Skeletal stem cells
Open accessAbstract
Skeletal stem cells (SSCs) reside in the postnatal bone marrow and give rise to cartilage, bone, hematopoiesis-supportive stroma and marrow adipocytes in defined in vivo assays. These lineages emerge in a specific sequence during embryonic development and post natal growth, and together comprise a continuous anatomical system, the bone-bone marrow organ. SSCs conjoin skeletal and hematopoietic physiology, and are a tool for understanding and ameliorating skeletal and hematopoietic disorders. Here and in the accompanying poster, we concisely discuss the biology of SSCs in the context of the development and postnatal physiology of skeletal lineages, to which their use in medicine must remain anchored.
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Bone marrow stroma contains self-renewing, multipotent progenitors that can give rise to osteoblasts, ensuring a reservoir of bone-forming cells for bone growth, modeling and remodeling.
“The bone marrow stroma contains self-renewing, multipotent progenitors that can give rise to osteoblasts, thus ensuring a reservoir of bone-forming cells for bone growth, modeling and remodeling.273”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [273]
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Muraglia, A., Corsi, A., Riminucci, M., Mastrogiacomo, M., Cancedda, R., Bianco, P., & Quarto, R. (2003) · Journal of Cell Science · doi:10.1242/jcs.00527 · Cited by 146 · see citing works
Self-citationPolarized expression of bone morphogenetic protein-4 in the human aorta-gonad-mesonephros region
Marshall, C. J., Kinnon, C., & Thrasher, A. J. (2000) · Blood · doi:10.1182/blood.v96.4.1591.h8001591_1591_1593 · Cited by 139 · see citing works
Mahmood, A., Harkness, L., Schrøder, H. D., Abdallah, B., & Kassem, M. (2010) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.34 · Cited by 138 · see citing works
MT1-MMP–dependent, apoptotic remodeling of unmineralized cartilage
Holmbeck, K., Bianco, P., Chrysovergis, K., Yamada, S. S., & Birkedal‐Hansen, H. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200307061 · Cited by 134 · see citing works
Self-citationUno, nessuno e centomila: Searching for the Identity of Mesodermal Progenitors
Bianco, P., & Cossu, G. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4592 · Cited by 132 · see citing works
Self-citationWalsh, S., Jefferiss, C. M., Stewart, K., Jordan, G. R., Screen, J., & Beresford, J. N. (2000) · Bone · doi:10.1016/s8756-3282(00)00319-7 · Cited by 131 · see citing works
Multipotential Cells in the Bone Marrow Stroma: Regulation in the Context of Organ Physiology
Bianco, P., Riminucci, M., Kuznetsov, S. A., & Robey, P. G. (1999) · Critical Reviews in Eukaryotic Gene Expression · doi:10.1615/critreveukargeneexpr.v9.i2.30 · Cited by 127 · see citing works
Self-citationNew factors controlling the balance between osteoblastogenesis and adipogenesis
Abdallah, B. M., & Kassem, M. S. (2011) · Bone · doi:10.1016/j.bone.2011.06.030 · Cited by 124 · see citing works
Asymmetric Cell Kinetics Genes: The Key to Expansion of Adult Stem Cells in Culture
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Joyner, C. J., Bennett, A., & Triffitt, J. T. (1997) · Bone · doi:10.1016/s8756-3282(97)00074-4 · Cited by 117 · see citing works
Cell Sources for Bone Regeneration: The Good, the Bad, and the Ugly (But Promising)
Robey, P. G. (2011) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2011.0199 · Cited by 114 · see citing works
Self-citationGentili, C., Bianco, P., Neri, M., et al. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.122.3.703 · Cited by 114 · see citing works
Self-citationBianco, P., Riminucci, M., BONUCCI, E., Termine, J. D., & Robey, P. G. (1993) · Journal of Histochemistry & Cytochemistry · doi:10.1177/41.2.8419458 · Cited by 113 · see citing works
Self-citationAlkaline phosphatase positive precursors of adipocytes in the human bone marrow
Bianco, P., Costantini, M., Dearden, L. C., et al. (1988) · British Journal of Haematology · doi:10.1111/j.1365-2141.1988.tb04225.x · Cited by 112 · see citing works
Self-citationThe interplay of osteogenesis and hematopoiesis
Kuznetsov, S. A., Riminucci, M., Ziran, N. M., Tsutsui, T. W., Corsi, A., Calvi, L. M., Kronenberg, H. M., Schipani, E., Robey, P. G., & Bianco, P. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200408079 · Cited by 112 · see citing works
Self-citationPath to the Clinic: Assessment of iPSC-Based Cell Therapies In Vivo in a Nonhuman Primate Model
Hong, S. G., Winkler, T., Wu, C., Guo, V., Pittaluga, S., Nicolae, A., Donahue, R. E., Metzger, M. E., Price, S. D., Uchida, N., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.019 · Cited by 100 · see citing works
Self-citationGuanine nucleotide biosynthesis is regulated by the cellular p53 concentration.
