Remodeling of Bone Marrow Hematopoietic Stem Cell Niches Promotes Myeloid Cell Expansion during Premature or Physiological Aging
Open accessAbstract
Hematopoietic stem cells (HSCs) residing in the bone marrow (BM) accumulate during aging but are functionally impaired. However, the role of HSC-intrinsic and -extrinsic aging mechanisms remains debated. Megakaryocytes promote quiescence of neighboring HSCs. Nonetheless, whether megakaryocyte-HSC interactions change during pathological/natural aging is unclear. Premature aging in Hutchinson-Gilford progeria syndrome recapitulates physiological aging features, but whether these arise from altered stem or niche cells is unknown. Here, we show that the BM microenvironment promotes myelopoiesis in premature/physiological aging. During physiological aging, HSC-supporting niches decrease near bone but expand further from bone. Increased BM noradrenergic innervation promotes β 2 -adrenergic-receptor(AR)-interleukin-6-dependent megakaryopoiesis. Reduced β 3 -AR-Nos1 activity correlates with decreased endosteal niches and megakaryocyte apposition to sinusoids. However, chronic treatment of progeroid mice with β 3 -AR agonist decreases premature myeloid and HSC expansion and restores the proximal association of HSCs to megakaryocytes. Therefore, normal/premature aging of BM niches promotes myeloid expansion and can be improved by targeting the microenvironment.
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Inflammatory cytokines, including TNF, TGF1β, IL-6 and IL-1β, have been found to be upregulated in aged bone marrow (HSC niche).
“Inflammatory cytokines, including TNF76, transforming growth factor-β1 (TGF1β)77, IL-6 (REF.78) and IL-1β (REF.79), have also been found to be upregulated in aged bone marrow (HSC niche).”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [78]
In the bone marrow, megakaryocytes show increased production of IL-6, which is modulated by β-adrenergic signalling and inducible nitric oxide synthase signalling; β3-adrenergic receptor agonist treatment reduces the myeloid shift of HSCs in prematurely aged mice caused by lamin A mutations.
“In the bone marrow, megakaryocytes appear to show increased production of the inflammatory cytokine IL-6 (REF.78), which is modulated by both β-adrenergic signalling (from sympathetic nerves) and inducible nitric oxide synthase signalling78. Indeed, β3-adrenergic receptor agonist treatment reduces the myeloid shift of HSCs in prematurely aged mice, caused by germ line mutations in lamin A78.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [78]
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- Authors
- Ho, Y.-H., del Toro, R., Rivera-Torres, J., Rak, J., Korn, C., García-García, A., Macías, D., González-Gómez, C., del Monte, A., Wittner, M., Waller, A. K., Foster, H. R., López-Otín, C., Johnson, R. S., Nerlov, C., Ghevaert, C., Vainchenker, W., Louache, F., Andrés, V., & Méndez-Ferrer, S.
- Affiliations
- National Health Service (GB)
- University of Cambridge (GB)
- Centre National de la Recherche Scientifique (FR)
- John Radcliffe Hospital (GB)
- Inserm (FR)
- Spanish National Centre for Cardiovascular Research (ES)
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2019-09
- Volume
- 25
- Issue
- 3
- Pages
- 407-418.e6
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC6739444
- OpenAlex
- W2957271680
- Cited by
- 315
- References
- 64
- Citations by year
- 2026: 32 · 2025: 49 · 2024: 43 · 2023: 44 · 2022: 38 · 2021: 56 · 2020: 43 · 2019: 10
- FWCI
- 25.97
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- HAL (submittedVersion)
- ABACUS. Repositorio de Producción Científica (Universidad Europea) (submittedVersion, cc-by)
- Consultation of the Doctoral Thesis Database (TESEO) (Ministerio de Educación, Cultura y Deporte) (submittedVersion, cc-by-nc-nd)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-sa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by)
- Deposito de Investigacion Universidad de Sevilla (University of Seville) (submittedVersion, cc-by)
- Apollo (cc-by)
- Greater South Information System
- Funders
- Medical Research Council (RYC-2009-04703, SAF-2011-30308, S2010/BMD-2542)
- Instituto de Salud Carlos III (TV3, 122/C/2015, AC17/00067, AC16/00091)
- Progeria Research Foundation (2014\u201352)
- “la Caixa” Foundation
- Ministerio de Ciencia e Innovación
- Ministerio de Ciencia, Innovación y Universidades
- Marie Curie (H2020-MSCA-IF-2015-70841)
- Cancer Research UK
- University of Cambridge
- European Regional Development Fund (SAF2016-79490-R)
- Wellcome Trust
- Fundación Ramón Areces
- Fundació la Marató de TV3
- NHS Blood and Transplant
- European Research Council (ERC-2014-CoG-64765)
- European Molecular Biology Laboratory
- Ministerio de Economía, Industria y Competitividad, Gobierno de España
- Ministry of Education of the People's Republic of China
- FP7 People: Marie-Curie Actions
- Howard Hughes Medical Institute
- Center for Outcomes Research and Evaluation, Yale School of Medicine
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Blood disorders and treatments
- Keywords
- hematopoietic stem cells, bone marrow microenvironment, aging, myeloid expansion, megakaryocytes, beta3-adrenergic receptor, beta2-adrenergic receptor, interleukin-6, noradrenergic innervation, endosteal niche, Hutchinson-Gilford progeria syndrome, myelopoiesis, niche remodeling
- MeSH terms
- Cell Encapsulation, Adrenergic Agonists, Aging, Animals, Bone Marrow, Cell Differentiation, Disease Models, Animal, Hematopoietic Stem Cells, Humans, Megakaryocytes, Progeria, Signal Transduction, Interleukin-6, Receptors, Adrenergic, beta-2, Aging, Premature, Myeloid Cells, Cell Proliferation, Mice, Nitric Oxide Synthase Type I, Stem Cell Niche
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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