Cited by 419Zebrafish Biomedical Research ApplicationsHematopoietic Stem Cell TransplantationDevelopmental Biology and Gene Regulation

The DOI matches its Crossref record; 108 of the 108 references it cites were found in a registry or an index.

The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis

Davidson, Alan J, Zon, Leonard I·2004·Oncogene

DOI 10.1038/sj.onc.1207943

Open this paper in CoChat — free account

Abstract

Progressive advances using zebrafish as a model organism have provided hematologists with an additional genetic system to study blood cell formation and hematological malignancies. Despite extensive evolutionary divergence between bony fish (teleosts) and mammals, the molecular pathways governing hematopoiesis have been highly conserved. As a result, most (if not all) of the critical hematopoietic transcription factor genes identified in mammals have orthologues in zebrafish. As in other vertebrates, all of the teleost blood lineages are believed to originate from a pool of pluripotent, self-renewing hematopoietic stem cells. Here, we provide a detailed review of the timing, anatomical location, and transcriptional regulation of zebrafish 'primitive' and 'definitive' hematopoiesis as well as discuss a model of T-cell leukemia and recent advances in blood cell transplantation. Given that many of the regulatory genes that control embryonic hematopoiesis have been implicated in oncogenic pathways in adults, an understanding of blood cell ontogeny is likely to provide insights into the pathophysiology of human leukemias.

Integrity signals

Registry

Crossref · 10.1038/sj.onc.1207943

Cites

108 of 108 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Stages of embryonic development of the zebrafish
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., & Schilling, T. F. (1995) · Developmental Dynamics · doi:10.1002/aja.1002030302 · Cited by 12,037
Hox genes in vertebrate development
Krumlauf, R. K. (1994) · Cell · doi:10.1016/0092-8674(94)90290-9 · Cited by 2,079
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
The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio
Haffter, P., Granato, M., Brand, M., Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., van Eeden, F. J. M., Jiang, Y., Heisenberg, C., et al. (1996) · Development · doi:10.1242/dev.123.1.1 · Cited by 1,691
Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter
Donovan, A., Brownlie, A., Zhou, Y., Shepard, J., Pratt, S. J., Moynihan, J., Paw, B. H., Drejer, A., Barut, B., Zapata, A., et al. (2000) · Nature · doi:10.1038/35001596 · Cited by 1,667
Self-citation
Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis.
Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A. H., & Speck, N. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.8.3444 · Cited by 1,178
Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL
Shivdasani, R. A., Mayer, E. L., & Orkin, S. H. (1995) · Nature · doi:10.1038/373432a0 · Cited by 938
Ontogeny and behaviour of early macrophages in the zebrafish embryo
Herbomel, P., Thisse, B., & Thisse, C. (1999) · Development · doi:10.1242/dev.126.17.3735 · Cited by 813
Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants
Traver, D., Paw, B. H., Poss, K. D., Penberthy, W. T., Lin, S., & Zon, L. I. (2003) · Nature Immunology · doi:10.1038/ni1007 · Cited by 800
Self-citation
Origin and organization of the zebrafish fate map
Kimmel, C. B., Warga, R. M., & Schilling, T. F. (1990) · Development · doi:10.1242/dev.108.4.581 · Cited by 698

Show all 108 references

Research works printed but not linked: 6

Chase A, Reiter A, Burci L, Cazzaniga G, Biondi A, Pickard J, Roberts IA, Goldman JM and Cross NC . (1999). Blood, 93, 1025–1031. · DOI
Dooley KA, Davidson AJ and Zon LI . (2004). Dev. Biol., in press.
Lieschke GJ, Oates AC, Crowhurst MO, Ward AC and Layton JE . (2001). Blood, 98, 3087–3096. · DOI
Ransom DG, Bahary N, Niss K, Traver D, Burns C, Paffett-Lugassy N, Saganic WJ, Lim CA, Hersey C, Zhou Y, Barut BA, Lin S, Kingsley PD, Palis J, Orkin SH and Zon LI . (2004). PloS. Biol., in press.
Traver D, Winzeler A, Stern HM, Mayhall EA, Langenau DM, Kutok JL, Look AT and Zon LI . (2004). Blood (in press).
Yoder MC and Palis J . (2001). Hematopoiesis: A Developmental Approach. Zon LI (ed). Oxford University Press: New York, New York.

