The immunomodulatory properties of mesenchymal stem cells and their use for immunotherapy
Abstract
There is growing interest in the use of mesenchymal stem cells (MSC) for immune therapy. Clinical trials that use MSC for treatment of therapy resistant graft versus host disease, Crohn's disease and organ transplantation have initiated. Nevertheless, the immunomodulatory effects of MSC are only partly understood. Clinical trials that are supported by basic research will lead to better understanding of the potential of MSC for immunomodulatory applications and to optimization of such therapies. In this manuscript we review some recent literature on the mechanisms of immunomodulation by MSC in vitro and animal models, present new data on the secretion of pro-inflammatory and anti-inflammatory cytokines, chemokines and prostaglandins by MSC under resting and inflammatory conditions and discuss the hopes and expectations of MSC-based immune therapy.
Integrity signals
Registry
Cites
Statistics
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?
Mesenchymal stem cells secrete anti-inflammatory cytokines such as IL-10 and vascular endothelial growth factor (VEGF), and are being explored for their immunomodulatory capabilities.
“Due to their ability to secrete anti-inflammatory cytokines such as IL-10 and vascular endothelial growth factor (VEGF), they are additionally being explored for their immunomodulatory capabilities [76,77].”
From Biomaterial based modulation of macrophage polarization: a review and suggested design principles (2015) · cites this paper as [77]
Cites
Multilineage 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 · see citing works
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 6,669 · see citing works
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 · see citing works
Di Nicola, M., Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D., Matteucci, P., Grisanti, S., & Gianni, A. M. (2002) · Blood · doi:10.1182/blood.v99.10.3838 · Cited by 3,226 · see citing works
Blanc, K. L., Frassoni, F., Ball, L. M., Locatelli, F., Roelofs, H., Lewis, I., Lanino, E., Sundberg, B., Bernardo, M. E., Remberger, M., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60690-x · Cited by 2,692 · see citing works
Bartholomew, A. M., Sturgeon, C., Siatskas, M., Ferrer, K., McIntosh, K. R., Patil, S., Hardy, W., Devine, S. M., Ucker, D. S., Deans, R., et al. (2002) · Experimental Hematology · doi:10.1016/s0301-472x(01)00769-x · Cited by 2,296 · see citing works
Phinney, D. G., & Prockop, D. J. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0637 · Cited by 1,910 · see citing works
Meisel, R., Zibert, A., Laryea, M. D., Göbel, U., Däubener, W., & Dilloo, D. (2004) · Blood · doi:10.1182/blood-2003-11-3909 · Cited by 1,638 · see citing works
Blanc, K. L., Tammik, C., Rosendahl, K., Zetterberg, E., & Ringdén, O. T. H. (2003) · Experimental Hematology · doi:10.1016/s0301-472x(03)00110-3 · Cited by 1,624 · see citing works
Krampera, M., Glennie, S. J., Dyson, J., Scott, D. M., Laylor, R. M., Simpson, E., & Dazzi, F. (2003) · Blood · doi:10.1182/blood-2002-07-2104 · Cited by 1,597 · see citing works
Isolation of multipotent adult stem cells from the dermis of mammalian skin
Toma, J. G., Akhavan, M., Fernandes, K. J. L., Barnabé‐Heider, F., Sadikot, A. F., Kaplan, D. R., & Miller, F. D. (2001) · Nature Cell Biology · doi:10.1038/ncb0901-778 · Cited by 1,593 · see citing works
Role for Interferon-γ in the Immunomodulatory Activity of Human Bone Marrow Mesenchymal Stem Cells
Krampera, M., Cosmi, L., Angeli, R., Pasini, A., Liotta, F., Andreini, A., Santarlasci, V., Mazzinghi, B., Pizzolo, G., Vinante, F., et al. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0008 · Cited by 1,311 · see citing works
Puissant‐Lubrano, B., Barreau, C., Bourin, P., Clavel, C., Corre, J., Bousquet, C., Taureau, C., Cousin, B., Abbal, M., Laharrague, P. F., et al. (2005) · British Journal of Haematology · doi:10.1111/j.1365-2141.2005.05409.x · Cited by 957 · see citing works
Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells
Sato, K., Ozaki, K., Oh, I., Meguro, A., Hatanaka, K., Nagai, T., Muroi, K., & Ozawa, K. (2006) · Blood · doi:10.1182/blood-2006-02-002246 · Cited by 952 · see citing works
García‐Olmo, D., García‐Arranz, M., Herreros, D., Pascual, I., Peiró, C., & Rodríguez‐Montes, J. A. (2005) · Diseases of the Colon & Rectum · doi:10.1007/s10350-005-0052-6 · Cited by 799 · see citing works
