The DOI matches its Crossref record; 236 of the 236 references it cites were found in a registry or an index.
Mesenchymal Stem Cell: Keystone of the Hematopoietic Stem Cell Niche and a Stepping-Stone for Regenerative Medicine
Open accessAbstract
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“For instance, reprogrammed immune cells can use the immune system to treat cancer and administer vaccinations, while microorganisms can interact with the microbiome to control metabolic processes, chronic inflammatory processes, and mucosal immunity.320–322”
From Smart nanoparticles for cancer therapy (2023) · cites this paper as [322]
In the citing paper
“For instance, reprogrammed immune cells can use the immune system to treat cancer and administer vaccinations, while microorganisms can interact with the microbiome to control metabolic processes, chronic inflammatory processes, and mucosal immunity.320–322”
From Smart nanoparticles for cancer therapy (2023) · cites this paper as [322]
Citations
Cites
1 retracted
RETRACTED ARTICLE: Pluripotency of mesenchymal stem cells derived from adult marrow
Jiang, Y., Jahagirdar, B., Reinhardt, R. L., Schwartz, R. E., Keene, C. D., Ortiz-Gonzalez, X. R., Reyes, M., Lenvik, T. R., Lund, T. C., Blackstad, M., et al. (2002) · Nature · doi:10.1038/nature00870 · Cited by 5,523
RetractedMultilineage potential of adult human mesenchymal stem cells
Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., & Marshak, D. R. (1999) · Science · doi:10.1126/science.284.5411.143 · Cited by 21,052
Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F. C., Krause, D. S., Deans, R. J., Keating, A., Prockop, D. J., & Horwitz, E. M. (2006) · Cytotherapy · doi:10.1080/14653240600855905 · Cited by 17,766
Human Adipose Tissue Is a Source of Multipotent Stem Cells
Zuk, P. A., Zhu, M., Ashjian, P. H., Ugarte, D. A. D., Huang, J. I., Mizuno, H., Alfonso, Z. C., Fraser, J. K., Benhaim, P., & Hedrick, M. H. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-02-0105 · Cited by 6,762
Caplan, A. I. (1991) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100090504 · Cited by 6,559
Marrow Stromal Cells as Stem Cells for Nonhematopoietic Tissues
Prockop, D. J. (1997) · Science · doi:10.1126/science.276.5309.71 · Cited by 4,629
Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo
Gronthos, S., Mankani, M. H., Brahim, J. S., Robey, P. G., & Shi, S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240309797 · Cited by 4,580
Human mesenchymal stem cells modulate allogeneic immune cell responses
Aggarwal, S., & Pittenger, M. F. (2005) · Blood · doi:10.1182/blood-2004-04-1559 · Cited by 4,511
A Direct Measurement of the Radiation Sensitivity of Normal Mouse Bone Marrow Cells1
Till, J. E., & McCulloch, E. A. (2010) · Radiation Research · doi:10.1667/rrxx28.1 · Cited by 4,036
A perivascular origin for mesenchymal stem cells in multiple human organs
Crisan, M., Yap, S., Casteilla, L., Chen, C.-W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.07.003 · Cited by 3,991
Research works printed but not linked: 10
- Friedenstein AJ, 1976, Exp. Hematol., 4, 267
- Friedenstein AJ, 1982, Exp. Hematol., 10, 217
- Dexter TM, 1977, Biomedicine, 27, 344
- Maltman DJ, 2011, Neurochem. Int., 59, 347
- in ‘t Anker PS, 2003, Haematologica, 88, 845
- Owen M, 1988, Ciba Found. Symp., 136, 42
- 10.1016/0008-6363(96)00063-6 · DOI
- Schofield R, 1978, Blood Cells, 4, 7
- Studeny M, 2002, Cancer Res., 62, 3603
- Cyranoski D, 2011, Nature, 477, 377
Cited by
Sorted by citations
Immunogenic Cell Death in Cancer Therapy
Kroemer, G., Galluzzi, L., Kepp, O., & Zitvogel, L. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-100008 · Cited by 3,303
The evolution of commercial drug delivery technologies
Vargason, A. M., Anselmo, A. C., & Mitragotri, S. (2021) · Nature Biomedical Engineering · doi:10.1038/s41551-021-00698-w · Cited by 1,361
Arteriolar niches maintain haematopoietic stem cell quiescence
Kunisaki, Y., Bruns, I., Scheiermann, C., Ahmed, J. U., Pinho, S., Zhang, D., Mizoguchi, T., Wei, Q., Lucas, D., Ito, K., et al. (2013) · Nature · doi:10.1038/nature12612 · Cited by 1,290
“The association and quiescence of both haematopoietic and mesenchymal stem cells at this site may thus endow arterioles with the potential for orchestrating haematopoietic and stromal regeneration 40 .”
