Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications

Ghannam, Soufiane; Bouffi, Carine; Djouad, Farida; Jorgensen, Christian; Noël, Danièle

doi:10.1186/scrt2

Cited by 507Mesenchymal stem cell researchHematopoietic Stem Cell TransplantationPluripotent Stem Cells Research

Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications

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Ghannam, Soufiane, Bouffi, Carine, Djouad, Farida, Jorgensen, Christian, Noël, Danièle·2010·Stem Cell Research & Therapy

DOI 10.1186/scrt2PMC PMC2873698

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Abstract

Mesenchymal stem cells (MSCs) are multipotential nonhematopoietic progenitor cells that are isolated from many adult tissues, in particular from the bone marrow and adipose tissue. Along with their capacity for differentiating into cells of mesodermal lineage, such as adipocytes, osteoblasts and chondrocytes, these cells have also generated great interest for their ability to display immunomodulatory capacities. Indeed, a major breakthrough came with the finding that they are able to induce peripheral tolerance, suggesting they may be used as therapeutic tools in immune-mediated disorders. The present review aims at discussing the current knowledge on the targets and mechanisms of MSC-mediated immunosuppression as well as the potential use of MSCs as modulators of immune responses in a variety of diseases related to alloreactive immunity or autoimmunity.

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A prerequisite for the immunomodulatory function of mesenchymal stromal cells in the tumour microenvironment is their activation by immune cells producing IFN-γ, TNF-a, IL-2a or IL-1b.
“A prerequisite for the immunomodulatory function of MSCs in the tumour microenvironment is their activation by immune cells producing IFN-γ, TNF-a, IL-2a or IL-1b [34], [35], [36].”
From Mesenchymal stromal cells for bone sarcoma treatment: Roadmap to clinical practice (2019) · cites this paper as [36]
The section “Immunosuppressive function of mesenchymal stem cells requires preliminary activation” says immune-cell cytokines activate MSCs before immunosuppression. It lists IFNγ, alone or with TNFα, IL-1α, or IL-1β—not IL-2α—and does not establish this prerequisite specifically in the tumour microenvironment. (LLM, conf=0.88)
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Mesenchymal stem cells might be used to induce tolerance in heart transplantation
Zhou, H., Jin, Z., Liu, J., Yu, S., Cui, Q., & Yi, D. (2007) · Medical Hypotheses · doi:10.1016/j.mehy.2007.08.010 · Cited by 20 · see citing works

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Secretion of immunoregulatory cytokines by mesenchymal stem cells
Kyurkchiev, D. S. (2014) · World Journal of Stem Cells · doi:10.4252/wjsc.v6.i5.552 · Cited by 619 · see citing works
Mesenchymal stem cell exosomes
Lai, R. C., Yeo, R. W. Y., & Lim, S. K. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.03.001 · Cited by 573 · see citing works
MSC exosome as a cell-free MSC therapy for cartilage regeneration: Implications for osteoarthritis treatment
Toh, W. S., Lai, R. C., Hui, J. H. P., & Lim, S. K. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.11.008 · Cited by 506 · see citing works
Immunoregulation by Mesenchymal Stem Cells: Biological Aspects and Clinical Applications
Castro-Manrreza, M. E., & Montesinos, J. J. (2015) · Journal of Immunology Research · doi:10.1155/2015/394917 · Cited by 400 · see citing works
IL-6-Dependent PGE2 Secretion by Mesenchymal Stem Cells Inhibits Local Inflammation in Experimental Arthritis
Bouffi, C., Bony, C., Courties, G., Jørgensen, C., & Noël, D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014247 · Cited by 383 · see citing works
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Chondrogenic Differentiation of Mesenchymal Stem Cells: Challenges and Unfulfilled Expectations
Somoza, R. A., Welter, J. F., Correa, D., & Caplan, A. I. (2014) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2013.0771 · Cited by 360 · see citing works
Umbilical Cord Mesenchymal Stem Cells: The New Gold Standard for Mesenchymal Stem Cell-Based Therapies?
