Cited by 1,381Mesenchymal stem cell researchHematopoietic Stem Cell TransplantationBone Metabolism and Diseases

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Leptin-Receptor-Expressing Mesenchymal Stromal Cells Represent the Main Source of Bone Formed by Adult Bone Marrow

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Zhou, Bo O., Yue, Rui, Murphy, Malea M., Peyer, James G., Morrison, Sean J.·2014·Cell Stem Cell

DOI 10.1016/j.stem.2014.06.008PMC PMC4127103

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Abstract

Studies of the identity and physiological function of mesenchymal stromal cells (MSCs) have been hampered by a lack of markers that permit both prospective identification and fate mapping in vivo. We found that Leptin Receptor (LepR) is a marker that highly enriches bone marrow MSCs. Approximately 0.3% of bone marrow cells were LepR(+), 10% of which were CFU-Fs, accounting for 94% of bone marrow CFU-Fs. LepR(+) cells formed bone, cartilage, and adipocytes in culture and upon transplantation in vivo. LepR(+) cells were Scf-GFP(+), Cxcl12-DsRed(high), and Nestin-GFP(low), markers which also highly enriched CFU-Fs, but negative for Nestin-CreER and NG2-CreER, markers which were unlikely to be found in CFU-Fs. Fate-mapping showed that LepR(+) cells arose postnatally and gave rise to most bone and adipocytes formed in adult bone marrow, including bone regenerated after irradiation or fracture. LepR(+) cells were quiescent, but they proliferated after injury. Therefore, LepR(+) cells are the major source of bone and adipocytes in adult bone marrow.