Self-citationSmart nanoparticles for cancer therapy
Sun, L., Liu, H., Ye, Y., Lei, Y., Islam, R., Tan, S., Tong, R., Miao, Y.-B., & Cai, L. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01642-x · Cited by 1,073
“322 Additionally, living cells are modi fi able.”
BackgroundHaematopoietic stem cell activity and interactions with the niche
Pinho, S., & Frenette, P. S. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0103-9 · Cited by 1,064
Self-citationGuidelines 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
Hematopoietic stem cell niche maintenance during homeostasis and regeneration
Mendelson, A., & Frenette, P. S. (2014) · Nature Medicine · doi:10.1038/nm.3647 · Cited by 819
Self-citationEvrard, M., Kwok, I., Chong, S. Z., Teng, K. W. W., Becht, É., Chen, J., Sieow, J. L., Penny, H. L., Ching, G. C., Devi, S., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.02.002 · Cited by 742
Denervation suppresses gastric tumorigenesis
Zhao, C., Hayakawa, Y., Kodama, Y., Muthupalani, S., Westphalen, C. B., Andersen, G. T., Flatberg, A., Johannessen, H., Friedman, R. A., Renz, B. W., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009569 · Cited by 687
“Previous studies suggested that nerves contribute to the normal stem cell niche (1, 2, 38), and a recent report has linked sympathetic nerves to prostate cancer progression (7).”
Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion
Bruns, I., Lucas, D., Pinho, S., Ahmed, J. U., Lambert, M. P., Kunisaki, Y., Scheiermann, C., Schiff, L., Poncz, M., Bergman, A., et al. (2014) · Nature Medicine · doi:10.1038/nm.3707 · Cited by 679
Self-citationSchepers, K., Pietras, E. M., Reynaud, D., Flach, J., Binnewies, M., Garg, T., Wagers, A. J., Hsiao, E. C., & Passegué, E. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.06.009 · Cited by 614
“…reside in the bone marrow (BM) cavity, where they interact with different types of stromal cells expressing important regulatory molecules including stem cell factor (SCF), C-X-C motif chemokine 12 (CXCL12, also called SDF1a), and transforming growth factor b (TGF-b) (Frenette et al., 2013).”
BackgroundResultInfluentialMesenchymal Stromal Cell Homing: Mechanisms and Strategies for Improvement
Ullah, M., Liu, D. D., & Thakor, A. S. (2019) · iScience · doi:10.1016/j.isci.2019.05.004 · Cited by 553
“Accordingly, MSCs have been investigated for a wide breadth of clinical applications, such as immune modulation in inflammatory and autoimmune diseases, tissue protection following injury, and regenerative medicine (Frenette et al., 2013).”
BackgroundInfluentialGuidelines for the use of flow cytometry and cell sorting in immunological studies *
Cossarizza, A., Chang, H., Radbruch, A., Akdiş, M., Andrä, I., Annunziato, F., Bächer, P., Barnaba, V., Battistini, L., Bauer, W. M., et al. (2017) · European Journal of Immunology · doi:10.1002/eji.201646632 · Cited by 595
Self-citationSkin tissue engineering: wound healing based on stem-cell-based therapeutic strategies
Dehkordi, A. N., Mirahmadi, F., Chehelgerdi, M., & Dehkordi, S. R. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1212-2 · Cited by 561
Matrix elasticity of void-forming hydrogels controls transplanted-stem-cell-mediated bone formation
Huebsch, N., Lippens, E., Lee, K., Mehta, M., Koshy, S. T., Darnell, M., Desai, R. M., Madl, C. M., Xu, M. M., Zhao, X., et al. (2015) · Nature Materials · doi:10.1038/nmat4407 · Cited by 530
Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531
Mesenchymal Stem Cell-Based Immunomodulation: Properties and Clinical Application
Wang, M., Yuan, Q., & Xie, L. (2018) · Stem Cells International · doi:10.1155/2018/3057624 · Cited by 506
“In fact, a variety of immune disorder diseases, including multiple sclerosis, Crohn’s disease, GVHD, SLEs, and type 1 diabetes, have entered clinical trials for treatment with MSCs [80].”
