Tissue-resident mesenchymal stem cells attract peripheral blood neutrophils and enhance their inflammatory activity in response to microbial challenge
Abstract
Human MSCs may respond to TLR ligation, and recent research has suggested that many tissues contain tissue-specific MSCs, possibly located in periendothelial and perivascular regions. At present, the functional consequences of these findings are unclear. We hypothesized that tissue-specific MSCs could play an instructional role during early phases of bacterial challenge. To investigate this hypothesis further, we set up a coculture system of glandular MSCs and peripheral blood neutrophils so that we could analyze the cellular interactions of these cells in response to LPS challenge. We found that stimulation with bacterial endotoxin induced chemokine receptor expression and mobility of MSCs. Activated MSCs secreted large amounts of inflammatory cytokines and recruited neutrophils in an IL-8- and MIF-dependent manner. Recruited and activated neutrophils showed a prolonged lifespan, an increased expression of inflammatory chemokines, and an enhanced responsiveness toward subsequent challenge with LPS. Our findings demonstrate a complex, functional interaction between tissue-resident MSCs and peripheral blood neutrophils upon bacterial challenge and suggest a role for MSCs in the early phases of pathogen challenge, when classical immune cells have not been recruited yet.
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?
MSCs secrete CXCL8 and macrophage migration inhibitory factor, which recruit neutrophils into the injured site.
“MSCs also secrete CXCL8 (also known as IL-8) and macrophage migration inhibitory factor (MIF), known for recruiting neutrophils into the injured site [42], [64].”
From Mesenchymal stem cell secretome for regenerative medicine: Where do we stand? (2025) · cites this paper as [64]
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
Toll-like receptor control of the adaptive immune responses
Iwasaki, A., & Medzhitov, R. M. (2004) · Nature Immunology · doi:10.1038/ni1112 · Cited by 4,166 · see citing works
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 · 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
Mesenchymal stem cells reside in virtually all post-natal organs and tissues
Meirelles, L. D. S., Chagastelles, P. C., & Nardi, N. B. (2006) · Journal of Cell Science · doi:10.1242/jcs.02932 · Cited by 2,488 · see citing works
Horwitz, E. M., Blanc, K. L., Dominici, M., Mueller, I., Slaper‐Cortenbach, I., Marini, F. C., Deans, R. J., Krause, D. S., & Keating, A. (2005) · Cytotherapy · doi:10.1080/14653240500319234 · Cited by 2,074 · see citing works
Human mesenchymal stem cells modulate B-cell functions
Corcione, A., Benvenuto, F., Ferretti, E., Giunti, D., Cappiello, V., Cazzanti, F., Risso, M., Gualandi, F., Mancardi, G. L., Pistoia, V., et al. (2006) · Blood · doi:10.1182/blood-2005-07-2657 · Cited by 1,767 · see citing works
Fibroblast precursors in normal and irradiated mouse hematopoietic organs.
Aj, F., Jf, G., & Nn, K. (1976) · PubMed · Cited by 1,645 · see citing works
Mesenchymal Stem Cells and Their Potential as Cardiac Therapeutics
Pittenger, M. F., & Martin, B. J. (2004) · