Resilient anatomy and local plasticity of naive and stress haematopoiesis

Qingqing Wu (), Jizhou Zhang, Sumit Kumar, Siyu Shen, Morgan Kincaid, Courtney B. Johnson, Yanan Sophia Zhang, Raphaël Turcotte, Clemens Alt, Kyoko Ito, Shelli Homan, Bryan E. Sherman, Tzu-Yu Shao, Anastasiya Slaughter, Benjamin Weinhaus, Baobao Song, Marie Dominique Filippi, H. Leighton Grimes, Charles P. Lin, Keisuke Ito, Sing Sing Way, J. Matthew Kofron and Daniel Lucas ()
Additional contact information
Qingqing Wu: Cincinnati Children’s Hospital Medical Center
Jizhou Zhang: Cincinnati Children’s Hospital Medical Center
Sumit Kumar: Cincinnati Children’s Hospital Medical Center
Siyu Shen: Cincinnati Children’s Hospital Medical Center
Morgan Kincaid: Cincinnati Children’s Hospital Medical Center
Courtney B. Johnson: Cincinnati Children’s Hospital Medical Center
Yanan Sophia Zhang: Cincinnati Children’s Hospital Medical Center
Raphaël Turcotte: Massachusetts General Hospital and Harvard Medical School
Clemens Alt: Massachusetts General Hospital and Harvard Medical School
Kyoko Ito: Albert Einstein College of Medicine
Shelli Homan: Cincinnati Children’s Hospital Medical Center
Bryan E. Sherman: University of Cincinnati College of Medicine
Tzu-Yu Shao: University of Cincinnati College of Medicine
Anastasiya Slaughter: Cincinnati Children’s Hospital Medical Center
Benjamin Weinhaus: Cincinnati Children’s Hospital Medical Center
Baobao Song: University of Cincinnati College of Medicine
Marie Dominique Filippi: Cincinnati Children’s Hospital Medical Center
H. Leighton Grimes: Cincinnati Children’s Hospital Medical Center
Charles P. Lin: Harvard Medical School
Keisuke Ito: Albert Einstein College of Medicine
Sing Sing Way: University of Cincinnati College of Medicine
J. Matthew Kofron: University of Cincinnati College of Medicine
Daniel Lucas: Cincinnati Children’s Hospital Medical Center

Nature, 2024, vol. 627, issue 8005, 839-846

Abstract: Abstract The bone marrow adjusts blood cell production to meet physiological demands in response to insults. The spatial organization of normal and stress responses are unknown owing to the lack of methods to visualize most steps of blood production. Here we develop strategies to image multipotent haematopoiesis, erythropoiesis and lymphopoiesis in mice. We combine these with imaging of myelopoiesis1 to define the anatomy of normal and stress haematopoiesis. In the steady state, across the skeleton, single stem cells and multipotent progenitors distribute through the marrow enriched near megakaryocytes. Lineage-committed progenitors are recruited to blood vessels, where they contribute to lineage-specific microanatomical structures composed of progenitors and immature cells, which function as the production sites for each major blood lineage. This overall anatomy is resilient to insults, as it was maintained after haemorrhage, systemic bacterial infection and granulocyte colony-stimulating factor (G-CSF) treatment, and during ageing. Production sites enable haematopoietic plasticity as they differentially and selectively modulate their numbers and output in response to insults. We found that stress responses are variable across the skeleton: the tibia and the sternum respond in opposite ways to G-CSF, and the skull does not increase erythropoiesis after haemorrhage. Our studies enable in situ analyses of haematopoiesis, define the anatomy of normal and stress responses, identify discrete microanatomical production sites that confer plasticity to haematopoiesis, and uncover unprecedented heterogeneity of stress responses across the skeleton.

Date: 2024
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DOI: 10.1038/s41586-024-07186-6

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