BackgroundPinho, S., Lacombe, J., Hanoun, M., Mizoguchi, T., Bruns, I., Kunisaki, Y., & Frenette, P. S. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20122252 · Cited by 504
“Nevertheless, these markers are not homogeneously expressed across cultures, varying with isolation protocols and passage and therefore not necessarily representative of MSCs in vivo (Bianco et al., 2013; Frenette et al., 2013).”
BackgroundSelf-citationMizoguchi, T., Pinho, S., Ahmed, J. U., Kunisaki, Y., Hanoun, M., Mendelson, A., Ono, N., Kronenberg, H. M., & Frenette, P. S. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.03.013 · Cited by 451
“The bone marrow (BM) environment is composed of multiple cell types, most of which are thought to be derived from mesenchymal stem and progenitor cells (MSPCs) (Bianco et al., 2013; Caplan, 1991; Frenette et al., 2013).”
BackgroundSelf-citationMesenchymal stem cells in fibrotic disease
El Agha, E., Kramann, R., Schneider, R. K., Li, X., Seeger, W., Humphreys, B. D., & Bellusci, S. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.07.011 · Cited by 430
“Although there is significant functional overlap between MSC populations in terms of multipotency and self-renewal capacities, their distribution in the BM cavity and their association with the endosteum or blood vessels are distinct (Frenette et al., 2013; Morrison and Scadden, 2014).”
BackgroundDifferential cytokine contributions of perivascular haematopoietic stem cell niches
Asada, N., Kunisaki, Y., Pierce, H., Wang, Z., Fernandez, N., Birbrair, A., Ma’ayan, A., & Frenette, P. S. (2017) · Nature Cell Biology · doi:10.1038/ncb3475 · Cited by 453
Self-citationNormal and Leukemic Stem Cell Niches: Insights and Therapeutic Opportunities
Schepers, K., Campbell, T., & Passegue, E. A. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.02.014 · Cited by 431
“However, additional studies have since refuted this observation and showed that mature OBs do not directly affect HSC maintenance in the BM (Frenette et al., 2013).”
InfluentialRecognition of Bacteria by Inflammasomes
von Moltke, J., Ayres, J. S., Kofoed, E. M., Chavarría‐Smith, J., & Vance, R. E. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095944 · Cited by 420
A subset of chondrogenic cells provides early mesenchymal progenitors in growing bones
Ono, N., Ono, W., Nagasawa, T., & Kronenberg, H. M. (2014) · Nature Cell Biology · doi:10.1038/ncb3067 · Cited by 418
Niches for Hematopoietic Stem Cells and Their Progeny
Wei, Q., & Frenette, P. S. (2018) · Immunity · doi:10.1016/j.immuni.2018.03.024 · Cited by 398
“…remains elusive in part due to different processing protocols, such as bone crushing or BM flushing, and difficulty in visualization comparisons (Hu et al., 2016, Pinho et al., 2013, Churchman et al., 2012, Morikawa et al., 2009, Sacchetti et al., 2007, Isern et al., 2013, Frenette et al., 2013).”
Self-citationHanoun, M., Zhang, D., Mizoguchi, T., Pinho, S., Pierce, H., Kunisaki, Y., Lacombe, J., Armstrong, S. A., Dührsen, U., & Frenette, P. S. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.06.020 · Cited by 381
“Recent studies have demonstrated that healthy HSCs reside in specific perivascular bone marrow niches, which tightly regulate their function (reviewed in Frenette et al., 2013).”
BackgroundSelf-citationStemness in Cancer: Stem Cells, Cancer Stem Cells, and Their Microenvironment
Aponte, P. M., & Caicedo, A. (2017) · Stem Cells International · doi:10.1155/2017/5619472 · Cited by 375
“Even thoughmore research is required to understand the stemness properties of MSCs, their role in providing support not only to SCs in normal niches but also to pathologic CSCs is well-documented [122, 136].”