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Influential
Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus
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Self-citation
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Background
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BackgroundInfluential
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Background
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“Moreover, proliferation of LepR cells was observed in bone marrow after an injury (Zhou et al., 2014).”
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Background
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“LepR-positive cells, including BMSCs, OBs, and adipose progenitor cells (75, 78 – 82) expressing LepR-positive BMSCs in the adult bone marrow is an important source of growth factors (83, 84); however, only a few markers that can be used to distinguish and compare their functions have been identi ﬁ…”
Background
Rekrutierung osteogener Zellen an den Ort der Knochenbildung während Entwicklung und Frakturheilung
Böhm, A.-M., Dirckx, N., & Maes, C. (2016) · Zeitschrift für Rheumatologie · doi:10.1007/s00393-016-0065-7 · Cited by 6
One Niche to Rule Both Maintenance and Loss of Stemness in HSCs
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“It is important to note that the decrease in the number of HSCs in the absence of CXCL12 in IL-7+ BM stromal cells is less profound than that in mice without CXCL12 in mesenchymal LEPR+ cells.”
BackgroundInfluential
The bone marrow microenvironment—driver of leukemia evolution?
García, M., & Chen, C. (2017) · Stem Cell Investigation · doi:10.21037/sci.2017.02.03 · Cited by 6
“Even within the mesenchymal stromal population there are primitive, intermediate and mature progenitor cells that maintain the microenvironment and provide support for HSPCs and various definitions of the different populations (9-11).”
Background
Abnormal bone marrow microenvironment: the “harbor” of acute lymphoblastic leukemia cells
Chen, Z., Zheng, Y., Yang, Y., Kang, J., You, M. J., & Tian, C. (2021) · Blood Science · doi:10.1097/bs9.0000000000000071 · Cited by 6
“Ang/Tie signaling pathway exerts a vital and rate-limiting role in tumor vascularization.(61) Tie-1 and Tie-2 tyrosine kinase receptors are”
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Periosteum Derived Cells in Skeletal Tissue Regeneration
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Constructing Injectable Bone-Forming Units by Loading a Subtype of Osteoprogenitors on Decellularized Bone Matrix Powders for Bone Regeneration
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“Several groups have further identified the MSCs by flow cytometry analysis using specific surface markers together with evaluating in vitro osteogenic, chondrogenic, and adipogenic differentiations (Méndez-Ferrer et al., 2010; Zhou et al., 2014).”
Background
Unraveling bone marrow architecture
Lucas, D., Salomonis, N., & Grimes, H. L. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0447-6 · Cited by 6
Signaling in Osteoblast Differentiation
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Heterogeneity of murine periosteum progenitors involved in fracture healingPreprint
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Depletion of marrow adipo-CAR cells in mice enhances bone formation by activating bone morphogenetic protein receptor (BMPR) in pre-osteoblasts
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Icaritin Improves the Hematopoiesis-Supportive Function of MSCs via A PRDX1–MAPK Axis After Chemotherapy
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“While intesti - nal microbiota metabolites likely help maintain HSCs, their effects on bone marrow niche cells are less understood [ 103, 105].”
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Local problems need global solutions: The metabolic needs of regenerating organisms
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Mdm2/p53 levels in bone marrow mesenchymal stromal cells are essential for maintaining the hematopoietic niche in response to DNA damage
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“The high level of apoptosis in MSCs observed in our study may contribute to the impaired bone formation in their trabecular bone compartment, which is known to be derived from MSCs [36].”
Background
The acquisition order of leukemic drug resistance mutations is directed by the selective fitness associated with each resistance mechanism
Leow, B. C. S., Kok, C. H., Yeung, D. T. O., Hughes, T. P., White, D. L., & Eadie, L. N. (2023) · Scientific Reports · doi:10.1038/s41598-023-40279-2 · Cited by 5
Nitric oxide-dependent immunosuppressive function of thymus-derived mesenchymal stromal/stem cells
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“MSCs are highly heterogeneous, and some subpopulations can be identified by the expression of Nestin [3], Leptin receptor (LEPR) [11], Neuron-glia antigen2 (NG2) [12], and Pairing the associated homeobox protein 1 (PRX1) [13], among others.”
Background
Comparative transcriptome analysis of bone marrow resident versus culture-expanded mouse mesenchymal stem/stromal cells
Haga, C. L., Booker, C. N., Strivelli, J., Boregowda, S. V., & Phinney, D. G. (2024) · Cytotherapy · doi:10.1016/j.jcyt.2024.01.008 · Cited by 5
Relationship between adipocytes and hematological tumors in the bone marrow microenvironment: a literature review
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“LepR + MSCs contribute to bone and adipocyte formation in adult bone marrow, and in addition, proliferation of LepR + cells was observed in bone marrow after injury (24).”
Single cell RNA sequencing shows that cells expressing Sox9 postnatally populate most skeletal lineages in mouse bone
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The Hematopoietic Microenvironment in Myeloproliferative Neoplasms: The Interplay Between Nature (Stem Cells) and Nurture (the Niche)
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CD271 + CD51 + PALLADIN − Human Mesenchymal Stromal Cells Possess Enhanced Ossicle-Forming Potential
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“…cells (hBMSCs) negatively gated for CD45, CD235a, and CD31 revealed co-expression of several MSC markers, VCAM1 (CD106) [16], ALCAM (CD166) [17], THY1 (CD90) [18], LEPR [19], and NG2 [20], especially in the Lin - CD271 + CD51 + subset compared to CD271 + CD51 - or double-negative cells (Fig.”
Niches of Hematopoietic Stem Cells in Bone Marrow
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Differential Blood Counts Do Not Consistently Predict Clinical Measurements of Bone Mineral Density and Microarchitecture at Homeostasis
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“As osteoblasts and adipocytes can be derived from the same adult marrow stromal cell (MSC) populations, namely skeletal stem cells, in vitro and in vivo,((26,27)) it has been proposed that osteoporosis could also be viewed as an imbalanced differentiation of skeletal progenitor cells toward adipocytes,((28)) a hypothe…”
