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Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone

Author

Listed:
  • Anjali P. Kusumbe

    (Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany)

  • Saravana K. Ramasamy

    (Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany)

  • Ralf H. Adams

    (Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany
    University of Münster, Faculty of Medicine, D-48149 Münster, Germany)

Abstract

The mammalian skeletal system harbours a hierarchical system of mesenchymal stem cells, osteoprogenitors and osteoblasts sustaining lifelong bone formation. Osteogenesis is indispensable for the homeostatic renewal of bone as well as regenerative fracture healing, but these processes frequently decline in ageing organisms, leading to loss of bone mass and increased fracture incidence. Evidence indicates that the growth of blood vessels in bone and osteogenesis are coupled, but relatively little is known about the underlying cellular and molecular mechanisms. Here we identify a new capillary subtype in the murine skeletal system with distinct morphological, molecular and functional properties. These vessels are found in specific locations, mediate growth of the bone vasculature, generate distinct metabolic and molecular microenvironments, maintain perivascular osteoprogenitors and couple angiogenesis to osteogenesis. The abundance of these vessels and associated osteoprogenitors was strongly reduced in bone from aged animals, and pharmacological reversal of this decline allowed the restoration of bone mass.

Suggested Citation

  • Anjali P. Kusumbe & Saravana K. Ramasamy & Ralf H. Adams, 2014. "Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone," Nature, Nature, vol. 507(7492), pages 323-328, March.
    • Handle: RePEc:nat:nature:v:507:y:2014:i:7492:d:10.1038_nature13145
    DOI: 10.1038/nature13145
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    Cited by:

    1. Young-Woong Kim & Greta Zara & HyunJun Kang & Sergio Branciamore & Denis O’Meally & Yuxin Feng & Chia-Yi Kuan & Yingjun Luo & Michael S. Nelson & Alex B. Brummer & Russell Rockne & Zhen Bouman Chen & , 2022. "Integration of single-cell transcriptomes and biological function reveals distinct behavioral patterns in bone marrow endothelium," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Joschka Heil & Victor Olsavszky & Katrin Busch & Kay Klapproth & Carolina Torre & Carsten Sticht & Kajetan Sandorski & Johannes Hoffmann & Hiltrud Schönhaber & Johanna Zierow & Manuel Winkler & Christ, 2021. "Bone marrow sinusoidal endothelium controls terminal erythroid differentiation and reticulocyte maturation," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Alexandra N. Rindone & Xiaonan Liu & Stephanie Farhat & Alexander Perdomo-Pantoja & Timothy F. Witham & Daniel L. Coutu & Mei Wan & Warren L. Grayson, 2021. "Quantitative 3D imaging of the cranial microvascular environment at single-cell resolution," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Jianping Wang & Bin Zhao & Jingmin Che & Peng Shang, 2023. "Hypoxia Pathway in Osteoporosis: Laboratory Data for Clinical Prospects," IJERPH, MDPI, vol. 20(4), pages 1-22, February.
    5. Eman Khatib-Massalha & Suditi Bhattacharya & Hassan Massalha & Adi Biram & Karin Golan & Orit Kollet & Anju Kumari & Francesca Avemaria & Ekaterina Petrovich-Kopitman & Shiri Gur-Cohen & Tomer Itkin &, 2020. "Lactate released by inflammatory bone marrow neutrophils induces their mobilization via endothelial GPR81 signaling," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    6. M. Gabriele Bixel & Kishor K. Sivaraj & Melanie Timmen & Vishal Mohanakrishnan & Anusha Aravamudhan & Susanne Adams & Bong-Ihn Koh & Hyun-Woo Jeong & Kai Kruse & Richard Stange & Ralf H. Adams, 2024. "Angiogenesis is uncoupled from osteogenesis during calvarial bone regeneration," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    7. Raymond K. H. Yip & Joel S. Rimes & Bianca D. Capaldo & François Vaillant & Kellie A. Mouchemore & Bhupinder Pal & Yunshun Chen & Elliot Surgenor & Andrew J. Murphy & Robin L. Anderson & Gordon K. Smy, 2021. "Mammary tumour cells remodel the bone marrow vascular microenvironment to support metastasis," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    8. Chee Ho H’ng & Shanika L. Amarasinghe & Boya Zhang & Hojin Chang & Xinli Qu & David R. Powell & Alberto Rosello-Diez, 2024. "Compensatory growth and recovery of cartilage cytoarchitecture after transient cell death in fetal mouse limbs," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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