BackgroundPathogenesis of immune thrombocytopenia
Audia, S., Mahévas, M., Samson, M., Godeau, B., & Bonnotte, B. (2017) · Autoimmunity Reviews · doi:10.1016/j.autrev.2017.04.012 · Cited by 395
Orlova, V. V., van den Hil, F. E., Petrus-Reurer, S., Drabsch, Y., ten Dijke, P., & Mummery, C. L. (2014) · Nature Protocols · doi:10.1038/nprot.2014.102 · Cited by 365
Stem Cell Extracellular Vesicles: Extended Messages of Regeneration
Riazifar, M., Pone, E. J., Lötvall, J. O., & Zhao, W. (2016) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-061616-030146 · Cited by 330
“In current practice, MSCs (usually obtained from adult bone marrow, adipose tissue, or neonatal umbilical cord) are among the most widely used types of adult stem cells in animal studies and human clinical trials (121, 122) for reasons that include easy isolation and expansion in culture, their comparatively infrequen…”
BackgroundChemotherapy-induced bone marrow nerve injury impairs hematopoietic regeneration
Lucas, D., Scheiermann, C., Chow, A. T., Kunisaki, Y., Bruns, I., Barrick, C. A., Tessarollo, L., & Frenette, P. S. (2013) · Nature Medicine · doi:10.1038/nm.3155 · Cited by 300
Self-citationInteractions between mesenchymal stem cells and the immune system
Li, N., & Hua, J. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2473-5 · Cited by 338
“[18, 19], with effective outcomes in several cases [41, 181–184].”
BackgroundEnhancing the Migration Ability of Mesenchymal Stromal Cells by Targeting the SDF-1/CXCR4 Axis
Marquez‐Curtis, L. A., & Janowska‐Wieczorek, A. (2013) · BioMed Research International · doi:10.1155/2013/561098 · Cited by 291
“Endogenous MSCs are mobilized and contribute to tissue repair by acting as a reservoir of cells for regeneration [30, 31] and guarding against inflammation [32].”
BackgroundCharacterization of bone marrow-derived mesenchymal stem cells in aging
Baker, N., Boyette, L. B., & Tuan, R. S. (2014) · Bone · doi:10.1016/j.bone.2014.10.014 · Cited by 287
“Furthermore, an age-related decline in BMSCs expressing CD146 has been reported [22] (For further information on novel MSC markers, see reviews by [10,17,18]).”
BackgroundInfluentialNeural Regulation of Hematopoiesis, Inflammation, and Cancer
Hanoun, M., Maryanovich, M., Arnal-Estapé, A., & Frenette, P. S. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.026 · Cited by 265
Self-citationEndothelial Jagged-1 Is Necessary for Homeostatic and Regenerative Hematopoiesis
Poulos, M. G., Guo, P., Kofler, N. M., Pinho, S., Gutkin, M. C., Tikhonova, A. N., Aifantis, I., Frenette, P. S., Kitajewski, J., Rafii, S., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.07.048 · Cited by 249
“, 2005), and PDGFRα+ CD51+ MSCs (Frenette et al., 2013; Pinho et al., 2013) or Leptin Receptor+ (Ding et al.”
BackgroundSelf-citationStem cell-based bone and dental regeneration: a view of microenvironmental modulation
Zheng, C., Chen, J., Liu, S., & Jin, Y. J. (2019) · International Journal of Oral Science · doi:10.1038/s41368-019-0060-3 · Cited by 246
Identification, discrimination and heterogeneity of fibroblasts
Lendahl, U., Muhl, L., & Betsholtz, C. (2022) · Nature Communications · doi:10.1038/s41467-022-30633-9 · Cited by 256
Regenerative Stem Cell Therapy for Neurodegenerative Diseases: An Overview
Sivandzade, F., & Cucullo, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22042153 · Cited by 224
“Scientists are continually trying to find sturdy, safe, and readily available stem cell sources while refining and/or developing new delivery methods to improve the treatment’s efficiency and effectiveness and reduce the side effects [11].”
BackgroundTriana, S., Vonficht, D., Jopp-Saile, L., Raffel, S., Lutz, R., Leonce, D., Antes, M., Hernández-Malmierca, P., Ordoñez-Rueda, D., Ramasz, B., et al. (2021) · Nature Immunology · doi:10.1038/s41590-021-01059-0 · Cited by 195
“MSCs constitute a rare and heterogeneous group of cells in the bone marrow (Al-Sabah et al., 2020; Frenette et al., 2013).”
BackgroundLuo, Y., Chen, G., Hannemann, N., Ipseiz, N., Krönke, G., Bäuerle, T., Munos, L., Wirtz, S. J., Schett, G. A., & Bözec, A. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.08.020 · Cited by 201
“Communication between the mesenchymal tissue and the hematopoietic system primarily occurs in the bone marrow (BM), where bone forms a niche based on mesenchymal cells for the developing blood and immune cells (Frenette et al., 2013).”
