Cited by 462Mesenchymal stem cell researchHematopoietic Stem Cell TransplantationPeriodontal Regeneration and Treatments

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Mesenchymal Stem Cell: Keystone of the Hematopoietic Stem Cell Niche and a Stepping-Stone for Regenerative Medicine

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Frenette, Paul S., Pinho, Sandra, Lucas, Daniel, Scheiermann, Christoph·2013·Annual Review of Immunology

DOI 10.1146/annurev-immunol-032712-095919

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Abstract

Mesenchymal stem cells (MSCs) are self-renewing precursor cells that can differentiate into bone, fat, cartilage, and stromal cells of the bone marrow. Recent studies suggest that MSCs themselves are critical for forming a niche that maintains hematopoietic stem cells (HSCs). The ease by which human MSC-like and stromal progenitor cells can be isolated from the bone marrow and other tissues has led to the rapid development of clinical investigations exploring their anti-inflammatory properties, tissue preservation capabilities, and regenerative potential. However, the identity of genuine MSCs and their specific contributions to these various beneficial effects have remained enigmatic. In this article, we examine the definition of MSCs and discuss the importance of rigorously characterizing their stem cell activity. We review their role and that of other putative niche constituents in the regulation of bone marrow HSCs. Additionally, how MSCs and their stromal progeny alter immune function is discussed, as well as potential therapeutic implications.

