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Myeloid cells promote interferon signaling-associated deterioration of the hematopoietic system

Author

Listed:
  • Jacqueline Feyen

    (Erasmus MC Cancer Institute)

  • Zhen Ping

    (Erasmus MC Cancer Institute)

  • Lanpeng Chen

    (Erasmus MC Cancer Institute)

  • Claire Dijk

    (Erasmus MC Cancer Institute)

  • Tim V. D. Tienhoven

    (Erasmus MC Cancer Institute)

  • Paulina M. H. Strien

    (Erasmus MC Cancer Institute)

  • Remco M. Hoogenboezem

    (Erasmus MC Cancer Institute)

  • Michiel J. W. Wevers

    (Erasmus MC Cancer Institute)

  • Mathijs A. Sanders

    (Erasmus MC Cancer Institute)

  • Ivo P. Touw

    (Erasmus MC Cancer Institute)

  • Marc H. G. P. Raaijmakers

    (Erasmus MC Cancer Institute)

Abstract

Innate and adaptive immune cells participate in the homeostatic regulation of hematopoietic stem cells (HSCs). Here, we interrogate the contribution of myeloid cells, the most abundant cell type in the mammalian bone marrow, in a clinically relevant mouse model of neutropenia. Long-term genetic depletion of neutrophils and eosinophils results in activation of multipotent progenitors but preservation of HSCs. Depletion of myeloid cells abrogates HSC expansion, loss of serial repopulation and lymphoid reconstitution capacity and remodeling of HSC niches, features previously associated with hematopoietic aging. This is associated with mitigation of interferon signaling in both HSCs and their niches via reduction of NK cell number and activation. These data implicate myeloid cells in the functional decline of hematopoiesis, associated with activation of interferon signaling via a putative neutrophil-NK cell axis. Innate immunity may thus come at the cost of system deterioration through enhanced chronic inflammatory signaling to stem cells and their niches.

Suggested Citation

  • Jacqueline Feyen & Zhen Ping & Lanpeng Chen & Claire Dijk & Tim V. D. Tienhoven & Paulina M. H. Strien & Remco M. Hoogenboezem & Michiel J. W. Wevers & Mathijs A. Sanders & Ivo P. Touw & Marc H. G. P., 2022. "Myeloid cells promote interferon signaling-associated deterioration of the hematopoietic system," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35318-x
    DOI: 10.1038/s41467-022-35318-x
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    1. Johanna Flach & Sietske T. Bakker & Mary Mohrin & Pauline C. Conroy & Eric M. Pietras & Damien Reynaud & Silvia Alvarez & Morgan E. Diolaiti & Fernando Ugarte & E. Camilla Forsberg & Michelle M. Le Be, 2014. "Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells," Nature, Nature, vol. 512(7513), pages 198-202, August.
    2. 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.
    3. Robert A. J. Signer & Jeffrey A. Magee & Adrian Salic & Sean J. Morrison, 2014. "Haematopoietic stem cells require a highly regulated protein synthesis rate," Nature, Nature, vol. 509(7498), pages 49-54, May.
    4. Tatyana Grinenko & Anne Eugster & Lars Thielecke & Beáta Ramasz & Anja Krüger & Sevina Dietz & Ingmar Glauche & Alexander Gerbaulet & Malte Bonin & Onur Basak & Hans Clevers & Triantafyllos Chavakis &, 2018. "Hematopoietic stem cells can differentiate into restricted myeloid progenitors before cell division in mice," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    5. Katrin Busch & Kay Klapproth & Melania Barile & Michael Flossdorf & Tim Holland-Letz & Susan M. Schlenner & Michael Reth & Thomas Höfer & Hans-Reimer Rodewald, 2015. "Fundamental properties of unperturbed haematopoiesis from stem cells in vivo," Nature, Nature, vol. 518(7540), pages 542-546, February.
    6. Joji Fujisaki & Juwell Wu & Alicia L. Carlson & Lev Silberstein & Prabhakar Putheti & Rafael Larocca & Wenda Gao & Toshiki I. Saito & Cristina Lo Celso & Hitoshi Tsuyuzaki & Tatsuyuki Sato & Daniel Cô, 2011. "In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche," Nature, Nature, vol. 474(7350), pages 216-219, June.
    7. Noushine Mossadegh-Keller & Sandrine Sarrazin & Prashanth K. Kandalla & Leon Espinosa & E. Richard Stanley & Stephen L. Nutt & Jordan Moore & Michael H. Sieweke, 2013. "M-CSF instructs myeloid lineage fate in single haematopoietic stem cells," Nature, Nature, vol. 497(7448), pages 239-243, May.
    8. Dagmar Walter & Amelie Lier & Anja Geiselhart & Frederic B. Thalheimer & Sina Huntscha & Mirko C. Sobotta & Bettina Moehrle & David Brocks & Irem Bayindir & Paul Kaschutnig & Katja Muedder & Corinna K, 2015. "Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells," Nature, Nature, vol. 520(7548), pages 549-552, April.
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