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Leptin-Receptor-Expressing Mesenchymal Stromal Cells Represent the Main Source of Bone Formed by Adult Bone Marrow
Open accessAbstract
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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“Type H vessels respond to the administration of intermittent anabolic PTH (iPTH), which promotes the detachment of leptin receptor-expressing (LepR+) cells, which are pericytes that can differentiate into osteoprogenitors,134 from CD31hi/Edmhi vessels.”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [134]
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InfluentialMesenchymal Stem Cells: Revisiting History, Concepts, and Assays
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InfluentialPten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells
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InfluentialSelf-citationPDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice
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InfluentialIn vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics
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InfluentialSelf-citationSelective deletion of leptin receptor in neurons leads to obesity
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InfluentialAge-dependent fate and lineage restriction of single NG2 cells
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InfluentialEndochondral ossification is required for haematopoietic stem-cell niche formation
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InfluentialVirus-Assisted Mapping of Neural Inputs to a Feeding Center in the Hypothalamus
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Self-citationCis -acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS
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mTOR Complex 1 Plays Critical Roles in Hematopoiesis and Pten-Loss-Evoked Leukemogenesis
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InfluentialSelf-citationMagee, J. A., Ikenoue, T., Nakada, D., Lee, J., Guan, K., & Morrison, S. J. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.05.026 · Cited by 188 · cited 9×
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InfluentialSelf-citationBalordi, F., & Fishell, G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1040-07.2007 · Cited by 185 · cited 7×
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InfluentialAdvancing cartilage tissue engineering: the application of stem cell technology
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Murfee, W. L., Skalak, T. C., & Peirce, S. M. (2005) · Microcirculation · doi:10.1080/10739680590904955 · Cited by 140 · cited 2×
“Smooth muscle cells (Murfee et al., 2005), peripheral nerve Schwann cells (Schneider et al.”
Origins and Properties of Dental, Thymic, and Bone Marrow Mesenchymal Cells and Their Stem Cells
Komada, Y., Yamane, T., Kadota, D., Isono, K., Takakura, N., Hayashi, S., & Yamazaki, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046436 · Cited by 83 · cited 3×
“These data suggested that LepR+ bonemarrow stromal cells might be highly enriched for MSCs. Consistent with this possibility, we found that LepR+CD45 Ter119 CD31 bone marrow stromal cells were uniformly positive for the MSC markers CD51 (Pinho et al., 2013) and PDGFRb (Komada et al., 2012) (Figure 1N).”
Schneider, S., Bosse, F., D’Urso, D., Müller, H.-W., Sereda, M. W., Nave, K., Niehaus, A., Kempf, T., Schnölzer, M., & Trotter, J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-03-00920.2001 · Cited by 75 · cited 2×
“Smooth muscle cells (Murfee et al., 2005), peripheral nerve Schwann cells (Schneider et al., 2001), cartilaginous cells, and osteoblasts (Fukushi et al., 2003) have all been previously re- ported to express NG2.”
Chou, D. B., Sworder, B. J., Bouladoux, N. J., Roy, C. N., Uchida, A. M., Grigg, M. E., Robey, P. G., & Belkaid, Y. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.1011527 · Cited by 71 · cited 2×
“, 2007) or CD146 with platelet-derived growth factor receptor b (PDGFRb), CD106, NG2, or some combination thereof (Chou et al., 2012; Crisan et al., 2008; Schwab and Gargett, 2007).”
Expression of NG2 proteoglycan during endochondral and intramembranous ossification
Fukushi, J., Inatani, M., Yamaguchi, Y., & Stallcup, W. B. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10359 · Cited by 45 · cited 2×
“, 2001), cartilaginous cells, and osteoblasts (Fukushi et al., 2003) have all been previously reported to express NG2.”
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Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications
Wang, Y., Chen, X., Cao, W., & Shi, Y. (2014) · Nature Immunology · doi:10.1038/ni.3002 · Cited by 1,452
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Ghaben, A. L., & Scherer, P. E. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0093-z · Cited by 1,395
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Shi, Y., Wang, Y., Li, Q., Liu, K., Hou, J., Shao, C., & Wang, Y. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0023-5 · Cited by 1,223
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Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition)
Cossarizza, A., Chang, H., Radbruch, A., Acs, A., Adam, D., Adam‐Klages, S., Agace, W. W., Aghaeepour, N., Akdiş, M., Allez, M., et al. (2019) · European Journal of Immunology · doi:10.1002/eji.201970107 · Cited by 1,007
Metadata
- 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.
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 15
- Issue
- 2
- Pages
- 154-168
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- 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
- 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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