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Perivascular niche cells sense thrombocytopenia and activate hematopoietic stem cells in an IL-1 dependent manner

Author

Listed:
  • Tiago C. Luis

    (University of Oxford
    University of Oxford
    Imperial College London
    Imperial College London)

  • Nikolaos Barkas

    (University of Oxford
    University of Oxford)

  • Joana Carrelha

    (University of Oxford
    University of Oxford)

  • Alice Giustacchini

    (University of Oxford
    University of Oxford
    UCL Great Ormond Street Institute of Child Health
    Viale Rita Levi-Montalcini 1)

  • Stefania Mazzi

    (Karolinska Institutet, Karolinska University Hospital)

  • Ruggiero Norfo

    (University of Oxford
    University of Oxford)

  • Bishan Wu

    (University of Oxford
    University of Oxford)

  • Affaf Aliouat

    (University of Oxford
    University of Oxford)

  • Jose A. Guerrero

    (University of Cambridge
    Cambridge Biomedical Campus)

  • Alba Rodriguez-Meira

    (University of Oxford
    University of Oxford)

  • Tiphaine Bouriez-Jones

    (University of Oxford
    University of Oxford)

  • Iain C. Macaulay

    (University of Oxford
    University of Oxford
    Norwich Research Park)

  • Maria Jasztal

    (University of Cambridge
    Cambridge Biomedical Campus)

  • Guangheng Zhu

    (St. Michael’s Hospital
    CCOA Therapeutics Inc)

  • Heyu Ni

    (St. Michael’s Hospital
    CCOA Therapeutics Inc
    University of Toronto
    Canadian Blood Services Centre for Innovation)

  • Matthew J. Robson

    (Florida Atlantic University
    University of Cincinnati)

  • Randy D. Blakely

    (Florida Atlantic University)

  • Adam J. Mead

    (University of Oxford
    University of Oxford)

  • Claus Nerlov

    (University of Oxford)

  • Cedric Ghevaert

    (University of Cambridge
    Cambridge Biomedical Campus)

  • Sten Eirik W. Jacobsen

    (University of Oxford
    University of Oxford
    Karolinska Institutet, Karolinska University Hospital
    Karolinska Institutet)

Abstract

Hematopoietic stem cells (HSCs) residing in specialized niches in the bone marrow are responsible for the balanced output of multiple short-lived blood cell lineages in steady-state and in response to different challenges. However, feedback mechanisms by which HSCs, through their niches, sense acute losses of specific blood cell lineages remain to be established. While all HSCs replenish platelets, previous studies have shown that a large fraction of HSCs are molecularly primed for the megakaryocyte-platelet lineage and are rapidly recruited into proliferation upon platelet depletion. Platelets normally turnover in an activation-dependent manner, herein mimicked by antibodies inducing platelet activation and depletion. Antibody-mediated platelet activation upregulates expression of Interleukin-1 (IL-1) in platelets, and in bone marrow extracellular fluid in vivo. Genetic experiments demonstrate that rather than IL-1 directly activating HSCs, activation of bone marrow Lepr+ perivascular niche cells expressing IL-1 receptor is critical for the optimal activation of quiescent HSCs upon platelet activation and depletion. These findings identify a feedback mechanism by which activation-induced depletion of a mature blood cell lineage leads to a niche-dependent activation of HSCs to reinstate its homeostasis.

Suggested Citation

  • Tiago C. Luis & Nikolaos Barkas & Joana Carrelha & Alice Giustacchini & Stefania Mazzi & Ruggiero Norfo & Bishan Wu & Affaf Aliouat & Jose A. Guerrero & Alba Rodriguez-Meira & Tiphaine Bouriez-Jones &, 2023. "Perivascular niche cells sense thrombocytopenia and activate hematopoietic stem cells in an IL-1 dependent manner," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41691-y
    DOI: 10.1038/s41467-023-41691-y
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    References listed on IDEAS

    as
    1. Megan T. Baldridge & Katherine Y. King & Nathan C. Boles & David C. Weksberg & Margaret A. Goodell, 2010. "Quiescent haematopoietic stem cells are activated by IFN-γ in response to chronic infection," Nature, Nature, vol. 465(7299), pages 793-797, June.
    2. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    3. Lei Ding & Thomas L. Saunders & Grigori Enikolopov & Sean J. Morrison, 2012. "Endothelial and perivascular cells maintain haematopoietic stem cells," Nature, Nature, vol. 481(7382), pages 457-462, January.
    4. Joana Carrelha & Yiran Meng & Laura M. Kettyle & Tiago C. Luis & Ruggiero Norfo & Verónica Alcolea & Hanane Boukarabila & Francesca Grasso & Adriana Gambardella & Amit Grover & Kari Högstrand & Allegr, 2018. "Hierarchically related lineage-restricted fates of multipotent haematopoietic stem cells," Nature, Nature, vol. 554(7690), pages 106-111, February.
    5. Dieter Egli & Jacqueline Rosains & Garrett Birkhoff & Kevin Eggan, 2007. "Developmental reprogramming after chromosome transfer into mitotic mouse zygotes," Nature, Nature, vol. 447(7145), pages 679-685, June.
    6. Alejandra Sanjuan-Pla & Iain C. Macaulay & Christina T. Jensen & Petter S. Woll & Tiago C. Luis & Adam Mead & Susan Moore & Cintia Carella & Sahoko Matsuoka & Tiphaine Bouriez Jones & Onima Chowdhury , 2013. "Platelet-biased stem cells reside at the apex of the haematopoietic stem-cell hierarchy," Nature, Nature, vol. 502(7470), pages 232-236, October.
    7. Lei Ding & Sean J. Morrison, 2013. "Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches," Nature, Nature, vol. 495(7440), pages 231-235, March.
    8. Yuya Kunisaki & Ingmar Bruns & Christoph Scheiermann & Jalal Ahmed & Sandra Pinho & Dachuan Zhang & Toshihide Mizoguchi & Qiaozhi Wei & Daniel Lucas & Keisuke Ito & Jessica C. Mar & Aviv Bergman & Pau, 2013. "Arteriolar niches maintain haematopoietic stem cell quiescence," Nature, Nature, vol. 502(7473), pages 637-643, October.
    9. June Li & Dianne E. van der Wal & Guangheng Zhu & Miao Xu & Issaka Yougbare & Li Ma & Brian Vadasz & Naadiya Carrim & Renata Grozovsky & Min Ruan & Lingyan Zhu & Qingshu Zeng & Lili Tao & Zhi-min Zhai, 2015. "Desialylation is a mechanism of Fc-independent platelet clearance and a therapeutic target in immune thrombocytopenia," Nature Communications, Nature, vol. 6(1), pages 1-16, November.
    10. Sean J. Morrison & David T. Scadden, 2014. "The bone marrow niche for haematopoietic stem cells," Nature, Nature, vol. 505(7483), pages 327-334, January.
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