Nauta, A. J., Kruisselbrink, A. B., Lurvink, E. G. A., Willemze, R., & Fibbe, W. E. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.4.2080 · Cited by 741 · see citing works
Yañez, R., Lamana, M. L., Garcı́a-Castro, J., Colmenero, I., Ramírez, M. R., & Bueren, J. A. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0228 · Cited by 719 · see citing works
Nauta, A. J., Westerhuis, G., Kruisselbrink, A. B., Lurvink, E. G. A., Willemze, R., & Fibbe, W. E. (2006) · Blood · doi:10.1182/blood-2005-11-011650 · Cited by 694 · see citing works
Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis
González‐Rey, E., Anderson, P. O., González, M. A., Rico, L., Büscher, D., & Delgado, M. (2009) · Gut · doi:10.1136/gut.2008.168534 · Cited by 677 · see citing works
Species Variation in the Mechanisms of Mesenchymal Stem Cell-Mediated Immunosuppression
Ren, G., Su, J., Zhang, L., Zhao, X., Ling, W., L'huillie, A., Zhang, J., Lu, Y., Roberts, A. I., Ji, W., et al. (2009) · Stem Cells · doi:10.1002/stem.118 · Cited by 597 · see citing works
IFN‐γ activation of mesenchymal stem cells for treatment and prevention of graft versus host disease
Polchert, D., Sobinsky, J., Douglas, G., Kidd, M. E., Moadsiri, A., Reina, E., Genrich, K., Mehrotra, S., Setty, S., Smith, B., et al. (2008) · European Journal of Immunology · doi:10.1002/eji.200738129 · Cited by 580 · see citing works
Yao, C., Sakata, D., Esaki, Y., Li, Y., Matsuoka, T., Kuroiwa, K., Sugimoto, Y., & Narumiya, S. (2009) · Nature Medicine · doi:10.1038/nm.1968 · Cited by 566 · see citing works
Casiraghi, F., Azzollini, N., Cassis, P., Imberti, B., Morigi, M., Cugini, D., Cavinato, R. A., Todeschini, M., Solini, S., Sonzogni, A., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.6.3933 · Cited by 423 · see citing works
IFN-γ and TNF-α differentially regulate immunomodulation by murine mesenchymal stem cells
English, K., Barry, F., Field-Corbett, C., & Mahon, B. P. (2007) · Immunology Letters · doi:10.1016/j.imlet.2007.04.001 · Cited by 417 · see citing works
Sudres, M., Norol, F., Trenado, A., Grégoire, S., Charlotte, F., Levacher, B., Lataillade, J., Bourin, P., Holy, X., Vernant, J., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.12.7761 · Cited by 412 · see citing works
Patel, S. A., Meyer, J. R., Greco, S. J., Corcoran, K. E., Bryan, M., & Rameshwar, P. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903143 · Cited by 364 · see citing works
Immunosuppressive Effects of Mesenchymal Stem Cells: Involvement of HLA-G
Nasef, A., Mathieu, N., Chapel, A., Frick, J., François, S., Mazurier, C., Boutarfa, A., Bouchet, S., Gorin, N.-C., Thierry, D., et al. (2007) · Transplantation · doi:10.1097/01.tp.0000267918.07906.08 · Cited by 350 · see citing works
Tumor Cell Invasion Inhibited by TIMP-2
Albini, A., Melchiori, A., Santi, L., Liotta, L. A., Brown, P. D. N., & Stetler‐Stevenson, W. G. (1991) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/83.11.775 · Cited by 321 · see citing works
Ge, W., Jiang, J., Baroja, M. L., Arp, J., Zassoko, R., Liu, W., Bartholomew, A. M., García, B., & Wang, H. (2009) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2009.02721.x · Cited by 271 · see citing works
Human Mesenchymal Stem Cells Promote Survival of T Cells in a Quiescent State
Benvenuto, F., Ferrari, S., Gerdoni, E., Gualandi, F., Frassoni, F., Pistoia, V., Mancardi, G., & Uccelli, A. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0068 · Cited by 258 · see citing works
Popp, F., Eggenhofer, E., Renner, P., Slowik, P., Lang, S. A., Kaspar, H., Geissler, E. K., Piso, P., Schlitt, H. J., & Dahlke, M. H. (2008) · Transplant Immunology · doi:10.1016/j.trim.2008.08.004 · Cited by 196 · see citing works
Self-citationHoogduijn, M. J., Crop, M. J., Peeters, A. M. A., van Osch, G. J. V. M., Balk, A. H. M. M., IJzermans, J. N. M., Weimar, W., & Baan, C. C. (2007) · Stem Cells and Development · doi:10.1089/scd.2006.0110 · Cited by 189 · see citing works
Self-citationHuman mesenchymal stem cells inhibit antibody production induced in vitro by allostimulation
Comoli, P., Ginevri, F., Maccario, R., Avanzini, M. A., Marconi, M., Groff, A., Cometa, A. M., Cioni, M., Porretti, L., Barberi, W., et al. (2007) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfm740 · Cited by 148 · see citing works
François, M., Romieu, R., Stock-Martineau, S., Boivin, M., Bramson, J. L., & Galipeau, J. (2009) · Blood · doi:10.1182/blood-2009-02-207795 · Cited by 146 · see citing works
Masoodi, M., & Nicolaou, A. (2006) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.2697 · Cited by 143 · see citing works