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“Evidence has manifested that the function of MSCs from AML patients has changed [8, 9].”
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Fostering mesenchymal stem cell therapy to halt cytokine storm in COVID-19
Jeyaraman, M., John, A. A., Koshy, S. K. G., Ranjan, R., Anudeep, T. C., Jain, R., Swati, K., Jha, N. K., Sharma, A., Kesari, K. K., et al. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.166014 · Cited by 37
Useful properties of undifferentiated mesenchymal stromal cells and adipose tissue as the source in liver-regenerative therapy studied in an animal model of severe acute fulminant hepatitis
Manzini, B. M., Duarte, A. S. S., Sankaramanivel, S., Ramos, A. L., Latuf-Filho, P., Escanhoela, C. A. F., Kharmandayan, P., Saad, S. T. O., Boin, I. D. F. S. F., & Luzo, Â. C. M. (2015) · Cytotherapy · doi:10.1016/j.jcyt.2015.04.010 · Cited by 36
Stromal cells in tissue homeostasis: balancing regeneration and fibrosis
Rabelink, T. J., & Little, M. H. (2013) · Nature Reviews Nephrology · doi:10.1038/nrneph.2013.152 · Cited by 36
Delayed post-treatment with bone marrow-derived mesenchymal stem cells is neurorestorative of striatal medium-spiny projection neurons and improves motor function after neonatal rat hypoxia–ischemia
Cameron, S. H., Alwakeel, A. J., Goddard, L., Hobbs, C. E., Gowing, E. K., Barnett, E. R., Kohe, S. E., Sizemore, R. J., & Oorschot, D. E. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.03.019 · Cited by 36
Hematopoietic niches, erythropoiesis and anemia of chronic infection
Gomes, A. C., & Gomes, M. S. (2015) · Experimental Hematology · doi:10.1016/j.exphem.2015.11.007 · Cited by 38
Stem cell transplantation in neurological diseases: improving effectiveness in animal models
Adami, R., Scesa, G., & Bottai, D. (2014) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2014.00017 · Cited by 38
Arthritic Microenvironment‐Dictated Fate Decisions for Stem Cells in Cartilage Repair
He, S., Deng, H., Li, P., Hu, J., Yang, Y., Xu, Z., Liu, S., Guo, W., & Guo, Q. (2023) · Advanced Science · doi:10.1002/advs.202207715 · Cited by 36
Wharton’s Jelly-Derived Mesenchymal Stromal Cells as a Promising Cellular Therapeutic Strategy for the Management of Graft-versus-Host Disease
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“As reviewed [124], nestin-positive cells have been shown as prospective markers for native MSC in mouse.”
Background
Nicorandil protects mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis
Zhang, F., Cui, J., Lv, B., & Yu, B. (2015) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2015.2229 · Cited by 35
“Since MSCs are easily obtained and exhibit impressive paracrine ability, multilineage differentiation potential (27) and the capacity to activate endogenous cardiac progenitor cells (CPCs) (28), they represent one of the most ideal seed cell candidates for tissue regeneration in several clinical…”
GATA2 regulates differentiation of bone marrow-derived mesenchymal stem cells
Kamata, M., Okitsu, Y., Fujiwara, T., Kanehira, M., Nakajima, S., Takahashi, T., Inoue, A., Fukuhara, N., Onishi, Y., Ishizawa, K., et al. (2014) · Haematologica · doi:10.3324/haematol.2014.105692 · Cited by 37
“Efforts to identify the regulatory mechanisms that control the differentiation of BM-MSC into adipocytes/osteoblasts may lead to the development of new clinical applications in the fields of regenerative medicine and tissue engineering and enhance our understanding of hematopoiesis, since BM-MSC are the primary source…”
Influential
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“Besides their marker profiles, these subsets differ also in parts with regard to their location within the BM cavity and their functional properties [1, 2, 4, 6].”
Background
Active Implant Combining Human Stem Cell Microtissues and Growth Factors for Bone-Regenerative Nanomedicine
Schiavi, J., Keller, L., Morand, D.-N., de Isla, N., Huck, O., Lutz, J. C., Mainard, D., Schwinté, P., & Benkirane-Jessel, N. (2015) · Nanomedicine · doi:10.2217/nnm.14.228 · Cited by 35
Tracing PRX1+ cells during molar formation and periodontal ligament reconstruction
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“Thus, the function of PRX1 cells in tissue regeneration and repair could be related to angiogenesis.(20) The development of molars significantly differs from incisors in mouse(21) and is more similar to that of humans.”
Background
Enhanced alleviation of aGVHD by TGF‐β1‐modified mesenchymal stem cells in mice through shifting MΦ into M2 phenotype and promoting the differentiation of Treg cells
Wu, R., Liu, C., Deng, X., Chen, L., Hao, S., & Ma, L. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14862 · Cited by 33
Chemical-defined medium supporting the expansion of human mesenchymal stem cells
Xu, J., Lian, W., Chen, J., Li, W., Li, L., & Huang, Z. W. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01641-7 · Cited by 33
Engineering human mini-bones for the standardized modeling of healthy hematopoiesis, leukemia, and solid tumor metastasis
Grigoryan, A., Zacharaki, D., Balhuizen, A., Côme, C., Garcia, A. G., Gil, D. H., Frank, A.-K., Aaltonen, K. E., Mañas, A., Esfandyari, J., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abm6391 · Cited by 37
Stretching human mesenchymal stromal cells on stiffness-customized collagen type I generates a smooth muscle marker profile without growth factor addition
Rothdiener, M., Hegemann, M., Uynuk‐Ool, T., Walters, B., Papugy, P., Nguyen, P. K., Claus, V., Seeger, T., Stoeckle, U., Boehme, K. A., et al. (2016) · Scientific Reports · doi:10.1038/srep35840 · Cited by 32
Co-Inflammatory Roles of TGFβ1 in the Presence of TNFα Drive a Pro-inflammatory Fate in Mesenchymal Stem Cells
Lerrer, S., Liubomirski, Y., Bott, A., Abnaof, K., Oren, N., Yousaf, A., Körner, C., Meshel, T., Wiemann, S., & Ben‐Baruch, A. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00479 · Cited by 33
“Among the signals regulating the migration patterns taken by MSCs and their functional diversification are cytokines, which typically are regarded as key regulators of acquired immunity or inflammation (4, 5).”
BackgroundMethodInfluential
Mesenchymal Stem Cells in Immune-Mediated Bone Marrow Failure Syndromes
Kastrinaki, M.-C., Pavlaki, K. I., Batsali, A. K., Kouvidi, E., Mavroudi, I., Pontikoglou, C. G., & Papadaki, H. Α. (2013) · Clinical and Developmental Immunology · doi:10.1155/2013/265608 · Cited by 33
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BackgroundInfluential
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Bone Marrow Endosteal Mesenchymal Progenitors Depend on HIF Factors for Maintenance and Regulation of Hematopoiesis
Guarnerio, J., Coltella, N., Ala, U., Tonon, G., Pandolfi, P. P., & Bernardi, R. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.04.002 · Cited by 30
“Hematopoiesis is a tightly regulated process orchestrated by cell-autonomous and non-cell-autonomous signals emanating from a variety of cell types within specialized bone marrow (BM) microenvironments (Wang and Wagers, 2011; Frenette et al., 2013).”