BackgroundVignais, M., Caicedo, A., Brondello, J., & Jørgensen, C. (2017) · Stem Cells International · doi:10.1155/2017/6917941 · Cited by 196
Hematopoiesis and Cardiovascular Disease
Poller, W. C., Nahrendorf, M., & Świrski, F. K. (2020) · Circulation Research · doi:10.1161/circresaha.120.315895 · Cited by 191
Kartogenin-Incorporated Thermogel Supports Stem Cells for Significant Cartilage Regeneration
Li, X., Ding, J., Zhang, Z., Yang, M., Yu, J., Wang, J., Chang, F., & Chen, X. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5b12212 · Cited by 183
Chiossone, L., Conte, R., Spaggiari, G. M., Serra, M., Romei, C., Bellora, F., Becchetti, F., Andaloro, A., Moretta, L., & Bottino, C. (2016) · Stem Cells · doi:10.1002/stem.2369 · Cited by 181
Roles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle
Uezumi, A., Ikemoto‐Uezumi, M., & Tsuchida, K. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00068 · Cited by 171
“Their differentiation might be undesired in most cases because adipogenic differentiation has a negative impact on hematopoiesis in bone marrow (Naveiras et al., 2009).”
BackgroundBone metastasis and the metastatic niche
Ren, G., Esposito, M., & Kang, Y. (2015) · Journal of Molecular Medicine · doi:10.1007/s00109-015-1329-4 · Cited by 167
“Accumulating evidence has shown that there is an intricately-organized microenvironment inside the bone that regulates the dynamic balance among various stem cells, progenitor cells, mature immune cells, and supporting stromal cells; this has been named the bone niche [12, 16].”
Functional inhibition of mesenchymal stromal cells in acute myeloid leukemia
Geyh, S., Rodríguez‐Paredes, M., Jäger, P. S., Khandanpour, C., Cadeddu, R.-P., Gutekunst, J., Wilk, C. M., Fenk, R. R., Zilkens, C., Hermsen, D. F., et al. (2015) · Leukemia · doi:10.1038/leu.2015.325 · Cited by 157
Focus on Extracellular Vesicles: Development of Extracellular Vesicle-Based Therapeutic Systems
Ohno, S., Drummen, G. P. C., & Kuroda, M. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17020172 · Cited by 152
“Mesenchymal stem cells (MSCs) are self-renewing precursor cells (multipotent stem cells) that are able to differentiate into a variety of cell types, including bone, cartilage, muscle, marrow, ligament, adipose and connective tissues [26,27].”
BackgroundSkrahin, A., Ahmed, R. K. S., Ferrara, G., Rane, L., Poiret, T., Isaikina, Y., Skrahina, A. M., Zumla, A. I., & Maeurer, M. J. (2014) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(13)70234-0 · Cited by 143
Liu, J., Zhang, H., Zhang, Y., Li, N., Wen, Y., Cao, F., Ai, H., & Xue, X. (2014) · Molecules and Cells · doi:10.14348/molcells.2014.0145 · Cited by 139
“Cells 871 Frenette et al., 2013).”
Haider, K. H., & Aramini, B. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1548-7 · Cited by 139
“tors and cytokines to regulate their activity [13, 14].”
BackgroundMetabolism and the Control of Cell Fate Decisions and Stem Cell Renewal
Ito, K., & Ito, K. (2016) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111315-125134 · Cited by 143
“…2009, Suda et al. 2011), and cell-intrinsic networks integrate and cooperate with cumulative signals from the microenvironment to fine-tune their self-renewal capacity and maintain whole-tissue balance (Frenette et al. 2013, Morrison & Scadden 2014, Scadden 2006, Watt & Hogan 2000, Zon 2008).”
Conforti, A., Scarsella, M., Starc, N., Giorda, E., Biagini, S., Proia, A., Carsetti, R., Locatelli, F., & Bernardo, M. E. (2014) · Stem Cells and Development · doi:10.1089/scd.2014.0091 · Cited by 134
“…in vitro data, MSCs have been tested in phase I/II clinical trials aimed at treating steroid-resistant acute graft-versus-host disease (aGvHD) and favoring hematopoietic engraftment/recovery after hematopoietic stem cell transplantation [12–14], and in strategies of Regenerative Medicine [15,16].”
Jiang, B., Yan, L., Wang, X., Li, E., Murphy, K. A., Vaccaro, K., Li, Y., & Xu, R. (2018) · Stem Cells · doi:10.1002/stem.2964 · Cited by 125
Neural regulation of bone and bone marrow
Maryanovich, M., Takeishi, S., & Frenette, P. S. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a031344 · Cited by 114
“Bones not only play a variety of mechanical roles, but also have synthetic aspects, one of which is production of blood cells from hematopoietic stem cells (HSCs) in the bone marrow (BM) (Frenette et al. 2013; Mendelson and Frenette 2014).”