Background
Imputation of Human Primary Osteoblast Single Cell RNA-Seq Data Identified Three Novel Osteoblastic Subtypes
Zhang, H.-X., Cao, C., Li, X., Chen, Y., Zhang, Y., Liu, Y., Gong, Y. Y., Qiu, X., Zhou, C. L., Chen, Y., et al. (2022) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2710295 · Cited by 5
“…3 (OB3, 16.85%), not only expressing MSC specific markers (e.g., leptin receptor ( LEPR ), vascular cell adhesion molecule 1 ( VCAM1 ) [22,43,44] but also distinctively expressing high levels of CD99 and amyloid beta precursor protein ( APP ); (4) Osteoblast 4 (OB4, 7.22%), significantly…”
BackgroundInfluential
Identification of small molecules as novel anti-adipogenic compounds based on Connectivity Map
Zhang, S., Lyons, N., Koedam, M., van de Peppel, J., van Leeuwen, J. P. T. M., & van der Eerden, B. C. J. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1017832 · Cited by 5
“Lineage tracing and single cell RNA-seq experiments demonstrated adipogenesisprimed MSCs expressed high levels of leptin receptor (LEPR) and C-X-C motif chemokine ligand 12 (CXCL12), while these markers decreased in osteogenesis-primed MSC (8, 9).”
Background
Endothelial-to-osteoblast transition in normal mouse bone development
Lin, S.-C., Yu, G., Lee, Y., Song, J. H., Song, X., Zhang, J., Panaretakis, T., Logothetis, C. J., Komatsu, Y., Yu‐Lee, L., et al. (2023) · iScience · doi:10.1016/j.isci.2023.105994 · Cited by 5
Skeletal stem/progenitor cells provide the niche for extramedullary hematopoiesis in spleen
O'Neill, H. C., & Lim, H. K. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1148414 · Cited by 6
“, 2018), or as bone marrow subsets of skeletal progenitors (Zhou et al., 2014; Baccin et al., 2020; Tournaire et al., 2020; Matsushita et al., 2021; Shen et al., 2021), and also within the pericyte and adventitial cell populations that surround blood vessels in vascularised tissues (Sacchetti et al.”
BackgroundInfluential
Basement membrane extract potentiates the endochondral ossification phenotype of bone marrow-derived mesenchymal stem cell-based cartilage organoids
Notoh, H., Yamasaki, S., Suzuki, N., Suzuki, A., Okamoto, S., Kanematsu, T., Suzuki, N., Katsumi, A., Kojima, T., Matsushita, T., et al. (2023) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.149583 · Cited by 5
A Senescence-Associated Secretory Phenotype of Bone Marrow Mesenchymal Stem Cells Inhibits the Viability of Breast Cancer Cells
Li, M., Liu, J.-X., Ma, B., Liu, J., Chen, J., Jin, F., Hu, C., Xu, H., Zheng, C., & Hou, R. (2024) · Stem Cell Reviews and Reports · doi:10.1007/s12015-024-10710-w · Cited by 5
“However, the BMMSCs from SAMP6 mice demonstrated a lower expression level of SCA1 (81.6% in SAMP6 vs. 92.7% in SAMR1), which is a marker for stemness [36].”
Influential
Pharmacological inhibition of HIF2 protects against bone loss in an experimental model of estrogen deficiency
Lanzolla, G., Sabini, E., Beigel, K., Khan, M. P., Liu, X. S., Wang, D., Laslow, B., Taylor, D. M., Bellido, T., Giaccia, A. J., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2416004121 · Cited by 5
“Interestingly, LepR - positive cells are found near sinusoids ( 20 , 22 , 23 ), suggesting their behavior may be intimately tied to the hypoxic bone marrow niche.”
Influential
Skeletal stem cells for bone development, homeostasis and repair: one or many?
Mortensen, L. J., & Hill, W. (2015) · BoneKEy Reports · doi:10.1038/bonekey.2015.139 · Cited by 5
“3-green fluorescent protein osteoblastic cells, Aggrecanþ cartilage cells orPerilipinþ bone marrowfat cells.(3) Although fatemapping cells derived from these LepRþ cells using Lepr-cre reporter mice showed very limited numbers of osteoblasts/osteocytes that originated from them at 2 months, the numbers markedly increa…”
Influential
Developmental Biology of Musculoskeletal Tissues for Tissue Engineers
Ono, N., & Kronenberg, H. M. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811467-4.00001-2 · Cited by 6
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New Insights on the Role of the Mesenchymal–Hematopoietic Stem Cell Axis in Autologous and Allogeneic Hematopoiesis
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Mesenchymal Stromal Cells as a Cellular Target in Myeloid Malignancy: Chances and Challenges in the Genome Editing of Stromal Alterations
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Loss of Parathyroid Hormone Receptor Signaling in Osteoprogenitors Is Associated With Accumulation of Multiple Hematopoietic Lineages in the Bone Marrow
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“LepR expression has been reported in murine perivascular stromal cells at 3 to 4 months of age.((34)) We therefore examined PTH1R-LepRKO and control mice at 3 months of age and found no differences in body weight, BM cellularity, spleen weight, or spleen cellularity (Fig.”
Influential
Harnessing the Biology of Stem Cells' Niche
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DEL‐1 is an Endogenous Senolytic Protein that Inhibits Senescence‐Associated Bone Loss
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Complementary and Inducible creERT2 Mouse Models for Functional Evaluation of Endothelial Cell Subtypes in the Bone Marrow
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Authors: Zhou, B. O., Yue, R., Murphy, M. M., Peyer, J. G., & Morrison, S. J.
Affiliations: The University of Texas Southwestern Medical Center (US)
Howard Hughes Medical Institute (US)
Corresponding author: Morrison, Sean J.
ORCID: Zhou, Bo O.
Yue, Rui
Murphy, Malea M.
Peyer, James G.
Morrison, Sean J.
Venue: Cell Stem Cell
Publisher: Elsevier BV
Published: 2014-08
Volume: 15
Issue: 2
Pages: 154-168
ISSN: 1875-9777 (ISSN-L)
1934-5909
DOI: 10.1016/j.stem.2014.06.008
PMC: PMC4127103
OpenAlex: W2078719918
Cited by: 1,381
References: 53
Citations by year: 2026: 84 · 2025: 92 · 2024: 133 · 2023: 153 · 2022: 148 · 2021: 147 · 2020: 153 · 2019: 114 · 2018: 99 · 2017: 87 · 2016: 89 · 2015: 66 · 2014: 12
FWCI: 42.43
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 371 d)
Locations: Cell stem cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
National Heart, Lung, and Blood Institute (HL097760, R01HL097760)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Keywords: mesenchymal stem cells, leptin receptor, bone marrow, bone formation, adipogenesis, chondrogenesis, CFU-F, fate mapping, cell markers, fracture healing, quiescent cells, stem cell proliferation
MeSH terms: Animals, Bone and Bones, Bone Marrow, Bone Marrow Cells, Flow Cytometry, Male, Mice, Inbred C57BL, Osteoblasts, Osteogenesis, Regeneration, Stem Cells, Tamoxifen, Adipocytes, Transgenes, Chondrocytes, Leptin, Cell Proliferation, Green Fluorescent Proteins, Mice, Receptors, Leptin, Mesenchymal Stem Cells

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Leptin-Receptor-Expressing Mesenchymal Stromal Cells Represent the Main Source of Bone Formed by Adult Bone Marrow

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