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Competition between hematopoietic stem and progenitor cells controls hematopoietic stem cell compartment size

Author

Listed:
  • Runfeng Miao

    (Yale University School of Medicine)

  • Harim Chun

    (Korea University College of Medicine)

  • Xing Feng

    (Yale University School of Medicine)

  • Ana Cordeiro Gomes

    (Yale University School of Medicine
    i3S – Instituto de Investigação e Inovação em Saúde, University of Porto)

  • Jungmin Choi

    (Korea University College of Medicine
    Yale University School of Medicine)

  • João P. Pereira

    (Yale University School of Medicine)

Abstract

Cellular competition for limiting hematopoietic factors is a physiologically regulated but poorly understood process. Here, we studied this phenomenon by hampering hematopoietic progenitor access to Leptin receptor+ mesenchymal stem/progenitor cells (MSPCs) and endothelial cells (ECs). We show that HSC numbers increase by 2-fold when multipotent and lineage-restricted progenitors fail to respond to CXCL12 produced by MSPCs and ECs. HSCs are qualitatively normal, and HSC expansion only occurs when early hematopoietic progenitors but not differentiated hematopoietic cells lack CXCR4. Furthermore, the MSPC and EC transcriptomic heterogeneity is stable, suggesting that it is impervious to major changes in hematopoietic progenitor interactions. Instead, HSC expansion correlates with increased availability of membrane-bound stem cell factor (mSCF) on MSPCs and ECs presumably due to reduced consumption by cKit-expressing hematopoietic progenitors. These studies suggest that an intricate homeostatic balance between HSCs and proximal hematopoietic progenitors is regulated by cell competition for limited amounts of mSCF.

Suggested Citation

  • Runfeng Miao & Harim Chun & Xing Feng & Ana Cordeiro Gomes & Jungmin Choi & João P. Pereira, 2022. "Competition between hematopoietic stem and progenitor cells controls hematopoietic stem cell compartment size," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32228-w
    DOI: 10.1038/s41467-022-32228-w
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    as
    1. Jizhou Zhang & Qingqing Wu & Courtney B. Johnson & Giang Pham & Jeremy M. Kinder & Andre Olsson & Anastasiya Slaughter & Margot May & Benjamin Weinhaus & Angelo D’Alessandro & James Douglas Engel & Je, 2021. "In situ mapping identifies distinct vascular niches for myelopoiesis," Nature, Nature, vol. 590(7846), pages 457-462, February.
    2. Cristina Lo Celso & Heather E. Fleming & Juwell W. Wu & Cher X. Zhao & Sam Miake-Lye & Joji Fujisaki & Daniel Côté & David W. Rowe & Charles P. Lin & David T. Scadden, 2009. "Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche," Nature, Nature, vol. 457(7225), pages 92-96, January.
    3. Sean J. Morrison & David T. Scadden, 2014. "The bone marrow niche for haematopoietic stem cells," Nature, Nature, vol. 505(7483), pages 327-334, January.
    4. Dantong Li & Wenzhi Xue & Mei Li & Mei Dong & Jianwei Wang & Xianda Wang & Xiyue Li & Kai Chen & Wenjuan Zhang & Shuang Wu & Yingqi Zhang & Lei Gao & Yujie Chen & Jianfeng Chen & Bo O. Zhou & Yi Zhou , 2018. "VCAM-1+ macrophages guide the homing of HSPCs to a vascular niche," Nature, Nature, vol. 564(7734), pages 119-124, December.
    5. Anastasia N. Tikhonova & Igor Dolgalev & Hai Hu & Kishor K. Sivaraj & Edlira Hoxha & Álvaro Cuesta-Domínguez & Sandra Pinho & Ilseyar Akhmetzyanova & Jie Gao & Matthew Witkowski & Maria Guillamot & Mi, 2019. "The bone marrow microenvironment at single-cell resolution," Nature, Nature, vol. 569(7755), pages 222-228, May.
    6. 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.
    7. Anastasia N. Tikhonova & Igor Dolgalev & Hai Hu & Kishor K. Sivaraj & Edlira Hoxha & Álvaro Cuesta-Domínguez & Sandra Pinho & Ilseyar Akhmetzyanova & Jie Gao & Matthew Witkowski & Maria Guillamot & Mi, 2019. "Author Correction: The bone marrow microenvironment at single-cell resolution," Nature, Nature, vol. 572(7767), pages 6-6, August.
    8. Constantina Christodoulou & Joel A. Spencer & Shu-Chi A. Yeh & Raphaël Turcotte & Konstantinos D. Kokkaliaris & Riccardo Panero & Azucena Ramos & Guoji Guo & Negar Seyedhassantehrani & Tatiana V. Esip, 2020. "Live-animal imaging of native haematopoietic stem and progenitor cells," Nature, Nature, vol. 578(7794), pages 278-283, February.
    9. Chunliang Xu & Xin Gao & Qiaozhi Wei & Fumio Nakahara & Samuel E. Zimmerman & Jessica Mar & Paul S. Frenette, 2018. "Stem cell factor is selectively secreted by arterial endothelial cells in bone marrow," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    10. Adam Greenbaum & Yen-Michael S. Hsu & Ryan B. Day & Laura G. Schuettpelz & Matthew J. Christopher & Joshua N. Borgerding & Takashi Nagasawa & Daniel C. Link, 2013. "CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance," Nature, Nature, vol. 495(7440), pages 227-230, March.
    11. 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.
    12. 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.
    13. Simón Méndez-Ferrer & Tatyana V. Michurina & Francesca Ferraro & Amin R. Mazloom & Ben D. MacArthur & Sergio A. Lira & David T. Scadden & Avi Ma’ayan & Grigori N. Enikolopov & Paul S. Frenette, 2010. "Mesenchymal and haematopoietic stem cells form a unique bone marrow niche," Nature, Nature, vol. 466(7308), pages 829-834, August.
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