Adult skull bone marrow is an expanding and resilient haematopoietic reservoir

Bong Ihn Koh (), Vishal Mohanakrishnan, Hyun-Woo Jeong, Hongryeol Park, Kai Kruse, Young Jun Choi, Melina Nieminen-Kelhä, Rahul Kumar, Raquel S. Pereira, Susanne Adams, Hyuek Jong Lee, M. Gabriele Bixel, Peter Vajkoczy, Daniela S. Krause and Ralf H. Adams ()
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Bong Ihn Koh: Max Planck Institute for Molecular Biomedicine
Vishal Mohanakrishnan: Max Planck Institute for Molecular Biomedicine
Hyun-Woo Jeong: Max Planck Institute for Molecular Biomedicine
Hongryeol Park: Max Planck Institute for Molecular Biomedicine
Kai Kruse: Max Planck Institute for Molecular Biomedicine
Young Jun Choi: University of Ulsan College of Medicine
Melina Nieminen-Kelhä: Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Rahul Kumar: University Medicine Mainz
Raquel S. Pereira: Georg-Speyer-Haus Institute for Tumor Biology and Experimental Medicine and Goethe University Frankfurt
Susanne Adams: Max Planck Institute for Molecular Biomedicine
Hyuek Jong Lee: Institute for Basic Science
M. Gabriele Bixel: Max Planck Institute for Molecular Biomedicine
Peter Vajkoczy: Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Daniela S. Krause: University Medicine Mainz
Ralf H. Adams: Max Planck Institute for Molecular Biomedicine

Nature, 2024, vol. 636, issue 8041, 172-181

Abstract: Abstract The bone marrow microenvironment is a critical regulator of haematopoietic stem cell self-renewal and fate1. Although it is appreciated that ageing, chronic inflammation and other insults compromise bone marrow function and thereby negatively affect haematopoiesis2, it is not known whether different bone compartments exhibit distinct microenvironmental properties and functional resilience. Here we use imaging, pharmacological approaches and mouse genetics to uncover specialized properties of bone marrow in adult and ageing skull. Specifically, we show that the skull bone marrow undergoes lifelong expansion involving vascular growth, which results in an increasing contribution to total haematopoietic output. Furthermore, skull is largely protected against major hallmarks of ageing, including upregulation of pro-inflammatory cytokines, adipogenesis and loss of vascular integrity. Conspicuous rapid and dynamic changes to the skull vasculature and bone marrow are induced by physiological alterations, namely pregnancy, but also pathological challenges, such as stroke and experimental chronic myeloid leukaemia. These responses are highly distinct from femur, the most extensively studied bone marrow compartment. We propose that skull harbours a protected and dynamically expanding bone marrow microenvironment, which is relevant for experimental studies and, potentially, for clinical treatments in humans.

Date: 2024
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DOI: 10.1038/s41586-024-08163-9

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