In situ mapping identifies distinct vascular niches for myelopoiesis

Jizhou Zhang, Qingqing Wu, Courtney B. Johnson, Giang Pham, Jeremy M. Kinder, Andre Olsson, Anastasiya Slaughter, Margot May, Benjamin Weinhaus, Angelo D’Alessandro, James Douglas Engel, Jean X. Jiang, J. Matthew Kofron, L. Frank Huang, V. B. Surya Prasath, Sing Sing Way, Nathan Salomonis, H. Leighton Grimes and Daniel Lucas ()
Additional contact information
Jizhou Zhang: Cincinnati Children’s Medical Center
Qingqing Wu: Cincinnati Children’s Medical Center
Courtney B. Johnson: Cincinnati Children’s Medical Center
Giang Pham: Cincinnati Children’s Hospital Medical Center
Jeremy M. Kinder: Cincinnati Children’s Hospital Medical Center
Andre Olsson: Cincinnati Children’s Hospital Medical Center
Anastasiya Slaughter: Cincinnati Children’s Medical Center
Margot May: Cincinnati Children’s Medical Center
Benjamin Weinhaus: Cincinnati Children’s Medical Center
Angelo D’Alessandro: University of Colorado Denver–Anschutz Medical Campus
James Douglas Engel: University of Michigan Medical School
Jean X. Jiang: University of Texas Health Science Center
J. Matthew Kofron: Cincinnati Children’s Hospital Medical Center
L. Frank Huang: Cincinnati Children’s Medical Center
V. B. Surya Prasath: University of Cincinnati College of Medicine
Sing Sing Way: Cincinnati Children’s Hospital Medical Center
Nathan Salomonis: University of Cincinnati College of Medicine
H. Leighton Grimes: Cincinnati Children’s Medical Center
Daniel Lucas: Cincinnati Children’s Medical Center

Nature, 2021, vol. 590, issue 7846, 457-462

Abstract: Abstract In contrast to nearly all other tissues, the anatomy of cell differentiation in the bone marrow remains unknown. This is owing to a lack of strategies for examining myelopoiesis—the differentiation of myeloid progenitors into a large variety of innate immune cells—in situ in the bone marrow. Such strategies are required to understand differentiation and lineage-commitment decisions, and to define how spatial organizing cues inform tissue function. Here we develop approaches for imaging myelopoiesis in mice, and generate atlases showing the differentiation of granulocytes, monocytes and dendritic cells. The generation of granulocytes and dendritic cells–monocytes localizes to different blood-vessel structures known as sinusoids, and displays lineage-specific spatial and clonal architectures. Acute systemic infection with Listeria monocytogenes induces lineage-specific progenitor clusters to undergo increased self-renewal of progenitors, but the different lineages remain spatially separated. Monocyte–dendritic cell progenitors (MDPs) map with nonclassical monocytes and conventional dendritic cells; these localize to a subset of blood vessels expressing a major regulator of myelopoiesis, colony-stimulating factor 1 (CSF1, also known as M-CSF)1. Specific deletion of Csf1 in endothelium disrupts the architecture around MDPs and their localization to sinusoids. Subsequently, there are fewer MDPs and their ability to differentiate is reduced, leading to a loss of nonclassical monocytes and dendritic cells during both homeostasis and infection. These data indicate that local cues produced by distinct blood vessels are responsible for the spatial organization of definitive blood cell differentiation.

Date: 2021
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DOI: 10.1038/s41586-021-03201-2

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