|
|
|
|||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 126, Issue 17 3735-3745, Copyright © 1999 by Company of Biologists
JOURNAL ARTICLES |
P Herbomel, B Thisse and C Thisse
Unite de Biologie Moleculaire du Developpement, URA1947 du CNRS, Departement de Biologie Moleculaire, Institut Pasteur, 75724 Paris Cedex 15, France. herbomel@pasteur.fr
In the zebrafish embryo, the only known site of hemopoieisis is an intra-embryonic blood island at the junction between trunk and tail that gives rise to erythroid cells. Using video-enhanced differential interference contrast microscopy, as well as in-situ hybridization for the expression of two new hemopoietic marker genes, draculin and leucocyte-specific plastin, we show that macrophages appear in the embryo at least as early as erythroid cells, but originate from ventro-lateral mesoderm situated at the other end of the embryo, just anterior to the cardiac field. These macrophage precursors migrate to the yolksac, and differentiate. From the yolksac, many invade the mesenchyme of the head, while others join the blood circulation. Apart from phagocytosing apoptotic corpses, these macrophages were observed to engulf and destroy large amounts of bacteria injected intravenously; the macrophages also sensed the presence of bacteria injected into body cavities that are isolated from the blood, migrated into these cavities and eradicated the microorganisms. Moreover, we observed that although only a fraction of the macrophage population goes to the site of infection, the entire population acquires an activated behaviour, similar to that of activated macrophages in mammals. Our results support the notion that in vertebrate embryos, macrophages endowed with proliferative capacity arise early from the hemopoietic lineage through a non-classical, rapid differentiation pathway, which bypasses the monocytic series that is well-documented in adult hemopoietic organs.
This article has been cited by other articles:
![]() |
C. Rampon, M. Bouzaffour, M. A. Ostuni, P. Dufourcq, C. Girard, J. M. Freyssinet, J.-J. Lacapere, G. Schweizer-Groyer, and S. Vriz Translocator protein (18 kDa) is involved in primitive erythropoiesis in zebrafish FASEB J, December 1, 2009; 23(12): 4181 - 4192. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Lin, J. A. Loughman, B. H. Zinselmeyer, M. J. Miller, and M. G. Caparon Streptolysin S Inhibits Neutrophil Recruitment during the Early Stages of Streptococcus pyogenes Infection Infect. Immun., November 1, 2009; 77(11): 5190 - 5201. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Sieger, C. Stein, D. Neifer, A. M. van der Sar, and M. Leptin The role of gamma interferon in innate immunity in the zebrafish embryo Dis. Model. Mech., November 1, 2009; 2(11-12): 571 - 581. [Abstract] [Full Text] [PDF] |
||||
![]() |
J.-P. Levraud, O. Disson, K. Kissa, I. Bonne, P. Cossart, P. Herbomel, and M. Lecuit Real-Time Observation of Listeria monocytogenes-Phagocyte Interactions in Living Zebrafish Larvae Infect. Immun., September 1, 2009; 77(9): 3651 - 3660. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Chen, R. M. B. Costa, N. R. Love, X. Soto, M. Roth, R. Paredes, and E. Amaya C/EBP{alpha} initiates primitive myelopoiesis in pluripotent embryonic cells Blood, July 2, 2009; 114(1): 40 - 48. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. van Rooijen, E. E. Voest, I. Logister, J. Korving, T. Schwerte, S. Schulte-Merker, R. H. Giles, and F. J. van Eeden Zebrafish mutants in the von Hippel-Lindau tumor suppressor display a hypoxic response and recapitulate key aspects of Chuvash polycythemia Blood, June 18, 2009; 113(25): 6449 - 6460. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Hall, M. V. Flores, A. Chien, A. Davidson, K. Crosier, and P. Crosier Transgenic zebrafish reporter lines reveal conserved Toll-like receptor signaling potential in embryonic myeloid leukocytes and adult immune cell lineages J. Leukoc. Biol., May 1, 2009; 85(5): 751 - 765. [Abstract] [Full Text] [PDF] |
||||
![]() |
