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A mechanosensitive peri-arteriolar niche for osteogenesis and lymphopoiesis

Author

Listed:
  • Bo Shen

    (University of Texas Southwestern Medical Center)

  • Alpaslan Tasdogan

    (University of Texas Southwestern Medical Center)

  • Jessalyn M. Ubellacker

    (University of Texas Southwestern Medical Center)

  • Jingzhu Zhang

    (University of Texas Southwestern Medical Center)

  • Elena D. Nosyreva

    (University of Texas Southwestern Medical Center)

  • Liming Du

    (University of Texas Southwestern Medical Center)

  • Malea M. Murphy

    (University of Texas Southwestern Medical Center)

  • Shuiqing Hu

    (University of Texas Southwestern Medical Center)

  • Yating Yi

    (School of Dentistry, Texas A&M University)

  • Nergis Kara

    (University of Texas Southwestern Medical Center)

  • Xin Liu

    (University of Texas Southwestern Medical Center)

  • Shay Guela

    (University of Texas Southwestern Medical Center)

  • Yuemeng Jia

    (University of Texas Southwestern Medical Center)

  • Vijayashree Ramesh

    (University of Texas Southwestern Medical Center)

  • Claire Embree

    (University of Texas Southwestern Medical Center)

  • Evann C. Mitchell

    (University of Texas Southwestern Medical Center)

  • Yunduo C. Zhao

    (The University of Sydney)

  • Lining A. Ju

    (The University of Sydney)

  • Zhao Hu

    (The University of Sydney)

  • Genevieve M. Crane

    (Robert J. Tomsich Pathology & Laboratory Medicine Institute, Cleveland Clinic)

  • Zhiyu Zhao

    (University of Texas Southwestern Medical Center)

  • Ruhma Syeda

    (University of Texas Southwestern Medical Center)

  • Sean J. Morrison

    (University of Texas Southwestern Medical Center
    University of Texas Southwestern Medical Center)

Abstract

Stromal cells in adult bone marrow that express leptin receptor (LEPR) are a critical source of growth factors, including stem cell factor (SCF), for the maintenance of haematopoietic stem cells and early restricted progenitors1–6. LEPR+ cells are heterogeneous, including skeletal stem cells and osteogenic and adipogenic progenitors7–12, although few markers have been available to distinguish these subsets or to compare their functions. Here we show that expression of an osteogenic growth factor, osteolectin13,14, distinguishes peri-arteriolar LEPR+ cells poised to undergo osteogenesis from peri-sinusoidal LEPR+ cells poised to undergo adipogenesis (but retaining osteogenic potential). Peri-arteriolar LEPR+osteolectin+ cells are rapidly dividing, short-lived osteogenic progenitors that increase in number after fracture and are depleted during ageing. Deletion of Scf from adult osteolectin+ cells did not affect the maintenance of haematopoietic stem cells or most restricted progenitors but depleted common lymphoid progenitors, impairing lymphopoiesis, bacterial clearance, and survival after acute bacterial infection. Peri-arteriolar osteolectin+ cell maintenance required mechanical stimulation. Voluntary running increased, whereas hindlimb unloading decreased, the frequencies of peri-arteriolar osteolectin+ cells and common lymphoid progenitors. Deletion of the mechanosensitive ion channel PIEZO1 from osteolectin+ cells depleted osteolectin+ cells and common lymphoid progenitors. These results show that a peri-arteriolar niche for osteogenesis and lymphopoiesis in bone marrow is maintained by mechanical stimulation and depleted during ageing.

Suggested Citation

  • Bo Shen & Alpaslan Tasdogan & Jessalyn M. Ubellacker & Jingzhu Zhang & Elena D. Nosyreva & Liming Du & Malea M. Murphy & Shuiqing Hu & Yating Yi & Nergis Kara & Xin Liu & Shay Guela & Yuemeng Jia & Vi, 2021. "A mechanosensitive peri-arteriolar niche for osteogenesis and lymphopoiesis," Nature, Nature, vol. 591(7850), pages 438-444, March.
  • Handle: RePEc:nat:nature:v:591:y:2021:i:7850:d:10.1038_s41586-021-03298-5
    DOI: 10.1038/s41586-021-03298-5
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    Citations

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    Cited by:

    1. Yuki Matsushita & Angel Ka Yan Chu & Chiaki Tsutsumi-Arai & Shion Orikasa & Mizuki Nagata & Sunny Y. Wong & Joshua D. Welch & Wanida Ono & Noriaki Ono, 2022. "The fate of early perichondrial cells in developing bones," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Haoqing Jerry Wang & Yao Wang & Seyed Sajad Mirjavadi & Tomas Andersen & Laura Moldovan & Parham Vatankhah & Blake Russell & Jasmine Jin & Zijing Zhou & Qing Li & Charles D. Cox & Qian Peter Su & Lini, 2024. "Microscale geometrical modulation of PIEZO1 mediated mechanosensing through cytoskeletal redistribution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Xianzhu Zhang & Wei Jiang & Chang Xie & Xinyu Wu & Qian Ren & Fei Wang & Xilin Shen & Yi Hong & Hongwei Wu & Youguo Liao & Yi Zhang & Renjie Liang & Wei Sun & Yuqing Gu & Tao Zhang & Yishan Chen & Wei, 2022. "Msx1+ stem cells recruited by bioactive tissue engineering graft for bone regeneration," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. Adrienne Anginot & Julie Nguyen & Zeina Abou Nader & Vincent Rondeau & Amélie Bonaud & Maria Kalogeraki & Antoine Boutin & Julia P. Lemos & Valeria Bisio & Joyce Koenen & Lea Hanna Doumit Sakr & Amand, 2023. "WHIM Syndrome-linked CXCR4 mutations drive osteoporosis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Hyuek Jong Lee & Jueun Lee & Myung Jin Yang & Young-Chan Kim & Seon Pyo Hong & Jung Mo Kim & Geum-Sook Hwang & Gou Young Koh, 2023. "Endothelial cell-derived stem cell factor promotes lipid accumulation through c-Kit-mediated increase of lipogenic enzymes in brown adipocytes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Nathalia G. Amado & Elena D. Nosyreva & David Thompson & Thomas J. Egeland & Osita W. Ogujiofor & Michelle Yang & Alexandria N. Fusco & Niccolo Passoni & Jeremy Mathews & Brandi Cantarel & Linda A. Ba, 2024. "PIEZO1 loss-of-function compound heterozygous mutations in the rare congenital human disorder Prune Belly Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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