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Sympathetic neural-immune interactions regulate hematopoiesis, thermoregulation and inflammation in mammals
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Sensory nerves in the spotlight of the stem cell niche
Picoli, C. C., Costa, A. C., Rocha, B. G. S., da Silva, W. N., Santos, G. S. P., Prazeres, P. H. D. M., Costa, P. A. C., Oropeza, A., da Silva, R. A., Azevedo, V., et al. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.20-0284 · Cited by 30
TGF-Beta Induced Key Genes of Osteogenic and Adipogenic Differentiation in Human Mesenchymal Stem Cells and MiRNA–mRNA Regulatory Networks
Du, G., Cheng, X., Zhang, Z., Han, L., Wu, K., Li, Y., & Lin, X. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.759596 · Cited by 31
Perspectives on the Use of Stem Cells for Autism Treatment
Siniscalco, D., Bradstreet, J. J., Sych, N., & Antonucci, N. (2013) · Stem Cells International · doi:10.1155/2013/262438 · Cited by 30
A Genetic Platform to Model Sarcomagenesis from Primary Adult Mesenchymal Stem Cells
Guarnerio, J., Riccardi, L., Taulli, R., Maeda, T., Wang, G., Hobbs, R. M., Song, M. S., Sportoletti, P., Bernardi, R., Bronson, R. T., et al. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-14-1022 · Cited by 30
“osteosarcoma) have been successfully modeled in genetically engineered mice (9-12), current protocols to model undifferentiated sarcomas are generally based on transplantation of human tumor cell lines in immune compromised mice (13), in vitro expanded, and spontaneously transformed heterogeneous mouse primary mesench…”
Effects of bone marrow or mesenchymal stem cell transplantation on oral mucositis (mouse) induced by fractionated irradiation
Schmidt, M., Haagen, J., Noack, R., Siegemund, A., Gabriel, P., & Dörr, W. (2014) · Strahlentherapie und Onkologie · doi:10.1007/s00066-013-0510-3 · Cited by 30
[Erratum] Tanshinone�IIA and Astragaloside�IV promote the angiogenesis of mesenchymal stem cell‑derived endothelial cell‑like cells via upregulation of Cx37, Cx40 and Cx43
Li, Z., Zhang, S., Cao, L., Li, W., Ye, Y., Shi, Z., Wang, Z., Sun, L., Wang, J., Jia, L., et al. (2018) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2018.6428 · Cited by 30
Concise Review: Conceptualizing Paralogous Stem-Cell Niches and Unfolding Bone Marrow Progenitor Cell Identities
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Regulation of hematopoiesis by activators and inhibitors of Wnt signaling from the niche
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Trends in Bone Metastasis Modeling
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“The MSCs are multipotent cells that are able to differentiate into the mesenchymal lineage cells, which include osteoblasts, adipocytes, chondrocytes, fibroblasts, and other stromal cells [19,20].”
Background
Allogeneic Bone Marrow-Derived Mesenchymal Stromal Cells Expanded In Vitro for Treatment of Aplastic Anemia: A Multicenter Phase II Trial
Pang, Y., Xiao, H., Zhang, H., Liu, Z., Li, L., Gao, Y., Li, H., Jiang, Z., Tan, H., Lin, J., et al. (2017) · Stem Cells Translational Medicine · doi:10.1002/sctm.16-0227 · Cited by 28
Disease Progression in Myelodysplastic Syndromes: Do Mesenchymal Cells Pave the Way?
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“…cells could contribute to disease pathogenesis in MDS within the framework of our current knowledge of their biology (Morrison and Scadden, 2014, Frenette et al., 2013) and the ‘‘enabling’’ processes underlying neoplastic initiation and progression in other systems (Hanahan and Weinberg, 2011).”
Background
A non-cell-autonomous role for Pml in the maintenance of leukemia from the niche
Guarnerio, J., Mendez, L., Asada, N., Menon, A. V., Fung, J., Berry, K., Frenette, P. S., Ito, K., & Pandolfi, P. P. (2017) · Nature Communications · doi:10.1038/s41467-017-02427-x · Cited by 27
Self-citation
The Role of Growth Hormone in Mesenchymal Stem Cell Commitment
Bolamperti, S., GUIDOBONO, F., Rubinacci, A., & Villa, I. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20215264 · Cited by 27
Kidney inflammaging is promoted by CCR2+ macrophages and tissue-derived micro-environmental factors
Lefèvre, L., Iacovoni, J. S., Martini, H., Bellière, J., Maggiorani, D., Dutaur, M., Marsal, D. J., Decaunes, P., Pizzinat, N., Mialet‐Perez, J., et al. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03719-0 · Cited by 27
“Study of other surface markers related to the mesenchymal lineage such as the integrin ß1 (CD29) and the integrin Vα (CD51) [17] by young and aged kMSCs showed no modification with aging (Supp Fig.”
Background
Thymic Mesenchymal Cells Have a Distinct Transcriptomic Profile
Patenaude, J., & Perreault, C. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502499 · Cited by 26
“Hence, it provides a systems-level appraisal of commonalities and discrepancies between MCs from different organs without being tainted by changes induced by in vitro culture (6).”
Background
Bone marrow mesenchymal stromal cell (MSC) gene profiling in chronic myeloid leukemia (CML) patients at diagnosis and in deep molecular response induced by tyrosine kinase inhibitors (TKIs)
Aggoune, D., Sorel, N., Bonnet, M., Goujon, J., Tarte, K., Hérault, O., Domenech, J., Réa, D., Legros, L., Johnson‐Ansah, H., et al. (2017) · Leukemia Research · doi:10.1016/j.leukres.2017.07.007 · Cited by 26
“MSCs are critical self-renewing cells that can differentiate into osteogenic, adipogenic, chondrogenic, and stromal cells of the bone marrow niche [23].”
Background
The impact of gut microbial signals on hematopoietic stem cells and the bone marrow microenvironment
Liu, X., Zhang, H., Shi, G., Zheng, X., Chang, J., Lin, Q., Tian, Z., & Yang, H. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1338178 · Cited by 30
“MSCs are distributed around blood vessels and contribute to the formation of the hematopoietic niche (24).”
Background
Mouse Genetic Analysis of Bone Marrow Stem Cell Niches: Technological Pitfalls, Challenges, and Translational Considerations
Chen, K. G., Johnson, K. R., & Robey, P. G. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.09.014 · Cited by 25
“Mouse genetic models have dramatically advanced our understanding of many fundamental developmental processes in both the skeletal and hematological systems, thereby accelerating the processes of translational medicine (Bianco et al., 2013; Frenette et al., 2013; Morrison and Scadden, 2014).”
Background
NK cell development in a human stem cell niche: KIR expression occurs independently of the presence of HLA class I ligands
Zhao, X., Weinhold, S., Brands, J., Hejazi, M., Degistirici, Ö., Kögler, G., Meisel, R., & Uhrberg, M. (2018) · Blood Advances · doi:10.1182/bloodadvances.2018019059 · Cited by 25
“Mesenchymal stem cells (MSCs) are multipotent mesenchymal stromal cells that are able to differentiate into a variety of mesodermal cell types, such as osteoblasts, chondrocytes, and adipocytes.(11) After birth, MSCs primarily reside in the bone marrow (BM) but are also found at extramedullary sites, such as CB, fat,…”
Background

