Definitive Hematopoiesis is Dispensable to Sustain Erythrocytes and Macrophages During Zebrafish Ontogeny

Overview

Journal iScience

Publisher Cell Press

Date 2024 Feb 8

PMID 38327794

Authors

Ramy Elsaid

Aya Mikdache

Keinis Quintero Castillo

Yazan Salloum

Patricia Diabangouaya

Gwendoline Gros

Carmen G Feijoo

Pedro P Hernandez

Affiliations

Soon will be listed here.

Abstract

In all organisms studied, from flies to humans, blood cells emerge in several sequential waves and from distinct hematopoietic origins. However, the relative contribution of these ontogenetically distinct hematopoietic waves to embryonic blood lineages and to tissue regeneration during development is yet elusive. Here, using a lineage-specific "switch and trace" strategy in the zebrafish embryo, we report that the definitive hematopoietic progeny barely contributes to erythrocytes and macrophages during early development. Lineage tracing further shows that ontogenetically distinct macrophages exhibit differential recruitment to the site of injury based on the developmental stage of the organism. We further demonstrate that primitive macrophages can solely maintain tissue regeneration during early larval developmental stages after selective ablation of definitive macrophages. Our findings highlight that the sequential emergence of hematopoietic waves in embryos ensures the abundance of blood cells required for tissue homeostasis and integrity during development.

References

Herbomel P, Thisse B, Thisse C . Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development. 1999; 126(17):3735-45. DOI: 10.1242/dev.126.17.3735. View

Jagadeeswaran P, Lin S, Weinstein B, Hutson A, Kim S . Loss of GATA1 and gain of FLI1 expression during thrombocyte maturation. Blood Cells Mol Dis. 2010; 44(3):175-80. PMC: 2829368. DOI: 10.1016/j.bcmd.2009.12.012. View

He S, Chen J, Jiang Y, Wu Y, Zhu L, Jin W . Adult zebrafish Langerhans cells arise from hematopoietic stem/progenitor cells. Elife. 2018; 7. PMC: 6017808. DOI: 10.7554/eLife.36131. View

Boisset J, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C . In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature. 2010; 464(7285):116-20. DOI: 10.1038/nature08764. View

Bertrand J, Kim A, Violette E, Stachura D, Cisson J, Traver D . Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development. 2007; 134(23):4147-56. PMC: 2735398. DOI: 10.1242/dev.012385. View

Soza-Ried C, Hess I, Netuschil N, Schorpp M, Boehm T . Essential role of c-myb in definitive hematopoiesis is evolutionarily conserved. Proc Natl Acad Sci U S A. 2010; 107(40):17304-8. PMC: 2951452. DOI: 10.1073/pnas.1004640107. View

Travnickova J, Tran Chau V, Julien E, Mateos-Langerak J, Gonzalez C, Lelievre E . Primitive macrophages control HSPC mobilization and definitive haematopoiesis. Nat Commun. 2015; 6:6227. DOI: 10.1038/ncomms7227. View

Kissa K, Herbomel P . Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature. 2010; 464(7285):112-5. DOI: 10.1038/nature08761. View

Lin X, Zhou Q, Zhao C, Lin G, Xu J, Wen Z . An Ectoderm-Derived Myeloid-like Cell Population Functions as Antigen Transporters for Langerhans Cells in Zebrafish Epidermis. Dev Cell. 2019; 49(4):605-617.e5. DOI: 10.1016/j.devcel.2019.03.028. View

10.

Hsia N, Zon L . Transcriptional regulation of hematopoietic stem cell development in zebrafish. Exp Hematol. 2005; 33(9):1007-14. DOI: 10.1016/j.exphem.2005.06.013. View

11.

Ganis J, Hsia N, Trompouki E, de Jong J, DiBiase A, Lambert J . Zebrafish globin switching occurs in two developmental stages and is controlled by the LCR. Dev Biol. 2012; 366(2):185-94. PMC: 3378398. DOI: 10.1016/j.ydbio.2012.03.021. View

12.

Tian Y, Xu J, Feng S, He S, Zhao S, Zhu L . The first wave of T lymphopoiesis in zebrafish arises from aorta endothelium independent of hematopoietic stem cells. J Exp Med. 2017; 214(11):3347-3360. PMC: 5679161. DOI: 10.1084/jem.20170488. View

13.

Curado S, Stainier D, Anderson R . Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat Protoc. 2008; 3(6):948-54. PMC: 2705989. DOI: 10.1038/nprot.2008.58. View

14.

Renaud O, Herbomel P, Kissa K . Studying cell behavior in whole zebrafish embryos by confocal live imaging: application to hematopoietic stem cells. Nat Protoc. 2011; 6(12):1897-904. DOI: 10.1038/nprot.2011.408. View

15.

Soares-da-Silva F, Freyer L, Elsaid R, Burlen-Defranoux O, Iturri L, Sismeiro O . Yolk sac, but not hematopoietic stem cell-derived progenitors, sustain erythropoiesis throughout murine embryonic life. J Exp Med. 2021; 218(4). PMC: 7879581. DOI: 10.1084/jem.20201729. View

16.

Ferrero G, Mahony C, Dupuis E, Yvernogeau L, Di Ruggiero E, Miserocchi M . Embryonic Microglia Derive from Primitive Macrophages and Are Replaced by cmyb-Dependent Definitive Microglia in Zebrafish. Cell Rep. 2018; 24(1):130-141. DOI: 10.1016/j.celrep.2018.05.066. View

17.

Herbomel P, Thisse B, Thisse C . Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol. 2002; 238(2):274-88. DOI: 10.1006/dbio.2001.0393. View

18.

Bertrand J, Chi N, Santoso B, Teng S, Stainier D, Traver D . Haematopoietic stem cells derive directly from aortic endothelium during development. Nature. 2010; 464(7285):108-11. PMC: 2858358. DOI: 10.1038/nature08738. View

19.

Carney T, Mosimann C . Switch and Trace: Recombinase Genetics in Zebrafish. Trends Genet. 2018; 34(5):362-378. DOI: 10.1016/j.tig.2018.01.004. View

20.

McGrath K, Frame J, Palis J . Early hematopoiesis and macrophage development. Semin Immunol. 2016; 27(6):379-87. PMC: 4856633. DOI: 10.1016/j.smim.2016.03.013. View