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Distinct bone marrow blood vessels differentially regulate haematopoiesis

Author

Listed:
  • Tomer Itkin

    (The Weizmann Institute of Science)

  • Shiri Gur-Cohen

    (The Weizmann Institute of Science)

  • Joel A. Spencer

    (Wellman Center for Photomedicine, Massachusetts General Hospital, Harvard Medical School
    Center for Systems Biology, Massachusetts General Hospital, Harvard Medical School)

  • Amir Schajnovitz

    (Harvard University
    Harvard Stem Cell Institute
    Center for Regenerative Medicine and Cancer Center, Massachusetts General Hospital)

  • Saravana K. Ramasamy

    (Max Planck Institute for Molecular Biomedicine, University of Münster)

  • Anjali P. Kusumbe

    (Max Planck Institute for Molecular Biomedicine, University of Münster)

  • Guy Ledergor

    (The Weizmann Institute of Science
    Tel-Aviv Sourasky Medical Center)

  • Yookyung Jung

    (Wellman Center for Photomedicine, Massachusetts General Hospital, Harvard Medical School
    Center for Systems Biology, Massachusetts General Hospital, Harvard Medical School)

  • Idan Milo

    (The Weizmann Institute of Science)

  • Michael G. Poulos

    (Weill Cornell Medical College)

  • Alexander Kalinkovich

    (The Weizmann Institute of Science)

  • Aya Ludin

    (The Weizmann Institute of Science)

  • Karin Golan

    (The Weizmann Institute of Science)

  • Eman Khatib

    (The Weizmann Institute of Science)

  • Anju Kumari

    (The Weizmann Institute of Science)

  • Orit Kollet

    (The Weizmann Institute of Science)

  • Guy Shakhar

    (The Weizmann Institute of Science)

  • Jason M. Butler

    (Weill Cornell Medical College)

  • Shahin Rafii

    (Weill Cornell Medical College)

  • Ralf H. Adams

    (Max Planck Institute for Molecular Biomedicine, University of Münster)

  • David T. Scadden

    (Harvard University
    Harvard Stem Cell Institute
    Center for Regenerative Medicine and Cancer Center, Massachusetts General Hospital)

  • Charles P. Lin

    (Wellman Center for Photomedicine, Massachusetts General Hospital, Harvard Medical School
    Center for Systems Biology, Massachusetts General Hospital, Harvard Medical School)

  • Tsvee Lapidot

    (The Weizmann Institute of Science)

Abstract

Bone marrow endothelial cells (BMECs) form a network of blood vessels that regulate both leukocyte trafficking and haematopoietic stem and progenitor cell (HSPC) maintenance. However, it is not clear how BMECs balance these dual roles, and whether these events occur at the same vascular site. We found that mammalian bone marrow stem cell maintenance and leukocyte trafficking are regulated by distinct blood vessel types with different permeability properties. Less permeable arterial blood vessels maintain haematopoietic stem cells in a low reactive oxygen species (ROS) state, whereas the more permeable sinusoids promote HSPC activation and are the exclusive site for immature and mature leukocyte trafficking to and from the bone marrow. A functional consequence of high permeability of blood vessels is that exposure to blood plasma increases bone marrow HSPC ROS levels, augmenting their migration and differentiation, while compromising their long-term repopulation and survival. These findings may have relevance for clinical haematopoietic stem cell transplantation and mobilization protocols.

Suggested Citation

  • Tomer Itkin & Shiri Gur-Cohen & Joel A. Spencer & Amir Schajnovitz & Saravana K. Ramasamy & Anjali P. Kusumbe & Guy Ledergor & Yookyung Jung & Idan Milo & Michael G. Poulos & Alexander Kalinkovich & A, 2016. "Distinct bone marrow blood vessels differentially regulate haematopoiesis," Nature, Nature, vol. 532(7599), pages 323-328, April.
    • Handle: RePEc:nat:nature:v:532:y:2016:i:7599:d:10.1038_nature17624
    DOI: 10.1038/nature17624
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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. Trent D. Hall & Hyunjin Kim & Mahmoud Dabbah & Jacquelyn A. Myers & Jeremy Chase Crawford & Antonio Morales-Hernandez & Claire E. Caprio & Pramika Sriram & Emilia Kooienga & Marta Derecka & Esther A. , 2022. "Murine fetal bone marrow does not support functional hematopoietic stem and progenitor cells until birth," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Christina M. Termini & Amara Pang & Tiancheng Fang & Martina Roos & Vivian Y. Chang & Yurun Zhang & Nicollette J. Setiawan & Lia Signaevskaia & Michelle Li & Mindy M. Kim & Orel Tabibi & Paulina K. Li, 2021. "Neuropilin 1 regulates bone marrow vascular regeneration and hematopoietic reconstitution," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    5. Till Fabian Mertens & Alina Tabea Liebheit & Johanna Ehl & Ralf Köhler & Asylkhan Rakhymzhan & Andrew Woehler & Lukas Katthän & Gernot Ebel & Wjatscheslaw Liublin & Ana Kasapi & Antigoni Triantafyllop, 2024. "MarShie: a clearing protocol for 3D analysis of single cells throughout the bone marrow at subcellular resolution," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    6. 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.
    7. 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.

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