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Regulation of Mesenchymal Stem Cell Differentiation
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Serafini, M., Sacchetti, B., Pievani, A., Redaelli, D., Remoli, C., Biondi, A., Riminucci, M., & Bianco, P. (2014) · Stem Cell Research · doi:10.1016/j.scr.2014.01.006 · Cited by 92 · see citing works
Self-citationPhillips, M., Kuznetsov, S. A., Cherman, N., Park, K., Chen, K. G., McClendon, B. N., Hamilton, R. S., McKay, R. D. G., Chenoweth, J. G., Mallon, B. S., et al. (2014) · Stem Cells Translational Medicine · doi:10.5966/sctm.2013-0154 · Cited by 92 · see citing works
Self-citationDiseases of Bone and the Stromal Cell Lineage
Bianco, P., & Robey, P. G. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.3.336 · Cited by 81 · see citing works
Self-citationDevelopmental horizons in human embryos; a review of the histogenesis of cartilage and bone.
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Identification of a clonally expanding haematopoietic compartment in bone marrow
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Cellular Senescence: Ex Vivo p53‐Dependent Asymmetric Cell Kinetics
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Bone Marrow Stromal Cell Assays: In Vitro and In Vivo
Robey, P. G., Kuznetsov, S. A., Riminucci, M., & Bianco, P. (2014) · Methods in molecular biology · doi:10.1007/978-1-62703-989-5_21 · Cited by 73 · see citing works
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Calcium deficiency induces expression of cartilage-like phenotype in chick embryonic calvaria
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Vis-à-Vis Cells and the Priming of Bone Formation
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The bone marrow stroma in vivo: ontogeny, structure, cellular composition and changes in disease
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Self-citationTransient Chondrogenic Phase in the Intramembranous Pathway During Normal Skeletal Development
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Ontogenic emergence of definitive hematopoietic stem cells
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Humoral Nature of Osteogenic Activity of Transitional Epithelium
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Confocal images of marrow stromal (Westen-Bainton) cells
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An animal model of fibrous dysplasia
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Sacchetti, B., Funari, A., Michienzi, S., Di Cesare, S., Piersanti, S., Saggio, I., Tagliafico, E., Ferrari, S., Robey, P. G., Riminucci, M., et al. (2007) · Cell · doi:10.1016/j.cell.2007.08.025 · Cited by 2,226 · see citing works
Self-citationAdult haematopoietic stem cell niches
Crane, G. M., Jeffery, E., & Morrison, S. J. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.53 · Cited by 712 · see citing works
Bone remodeling: an operational process ensuring survival and bone mechanical competence
Bolamperti, S., Villa, I., & Rubinacci, A. (2022) · Bone Research · doi:10.1038/s41413-022-00219-8 · Cited by 482 · see citing works
Sacchetti, B., Funari, A., Remoli, C., Giannicola, G., Kogler, G., Liedtke, S., Cossu, G., Serafini, M., Sampaolesi, M., Tagliafico, E., et al. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.05.011 · Cited by 428 · see citing works
Self-citationAged skeletal stem cells generate an inflammatory degenerative niche
Ambrosi, T. H., Marecic, O., McArdle, A., Sinha, R., Gulati, G. S., Tong, X., Wang, Y., Steininger, H. M., Hoover, M. Y., Koepke, L. S., et al. (2021) · Nature · doi:10.1038/s41586-021-03795-7 · Cited by 392 · see citing works
Glutamine Metabolism Regulates Proliferation and Lineage Allocation in Skeletal Stem Cells
Yu, Y., Newman, H., Shen, L., Sharma, D., Hu, G., Mirando, A. J., Zhang, H., Knudsen, E., Zhang, G.-F., Hilton, M. J., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.01.016 · Cited by 253 · see citing works
“Skeletal stem cells (SSC), also termed bone marrow mesenchymal stromal cells (BMSC) are critical regulators of postnatal bone homeostasis by providing a reservoir of osteoblasts throughout life (Bianco and Robey, 2015; Mizoguchi, et al., 2014; Zhou, et al., 2014).”
BackgroundScott, R. W., Arostegui, M., Schweitzer, R., Rossi, F. M. V., & Underhill, T. M. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.11.004 · Cited by 214 · see citing works
Dmitrieva, R. I., Minullina, I. R., Bilibina, A. A., Tarasova, O. V., Anisimov, S. V., & Zaritskey, A. Y. (2012) · Cell Cycle · doi:10.4161/cc.11.2.18858 · Cited by 195 · see citing works
Multipotent stromal cells: One name, multiple identities
Soliman, H., Theret, M., Scott, W., Hill, L., Underhill, T. M., Hinz, B., & Rossi, F. M. V. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.09.001 · Cited by 147 · see citing works
- Authors
- Bianco, P., & Robey, P. G.
- Affiliations
- Sapienza University of Rome (IT)
- National Institutes of Health (US)
- ORCID
- Robey, Pamela G.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2015-03-15
- Volume
- 142
- Issue
- 6
- Pages
- 1023-1027
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC4360182
- OpenAlex
- W2116104054
- Cited by
- 402
- References
- 142
- Citations by year
- 2026: 24 · 2025: 26 · 2024: 28 · 2023: 37 · 2022: 37 · 2021: 35 · 2020: 45 · 2019: 34 · 2018: 34 · 2017: 29 · 2016: 32 · 2015: 6 · 2014: 2 · 2013: 5 · 2012: 1
- FWCI
- 4.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Genetics › 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
- skeletal stem cells, bone marrow, hematopoietic stroma, skeletal development, chondrogenesis, hematopoiesis, postnatal growth, bone disease, hematopoietic disorders
- MeSH terms
- Bone and Bones, Cartilage, Humans, Terminology as Topic, Adipocytes, Cell Lineage, Multipotent Stem Cells, Stem Cell Niche, Mesenchymal Stem Cells
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.
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