Self-citationParekkadan, B., Tilles, A. W., & Yarmush, M. L. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0790 · Cited by 139 · see citing works
Chan, W. K., Lau, A. S. Y., Li, J., Law, H., Lau, Y., & Chan, G. (2008) · Experimental Hematology · doi:10.1016/j.exphem.2008.06.008 · Cited by 137 · see citing works
Renner, P., Eggenhofer, E., Rosenauer, A., Popp, F., Steinmann, J., Slowik, P., Geissler, E. K., Piso, P., Schlitt, H. J., & Dahlke, M. H. (2009) · Transplantation Proceedings · doi:10.1016/j.transproceed.2009.06.119 · Cited by 127 · see citing works
Self-citationHuman Adipose Tissue-Derived Mesenchymal Stem Cells Induce Explosive T-Cell Proliferation
Crop, M. J., Baan, C. C., Korevaar, S. S., IJzermans, J. N. M., Weimar, W., & Hoogduijn, M. J. (2010) · Stem Cells and Development · doi:10.1089/scd.2009.0368 · Cited by 104 · see citing works
Self-citationSusceptibility of Human Mesenchymal Stem Cells to Tacrolimus, Mycophenolic Acid, and Rapamycin
Hoogduijn, M. J., Crop, M. J., Korevaar, S. S., Peeters, A. M. A., Eijken, M., Maat, L. P. W. M., Balk, A. H. M. M., Weimar, W., & Baan, C. C. (2008) · Transplantation · doi:10.1097/tp.0b013e31818aa536 · Cited by 102 · see citing works
Self-citationSbano, P., Cuccia, A., Mazzanti, B., Urbani, S., Giusti, B., Lapini, I., Rossi, L., Abbate, R., Marseglia, G., Nannetti, G., et al. (2008) · Archives of Dermatological Research · doi:10.1007/s00403-007-0827-9 · Cited by 99 · see citing works
Buron, F., Perrin, H., Malcus, C., Héquet, O., Thaunat, O., Sarda-Kolopp, M.-N., Touraine‐Moulin, F., & Morélon, E. (2009) · Transplantation Proceedings · doi:10.1016/j.transproceed.2009.08.030 · Cited by 85 · see citing works
Toward MSC in Solid Organ Transplantation: 2008 Position Paper of the MISOT Study Group
Dahlke, M. H., Hoogduijn, M. J., Eggenhofer, E., Popp, F., Renner, P., Slowik, P., Rosenauer, A., Piso, P., Geissler, E. K., Lange, C., et al. (2009) · Transplantation · doi:10.1097/tp.0b013e3181b4425a · Cited by 71 · see citing works
Self-citationMesenchymal stem cells as immunomodulators after liver transplantation
Popp, F., Renner, P., Eggenhofer, E., Slowik, P., Geissler, E. K., Piso, P., Schlitt, H. J., & Dahlke, M. H. (2009) · Liver Transplantation · doi:10.1002/lt.21862 · Cited by 61 · see citing works
Self-citationCell contact interaction between adipose‐derived stromal cells and allo‐activated T lymphocytes
Quaedackers, M. E., Baan, C. C., Weimar, W., & Hoogduijn, M. J. (2009) · European Journal of Immunology · doi:10.1002/eji.200939584 · Cited by 60 · see citing works
Self-citationSuvà, D., Passweg, J. R., Arnaudeau, S., Hoffmeyer, P. J., & Kindler, V. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21244 · Cited by 52 · see citing works
Overview of stem cell therapy for Crohn's disease
Dryden, G. W. (2009) · Expert Opinion on Biological Therapy · doi:10.1517/14712590902956615 · Cited by 45 · see citing works
Donor-Derived Mesenchymal Stem Cells Remain Present and Functional in the Transplanted Human Heart
Hoogduijn, M. J., Crop, M. J., Peeters, A., Korevaar, S. S., Eijken, M., Drabbels, J. J. M., Roelen, D. L., Maat, A. P. W. M., Balk, A. H. M. M., Weimar, W., et al. (2008) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2008.02450.x · Cited by 41 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Biomaterial based modulation of macrophage polarization: a review and suggested design principles
Sridharan, R., Cameron, A. R., Kelly, D. J., Kearney, C. J., & O’Brien, F. J. (2015) · Materials Today · doi:10.1016/j.mattod.2015.01.019 · Cited by 826 · see citing works
Marquez-Curtis, L. A., Janowska-Wieczorek, A., McGann, L. E., & Elliott, J. A. W. (2015) · Cryobiology · doi:10.1016/j.cryobiol.2015.07.003 · Cited by 346 · see citing works
Lee, S., Choi, E., Cha, M., & Hwang, K. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/632902 · Cited by 269 · see citing works
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
Masaki, T., Qu, J., Cholewa-Waclaw, J., Burr, K., Raaum, R. L., & Rambukkana, A. (2013) · Cell · doi:10.1016/j.cell.2012.12.014 · Cited by 237 · see citing works
Spitzer, T., Rojas, A. M., Zelenko, Z., Aghajanova, L., Erikson, D. W., Barragan, F., Meyer, M., Tamaresis, J. S., Hamilton, A. E., Irwin, J. C., et al. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.095885 · Cited by 213 · see citing works
Franquesa, M., Mensah, F. K., Huizinga, R., Strini, T., Boon, L., Lombardo, E., DelaRosa, O., Laman, J. D., Grinyo, J. M., Weimar, W., et al. (2014) · Stem Cells · doi:10.1002/stem.1881 · Cited by 213 · see citing works