Sorted by citations

The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish
Hall, C. J., Flores, M. V., Storm, T., Crosier, K., & Crosier, P. S. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-42 · Cited by 589
Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development
Murayama, E., Kissa, K., Zapata, A. G., Mordelet, E., Briolat, V., Lin, H.-F., Handin, R. I., & Herbomel, P. (2006) · Immunity · doi:10.1016/j.immuni.2006.10.015 · Cited by 545
Molecular Genetics of Axis Formation in Zebrafish
Schier, A. F., & Talbot, W. S. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.37.110801.143752 · Cited by 499
Zebrafish: Model for the Study of Inflammation and the Innate Immune Response to Infectious Diseases
Novoa, B., & Figueras, A. J. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-0106-3_15 · Cited by 297
Spatially resolved transcriptomics reveals the architecture of the tumor-microenvironment interface
Hunter, M. V., Moncada, R. M., Weiss, J. M., Yanai, I., & White, R. M. (2021) · Nature Communications · doi:10.1038/s41467-021-26614-z · Cited by 295
Blood Cells and Blood Cell Development in the Animal Kingdom
Hartenstein, V. (2006) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.22.010605.093317 · Cited by 286
Use of the Zebrafish System to Study Primitive and Definitive Hematopoiesis
de Jong, J. L. O., & Zon, L. I. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.095931 · Cited by 286
Self-citation
Host-Pathogen Interactions Made Transparent with the Zebrafish Model
Meijer, A. H., & Spaink, H. P. (2011) · Current Drug Targets · doi:10.2174/138945011795677809 · Cited by 253
Loss of Gata1 but Not Gata2 Converts Erythropoiesis to Myelopoiesis in Zebrafish Embryos
Galloway, J. L., Wingert, R. A., Thisse, C., Thisse, B., & Zon, L. I. (2005) · Developmental Cell · doi:10.1016/j.devcel.2004.12.001 · Cited by 242
Self-citation
Host–microbe interactions in the developing zebrafish
Kanther, M., & Rawls, J. F. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.01.006 · Cited by 229
The zebrafish: A fintastic model for hematopoietic development and disease
Gore, A. V., Pillay, L. M., Galanternik, M. V., & Weinstein, B. M. (2018) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.312 · Cited by 235
Transcriptome Profiling and Functional Analyses of the Zebrafish Embryonic Innate Immune Response to Salmonella Infection
Stockhammer, O. W., Zakrzewska, A., Hegedüs, Z., Spaink, H. P., & Meijer, A. H. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900082 · Cited by 220
BMP and Wnt specify hematopoietic fate by activation of the Cdx-Hox pathway.
Lengerke, C., Schmitt, S., Bowman, T., Jang, I., Maouche-Chretien, L., McKinney-Freeman, S., Davidson, A., Hammerschmidt, M., Rentzsch, F., Green, J. B. A., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2007.10.022 · Cited by 225
Self-citation
Dissecting hematopoietic and renal cell heterogeneity in adult zebrafish at single-cell resolution using RNA sequencing
Tang, Q., Iyer, S., Lobbardi, R., Moore, J. C., Chen, H., Lareau, C. A., Hebert, C. M., Shaw, M. L., Neftel, C., Suvà, M. L., et al. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20170976 · Cited by 206
Gata4 regulates the formation of multiple organs
Holtzinger, A., & Evans, T. (2005) · Development · doi:10.1242/dev.01978 · Cited by 205
Zebrafish xenografts as a tool for in vivo studies on human cancer
Konantz, M., Balci, T. B., Hartwig, U. F., Dellaire, G., Andre, M. C., Berman, J. N., & Lengerke, C. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06575.x · Cited by 210
Macrophage-specific gene functions in Spi1-directed innate immunity
Zakrzewska, A., Cui, C., Stockhammer, O. W., Benard, E. L., Spaink, H. P., & Meijer, A. H. (2010) · Blood · doi:10.1182/blood-2010-01-262873 · Cited by 199
The zebrafish ( D anio rerio ) as a model organism, with emphasis on applications for finfish aquaculture research