Authors: Frenette, P. S., Pinho, S., Lucas, D., & Scheiermann, C.
Affiliations: Albert Einstein College of Medicine (US)
ORCID: Frenette, Paul S.
Pinho, Sandra
Lucas, Daniel
Scheiermann, Christoph
Venue: Annual Review of Immunology
Publisher: Annual Reviews
Published: 2013-03-21
Volume: 31
Issue: 1
Pages: 285-316
ISSN: 0732-0582 (ISSN-L)
1545-3278
DOI: 10.1146/annurev-immunol-032712-095919
OpenAlex: W2138953281
Cited by: 462
References: 235
Citations by year: 2026: 8 · 2025: 14 · 2024: 27 · 2023: 27 · 2022: 23 · 2021: 39 · 2020: 35 · 2019: 34 · 2018: 41 · 2017: 42 · 2016: 38 · 2015: 51 · 2014: 54 · 2013: 27
FWCI: 7.76
Type: journal article
Language: en
Open access: green
archive-ouverte.unige.ch
Licence: cc-by
Locations: Annual Review of Immunology (publishedVersion)
PubMed (publishedVersion)
Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
Funders: National Heart, Lung, and Blood Institute (R01HL116340, R01HL097700, R01HL069438, R01HL097819)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK056638)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Health Sciences › Dentistry › Periodontics › Periodontal Regeneration and Treatments
Keywords: mesenchymal stem cells, hematopoietic stem cells, bone marrow microenvironment, stromal progenitor cells, immune function, anti-inflammatory activity, regenerative medicine, stem cell therapy
MeSH terms: Animals, Bone Marrow Cells, Humans, Inflammation, Stem Cells, Stromal Cells, Hematopoietic Stem Cell Transplantation, Regenerative Medicine, Mesenchymal Stem Cell Transplantation

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Mesenchymal Stem Cell: Keystone of the Hematopoietic Stem Cell Niche and a Stepping-Stone for Regenerative Medicine

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