Self-citationLevy, O., Zhao, W., Mortensen, L. J., LeBlanc, S., Tsang, K., Fu, M., Phillips, J. A., Sagar, V., Anandakumaran, P. N., Ngai, J., et al. (2013) · Blood · doi:10.1182/blood-2013-04-495119 · Cited by 212 · see citing works
Gnani, D., Crippa, S., della Volpe, L., Rossella, V., Conti, A., Lettera, E., Rivis, S., Ometti, M., Fraschini, G., Bernardo, M. E., et al. (2019) · Aging Cell · doi:10.1111/acel.12933 · Cited by 188 · see citing works
Mesenchymal stem cell-educated macrophages
Eggenhofer, E., & Hoogduijn, M. J. (2012) · Transplantation Research · doi:10.1186/2047-1440-1-12 · Cited by 169 · see citing works
Self-citationMesenchymal Stem Cells in the Treatment of Traumatic Brain Injury
Hasan, A., Deeb, G., Rahal, R., Atwi, K. M., Mondello, S., Marei, H. E. S., Gali, A., & Sleiman, E. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00028 · Cited by 141 · see citing works
Anzalone, R., Iacono, M. L., Loria, T., di Stefano, A., Giannuzzi, P., Farina, F., & Larocca, G. (2011) · Stem Cell Reviews and Reports · doi:10.1007/s12015-010-9196-4 · Cited by 146 · see citing works
New Strategies for Overcoming Limitations of Mesenchymal Stem Cell-Based Immune Modulation
Kim, N., & Cho, S. (2015) · International Journal of Stem Cells · doi:10.15283/ijsc.2015.8.1.54 · Cited by 132 · see citing works
Mao, C.-Y., Wang, Y.-G., Zhang, X., Zheng, X.-Y., Tang, T.-T., & Lu, E. Y. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.204 · Cited by 132 · see citing works
Kim, Y., Jo, S.-H., Kim, W. H., & Kweon, O. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0236-5 · Cited by 125 · 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
Scaffold strategies for modulating immune microenvironment during bone regeneration
He, J., Chen, G., Liu, M., Xu, Z., Chen, H., Yang, L., & Lv, Y. (2019) · Materials Science and Engineering C · doi:10.1016/j.msec.2019.110411 · Cited by 127 · see citing works
Mesenchymal Stem Cells Induce an Inflammatory Response After Intravenous Infusion
Hoogduijn, M. J., Rhijn, M. R.-V., Engela, A. U., Korevaar, S. S., Mensah, F., Franquesa, M., de Bruin, R. W. F., Betjes, M. G. H., Weimar, W., & Baan, C. C. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0193 · Cited by 121 · see citing works
Self-citationFollin, B., Juhl, M., Cohen, S., Pedersen, A. E., Kastrup, J., & Ekblond, A. (2016) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2015.0532 · Cited by 113 · see citing works
Gu, F., Wang, D., Zhang, H., Feng, X., Gilkeson, G. S., Shi, S., & Sun, L. (2014) · Clinical Rheumatology · doi:10.1007/s10067-014-2754-4 · Cited by 112 · see citing works
Siniscalco, D., Giordano, C., Galderisi, U., Luongo, L., de Novellis, V., Rossi, F., & Maione, S. (2011) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2011.00079 · Cited by 112 · see citing works
Autologous Bone Marrow Mononuclear Cell Therapy for Autism: An Open Label Proof of Concept Study
Sharma, A., Gokulchandran, N., Sane, H., Nagrajan, A., Paranjape, A., Kulkarni, P., Shetty, A., Mishra, P., Kali, M., Biju, H., et al. (2013) · Stem Cells International · doi:10.1155/2013/623875 · Cited by 110 · see citing works
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
Immunomodulatory Effect of MSC on B Cells Is Independent of Secreted Extracellular Vesicles
Carreras‐Planella, L., Tortajada, M., Borràs, F. E., & Franquesa, M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01288 · Cited by 106 · see citing works
Toward Development of iMesenchymal Stem Cells for Immunomodulatory Therapy
de Witte, S. F. H., Franquesa, M., Baan, C. C., & Hoogduijn, M. J. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00648 · Cited by 103 · see citing works
Self-citationThe potential use of mesenchymal stem cells in hematopoietic stem cell transplantation
Kim, E., Kim, N., & Cho, S. (2013) · Experimental & Molecular Medicine · doi:10.1038/emm.2013.2 · Cited by 102 · see citing works
Insights into inflammatory priming of mesenchymal stromal cells: functional biological impacts
Najar, M., Krayem, M., Merimi, M., Burny, A., Meuleman, N., Bron, D., Raicevic, G., & Lagneaux, L. (2018) · Inflammation Research · doi:10.1007/s00011-018-1131-1 · Cited by 100 · see citing works
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
Li, W., Liu, Q., Shi, J., Xu, X. M., & Xu, J. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1074863 · Cited by 104 · see citing works