Ribas, L., & Piferrer, F. (2013) · Reviews in Aquaculture · doi:10.1111/raq.12041 · Cited by 203
MyD88 Innate Immune Function in a Zebrafish Embryo Infection Model
van der Sar, A. M., Stockhammer, O. W., van der Laan, C., Spaink, H. P., Bitter, W., & Meijer, A. H. (2006) · Infection and Immunity · doi:10.1128/iai.74.4.2436-2441.2006 · Cited by 184
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 189
Self-citation
Zebrafish in hematology: sushi or science?
Carradice, D., & Lieschke, G. J. (2008) · Blood · doi:10.1182/blood-2007-10-052761 · Cited by 182
Immunomodulation-accelerated neuronal regeneration following selective rod photoreceptor cell ablation in the zebrafish retina
White, D. T., Sengupta, S., Saxena, M. T., Xu, Q., Hanes, J. S., Ding, D., Ji, H., & Mumm, J. S. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1617721114 · Cited by 167
Understanding dioxin developmental toxicity using the zebrafish model
Carney, S. A., Prasch, A. L., Heideman, W., & Peterson, R. E. (2005) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20216 · Cited by 175
Zebrafish development and regeneration: new tools for biomedical research
Brittijn, S. A., van der Plas-Duivesteijn, S. J., Belmamoune, M., Bertens, L. M. F., Bitter, W., de Bruijn, J. D., Champagne, D. L., Cuppen, E. P. J. G., Flik, G., Vandenbroucke‐Grauls, C. M. J. E., et al. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082615sb · Cited by 164
Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development
Jin, H., Xu, J., & Wen, Z. (2007) · Blood · doi:10.1182/blood-2007-01-069005 · Cited by 163
The lateral plate mesoderm
Prummel, K. D., Nieuwenhuize, S., & Mosimann, C. (2020) · Development · doi:10.1242/dev.175059 · Cited by 173
Zebrafish as a model for normal and malignant hematopoiesis
Jing, L., & Zon, L. I. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.006791 · Cited by 164
Self-citation
Developmental toxicity screening in zebrafish
McCollum, C. W., Ducharme, N. A., Bondesson, M., & Gustafsson, J.-Α. (2011) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20210 · Cited by 161
Haematopoietic stem cell induction by somite-derived endothelial cells controlled by meox1
Nguyen, P. D., Hollway, G. E., Sonntag, C., Miles, L. B., Hall, T. E., Berger, S., Fernandez, K. J., Gurevich, D., Cole, N. J., Alaei, S., et al. (2014) · Nature · doi:10.1038/nature13678 · Cited by 154
Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish
Yoo, S. K., & Huttenlocher, A. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.1010567 · Cited by 153
Essential role of c-myb in definitive hematopoiesis is evolutionarily conserved
Soza‐Ried, C., Hess, I., Netuschil, N., Schorpp, M., & Boehm, T. L. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1004640107 · Cited by 153
Signalling pathways that control vertebrate haematopoietic stem cell specification
Clements, W. K., & Traver, D. J. (2013) · Nature reviews. Immunology · doi:10.1038/nri3443 · Cited by 148
A dominant gain-of-function mutation in universal tyrosine kinase SRC causes thrombocytopenia, myelofibrosis, bleeding, and bone pathologies
Turro, E., Greene, D. J., Wijgaerts, A., Thys, C., Lentaigne, C., Bariana, T. K., Westbury, S. K., Kelly, A. M., Selleslag, D., Stephens, J. C., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad7666 · Cited by 150
Neutrophil Development, Migration, and Function in Teleost Fish
Havixbeck, J. J., & Barreda, D. R. (2015) · Biology · doi:10.3390/biology4040715 · Cited by 147
Telomerase Is Required for Zebrafish Lifespan
Henriques, C. M., Carneiro, M. C., Tenente, I. M., Jacinto, A., & Ferreira, M. G. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003214 · Cited by 133
Is there a direct role for erythrocytes in the immune response?
Morera, D., & MacKenzie, S. A. (2011) · Veterinary Research · doi:10.1186/1297-9716-42-89 · Cited by 132
Functional conservation of erythropoietin signaling in zebrafish
Paffett-Lugassy, N., Hsia, N., Fraenkel, P. G., Paw, B. H., Leshinsky, I., Barut, B., Bahary, N., Caro, J., Handin, R. I., & Zon, L. I. (2007) · Blood · doi:10.1182/blood-2006-04-016535 · Cited by 139
Self-citation
Identification and real-time imaging of a myc-expressing neutrophil population involved in inflammation and mycobacterial granuloma formation in zebrafish
Meijer, A. H., van der Sar, A. M., da Cunha, C. B., Lamers, G. E. M., Laplante, M. A., Kikuta, H., Bitter, W., Becker, T. S., & Spaink, H. P. (2007) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2007.04.003 · Cited by 131
Echinodermata: The Complex Immune System in Echinoderms
Smith, L. C., Arizza, V., Hudgell, M. A. B., Barone, G., Bodnar, A. G., Buckley, K. M., Cunsolo, V., Dheilly, N. M., Franchi, N., Fugmann, S. D., et al. (2018) · Springer eBooks · doi:10.1007/978-3-319-76768-0_13 · Cited by 131
From hemangioblast to hematopoietic stem cell: An endothelial connection?
Jaffredo, T., Nottingham, W. T., Liddiard, K., Bollérot, K., Pouget, C., & Bruijn, M. F. T. R. D. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2005.06.005 · Cited by 129
Genome-Wide Analysis of the Zebrafish ETS Family Identifies Three Genes Required for Hemangioblast Differentiation or Angiogenesis
Liu, F., & Patient, R. K. (2008) · Circulation Research · doi:10.1161/circresaha.108.179713 · Cited by 129
Definitive hematopoietic stem/progenitor cells manifest distinct differentiation output in the zebrafish VDA and PBI
Jin, H., Sood, R. B., Xu, J., Zhen, F., English, M. A., Liu, P. P., & Wen, Z. (2009) · Development · doi:10.1242/dev.029637 · Cited by 132
Zebrafish erythropoiesis and the utility of fish as models of anemia
Kulkeaw, K., & Sugiyama, D. (2012) · Stem Cell Research & Therapy · doi:10.1186/scrt146 · Cited by 125
Zebrafish granulocyte colony-stimulating factor receptor signaling promotes myelopoiesis and myeloid cell migration
Liongue, C., Hall, C. J., O’Connell, B. A., Crosier, P. S., & Ward, A. C. (2009) · Blood · doi:10.1182/blood-2008-07-171967 · Cited by 124
Transplantable Tumor Lines Generated in Clonal Zebrafish
Мизгирев, И. В., & Revskoy, S. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3800 · Cited by 122
The role of macrophages during acute kidney injury: destruction and repair
Han, H. I., Skvarca, L. B., Espiritu, E. B., Davidson, A. J., & Hukriede, N. A. (2018) · Pediatric Nephrology · doi:10.1007/s00467-017-3883-1 · Cited by 124
Self-citation
Chapter 1 Genetic Models of Cancer in Zebrafish
Amatruda, J. F., & Patton, E. E. (2008) · International review of cytology · doi:10.1016/s1937-6448(08)01201-x · Cited by 119
Specificity of the zebrafish host transcriptome response to acute and chronic mycobacterial infection and the role of innate and adaptive immune components
van der Sar, A. M., Spaink, H. P., Zakrzewska, A., Bitter, W., & Meijer, A. H. (2009) · Molecular Immunology · doi:10.1016/j.molimm.2009.03.024 · Cited by 116
The caudal-related homeobox genes cdx1a and cdx4 act redundantly to regulate hox gene expression and the formation of putative hematopoietic stem cells during zebrafish embryogenesis
Davidson, A. J., & Zon, L. I. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.01.003 · Cited by 119
Self-citation
AML1-ETO reprograms hematopoietic cell fate by downregulatingsclexpression
Yeh, J.-R. J., Munson, K. M., Chao, Y. L., Peterson, Q. P., MacRae, C. A., & Peterson, R. T. (2007) · Development · doi:10.1242/dev.008904 · Cited by 119
Delineation of the cell-extrinsic apoptosis pathway in the zebrafish
Eimon, P. M., Kratz, E., Varfolomeev, E. E., Hymowitz, S. G., Stern, H. M., Zha, J., & Ashkenazi, A. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402015 · Cited by 115
Kidney organogenesis in the zebrafish: insights into vertebrate nephrogenesis and regeneration
Gerlach, G. F., & Wingert, R. A. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.92 · Cited by 114
Hypoxia-inducible factor-1 mediates adaptive developmental plasticity of hypoxia tolerance in zebrafish, Danio rerio
Robertson, C. E., Wright, P. A., Köblitz, L., & Bernier, N. J. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.0637 · Cited by 113
A multimodal zebrafish developmental atlas reveals the state-transition dynamics of late-vertebrate pluripotent axial progenitors
Lange, M., Granados, A. A., VijayKumar, S., Bragantini, J., Ancheta, S., Kim, Y. J., Santhosh, S., Borja, M., Kobayashi, H., McGeever, A., et al. (2024) · Cell · doi:10.1016/j.cell.2024.09.047 · Cited by 164
Loss of Hspa9b in zebrafish recapitulates the ineffective hematopoiesis of the myelodysplastic syndrome
Craven, S. E., French, D. M., Ye, W., de Sauvage, F. J., & Rosenthal, A. (2005) · Blood · doi:10.1182/blood-2004-03-1089 · Cited by 107
Discrete Notch signaling requirements in the specification of hematopoietic stem cells
Kim, A. D., Melick, C. H., Clements, W. K., Stachura, D. L., Distel, M., Panáková, D., MacRae, C. A., Barske, L. A., Crump, J. G., & Traver, D. J. (2014) · The EMBO Journal · doi:10.15252/embj.201488784 · Cited by 101
Interleukin-6 signaling regulates hematopoietic stem cell emergence
Tie, R., Li, H., Cai, S., Liang, Z., Shan, W., Wang, B., Tan, Y., Zheng, W., & Huang, H. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0320-5 · Cited by 97
Ribosomal protein L11 mutation in zebrafish leads to haematopoietic and metabolic defects
Danilova, N., Sakamoto, K. M., & Lin, S. (2010) · British Journal of Haematology · doi:10.1111/j.1365-2141.2010.08396.x · Cited by 99
Comparison of static immersion and intravenous injection systems for exposure of zebrafish embryos to the natural pathogen Edwardsiella tarda
van Soest, J. J., Stockhammer, O. W., Ordas, A., Bloemberg, G. V., Spaink, H. P., & Meijer, A. H. (2011) · BMC Immunology · doi:10.1186/1471-2172-12-58 · Cited by 93
Identification and comparative expression analysis of a second wt1 gene in zebrafish
Bollig, F., Mehringer, R., Perner, B., Hartung, C., Schäfer, M., Schartl, M., Volff, J., Winkler, C., & Englert, C. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20645 · Cited by 93
A genetic screen in zebrafish defines a hierarchical network of pathways required for hematopoietic stem cell emergence
Burns, C. E., Galloway, J. L., Smith, A. C. H., Keefe, M. D., Cashman, T. J., Paik, E. J., Mayhall, E. A., Amsterdam, A., & Zon, L. I. (2009) · Blood · doi:10.1182/blood-2008-12-193607 · Cited by 93
Self-citation
Fate Mapping Embryonic Blood in Zebrafish: Multi- and Unipotential Lineages Are Segregated at Gastrulation
Warga, R. M., Kane, D. A., & Ho, R. K. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.04.007 · Cited by 88
Smad1 and Smad5 differentially regulate embryonic hematopoiesis
McReynolds, L. J., Gupta, S. K., Figueroa, M. E., Mullins, M. C., & Evans, T. (2007) · Blood · doi:10.1182/blood-2007-04-085753 · Cited by 87
Zebrafish and Frog Models of Mycobacterium marinum Infection
Cosma, C. L., Swaim, L. E., Volkman, H. R., Ramakrishnan, L., & Davis, J. M. (2006) · Current Protocols in Microbiology · doi:10.1002/0471729256.mc10b02s3 · Cited by 84
Deep sequencing of the innate immune transcriptomic response of zebrafish embryos to Salmonella infection
Ordas, A., Hegedüs, Z., Henkel, C. V., Stockhammer, O. W., Butler, D., Jansen, H. J., Racz, P., Mink, M., Spaink, H. P., & Meijer, A. H. (2010) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2010.08.022 · Cited by 81
Distinct Functions for Different scl Isoforms in Zebrafish Primitive and Definitive Hematopoiesis
Qian, F., Zhen, F., Xu, J., Huang, M., Li, W., & Wen, Z. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050132 · Cited by 84
Specific Resistance to Pseudomonas aeruginosa Infection in Zebrafish Is Mediated by the Cystic Fibrosis Transmembrane Conductance Regulator
Phennicie, R., Sullivan, M. J., Singer, J. T., Yoder, J. A., & Kim, C. H. (2010) · Infection and Immunity · doi:10.1128/iai.00302-10 · Cited by 82
New Advances and Contributions to Fish Biology
Türker, H. (2012) · InTech eBooks · doi:10.5772/45635 · Cited by 82
The Notch pathway in the developing hematopoietic system
Bigas, A., Robert‐Moreno, A., & Espinosa, L. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.093049ab · Cited by 80
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
Infectious Disease Modeling and Innate Immune Function in Zebrafish Embryos
Cui, C., Benard, E. L., Kanwal, Z., Stockhammer, O. W., van der Vaart, M., Zakrzewska, A., Spaink, H. P., & Meijer, A. H. (2011) · Methods in cell biology · doi:10.1016/b978-0-12-381320-6.00012-6 · Cited by 76
The role of Wnt signaling in hematopoietic stem cell development
Richter, J., Traver, D. J., & Willert, K. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1325828 · Cited by 78
Transgenic zebrafish reporter lines reveal conserved Toll-like receptor signaling potential in embryonic myeloid leukocytes and adult immune cell lineages
Hall, C. J., Flores, M. V., Chien, A., Davidson, A. J., Crosier, K. E., & Crosier, P. S. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0708405 · Cited by 74
Self-citation
odd skipped related1reveals a novel role for endoderm in regulating kidney versus vascular cell fate
Mudumana, S. P., Hentschel, D. M., Liu, Y., Vasilyev, A., & Drummond, I. A. S. (2008) · Development · doi:10.1242/dev.022830 · Cited by 73
The Developmental Phases of Zebrafish Myogenesis
Keenan, S. R., & Currie, P. D. (2019) · Journal of Developmental Biology · doi:10.3390/jdb7020012 · Cited by 73
Characterization and localization of side population (SP) cells in zebrafish kidney hematopoietic tissue
Kobayashi, I., Saito, K., Moritomo, T., Araki, K., Takizawa, F., & Nakanishi, T. (2007) · Blood · doi:10.1182/blood-2007-08-104299 · Cited by 72
Proliferating cell nuclear antigen (PCNA) as a proliferative marker during embryonic and adult zebrafish hematopoiesis
Leung, A. Y., Leung, J. C. K., Chan, L. Y. Y., Ma, E. S. K., Kwan, T. T. F., Lai, K. N., Meng, A., & Liang, R. H. S. (2005) · Histochemistry and Cell Biology · doi:10.1007/s00418-005-0003-2 · Cited by 74
Zebrafish microRNA-126 determines hematopoietic cell fate through c-Myb
Grabher, C., Payne, E. M., Johnston, A. B., Bolli, N., Lechman, E. R., Dick, J. E., Kanki, J. P., & Look, A. T. (2010) · Leukemia · doi:10.1038/leu.2010.280 · Cited by 77
Characterization of Genetic and Epigenetic Variation in Sperm and Red Blood Cells from Adult Hatchery and Natural-Origin Steelhead, Oncorhynchus mykiss
Gavery, M. R., Nichols, K. M., Goetz, G., Middleton, M. A., & Swanson, P. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.118.200458 · Cited by 72
Glucocorticoid-Induced Attenuation of the Inflammatory Response in Zebrafish
Chatzopoulou, A., Heijmans, J. P. M., Burgerhout, E., Oskam, N., Spaink, H. P., Meijer, A. H., & Schaaf, M. J. M. (2016) · Endocrinology · doi:10.1210/en.2015-2050 · Cited by 72
Generation of clonal zebrafish lines and transplantable hepatic tumors
Мизгирев, И. В., & Revskoy, S. (2010) · Nature Protocols · doi:10.1038/nprot.2010.8 · Cited by 68
TET2 Plays an Essential Role in Erythropoiesis by Regulating Lineage-Specific Genes via DNA Oxidative Demethylation in a Zebrafish Model
Ge, L., Zhang, R., Wan, F., Guo, D., Wang, P., Xiang, L., & Shao, J.-Z. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01061-13 · Cited by 75
Zebrafish Thrombocytes: Functions and Origins
Khandekar, G., Kim, S., & Jagadeeswaran, P. (2012) · Advances in Hematology · doi:10.1155/2012/857058 · Cited by 70
Definitive hematopoietic stem cells minimally contribute to embryonic hematopoiesis
Ulloa, B. A., Habbsa, S. S., Potts, K. S., Lewis, A., McKinstry, M., Payne, S. G., Flores, J. C., Nizhnik, A., Norberto, M. F., Mosimann, C., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109703 · Cited by 66
ZebRA: An overview of retinoic acid signaling during zebrafish development
Samarut, É., Fraher, D., Laudet, V., & Gibert, Y. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.05.030 · Cited by 66
The role of jak2a in zebrafish hematopoiesis
Ma, A. C. H., Ward, A. C., Liang, R. H. S., & Leung, A. Y. H. (2007) · Blood · doi:10.1182/blood-2007-03-078287 · Cited by 66
Galectin-4 Reduces Migration and Metastasis Formation of Pancreatic Cancer Cells
Belo, A. I., van der Sar, A. M., Tefsen, B., & van Die, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065957 · Cited by 65
The embryonic origins of hematopoietic stem cells: a tale of hemangioblast and hemogenic endothelium
BOLLEROT, K., POUGET, C., & JAFFREDO, T. (2005) · APMIS · doi:10.1111/j.1600-0463.2005.apm_317.x · Cited by 65
Transcriptional regulation of hematopoietic stem cell development in zebrafish
Hsia, N., & Zon, L. I. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2005.06.013 · Cited by 69
Self-citation
Overcoming myelosuppression due to synthetic lethal toxicity for FLT3-targeted acute myeloid leukemia therapy
Warkentin, A. A., Lopez, M. S., Lasater, E. A., Lin, K. C., He, A. B.-L., Leung, A. Y., Smith, C. C., Shah, N. P., & Shokat, K. M. (2014) · eLife · doi:10.7554/elife.03445 · Cited by 63
Zebrafish (Danio rerio) as a Model System to Investigate the Role of the Innate Immune Response in Human Infectious Diseases
Franza, M., Varricchio, R., Alloisio, G., Simone, G. D., Bella, S. D., Ascenzi, P., & di Masi, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252212008 · Cited by 63
The SoLute Carrier (SLC) Family Series in Teleost Fish
Verri, T., Terova, G., Romano, A., Barca, A., Pisani, P., Storelli, C., & Saroglia, M. G. (2012) · Wiley eBooks · doi:10.1002/9781118350041.ch10 · Cited by 61
Characterization of Small, Mononuclear Blood Cells from Salmon Having High Phagocytic Capacity and Ability to Differentiate into Dendritic like Cells
Haugland, G. T., Jordal, A. O., & Wergeland, H. I. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049260 · Cited by 60
The mast cell plays a central role in the immune system of teleost fish
Sfacteria, A., Brines, M. L., & Blank, U. (2014) · Molecular Immunology · doi:10.1016/j.molimm.2014.02.007 · Cited by 60
Modeling Infectious Diseases in the Context of a Developing Immune System
Masud, S., Torraca, V., & Meijer, A. H. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.10.006 · Cited by 59
A conserved regulatory program initiates lateral plate mesoderm emergence across chordates
Prummel, K. D., Hess, C., Nieuwenhuize, S., Parker, H. J., Rogers, K. W., Kozmiková, I., Racioppi, C., Brombacher, E. C., Czarkwiani, A., Knapp, D., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11561-7 · Cited by 62
Inflammation, Aging and Hematopoiesis: A Complex Relationship
Bousounis, P., Bergo, V., & Trompouki, E. (2021) · Cells · doi:10.3390/cells10061386 · Cited by 64
Citrobacter freundii infection in silver catfish (Rhamdia quelen): Hematological and histological alterations
Bandeira, G., dos Santos, A. C., Souza, C. F., Baldissera, M. D., Moreira, K. L. D. S., da Veiga, M. L., da Rocha, M. I. D. U. M., de Vargas, Á. C., da Cunha, M. A., & Baldisserotto, B. (2018) · Microbial Pathogenesis · doi:10.1016/j.micpath.2018.09.038 · Cited by 59
A Non-Canonical Function of Zebrafish Telomerase Reverse Transcriptase Is Required for Developmental Hematopoiesis
Imamura, S., Uchiyama, J., Koshimizu, E., Hanai, J.-I., Raftopoulou, C., Murphey, R. D., Bayliss, P. E., Imai, Y., Burns, C. E., Masutomi, K., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003364 · Cited by 58
Self-citation
Characterization of the zebrafish matrix metalloproteinase 9 gene and its developmental expression pattern
Yoong, S., O’Connell, B. A., Soanes, A., Crowhurst, M. O., Lieschke, G. J., & Ward, A. C. (2006) · Gene Expression Patterns · doi:10.1016/j.modgep.2006.05.005 · Cited by 58