Omar, R. E., Beroud, J., Stoltz, J., Menu, P., Velot, É., & Decot, V. (2014) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2013.0664 · Cited by 335 · see citing works
Diabetes Mellitus: Insights from Epidemiology, Biochemistry, Risk Factors, Diagnosis, Complications and Comprehensive Management
Alam, S., Hasan, M. K., Neaz, S., Hussain, N., Hossain, M. F., & Rahman, T. (2021) · Diabetology · doi:10.3390/diabetology2020004 · Cited by 326 · see citing works
Adipose-Derived Mesenchymal Stem Cell Protects Kidneys against Ischemia-Reperfusion Injury through Suppressing Oxidative Stress and Inflammatory Reaction
Chen, Y.-T., Sun, C., Lin, Y., Chang, L., Chen, Y., Tsai, T., Chung, S., Chua, S. O., Kao, Y. H., Yen, C., et al. (2011) · Journal of Translational Medicine · doi:10.1186/1479-5876-9-51 · Cited by 320 · see citing works
Platelet lysate from whole blood-derived pooled platelet concentrates and apheresis-derived platelet concentrates for the isolation and expansion of human bone marrow mesenchymal stromal cells: production process, content and identification of active components
Fekete, N., Gadelorge, M., Fürst, D. E., Maurer, C., Dausend, J., Fleury‐Cappellesso, S., Mailänder, V., Lotfi, R., Ignatius, A. A., Sensebé, L., et al. (2012) · Cytotherapy · doi:10.3109/14653249.2012.655420 · Cited by 285 · see citing works
Mesenchymal stem cells in regenerative medicine applied to rheumatic diseases: Role of secretome and exosomes
Maumus, M., Jørgensen, C., & Noël, D. (2013) · Biochimie · doi:10.1016/j.biochi.2013.04.017 · Cited by 266 · see citing works
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Mesenchymal stem cells from umbilical cord matrix, adipose tissue and bone marrow exhibit different capability to suppress peripheral blood B, natural killer and T cells
Ribeiro, A., Laranjeira, P., Mendes, S., Velada, I., Leite, C., Andrade, P., dos Santos, F., Henriques, A., Grãos, M., Cardoso, C. M. P., et al. (2013) · Stem Cell Research & Therapy · doi:10.1186/scrt336 · Cited by 266 · see citing works
Immunomodulatory effects of mesenchymal stem cell–derived exosomes on experimental type‐1 autoimmune diabetes
Nojehdehi, S., Soudi, S., Hesampour, A., Rasouli, S., Soleimani, M., & Hashemi, S. M. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.27260 · Cited by 263 · see citing works
Enhancement of therapeutic potential of mesenchymal stem cell-derived extracellular vesicles
Park, K., Bandeira, E., Shelke, G. V., Lässer, C., & Lötvall, J. O. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1398-3 · Cited by 257 · see citing works
SIRT1 regulates differentiation of mesenchymal stem cells by deacetylating β‐catenin
Šimić, P., Zainabadi, K., Bell, E. L., Sykes, D. B., Sáez, B., Lotinun, S., Baron, R., Scadden, D. T., Schipani, E., & Guarente, L. (2013) · EMBO Molecular Medicine · doi:10.1002/emmm.201201606 · Cited by 256 · see citing works
Adipose‐Derived Mesenchymal Stem Cells Exert Antiinflammatory Effects on Chondrocytes and Synoviocytes From Osteoarthritis Patients Through Prostaglandin E2
Manferdini, C., Maumus, M., Gabusi, E., Piacentini, A., Filardo, G., Peyrafitte, J.-A., Jørgensen, C., Bourin, P., Fleury‐Cappellesso, S., Facchini, A., et al. (2013) · Arthritis & Rheumatism · doi:10.1002/art.37908 · Cited by 250 · see citing works
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Anti‐donor immune responses elicited by allogeneic mesenchymal stem cells: what have we learned so far?