BackgroundSelf-citationAzadniv, M., Myers, J. R., McMurray, H. R., Guo, N., Rock, P., Coppage, M. L., Ashton, J. M., Becker, M. W., Calvi, L. M., & Liesveld, J. L. (2019) · Leukemia · doi:10.1038/s41375-019-0568-8 · Cited by 117
Neuronal Activity in Ontogeny and Oncology
Venkatesh, H. S., & Monje, M. (2017) · Trends in cancer · doi:10.1016/j.trecan.2016.12.008 · Cited by 109
“Perivascular mesenchymal stem and progenitor cells (MSPCs) are also a key component of the BM niche and maintain the HSC population through expression of growth and retention factors including CXCL12, SCF, and ANGPT1 [135,136].”
BackgroundThe impact of tumor stroma on drug response in breast cancer
Dittmer, J., & Leyh, B. (2014) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2014.05.006 · Cited by 107
Hox genes in the adult skeleton: Novel functions beyond embryonic development
Rux, D. R., & Wellik, D. M. (2016) · Developmental Dynamics · doi:10.1002/dvdy.24482 · Cited by 105
“In addition, they have important roles in maintenance of the hematopoietic stem cell niche (Calvi et al., 2003; Zhang et al., 2003; Adams et al., 2007; Mendez-Ferrer et al., 2010; Frenette et al., 2013; Kunisaki et al., 2013).”
BackgroundModulation of TNF-Induced Macrophage Polarization by Synovial Fibroblasts
Donlin, L. T., Jayatilleke, A., Γιαννοπούλου, Ε., Kalliolias, G. D., & Ivashkiv, L. B. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400486 · Cited by 108
“Mesenchymal stromal cell–derived immunomodulatory factors are commonly secreted in response to inflammatory stimuli (1, 2).”
BackgroundMesenchymal Stromal Cells and Toll-Like Receptor Priming: A Critical Review
Najar, M., Krayem, M., Meuleman, N., Bron, D., & Lagneaux, L. (2017) · Immune Network · doi:10.4110/in.2017.17.2.89 · Cited by 104
“MSCs actively participate in the regulation of HSC survival, quiescence and, upon specific triggers, differentiation into mature cells (11) suggesting their role in the enhancement of hematopoietic engraftment during use in HSC transplantation (12).”
BackgroundRoles of microRNA-34a targeting SIRT1 in mesenchymal stem cells
Zhang, F., Cui, J., Liu, X., Lv, B., Liu, X., Xie, Z., & Yu, B. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0187-x · Cited by 99
“Since MSCs are easily obtained and exhibit impressive paracrine ability as well as multilineage differentiation potential [33], autologous MSCs offer a great advantage when transplanted into ischemic or infarcted heart to regenerate and repopulate the injured myocardium and restore heart function.”
BackgroundCellular players of hematopoietic stem cell mobilization in the bone marrow niche
Tay, J., Lévesque, J.-P., & Winkler, I. G. (2016) · International Journal of Hematology · doi:10.1007/s12185-016-2162-4 · Cited by 107
Advances in pathogenic mechanisms and management of radiation-induced fibrosis
Wang, B., Wei, J., Meng, L., Wang, H., Qu, C., Chen, X., Xin, Y., & Jiang, X. M. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.109560 · Cited by 100
Characterization of Nestin, a Selective Marker for Bone Marrow Derived Mesenchymal Stem Cells
Xie, L., Zeng, X. Y., Hu, J., & Chen, Q. (2015) · Stem Cells International · doi:10.1155/2015/762098 · Cited by 97
“Moreover, they are essential for HSC maintenance and mobilization via forming a structurally unique niche [47, 83, 116].”
BackgroundCorradi, G., Baldazzi, C., Očadlíková, D., Marconi, G., Parisi, S., Testoni, N., Finelli, C., Cavo, M., Curti, A., & Ciciarello, M. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1013-z · Cited by 102
Klinker, M. W. (2015) · World Journal of Stem Cells · doi:10.4252/wjsc.v7.i3.556 · Cited by 98
Kwack, K., & Lee, H.-W. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.857066 · Cited by 86
“Bone marrow-derived MSCs have been extensively studied for bone regeneration because they strongly regulate bone homeostasis by regulating osteoblast differentiation and osteoclast activity (Frenette et al., 2013; Liu et al., 2014; Fernandes and Yang, 2016; Guo et al., 2018).”
