Cited by 936Hematopoietic Stem Cell TransplantationSingle-cell and spatial transcriptomicsMesenchymal stem cell research

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The bone marrow microenvironment at single-cell resolution

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Tikhonova, Anastasia N., Dolgalev, Igor, Hu, Hai, Sivaraj, Kishor K., Hoxha, Edlira, Cuesta-Domínguez, Álvaro, Pinho, Sandra, Akhmetzyanova, Ilseyar, Gao, Jie, Witkowski, Matthew, Guillamot, Maria, Gutkin, Michael C., Zhang, Yutong, Marier, Christian, Diefenbach, Catherine, Kousteni, Stavroula, Heguy, Adriana, Zhong, Hua, Fooksman, David R., Butler, Jason M., Economides, Aris, Frenette, Paul S., Adams, Ralf H., Satija, Rahul, Tsirigos, Aristotelis, Aifantis, Iannis·2019·Nature

DOI 10.1038/s41586-019-1104-8PMC PMC6607432

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Abstract

The bone marrow microenvironment has a key role in regulating haematopoiesis, but its molecular complexity and response to stress are incompletely understood. Here we map the transcriptional landscape of mouse bone marrow vascular, perivascular and osteoblast cell populations at single-cell resolution, both at homeostasis and under conditions of stress-induced haematopoiesis. This analysis revealed previously unappreciated levels of cellular heterogeneity within the bone marrow niche and resolved cellular sources of pro-haematopoietic growth factors, chemokines and membrane-bound ligands. Our studies demonstrate a considerable transcriptional remodelling of niche elements under stress conditions, including an adipocytic skewing of perivascular cells. Among the stress-induced changes, we observed that vascular Notch delta-like ligands (encoded by Dll1 and Dll4) were downregulated. In the absence of vascular Dll4, haematopoietic stem cells prematurely induced a myeloid transcriptional program. These findings refine our understanding of the cellular architecture of the bone marrow niche, reveal a dynamic and heterogeneous molecular landscape that is highly sensitive to stress and illustrate the utility of single-cell transcriptomic data in evaluating the regulation of haematopoiesis by discrete niche populations.

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Authors: Tikhonova, A. N., Dolgalev, I., Hu, H., Sivaraj, K. K., Hoxha, E., Cuesta-Domínguez, Á., Pinho, S., Akhmetzyanova, I., Gao, J., Witkowski, M., Guillamot, M., Gutkin, M. C., Zhang, Y., Marier, C., Diefenbach, C., Kousteni, S., Heguy, A., Zhong, H., Fooksman, D. R., Butler, J. M., Economides, A., Frenette, P. S., Adams, R. H., Satija, R., Tsirigos, A., & Aifantis, I.
Affiliations: NYU Langone Health (US)
University of Münster (DE)
Albert Einstein College of Medicine (US)
Regeneron (United States) (US)
Hackensack University Medical Center (US)
Columbia University (US)
New York Genome Center (US)
Corresponding author: Tikhonova, Anastasia N.
Tsirigos, Aristotelis
Aifantis, Iannis
ORCID: Tikhonova, Anastasia N.
Dolgalev, Igor
Hu, Hai
Sivaraj, Kishor K.
Pinho, Sandra
Akhmetzyanova, Ilseyar
Gao, Jie
Witkowski, Matthew
Gutkin, Michael C.
Zhang, Yutong
Diefenbach, Catherine
Kousteni, Stavroula
Heguy, Adriana
Fooksman, David R.
Butler, Jason M.
Economides, Aris
Frenette, Paul S.
Adams, Ralf H.
Satija, Rahul
Tsirigos, Aristotelis
Aifantis, Iannis
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2019-04-10
Volume: 569
Issue: 7755
Pages: 222-228
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-019-1104-8
PMC: PMC6607432
OpenAlex: W2936664461
Cited by: 936
References: 73
Citations by year: 2026: 89 · 2025: 106 · 2024: 113 · 2023: 153 · 2022: 129 · 2021: 153 · 2020: 137 · 2019: 56
FWCI: 83.83
Type: journal article
Language: en
Update notices: correction (2019-07-12)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: NYU Langone Medical Center
Nature
National Institutes of Health (1dp2hg009623-01)
National Heart, Lung, and Blood Institute (R01HL130937, R01HL069438)
National Human Genome Research Institute (DP2-HG-009623)
National Cancer Institute (R01CA194923, R01CA202027, R01CA202025, R01CA169784, R01CA105129)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK112976, R01DK056638, U01DK116312)
Topics: Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
Keywords: bone marrow microenvironment, hematopoiesis, hematopoietic stem cells, single-cell transcriptomics, perivascular cells, osteoblasts, vascular cells, DLL4, DLL1, Notch signaling, myeloid differentiation, chemokines, growth factors, cellular heterogeneity
MeSH terms: RNA-Seq, Animals, Bone Marrow, Calcium-Binding Proteins, Cell Differentiation, Endothelium, Vascular, Female, Gene Expression Regulation, Hematopoiesis, Hematopoietic Stem Cells, Male, Osteoblasts, Stress, Physiological, Adipocytes, Cell Lineage, Myeloid Cells, Adaptor Proteins, Signal Transducing, Mice, Receptors, Notch, Stem Cell Niche, Single-Cell Analysis, Transcriptome, Cellular Microenvironment

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