells in mouse embryos

Hashimoto, K., Fujimoto, T., Shimoda, Y., Huang, X., Sakamoto, H., & Ogawa, M. (2007) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2007.00925.x · Cited by 33

Neuronal Nitric Oxide Synthase Contributes to the Regulation of Hematopoiesis

Krasnov, P. A., Michurina, T. V., Packer, M. A., Stasiv, Y., Nakaya, N., Moore, K. A., Drazan, K. E., & Enikolopov, G. (2008) · Molecular Medicine · doi:10.2119/2007-00011.krasnov · Cited by 32

The discovery of a source of adult hematopoietic cells in the embryo

Dzierzak, E. A., & Medvinsky, A. (2008) · Development · doi:10.1242/dev.021279 · Cited by 32

A novel method for the generation of reaggregated organotypic cultures that permits juxtaposition of defined cell populations

Sheridan, J. M., Taoudi, S., Medvinsky, A., & Blackburn, C. C. (2009) · genesis · doi:10.1002/dvg.20505 · Cited by 28

The differentiation program of embryonic definitive hematopoietic stem cells is largely α4 integrin independent

Gribi, R., Hook, L., Ure, J., & Medvinsky, A. (2006) · Blood · doi:10.1182/blood-2005-10-4209 · Cited by 26

Treatment of hypoplastic anemia in mice with placental transplants

Dancis, J., Jansen, V., Brown, G., Gorstein, F., & Balis, M. E. (1977) · Blood · doi:10.1182/blood.v50.4.663.663 · Cited by 21

Notch in the Niche

Gering, M., & Patient, R. K. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.03.016 · Cited by 10

C-Myb+ Erythro-Myeloid Progenitor-Derived Fetal Monocytes Give Rise to Adult Tissue-Resident Macrophages

Hoeffel, G., Chen, J., Lavin, Y., Low, D., Almeida, F. F., See, P., Beaudin, A. E., Lum, J., Low, I., Forsberg, E. C., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.03.011 · Cited by 1,135

Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)

Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531

Wnt signaling controls the specification of definitive and primitive hematopoiesis from human pluripotent stem cells

Sturgeon, C. M., Ditadi, A., Awong, G., Kennedy, M., & Keller, G. (2014) · Nature Biotechnology · doi:10.1038/nbt.2915 · Cited by 467

Cell cycle regulation in hematopoietic stem cells

Pietras, E. M., Warr, M. R., & Passegué, E. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201102131 · Cited by 447

Ontogeny of Tissue-Resident Macrophages

Hoeffel, G., & Ginhoux, F. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00486 · Cited by 364