Griffin, M. D., Ryan, A. E., Alagesan, S., Lohan, P., Treacy, O., & Ritter, T. (2012) · Immunology and Cell Biology · doi:10.1038/icb.2012.67 · Cited by 250 · see citing works
Mesenchymal Stem Cells: A Friend or Foe in Immune-Mediated Diseases
Gazdic, M., Volarević, V., Arsenijević, N., & Stojković, M. (2015) · Stem Cell Reviews and Reports · doi:10.1007/s12015-014-9583-3 · Cited by 250 · see citing works
Human Pericytes for Ischemic Heart Repair
Chen, C.-W., Okada, M., Proto, J. D., Gao, X., Sekiya, N., Beckman, S., Corselli, M., Crisan, M., Saparov, A., Tobita, K., et al. (2012) · Stem Cells · doi:10.1002/stem.1285 · Cited by 234 · see citing works
New insights into chronic inflammation-induced immunosuppression
Kanterman, J., Sade-Feldman, M., & Baniyash, M. (2012) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2012.02.008 · Cited by 230 · see citing works
Establishing Criteria for Human Mesenchymal Stem Cell Potency
Samsonraj, R. M., Rai, B., Sathiyanathan, P., Puan, K. J., Rötzschke, O., Hui, J. H. P., Raghunath, M., Stanton, L. W., Nurcombe, V., & Cool, S. M. (2015) · Stem Cells · doi:10.1002/stem.1982 · Cited by 221 · see citing works
Secretome of adipose-derived mesenchymal stem cells promotes skeletal muscle regeneration through synergistic action of extracellular vesicle cargo and soluble proteins
Mitchell, R., Mellows, B., Sheard, J., Antonioli, M., Kretz, O., Chambers, D., Zeuner, M.-T., Tomkins, J. E., Denecke, B., Musante, L., et al. (2019) · Stem cell research & therapeutics · doi:10.1186/s13287-019-1213-1 · Cited by 186 · see citing works
Stemming retinal regeneration with pluripotent stem cells
Jin, Z., Gao, M.-L., Deng, W.-L., Wu, K., Sugita, S., Mandai, M., & Takahashi, M. (2018) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.11.003 · Cited by 218 · see citing works
Adipose-derived stem cells secretome and its potential application in “stem cell-free therapy”
Trzyna, A., & Banaś-Ząbczyk, A. (2021) · Biomolecules · doi:10.3390/biom11060878 · Cited by 201 · see citing works
Mesenchymal Stem Cells Use IDO to Regulate Immunity in Tumor Microenvironment
Ling, W., Zhang, J., Yuan, Z., Ren, G., Zhang, L., Chen, X., Rabson, A. B., Roberts, A. I., Wang, Y., & Shi, Y. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-1656 · Cited by 198 · see citing works
Therapeutic Potential of Multipotent Mesenchymal Stromal Cells and Their Extracellular Vesicles
Heldring, N., Mäger, I., Wood, M. J. A., Blanc, K. L., & Andaloussi, S. E. (2015) · Human Gene Therapy · doi:10.1089/hum.2015.072 · Cited by 191 · see citing works
Cell Connections by Tunneling Nanotubes: Effects of Mitochondrial Trafficking on Target Cell Metabolism, Homeostasis, and Response to Therapy
Vignais, M., Caicedo, A., Brondello, J., & Jørgensen, C. (2017) · Stem Cells International · doi:10.1155/2017/6917941 · Cited by 190 · see citing works
Adipose stromal cells mediated switching of the pro-inflammatory profile of M1-like macrophages is facilitated by PGE2: in vitro evaluation.
Manferdini, C., Paolella, F., Gabusi, E., Gambari, L., Piacentini, A., Filardo, G., Fleury-Cappellesso, S., Barbero, A., Murphy, M., & Lisignoli, G. (2017) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2017.01.011 · Cited by 162 · see citing works
Mesenchymal Stromal Cells Induce Peculiar Alternatively Activated Macrophages Capable of Dampening Both Innate and Adaptive Immune Responses
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 · see citing works
A potent immunomodulatory role of exosomes derived from mesenchymal stromal cells in preventing cGVHD
Lai, P., Chen, X., Guo, L., Wang, Y., Liu, X., Liu, Y., Zhou, T., Huang, T., Geng, S., Luo, C., et al. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0680-7 · Cited by 178 · see citing works
Mesenchymal stem cells repress Th17 molecular program through the PD-1 pathway
Luz-Crawford, P., Noël, D., Fernandez, X., Khoury, M., Figueroa, F., Carrión, F., Jorgensen, C., & Djouad, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045272 · Cited by 195 · see citing works
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Immunotherapeutic Potential of Extracellular Vesicles
Zhang, B., Yin, Y., Lai, R. C., & Lim, S. K. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00518 · Cited by 173 · see citing works
Effects of Donor Age, Gender, and In Vitro Cellular Aging on the Phenotypic, Functional, and Molecular Characteristics of Mouse Bone Marrow-Derived Mesenchymal Stem Cells
Katsara, O., Mahaira, L. G., Iliopoulou, E. G., Moustaki, A., Antsaklis, A., Loutradis, D., Stefanidis, K., Baxevanis, C. N., Papamichail, M., & Perez, S. A. (2011) · Stem Cells and Development · doi:10.1089/scd.2010.0280 · Cited by 170 · see citing works
Mesenchymal stem cell-based therapies in regenerative medicine: applications in rheumatology
Maumus, M., Guérit, D., Toupet, K., Jørgensen, C., & Noël, D. (2011) · Stem Cell Research & Therapy · doi:10.1186/scrt55 · Cited by 169 · see citing works
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Graphene nanomaterials as biocompatible and conductive scaffolds for stem cells: impact for tissue engineering and regenerative medicine
Menaa, F., Abdelghani, A., & Menaa, B. (2014) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.1910 · Cited by 163 · see citing works
New Paradigms in Cell Therapy
Wysoczynki, M., Khan, A. R., & Bolli, R. (2018) · Circulation Research · doi:10.1161/circresaha.118.313251 · Cited by 161 · see citing works
Engineering the MSC Secretome: A Hydrogel Focused Approach
Wechsler, M. E., Rao, V. V., Borelli, A. N., & Anseth, K. S. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202001948 · Cited by 160 · see citing works
The bone-marrow niche in MDS and MGUS: implications for AML and MM
Ghobrial, I. M., Detappe, A., Anderson, K. C., & Steensma, D. P. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.197 · Cited by 151 · see citing works
Mesenchymal Stem Cell-Conditioned Medium Reduces Disease Severity and Immune Responses in Inflammatory Arthritis
Kay, A. G., Long, G., Tyler, G., Stefan, A. L., Broadfoot, S. J., Piccinini, A. M., Middleton, J., & Kehoe, O. (2017) · Scientific Reports · doi:10.1038/s41598-017-18144-w · Cited by 152 · see citing works
Five Decades Later, Are Mesenchymal Stem Cells Still Relevant?
Gomez-Salazar, M. A., Gonzalez-Galofre, Z. N., Casamitjana, J., Crisan, M., James, A. W., & Péault, B. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00148 · Cited by 141 · see citing works
Nitric‐Oxide‐Releasing Biomaterial Regulation of the Stem Cell Microenvironment in Regenerative Medicine
Midgley, A. C., Wei, Y., Li, Z., Kong, D., & Zhao, Q. (2019) · Advanced Materials · doi:10.1002/adma.201805818 · Cited by 139 · see citing works
Human adipose mesenchymal stem cells as potent anti-fibrosis therapy for systemic sclerosis
Maria, A. T. J., Toupet, K., Maumus, M., Fonteneau, G., Quellec, A. L., Jørgensen, C., Guilpain, P., & Noël, D. (2016) · Journal of Autoimmunity · doi:10.1016/j.jaut.2016.03.013 · Cited by 138 · see citing works
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Adipose-Derived Mesenchymal Stem Cells in Autoimmune Disorders: State of the Art and Perspectives for Systemic Sclerosis
Maria, A. T. J., Maumus, M., Quellec, A. L., Jørgensen, C., Noël, D., & Guilpain, P. (2016) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-016-8552-9 · Cited by 135 · see citing works
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Regulatory perspective on in vitro potency assays for human mesenchymal stromal cells used in immunotherapy
de Wolf, C., van de Bovenkamp, M., & Hoefnagel, M. H. N. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2017.03.076 · Cited by 135 · see citing works
IL-17A improves the efficacy of mesenchymal stem cells in ischemic-reperfusion renal injury by increasing Treg percentages by the COX-2/PGE2 pathway
Bai, M., Zhang, L., Fu, B., Bai, J., Zhang, Y., Cai, G., Bai, X., Feng, Z., Sun, S., & Chen, X. (2017) · Kidney International · doi:10.1016/j.kint.2017.08.030 · Cited by 134 · see citing works
Beyond T-Cells: Functional Characterization of CTLA-4 Expression in Immune and Non-Immune Cell Types
Oyewole-Said, D., Konduri, V., Vazquez‐Perez, J., Weldon, S. A., Levitt, J. M., & Decker, W. K. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.608024 · Cited by 134 · see citing works
Regenerative Medicine and Tissue Engineering
Luyten, F. P. (2013) · Elsevier eBooks · doi:10.1016/b978-1-4377-1738-9.00007-4 · Cited by 135 · see citing works
Intra-articular Delivery of Purified Mesenchymal Stem Cells from C57BL/6 or MRL/MpJ Superhealer Mice Prevents Posttraumatic Arthritis
Diekman, B. O., Wu, C., Louer, C. R., Furman, B. D., Huebner, J. L., Kraus, V. B., Olson, S. A., & Guilak, F. (2012) · Cell Transplantation · doi:10.3727/096368912x653264 · Cited by 133 · see citing works
Recent Trends in Therapeutic Approaches for Diabetes Management: A Comprehensive Update
Tiwari, P. (2015) · Journal of Diabetes Research · doi:10.1155/2015/340838 · Cited by 132 · see citing works
Topical delivery of mesenchymal stem cells and their function in wounds
Sorrell, J. M., & Caplan, A. I. (2010) · Stem Cell Research & Therapy · doi:10.1186/scrt30 · Cited by 129 · see citing works
Chronic inflammation and sarcopenia: A regenerative cell therapy perspective
Chhetri, J. K., Barreto, P. D. S., Fougère, B., Rolland, Y., Vellas, B. J., & Cesari, M. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2017.12.023 · Cited by 126 · see citing works
Implications of mesenchymal stem cells in regenerative medicine
Kariminekoo, S., Movassaghpour, A. A., Rahimzadeh, A., Talebi, M., Shamsasenjan, K., & Akbarzadeh, A. (2016) · Artificial Cells Nanomedicine and Biotechnology · doi:10.3109/21691401.2015.1129620 · Cited by 125 · see citing works
Molecular Mechanisms Responsible for Anti-inflammatory and Immunosuppressive Effects of Mesenchymal Stem Cell-Derived Factors
Harrell, C. R., Gazdic, M., Fellabaum, C., Volarevic, A., Djonov, V., Arsenijević, A., & Volarević, V. (2018) · Advances in experimental medicine and biology · doi:10.1007/5584_2018_306 · Cited by 127 · see citing works
Mesenchymal stromal cells and regulatory T cells: the Yin and Yang of peripheral tolerance?
Burr, S. P., Dazzi, F., & Garden, O. A. (2012) · Immunology and Cell Biology · doi:10.1038/icb.2012.60 · Cited by 122 · see citing works
Mesenchymal Stem Cell Paracrine Factors in Vascular Repair and Regeneration
Pankajakshan, D., & Agrawal, D. K. (2014) · Journal of Biomedical Technology and Research · doi:10.19104/jbtr.2014.107 · Cited by 120 · see citing works
Mesenchymal Stem Cell Therapy for Cardiac Inflammation: Immunomodulatory Properties and the Influence of Toll-Like Receptors
van den Akker, F., de Jager, S. C. A., & Sluijter, J. P. G. (2013) · Mediators of Inflammation · doi:10.1155/2013/181020 · Cited by 118 · see citing works
Endoglin: Beyond the Endothelium
Schoonderwoerd, M. J. A., Goumans, M., & Hawinkels, L. J. A. C. (2020) · Biomolecules · doi:10.3390/biom10020289 · Cited by 119 · see citing works
Mesenchymal stem cells and their use in therapy: What has been achieved?
Vallone, V. B. F., Romaniuk, M. A., Choi, H., Labovsky, V., Otaegui, J., & Chasseing, N. A. (2013) · Differentiation · doi:10.1016/j.diff.2012.08.004 · Cited by 114 · see citing works
Human Wharton's Jelly-Derived Stem Cells Display a Distinct Immunomodulatory and Proregenerative Transcriptional Signature Compared to Bone Marrow-Derived Stem Cells
Donders, R., Bogie, J. F. J., Ravanidis, S., Gervois, P., Vanheusden, M., Marée, R., Schrynemackers, M., Smeets, H. J. M., Pinxteren, J., Gijbels, K., et al. (2017) · Stem Cells and Development · doi:10.1089/scd.2017.0029 · Cited by 113 · see citing works
Mesenchymal Stem Cells Tune the Development of Monocyte-Derived Dendritic Cells Toward a Myeloid-Derived Suppressive Phenotype through Growth-Regulated Oncogene Chemokines
Chen, H., Chen, H.-Y., Wang, L., Wang, F.-H., Fang, L.-W., Lai, H.-Y., Chen, H.-H., Lu, J., Hung, M., Cheng, Y., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202775 · Cited by 110 · see citing works
Immune characterization of mesenchymal stem cells in human umbilical cord Wharton’s jelly and derived cartilage cells
Liu, S., Yuan, M., Hou, K., Zhang, L., Zheng, X., Zhao, B., Sui, X., Xu, W., Lu, S., & Guo, Q. (2012) · Cellular Immunology · doi:10.1016/j.cellimm.2012.06.010 · Cited by 108 · see citing works
Single-cell RNA-seq highlights heterogeneity in human primary Wharton’s jelly mesenchymal stem/stromal cells cultured in vitro
Sun, C., Wang, L., Wang, H., Huang, T., Yao, W., Li, J., & Zhang, X. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01660-4 · Cited by 108 · see citing works
Stem Cells from Trabecular Meshwork Home to TM Tissue In Vivo
Du, Y., Yun, H., Yang, E., & Schuman, J. S. (2013) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-11056 · Cited by 108 · see citing works
Human Adipose-Derived Stem Cells Impair Natural Killer Cell Function and Exhibit Low Susceptibility to Natural Killer-Mediated Lysis
DelaRosa, O., Sánchez-Correa, B., Morgado, S., Ramírez, C., del Río, B., Menta, R., Lombardo, E., Tarazona, R., & Casado, J. G. (2011) · Stem Cells and Development · doi:10.1089/scd.2011.0139 · Cited by 106 · see citing works
Emerging Potential of Exosomes in Regenerative Medicine for Temporomandibular Joint Osteoarthritis
Lee, Y., Park, H., Auh, Q., Nah, H., Lee, J. S., Moon, H., Heo, D. N., Kim, I. S., & Kwon, I. K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041541 · Cited by 105 · see citing works
Pathogenic or Therapeutic Extracellular Vesicles in Rheumatic Diseases: Role of Mesenchymal Stem Cell-Derived Vesicles
Cosenza, S., Ruiz, M., Maumus, M., Jørgensen, C., & Noël, D. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040889 · Cited by 104 · see citing works
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Galectin-9 Is a Suppressor of T and B Cells and Predicts the Immune Modulatory Potential of Mesenchymal Stromal Cell Preparations
Ungerer, C., Quade-Lyssy, P., Radeke, H. H., Henschler, R., Königs, C., Koehl, U., Seifried, E., & Schüttrumpf, J. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0335 · Cited by 103 · see citing works
Equine Mesenchymal Stem Cells Inhibit T Cell Proliferation Through Different Mechanisms Depending on Tissue Source
Holt, D. D. C., Wood, J. A., Granick, J. L., Walker, N. J., Clark, K. C., & Borjesson, D. L. (2014) · Stem Cells and Development · doi:10.1089/scd.2013.0537 · Cited by 101 · see citing works
Potential implications of mesenchymal stem cells in cancer therapy
Dai, L.-J., Moniri, M. R., Zeng, Z.-R., Zhou, J. X., Rayat, J., & Warnock, G. L. (2011) · Cancer Letters · doi:10.1016/j.canlet.2011.02.012 · Cited by 99 · see citing works
Embryonic and Induced Pluripotent Stem Cells: Understanding, Creating, and Exploiting the Nano-Niche for Regenerative Medicine
Kingham, E., & Oreffo, R. O. C. (2013) · ACS Nano · doi:10.1021/nn3037094 · Cited by 98 · see citing works
Immune regulatory targets of mesenchymal stromal cell exosomes/small extracellular vesicles in tissue regeneration
Toh, W. S., Zhang, B., Lai, R. C., & Lim, S. K. (2018) · Cytotherapy · doi:10.1016/j.jcyt.2018.09.008 · Cited by 98 · see citing works
Biomineralized hydroxyapatite nanoclay composite scaffolds with polycaprolactone for stem cell‐based bone tissue engineering
Ambre, A. H., Katti, D. R., & Katti, K. S. (2014) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.35342 · Cited by 98 · see citing works
Mesenchymal stem cell (MSC)-derived exosomes as novel vehicles for delivery of miRNAs in cancer therapy