Engela, A. U., Hoogduijn, M. J., Boer, K., Litjens, N. H. R., Betjes, M. G. H., Weimar, W., & Baan, C. C. (2013) · Clinical & Experimental Immunology · doi:10.1111/cei.12120 · Cited by 92 · see citing works
Self-citationGonçalves, F. D. C., Luk, F., Korevaar, S. S., Bouzid, R., Paz, A. H. D. R., López‐Iglesias, C., Baan, C. C., Merino, A. M., & Hoogduijn, M. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-12121-z · Cited by 87 · see citing works
Self-citationTherapeutic 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 88 · see citing works
miRNA Control of Tissue Repair and Regeneration
Sen, C. K., & Ghatak, S. (2015) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.04.001 · Cited by 87 · see citing works
Engela, A. U., Baan, C. C., Dor, F. J. M. F., Weimar, W., & Hoogduijn, M. J. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00126 · Cited by 82 · see citing works
Self-citationAging of bone marrow– and umbilical cord–derived mesenchymal stromal cells during expansion
de Witte, S. F. H., Lambert, E. E., Merino, A. M., Strini, T., Douben, H., O’Flynn, L., Elliman, S. J., de Klein, A., Newsome, P. N., Baan, C. C., et al. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2017.03.071 · Cited by 81 · see citing works
Self-citationChow, L., Johnson, V., Coy, J. W., Regan, D. P., & DOW, S. W. (2016) · Stem Cells and Development · doi:10.1089/scd.2016.0207 · Cited by 78 · see citing works
Partnership between platelet-rich plasma and mesenchymal stem cells: in vitro experience
Rubio‐Azpeitia, E. (2014) · Muscles Ligaments and Tendons Journal · doi:10.11138/mltj/2014.4.1.052 · Cited by 76 · see citing works
Kim, N., Im, K.-I., Lim, J.-Y., Jeon, E.-J., Nam, Y.-S., Kim, E., & Cho, S. (2013) · Annals of Hematology · doi:10.1007/s00277-013-1796-z · Cited by 71 · see citing works
Escacena, N., Quesada-Hernández, E., Capilla‐González, V., Soria, B., & Hmadcha, A. (2015) · Stem Cells International · doi:10.1155/2015/895714 · Cited by 71 · see citing works
Lim, J.-Y., Im, K.-I., Lee, E., Kim, N., Nam, Y.-S., Jeon, Y., & Cho, S. (2016) · Scientific Reports · doi:10.1038/srep26851 · Cited by 71 · see citing works
Allogeneic Mesenchymal Stem Cell Transplantation in Dogs with Keratoconjunctivitis Sicca
Bittencourt, M. K. W., Barros, M. A., Martins, J. F. P., de Vasconcellos, J. P. C., de Morais, B. P., Pompéia, C., Bittencourt, M. D., Evangelho, K. D. S., Kerkis, I., & Wenceslau, C. V. (2016) · Cell Medicine · doi:10.3727/215517916x693366 · Cited by 70 · see citing works
Zhao, L., Hu, C., Zhang, P., Jiang, H., & Chen, J. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14035 · Cited by 70 · see citing works
Hatlapatka, T., Moretti, P., Lavrentieva, A. V., Hass, R., Marquardt, N., Jacobs, R., & Kasper, C. (2010) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2010.0406 · Cited by 67 · see citing works
Interaction between Adipose Tissue-Derived Mesenchymal Stem Cells and Regulatory T-Cells
Engela, A. U., Baan, C. C., Peeters, A. M. A., Weimar, W., & Hoogduijn, M. J. (2013) · Cell Transplantation · doi:10.3727/096368912x636984 · Cited by 69 · see citing works
Self-citationPartnership between platelet-rich plasma and mesenchymal stem cells: in vitro experience
Rubio‐Azpeitia, E., & Andı́a, I. (2019) · Muscles Ligaments and Tendons Journal · doi:10.32098/mltj.01.2014.10 · Cited by 67 · see citing works
Improving Immunotherapy Through Glycodesign
Buettner, M. J., Shah, S. R., Saeui, C. T., Ariss, R., & Yarema, K. J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02485 · Cited by 66 · see citing works
Prospects of Stem Cell Therapy in Osteoarthritis
Roberts, S., Genever, P. G., McCaskie, A. W., & Bari, C. D. (2011) · Regenerative Medicine · doi:10.2217/rme.11.21 · Cited by 65 · see citing works
The Stem Cell Niche Should be a Key Issue for Cell Therapy in Regenerative Medicine
Becerra, J., Santos‐Ruiz, L., Andrades, J. A., & Marí‐Beffa, M. (2010) · Stem Cell Reviews and Reports · doi:10.1007/s12015-010-9195-5 · Cited by 62 · see citing works
Soria-Juan, B., Escacena, N., Capilla‐González, V., Aguilera, Y., Llanos, L., Tejedo, J. R., Bedoya, F. J., Juan, V., de la Cuesta, A., Ruiz-Salmeron, R. J., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01151 · Cited by 61 · see citing works
Strategies to improve the immunosuppressive properties of human mesenchymal stem cells
Lee, M. W., Ryu, S., Kim, D. S., Sung, K. W., Koo, H. H., & Yoo, K. H. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0178-y · Cited by 61 · see citing works
Autism Spectrum Disorders: Is Mesenchymal Stem Cell Personalized Therapy the Future?