BackgroundHematopoietic stem cell fate through metabolic control
Ito, K., & Ito, K. (2018) · Experimental Hematology · doi:10.1016/j.exphem.2018.05.005 · Cited by 98
Mesenchymal stromal cells (MSCs) for neurodegenerative disease: A promising frontier
Shariati, A., Nemati, R., Sadeghipour, Y., Yaghoubi, Y., Baghbani, R., Javidi-Aghdam, K., Zamani, M., & Hassanzadeh, A. (2020) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2020.151097 · Cited by 95
Dezutter‐Dambuyant, C., Durand, I., Alberti, L., Bendriss‐Vermare, N., Valladeau‐Guilemond, J., Duc, A., Magron, A., Morel, A., Sisirak, V., Rodriguez, C., et al. (2015) · OncoImmunology · doi:10.1080/2162402x.2015.1091146 · Cited by 96
Biological feedback control-Respect the loops
El-Samad, H. (2021) · Cell Systems · doi:10.1016/j.cels.2021.05.004 · Cited by 90
Regionally Restricted Hox Function in Adult Bone Marrow Multipotent Mesenchymal Stem/Stromal Cells
Rux, D. R., Song, J. Y., Swinehart, I. T., Pineault, K. M., Schlientz, A. J., Trulik, K. G., Goldstein, S. A., Kozloff, K. M., Lucas, D., & Wellik, D. M. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.11.008 · Cited by 90
“If regional BM-MSC populations possess unique functional characteristics imparted by differential Hox expression, there are critical implications for use of mesenchymal progenitor cells obtained from bone marrow in regenerative therapies (Bianco et al., 2013; Frenette et al., 2013).”
BackgroundSelf-citationDownregulation of CXCL12 in mesenchymal stromal cells by TGFβ promotes breast cancer metastasis
Yu, P. F., Huang, Y., Xu, C. L., Lin, L. Y., Han, Y. Y., Sun, W. H., Hu, G. H., Rabson, A. B., Wang, Y., & Shi, Y. F. (2017) · Oncogene · doi:10.1038/onc.2016.252 · Cited by 88
Rogler, L. E., Kosmyna, B., Moskowitz, D. M., Bebawee, R. S., Rahimzadeh, J., Kutchko, K. M., Laederach, A., Notarangelo, L. D., Giliani, S. C., Bouhassira, E. E., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt427 · Cited by 88
Self-citationMesenchymal stem cell aging: Mechanisms and influences on skeletal and non-skeletal tissues
Liu, H., Xia, X., & Li, B. (2015) · Experimental Biology and Medicine · doi:10.1177/1535370215591828 · Cited by 91
“Mobilization, self-renewal, and multi-lineage differentiations of HSCs are orchestrated by their niches: the endosteal niche and the vascular niche, both of which involve MSCs or their progenies.(17,18) The endosteal niche is mainly composed of stromal cells, osteoprogenitors, and osteoblasts.”
BackgroundTherapeutic Mesenchymal Stromal Cells for Immunotherapy and for Gene and Drug Delivery
Almeida-Porada, G. D., Atala, A., & Porada, C. D. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.01.005 · Cited by 92
Parolini, O., Souza‐Moreira, L., O’Valle, F., Magatti, M., Hernández‐Cortés, P., González‐Rey, E., & Delgado, M. (2013) · Arthritis & Rheumatology · doi:10.1002/art.38206 · Cited by 87
Inflammatory bone marrow microenvironment
Leimkühler, N. B., & Schneider, R. K. (2019) · Hematology · doi:10.1182/hematology.2019000045 · Cited by 82
Mesenchymal stromal cells; a new horizon in regenerative medicine
Tavakoli, S., Jafarbeigloo, H. R. G., Shariati, A., Jahangiryan, A., Jadidi, F., Kouhbanani, M. A. J., Hassanzadeh, A., Zamani, M., Javidi-Aghdam, K., & Naimi, A. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29803 · Cited by 87
Zhang, F., Lu, Y., Wang, M., Zhu, J., Li, J., Zhang, P., Yuan, Y., & Zhu, F. (2020) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2020.101513 · Cited by 84
The role of ultrasound in enhancing mesenchymal stromal cell-based therapies
Liu, D. D., Ullah, M., Concepcion, W., Dahl, J., & Thakor, A. S. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0391 · Cited by 84
Leukemic Stem Cells: From Leukemic Niche Biology to Treatment Opportunities
Marchand, T., & Pinho, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.775128 · Cited by 94
“characterized by their ability to self-renew and differentiate into osteoblasts, chrondrocytes and adipocytes (63).”