O. W. Stockhammer, A. Zakrzewska, Z. Hegedus, H. P. Spaink, and A. H. Meijer Transcriptome Profiling and Functional Analyses of the Zebrafish Embryonic Innate Immune Response to Salmonella Infection J. Immunol., May 1, 2009; 182(9): 5641 - 5653. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Peterkin, A. Gibson, and R. Patient Common genetic control of haemangioblast and cardiac development in zebrafish Development, May 1, 2009; 136(9): 1465 - 1474. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. E. Clatworthy, J. S.-W. Lee, M. Leibman, Z. Kostun, A. J. Davidson, and D. T. Hung Pseudomonas aeruginosa Infection of Zebrafish Involves both Host and Pathogen Determinants Infect. Immun., April 1, 2009; 77(4): 1293 - 1303. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. R. Swift and B. M. Weinstein Arterial-Venous Specification During Development Circ. Res., March 13, 2009; 104(5): 576 - 588. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Liongue, C. J. Hall, B. A. O'Connell, P. Crosier, and A. C. Ward Zebrafish granulocyte colony-stimulating factor receptor signaling promotes myelopoiesis and myeloid cell migration Blood, March 12, 2009; 113(11): 2535 - 2546. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Bukrinsky, K. J. P. Griffin, Y. Zhao, S. Lin, and U. Banerjee Essential role of spi-1-like (spi-1l) in zebrafish myeloid cell differentiation Blood, February 26, 2009; 113(9): 2038 - 2046. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Pase, J. E. Layton, W. P. Kloosterman, D. Carradice, P. M. Waterhouse, and G. J. Lieschke miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2 Blood, February 19, 2009; 113(8): 1794 - 1804. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Jin, R. Sood, J. Xu, F. Zhen, M. A. English, P. P. Liu, and Z. Wen Definitive hematopoietic stem/progenitor cells manifest distinct differentiation output in the zebrafish VDA and PBI Development, February 15, 2009; 136(4): 647 - 654. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Yi Ni Lam, J. Y. M. Chau, M. L. Kalev-Zylinska, T. M. Fountaine, R. S. Mead, C. J. Hall, P. S. Crosier, K. E. Crosier, and M. Vega Flores Zebrafish runx1 promoter-EGFP transgenics mark discrete sites of definitive blood progenitors Blood, February 5, 2009; 113(6): 1241 - 1249. [Abstract] [Full Text] [PDF] |
||||
![]() |
H.-T. Huang and L.I. Zon Regulation of Stem Cells in the Zebra Fish Hematopoietic System Cold Spring Harb Symp Quant Biol, November 6, 2008; (2008) sqb.2008.73.029v1. [Abstract] [PDF] |
||||
![]() |
T. Uechi, Y. Nakajima, A. Chakraborty, H. Torihara, S. Higa, and N. Kenmochi Deficiency of ribosomal protein S19 during early embryogenesis leads to reduction of erythrocytes in a zebrafish model of Diamond-Blackfan anemia Hum. Mol. Genet., October 15, 2008; 17(20): 3204 - 3211. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Cvejic, C. Hall, M. Bak-Maier, M. V. Flores, P. Crosier, M. J. Redd, and P. Martin Analysis of WASp function during the wound inflammatory response - live-imaging studies in zebrafish larvae J. Cell Sci., October 1, 2008; 121(19): 3196 - 3206. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. T. Dobson, J. Seibert, E. M. Teh, S. Da'as, R. B. Fraser, B. H. Paw, T.-J. Lin, and J. N. Berman Carboxypeptidase A5 identifies a novel mast cell lineage in the zebrafish providing new insight into mast cell fate determination Blood, October 1, 2008; 112(7): 2969 - 2972. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. M. B. Costa, X. Soto, Y. Chen, A. M. Zorn, and E. Amaya spib is required for primitive myeloid development in Xenopus Blood, September 15, 2008; 112(6): 2287 - 2296. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Zhang, X.-T. Bai, K.-Y. Zhu, Y. Jin, M. Deng, H.-Y. Le, Y.-F. Fu, Y. Chen, J. Zhu, A. T. Look, et al. In Vivo Interstitial Migration of Primitive Macrophages Mediated by JNK-Matrix Metalloproteinase 13 Signaling in Response to Acute Injury J. Immunol., August 1, 2008; 181(3): 2155 - 2164. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Y. Bertrand, A. D. Kim, S. Teng, and D. Traver CD41+ cmyb+ precursors colonize the zebrafish pronephros by a novel migration route to initiate adult hematopoiesis Development, May 15, 2008; 135(10): 1853 - 1862. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Sumanas, G. Gomez, Y. Zhao, C. Park, K. Choi, and S. Lin Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation Blood, May 1, 2008; 111(9): 4500 - 4510. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. B. Goldberg, R. E. W. Hancock, R. E. Parales, J. Loper, and P. Cornelis Pseudomonas 2007 J. Bacteriol., April 15, 2008; 190(8): 2649 - 2662. [Full Text] [PDF] |
||||
![]() |