Siniscalco, D., Sapone, A., Cirillo, A., Giordano, C., Maione, S., & Antonucci, N. (2012) · BioMed Research International · doi:10.1155/2012/480289 · Cited by 61 · see citing works
Pleyer, L., Valent, P., & Greil, R. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17071009 · Cited by 60 · see citing works
The Immunomodulatory Potential of Wharton’s Jelly Mesenchymal Stem/Stromal Cells
Paladino, F. V., Rodrigues, J. D. M., da Silva, A., & Goldberg, A. C. (2019) · Stem Cells International · doi:10.1155/2019/3548917 · Cited by 60 · see citing works
Sadek, K. M., Moshy, S. E., Radwan, I. A., Rady, D., Abbass, M. M. S., El‐Rashidy, A. A., Dörfer, C. E., & El‐Sayed, K. M. F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054599 · Cited by 62 · see citing works
Higashimoto, M., Sakai, Y., Takamura, M., Usui, S., Nasti, A., Yoshida, K., Seki, A., Komura, T., Honda, M., Wada, T., et al. (2013) · European Journal of Immunology · doi:10.1002/eji.201343531 · Cited by 56 · see citing works
Gebraad, A., Kornilov, R., Kaur, S., Miettinen, S., Haimi, S. P., Peltoniemi, H. H., Mannerström, B., & Seppänen‐Kaijansinkko, R. (2018) · FEBS Journal · doi:10.1111/febs.14485 · Cited by 56 · see citing works
Mesenchymal stem cells decrease splenocytes apoptosis in a sepsis experimental model
Pedrazza, L., Lunardelli, A., Luft, C., Cruz, C. U., de Mesquita, F. C., Bitencourt, S., Nunes, F. B., & de Oliveira, J. R. (2014) · Inflammation Research · doi:10.1007/s00011-014-0745-1 · Cited by 55 · see citing works
Mesenchymal stem cells derived from adipose tissue are not affected by renal disease
Rhijn, M. R.-V., Reinders, M. E. J., de Klein, A., Douben, H., Korevaar, S. S., Mensah, F., Dor, F. J. M. F., IJzermans, J. N. M., Betjes, M. G. H., Baan, C. C., et al. (2012) · Kidney International · doi:10.1038/ki.2012.187 · Cited by 55 · see citing works
Self-citationWang, D., Akiyama, K., Zhang, H., Yamaza, T., Li, X., Feng, X., Wang, H., Hua, B., Liu, B., Xu, H., et al. (2012) · Clinical and Developmental Immunology · doi:10.1155/2012/273291 · Cited by 54 · see citing works
Are mesenchymal stromal cells immune cells?
Hoogduijn, M. J. (2015) · Arthritis Research & Therapy · doi:10.1186/s13075-015-0596-3 · Cited by 54 · see citing works
Self-citationGuo, L., Lai, P., Wang, Y., Huang, T., Chen, X., Luo, C., Geng, S., Huang, X., Wu, S., Ling, W., et al. (2019) · International Immunopharmacology · doi:10.1016/j.intimp.2019.05.048 · Cited by 54 · see citing works
Extracellular Vesicles as Therapeutic Tools for the Treatment of Chronic Wounds
Bray, E. R., Oropallo, A., Grande, D. A., Kirsner, R. S., & Badiavas, E. V. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13101543 · Cited by 56 · see citing works
Rahavi, H., Hashemi, S. M., Soleimani, M., Mohammadi, J., & Tajik, N. (2015) · Journal of Diabetes Research · doi:10.1155/2015/878535 · Cited by 52 · see citing works
Chang, H., Kim, P., Cho, H., Yum, S., Choi, Y., Son, Y., Lee, D., Kang, I., Kang, K., Jang, G., et al. (2016) · Molecular Therapy · doi:10.1038/mt.2016.120 · Cited by 52 · see citing works
A Small-Molecule Screen for Enhanced Homing of Systemically Infused Cells
Levy, O., Mortensen, L. J., Boquet, G., Tong, Z., Perrault, C., Benhamou, B., Zhang, J., Stratton, T., Han, E., Safaee, H., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.057 · Cited by 50 · see citing works
Leijs, M. J. C., van Buul, G. M., Lubberts, E., Bos, P. K., Verhaar, J. A. N., Hoogduijn, M. J., & van Osch, G. J. V. M. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00231 · Cited by 50 · see citing works
Self-citationEmerging roles of mesenchymal stem cell therapy in patients with critical limb ischemia
Shirbaghaee, Z., Hassani, M., Keshel, S. H., & Soleimani, M. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03148-9 · Cited by 49 · see citing works
Wound-Healing Effects of Mesenchymal Stromal Cell Secretome in the Cornea and the Role of Exosomes
An, S., Anwar, K. N., Ashraf, M. J., Lee, H., Jung, R., Koganti, R., Ghassemi, M., & Djalilian, A. R. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15051486 · Cited by 48 · see citing works
Tolerance in Organ Transplantation: From Conventional Immunosuppression to Extracellular Vesicles
Tortajada, M., Lauzurica, R., & Borràs, F. E. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00416 · Cited by 47 · see citing works
Wu, T., Yang, L., Wang, B., Sun, Y., Xu, J., Lee, W., Xu, L., Zhang, J., & Li, G. (2016) · Tissue Engineering Part A · doi:10.1089/ten.tea.2016.0248 · Cited by 46 · see citing works
Interaction of multipotent mesenchymal stromal and immune cells: Bidirectional effects
Andreeva, E. R., Бобылева, П. И., Gornostaeva, A. N., & Buravkova, L. B. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2017.07.001 · Cited by 45 · see citing works
van den Akker, F., Vrijsen, K. R., Deddens, J. C., Buikema, J. W., Mokrý, M., Laake, L. W. V., Doevendans, P. A., & Sluijter, J. P. G. (2018) · Heliyon · doi:10.1016/j.heliyon.2018.e00642 · Cited by 46 · see citing works
Gonzalo-Gil, E., Pérez-Lorenzo, M. J., Galindo-Izquierdo, M., de la Guardia, R. D., López‐Millán, B., Bueno, C., Menéndez, P. R., Pablos, J. L., & Criado, G. (2016) · Arthritis Research & Therapy · doi:10.1186/s13075-016-0979-0 · Cited by 45 · see citing works
Biotechnological and biomedical applications of mesenchymal stem cells as a therapeutic system
Rahimzadeh, A., Mirakabad, F. S. T., Movassaghpour, A. A., Shamsasenjan, K., Kariminekoo, S., Talebi, M., Shekari, A., Zeighamian, V., Ghalhar, M. G., & Akbarzadeh, A. (2014) · Artificial Cells Nanomedicine and Biotechnology · doi:10.3109/21691401.2014.968823 · Cited by 44 · see citing works
Etanercept-Synthesising Mesenchymal Stem Cells Efficiently Ameliorate Collagen-Induced Arthritis
Park, N., Rim, Y. A., Jung, H., Kim, J., Yi, H., Kim, Y., Jang, Y., Jung, S. M., Lee, J. J., Kwok, S., et al. (2017) · Scientific Reports · doi:10.1038/srep39593 · Cited by 42 · see citing works
Human Mesenchymal Stem Cell Secretome Driven T Cell Immunomodulation Is IL-10 Dependent
Shephard, M. T., Merkhan, M. M., & Forsyth, N. R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113596 · Cited by 42 · see citing works
Stem cell therapy emerging as the key player in treating type 1 diabetes mellitus
Vanikar, A. V., Trivedi, H. L., & Thakkar, U. G. (2016) · Cytotherapy · doi:10.1016/j.jcyt.2016.06.006 · Cited by 42 · see citing works
Schäfer, S., Calas, A.-G., Vergouts, M., & Hermans, E. (2012) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2012.04.018 · Cited by 42 · see citing works
Canseco, J. A., Kojima, K., Penvose, A. R., Ross, J. D., Obokata, H., Gomoll, A. H., & Vacanti, C. A. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2012.0030 · Cited by 41 · see citing works
Zinöcker, S., & Vaage, J. T. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00062 · Cited by 41 · see citing works
Gregoire-Gauthier, J., Selleri, S., Fontaine, F., Dieng, M. M., Patey, N., Despars, G., Beausejour, C. M., & Haddad, É. (2011) · Stem Cells and Development · doi:10.1089/scd.2011.0413 · Cited by 41 · see citing works
Cassano, J. M., Schnabel, L. V., Goodale, M. B., & Fortier, L. A. (2017) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2017.10.003 · Cited by 41 · see citing works
High-risk corneal allografts: A therapeutic challenge
Tian, Y., Rajendran, V., Griffith, M., Forrester, J. V., & Kuffová, L. (2016) · World Journal of Transplantation · doi:10.5500/wjt.v6.i1.10 · Cited by 40 · see citing works
Interleukin‐12 modulates the immunomodulatory properties of human periodontal ligament cells
Ayuthaya, B. I. N., Satravaha, P., & Pavasant, P. (2016) · Journal of Periodontal Research · doi:10.1111/jre.12421 · Cited by 40 · see citing works
Park, A., Park, H., Yoon, J., Kang, D., Kang, M.-H., Park, Y.-Y., Suh, N., & Yu, J. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1164-6 · Cited by 39 · see citing works
Mesenchymal stem cell therapy in proteoglycan induced arthritis
Swart, J. F., de Roock, S., Hofhuis, F. M., Rozemuller, H., van den Broek, T., Moerer, P., Broere, F., van Wijk, F., Kuis, W., Prakken, B. J., et al. (2014) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2013-204147 · Cited by 37 · see citing works
Eltoukhy, H. S., Sinha, G., Moore, C. A., Gergues, M., & Rameshwar, P. (2018) · Biochimie · doi:10.1016/j.biochi.2018.05.018 · Cited by 36 · see citing works