BackgroundSelf-citationParacrine effects of stem cells in wound healing and cancer progression
Dittmer, J., & Leyh, B. (2014) · International Journal of Oncology · doi:10.3892/ijo.2014.2385 · Cited by 82
“One example is the haematopoietic stem cells which are positioned next to endothelial cells when residing in the endothelial niche in the bone marrow and whose expansion is dependent on endothelial cells (30).”
BackgroundGATA Transcription Factors: Basic Principles and Related Human Disorders
Fujiwara, T. (2017) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.242.83 · Cited by 80
“BM-MSCs are self-renewing precursor cells that differentiate into bone, fat, cartilage, and stromal cells of the bone marrow, thereby forming a microenvironment that maintains HSCs (Frenette et al. 2013).”
Metabolism as master of hematopoietic stem cell fate
Ito, K., Bonora, M., & Ito, K. (2018) · International Journal of Hematology · doi:10.1007/s12185-018-2534-z · Cited by 85
Zhu, H., Yang, F., Tang, B., Li, X., Chu, Y., Liu, Y., Wang, S.-G., Wu, D., & Zhang, Y. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.03.005 · Cited by 80
Feng, Y., Zhu, M., Dangelmajer, S., Lee, Y. M., Wijesekera, O., Castellanos, C. X., Denduluri, A. J., Chaichana, K. L., Li, Q., Zhang, H., et al. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.521 · Cited by 80
Cell circuits and niches controlling B cell development
Zehentmeier, S., & Pereira, J. P. (2019) · Immunological Reviews · doi:10.1111/imr.12749 · Cited by 83
Boehme, K. A., Schleicher, S., Traub, F., & Rolauffs, B. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19010311 · Cited by 77
“Indeed, MSPC express a mixture of markers which undergo dynamic changes according to growth factor and cytokine availability during development and disease or artificial plastic adherence in cell culture [26,27].”
BackgroundYang, W. C., Zhu, P., Huang, H., Zheng, Y., Liu, J., Feng, L., Guo, H., Tang, S., & Guo, R. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b12288 · Cited by 77
Choi, J. R., Yong, K. W., & Zaman, W. S. W. K. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2484-2 · Cited by 78
Pramanik, S., Sulistio, Y. A., & Heese, K. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0214-7 · Cited by 77
Bone marrow niches in the regulation of bone metastasis
Chen, F., Han, Y., & Kang, Y. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01329-6 · Cited by 77
Cheng, L., Yao, B., Hu, T. H., Cui, X., Shu, X., Tang, S., Wang, R., Wang, Y., Liu, Y., Song, W., et al. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.06.017 · Cited by 73
Mesenchymal stem cells in idiopathic pulmonary fibrosis
Li, X., Yue, S., & Luo, Z. (2017) · Oncotarget · doi:10.18632/oncotarget.18126 · Cited by 72
“Endogenous MSCs from BM can be mobilized and have the capability to proceed from the circulatory system to various, experimental, and damaged tissues, where they can promote to tissue repair and regeneration by secreting various paracrine factors and directly differentiating into different cells [54-57].”
Backgroundp53 Loss Increases the Osteogenic Differentiation of Bone Marrow Stromal Cells
He, Y., de Castro, L. F., Shin, M. H., Dubois, W., Yang, H. H., Jiang, S., Mishra, P. J., Ren, L., Gou, H., Lal, A., et al. (2014) · Stem Cells · doi:10.1002/stem.1925 · Cited by 72
Goloviznina, N. A., Verghese, S. C., Yoon, Y. M., Taratula, O., Marks, D. L., & Kurre, P. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.745653 · Cited by 72
“natally, the bone marrow and MSCs within provide critical stimuli for HSPC maintenance (5, 28).”
BackgroundSharma, P. M., Kumar, A., Dey, A. D., Behl, T., & Chadha, S. (2021) · Life Sciences · doi:10.1016/j.lfs.2020.118932 · Cited by 70
Metadata
- Authors
- Frenette, P. S., Pinho, S., Lucas, D., & Scheiermann, C.
- Affiliations
- Albert Einstein College of Medicine (US)
- 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
- 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
- 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
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 ›
Are you an author, or do you see a problem with this page? Request a review