D. Carradice and G. J. Lieschke Zebrafish in hematology: sushi or science? Blood, April 1, 2008; 111(7): 3331 - 3342. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Le Guyader, M. J. Redd, E. Colucci-Guyon, E. Murayama, K. Kissa, V. Briolat, E. Mordelet, A. Zapata, H. Shinomiya, and P. Herbomel Origins and unconventional behavior of neutrophils in developing zebrafish Blood, January 1, 2008; 111(1): 132 - 141. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Y. Bertrand, A. D. Kim, E. P. Violette, D. L. Stachura, J. L. Cisson, and D. Traver Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo Development, December 1, 2007; 134(23): 4147 - 4156. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. J. Carney, S. von der Hardt, C. Sonntag, A. Amsterdam, J. Topczewski, N. Hopkins, and M. Hammerschmidt Inactivation of serine protease Matriptase1a by its inhibitor Hai1 is required for epithelial integrity of the zebrafish epidermis Development, October 1, 2007; 134(19): 3461 - 3471. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. C. H. Ma, A. C. Ward, R. Liang, and A. Y. H. Leung The role of jak2a in zebrafish hematopoiesis Blood, September 15, 2007; 110(6): 1824 - 1830. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. A. Phelps and M. N. Neely SalY of the Streptococcus pyogenes Lantibiotic Locus Is Required for Full Virulence and Intracellular Survival in Macrophages Infect. Immun., September 1, 2007; 75(9): 4541 - 4551. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Liu, L. Du, M. Osato, E. H. Teo, F. Qian, H. Jin, F. Zhen, J. Xu, L. Guo, H. Huang, et al. The zebrafish udu gene encodes a novel nuclear factor and is essential for primitive erythroid cell development Blood, July 1, 2007; 110(1): 99 - 106. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Le, D. M. Langenau, M. D. Keefe, J. L. Kutok, D. S. Neuberg, and L. I. Zon Heat shock-inducible Cre/Lox approaches to induce diverse types of tumors and hyperplasia in transgenic zebrafish PNAS, May 29, 2007; 104(22): 9410 - 9415. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. J. Patterson, M. Gering, C. E. Eckfeldt, A. R. Green, C. M. Verfaillie, S. C. Ekker, and R. Patient The transcription factors Scl and Lmo2 act together during development of the hemangioblast in zebrafish Blood, March 15, 2007; 109(6): 2389 - 2398. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Grabher, A. Cliffe, K. Miura, J. Hayflick, R. Pepperkok, P. Rorth, and J. Wittbrodt Birth and life of tissue macrophages and their migration in embryogenesis and inflammation in medaka J. Leukoc. Biol., January 1, 2007; 81(1): 263 - 271. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. R. Lage, A. Nayak, and C. H. Kim Arsenic ecotoxicology and innate immunity Integr. Comp. Biol., December 1, 2006; 46(6): 1040 - 1054. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Li, J.-W. Xiong, C. S. Shelley, H. Park, and M. A. Arnaout The transcription factor ZBP-89 controls generation of the hematopoietic lineage in zebrafish and mouse embryonic stem cells Development, September 15, 2006; 133(18): 3641 - 3650. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Gupta, H. Zhu, L. I. Zon, and T. Evans BMP signaling restricts hemato-vascular development from lateral mesoderm during somitogenesis Development, June 1, 2006; 133(11): 2177 - 2187. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. M. van der Sar, O. W. Stockhammer, C. van der Laan, H. P. Spaink, W. Bitter, and A. H. Meijer MyD88 Innate Immune Function in a Zebrafish Embryo Infection Model Infect. Immun., April 1, 2006; 74(4): 2436 - 2441. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Juarez, F. Su, S. Chun, M. J. Kiel, and S. E. Lyons Distinct Roles for SCL in Erythroid Specification and Maturation in Zebrafish J. Biol. Chem., December 16, 2005; 280(50): 41636 - 41644. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Y. Bertrand, A. Jalil, M. Klaine, S. Jung, A. Cumano, and I. Godin Three pathways to mature macrophages in the early mouse yolk sac Blood, November 1, 2005; 106(9): 3004 - 3011. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. J. Weber, S. E. Choe, K. A. Dooley, N. N. Paffett-Lugassy, Y. Zhou, and L. I. Zon Mutant-specific gene programs in the zebrafish Blood, July 15, 2005; 106(2): 521 - 530. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. J. Patterson, M. Gering, and R. Patient Scl is required for dorsal aorta as well as blood formation in zebrafish embryos Blood, May 1, 2005; 105(9): 3502 - 3511. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. D. Miller and M. N. Neely Large-Scale Screen Highlights the Importance of Capsule for Virulence in the Zoonotic Pathogen Streptococcus iniae Infect. Immun., February 1, 2005; 73(2): 921 - 934. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Y. Bertrand, S. Giroux, R. Golub, M. Klaine, A. Jalil, L. Boucontet, I. Godin, and A. Cumano Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin PNAS, January 4, 2005; 102(1): 134 - 139. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. K. Quigley, J. M. Turner, R. J. Nuckels, J. L. Manuel, E. H. Budi, E. L. MacDonald, and D. M. Parichy Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes Development, December 15, 2004; 131(24): 6053 - 6069. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. R. Keegan, D. Meyer, and D. Yelon Organization of cardiac chamber progenitors in the zebrafish blastula Development, July 1, 2004; 131(13): 3081 - 3091. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Furthauer, J. Van Celst, C. Thisse, and B. Thisse Fgf signalling controls the dorsoventral patterning of the zebrafish embryo Development, June 15, 2004; 131(12): 2853 - 2864. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Gering, Y. Yamada, T. H. Rabbitts, and R. K. Patient Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1 Development, December 22, 2003; 130(25): 6187 - 6199. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. C. Ward, D. O. McPhee, M. M. Condron, S. Varma, S. H. Cody, S. M. N. Onnebo, B. H. Paw, L. I. Zon, and G. J. Lieschke The zebrafish spi1 promoter drives myeloid-specific expression in stable transgenic fish Blood, November 1, 2003; 102(9): 3238 - 3240. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. A. Farber, R. A. De Rose, E. S. Olson, and M. E. Halpern The Zebrafish Annexin Gene Family Genome Res., June 1, 2003; 13(6): 1082 - 1096. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Spitsbergen and M. L. Kent The State of the Art of the Zebrafish Model for Toxicology and Toxicologic Pathology Research--Advantages and Current Limitations Toxicol Pathol, January 1, 2003; 31(1_suppl): 62 - 87. [Abstract] [PDF] |
||||
![]() |
D. A. Hume, I. L. Ross, S. R. Himes, R. T. Sasmono, C. A. Wells, and T. Ravasi The mononuclear phagocyte system revisited J. Leukoc. Biol., October 1, 2002; 72(4): 621 - 627. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. N. Neely, J. D. Pfeifer, and M. Caparon Streptococcus-Zebrafish Model of Bacterial Pathogenesis Infect. Immun., July 1, 2002; 70(7): 3904 - 3914. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. E. Lyons, N. D. Lawson, L. Lei, P. E. Bennett, B. M. Weinstein, and P. P. Liu A nonsense mutation in zebrafish gata1 causes the bloodless phenotype in vlad tepes PNAS, April 16, 2002; 99(8): 5454 - 5459. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. P. Szeto, K. J. P. Griffin, and D. Kimelman hrT is required for cardiovascular development in zebrafish Development, January 11, 2002; 129(21): 5093 - 5101. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. C. Liao, N. S. Trede, D. Ransom, A. Zapata, M. Kieran, and L. I. Zon Non-cell autonomous requirement for the bloodless gene in primitive hematopoiesis of zebrafish Development, January 2, 2002; 129(3): 649 - 659. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. J. Lieschke, A. C. Oates, M. O. Crowhurst, A. C. Ward, and J. E. Layton Morphologic and functional characterization of granulocytes and macrophages in embryonic and adult zebrafish Blood, November 15, 2001; 98(10): 3087 - 3096. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. M. Bennett, J. P. Kanki, J. Rhodes, T. X. Liu, B. H. Paw, M. W. Kieran, D. M. Langenau, A. Delahaye-Brown, L. I. Zon, M. D. Fleming, et al. Myelopoiesis in the zebrafish, Danio rerio Blood, August 1, 2001; 98(3): 643 - 651. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. E. Lyons, B. C. Shue, A. C. Oates, L. I. Zon, and P. P. Liu A novel myeloid-restricted zebrafish CCAAT/enhancer-binding protein with a potent transcriptional activation domain Blood, May 1, 2001; 97(9): 2611 - 2617. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. A. Wayman, M. J. Walters, K. Kolibaba, T. R. Soderling, and J. L. Christian CAM Kinase IV Regulates Lineage Commitment and Survival of Erythroid Progenitors in a Non-Cell-Autonomous Manner J. Cell Biol., November 13, 2000; 151(4): 811 - 824. [Abstract] [Full Text] [PDF] |
||||