Sohrabi, B., Dayeri, B., Zahedi, E., Khoshbakht, S., Pour, N. N., Ranjbar, H., Nejad, A. D., Noureddini, M., & Alani, B. (2022) · Cancer Gene Therapy · doi:10.1038/s41417-022-00427-8 · Cited by 97 · see citing works
Alteration of cellular and immune‐related properties of bone marrow mesenchymal stem cells and macrophages by K562 chronic myeloid leukemia cell derived exosomes
Jafarzadeh, N., Safari, Z., Pornour, M., Amirizadeh, N., Moghadam, M. F., & Sadeghizadeh, M. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27142 · Cited by 95 · see citing works
Mesenchymal stroma cells trigger early attraction of M1 macrophages and endothelial cells into fibrin hydrogels, stimulating long bone healing without long-term engraftment
Seebach, E., Freischmidt, H., Holschbach, J., Fellenberg, J., & Richter, W. (2014) · Acta Biomaterialia · doi:10.1016/j.actbio.2014.07.017 · Cited by 92 · see citing works
Mesenchymal stem cell-based therapy for autoimmune diseases: emerging roles of extracellular vesicles
Rad, F., Ghorbani, M., Roushandeh, A. M., & Roudkenar, M. H. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-04588-y · Cited by 93 · see citing works
Perspectives for Clinical Translation of Adipose Stromal/Stem Cells
Patrikoski, M., Mannerström, B., & Miettinen, S. (2019) · Stem Cells International · doi:10.1155/2019/5858247 · Cited by 93 · see citing works
Mesenchymal Stem Cell-Derived Extracellular Vesicles and Their Therapeutic Potential
Zhao, A. G., Shah, K., Cromer, B. A., & Sümer, H. (2020) · Stem Cells International · doi:10.1155/2020/8825771 · Cited by 95 · see citing works
Human Mesenchymal Stem Cells Overexpressing the IL-33 Antagonist Soluble IL-1 Receptor–Like–1 Attenuate Endotoxin-Induced Acute Lung Injury
Martínez-González, I., Roca, O., Masclans, J. R., Moreno, R., Salcedo, M. T., Baekelandt, V., Cruz, M. J., Rello, J., & Aran, J. M. (2013) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2012-0406oc · Cited by 92 · see citing works
Therapeutic application of mesenchymal stem cells in osteoarthritis
Ruiz, M., Cosenza, S., Maumus, M., Jørgensen, C., & Noël, D. (2015) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2016.1093108 · Cited by 91 · see citing works
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The enhanced performance of bone allografts using osteogenic-differentiated adipose-derived mesenchymal stem cells
Schubert, T., Xhema, D., Vériter, S., Schubert, M., Behets, C., Delloye, C., Gianello, P., & Dufrane, D. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.08.009 · Cited by 90 · see citing works
Human lung epithelial BEAS-2B cells exhibit characteristics of mesenchymal stem cells
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Authors: Ghannam, S., Bouffi, C., Djouad, F., Jorgensen, C., & Noël, D.
Affiliations: Inserm (FR)
Corresponding author: Noël, Danièle
ORCID: Djouad, Farida
Noël, Danièle
Venue: Stem Cell Research & Therapy
Publisher: Springer Science and Business Media LLC
Published: 2010-03
Volume: 1
Issue: 1
Pages: 2-2
ISSN: 1757-6512 (ISSN-L)
DOI: 10.1186/scrt2
PMC: PMC2873698
OpenAlex: W2161905225
Cited by: 507
References: 68
Citations by year: 2026: 4 · 2025: 10 · 2024: 24 · 2023: 24 · 2022: 26 · 2021: 35 · 2020: 36 · 2019: 31 · 2018: 32 · 2017: 33 · 2016: 41 · 2015: 46 · 2014: 46 · 2013: 44 · 2012: 36
FWCI: 16.80
Type: journal article
Language: en
Open access: gold
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Stem Cell Research & Therapy (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Funders: Agence Nationale de la Recherche
Institut National de la Santé et de la Recherche Médicale
Université de Montpellier
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 › Pluripotent Stem Cells Research
Keywords: mesenchymal stem cells, immunosuppression, immunomodulation, peripheral tolerance, autoimmunity, immune-mediated diseases, bone marrow-derived stem cells, adipose-derived stem cells, mesoderm differentiation
MeSH terms: Animals, Autoimmune Diseases, Dendritic Cells, Graft vs Host Disease, Humans, Immunosuppression Therapy, Neutrophils, Transplantation Immunology, CD4-Positive T-Lymphocytes, CD8-Positive T-Lymphocytes, Mesenchymal Stem Cell Transplantation, Mice, Mesenchymal Stem Cells, Peripheral Tolerance

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Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications

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