Authors: Davidson, A. J., & Zon, L. I.
Affiliations: Howard Hughes Medical Institute (US)
Corresponding author: Zon, Leonard I
ORCID: Davidson, Alan J
Zon, Leonard I
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2004-09-20
Volume: 23
Issue: 43
Pages: 7233-7246
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/sj.onc.1207943
OpenAlex: W2032417286
Cited by: 419
References: 108
Citations by year: 2026: 8 · 2025: 11 · 2024: 19 · 2023: 12 · 2022: 21 · 2021: 18 · 2020: 18 · 2019: 20 · 2018: 25 · 2017: 24 · 2016: 26 · 2015: 16 · 2014: 25 · 2013: 17 · 2012: 21
FWCI: 1.14
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: definitive hematopoiesis, primitive hematopoiesis, hematopoietic stem cells, hematopoietic transcription factors, orthologs, T-cell leukemia, hematologic malignancies, leukemogenesis
MeSH terms: Animals, Blood Cells, Embryo, Nonmammalian, Forecasting, Gastrula, Genetic Complementation Test, Growth Substances, Hematopoiesis, Hematopoietic Stem Cells, Leukemia, Mesoderm, Radiation Chimera, Transcription Factors, Transcription, Genetic, Zebrafish, Mutagenesis, Hematopoietic Stem Cell Transplantation, Gene Expression Regulation, Developmental, Cell Lineage, Models, Animal, Zebrafish Proteins, Animals, Genetically Modified, Pluripotent Stem Cells

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks