The heart is a resident tissue for hematopoietic stem and progenitor cells in zebrafish

Dorothee Bornhorst, Amulya V. Hejjaji, Lena Steuter, Nicole M. Woodhead, Paul Maier, Alessandra Gentile, Alice Alhajkadour, Octavia Santis Larrain, Michael Weber, Khrievono Kikhi, Stefan Guenther, Jan Huisken, Owen J. Tamplin, Didier Y. R. Stainier and Felix Gunawan ()
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Dorothee Bornhorst: University of Münster
Amulya V. Hejjaji: University of Münster
Lena Steuter: University of Münster
Nicole M. Woodhead: University of Wisconsin-Madison
Paul Maier: Georg-August-University Göttingen
Alessandra Gentile: Max Planck Institute for Heart and Lung Research (MPI-HLR)
Alice Alhajkadour: University of Wisconsin-Madison
Octavia Santis Larrain: University of Wisconsin-Madison
Khrievono Kikhi: MPI-HLR
Stefan Guenther: MPI-HLR
Jan Huisken: Georg-August-University Göttingen
Owen J. Tamplin: University of Wisconsin-Madison
Didier Y. R. Stainier: Max Planck Institute for Heart and Lung Research (MPI-HLR)
Felix Gunawan: University of Münster

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract The contribution of endocardial cells (EdCs) to the hematopoietic lineages has been strongly debated. Here, we provide evidence that in zebrafish, the endocardium gives rise to and maintains a stable population of hematopoietic cells. Using single-cell sequencing, we identify an endocardial subpopulation expressing enriched levels of hematopoietic-promoting genes. High-resolution microscopy and photoconversion tracing experiments uncover hematopoietic cells, mainly hematopoietic stem and progenitor cells (HSPCs)/megakaryocyte-erythroid precursors (MEPs), derived from EdCs as well as the dorsal aorta stably attached to the endocardium. Emergence of HSPCs/MEPs in hearts cultured ex vivo without external hematopoietic sources, as well as longitudinal imaging of the beating heart using light sheet microscopy, support endocardial contribution to hematopoiesis. Maintenance of these hematopoietic cells depends on the adhesion factors Integrin α4 and Vcam1 but is at least partly independent of cardiac trabeculation or shear stress. Finally, blocking primitive erythropoiesis increases cardiac-residing hematopoietic cells, suggesting that the endocardium is a hematopoietic reservoir. Altogether, these studies uncover the endocardium as a resident tissue for HSPCs/MEPs and a de novo source of hematopoietic cells.

Date: 2024
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DOI: 10.1038/s41467-024-51920-7

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