Potential benefits of allogeneic bone marrow mesenchymal stem cells for wound healing
Badiavas, A. R., & Badiavas, E. V. (2011) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2011.606212 · Cited by 36 · see citing works
Interface Oral Health Science 2016
Takahashi, N., Sasaki, K., & Suzuki, O. (2016) · Springer eBooks · doi:10.1007/978-981-10-1560-1 · Cited by 36 · see citing works
Zhao, Y., Dong, H., Xia, Q., Wang, Y., Zhu, L., Hu, Z., Xia, J., Mao, Q., Weng, Z., Yi, J., et al. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116238 · Cited by 35 · see citing works
hMSCs suppress neutrophil-dominant airway inflammation in a murine model of asthma
Hong, G. H., Kwon, H., Lee, K. Y., Ha, E., Moon, K., Kim, S. W., Oh, W., Kim, T., Moon, H., & Cho, Y. S. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2016.135 · Cited by 34 · see citing works
Ahmed, E. A., Ahmed, O. M., Fahim, H. I., Mahdi, E. A., Ali, T. M., Elesawy, B. H., & Ashour, M. B. (2021) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2021/8899143 · Cited by 33 · see citing works
Ranjbar, A., Hassanzadeh, H., Jahandoust, F., Miri, R., Bidkhori, H. R., Monzavi, S. M., Moussavi, N. S., Matin, M. M., & Shariati‐Sarabi, Z. (2021) · Current Research in Translational Medicine · doi:10.1016/j.retram.2021.103324 · Cited by 34 · see citing works
Kiernan, C. H., Wolvius, E. B., Brama, P. A. J., & Farrell, E. (2017) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2017.0175 · Cited by 34 · see citing works
Overcoming biological barriers to improve solid tumor immunotherapy
Ukidve, A., Cu, K., Kumbhojkar, N., Lahann, J., & Mitragotri, S. (2021) · Drug Delivery and Translational Research · doi:10.1007/s13346-021-00923-8 · Cited by 33 · see citing works
Mesenchymal stem cell therapy targeting mitochondrial dysfunction in acute kidney injury
Zhao, L., Hu, C., Zhang, P., Jiang, H., & Chen, J. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-019-1893-4 · Cited by 31 · see citing works
Therapeutic Potential of Mesenchymal Stem Cells for Oral and Systemic Diseases
Kim, R. H., Mehrazarin, S., & Kang, M. (2012) · Dental Clinics of North America · doi:10.1016/j.cden.2012.05.006 · Cited by 31 · see citing works
Li, Q., Liu, J., Su, R., Zhen, J., Liu, X., & Liu, G. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.112667 · Cited by 30 · see citing works
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 · see citing works
A Novel Therapeutic Approach Using Mesenchymal Stem Cells to Protect Against Mycobacterium abscessus
Kim, J.-S., Cha, S., Kim, W. S., Han, S. J., Bin, S., Kim, H. M., Kwon, K. W., Kim, S. J., Choi, H.-H., Lee, J., et al. (2016) · Stem Cells · doi:10.1002/stem.2353 · Cited by 30 · see citing works
- Authors
- Hoogduijn, M. J., Popp, F., Verbeek, R., Masoodi, M., Nicolaou, A., Baan, C., & Dahlke, M.-H.
- Affiliations
- Erasmus MC (NL)
- University of Regensburg (DE)
- University of Bradford (GB)
- Corresponding author
- Hoogduijn, Martin J
- Venue
- International Immunopharmacology
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 10
- Issue
- 12
- Pages
- 1496-1500
- ISSN
- 1567-5769 (ISSN-L)
- OpenAlex
- W2166106062
- Cited by
- 248
- References
- 48
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 5 · 2023: 5 · 2022: 10 · 2021: 15 · 2020: 5 · 2019: 18 · 2018: 26 · 2017: 23 · 2016: 27 · 2015: 23 · 2014: 23 · 2013: 24 · 2012: 17
- FWCI
- 8.08
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Immunopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- University of Regensburg Publication Server (University of Regensburg) (acceptedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Bradford Scholars (University of Bradford) (submittedVersion)
- 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, immunomodulation, immunotherapy, graft-versus-host disease, Crohn's disease, organ transplantation, cytokine production, chemokines, prostaglandins, anti-inflammatory activity, pro-inflammatory effects
- MeSH terms
- Animals, Clinical Trials as Topic, Graft vs Host Disease, Humans, Immunotherapy, Prostaglandins, Cytokines, 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.
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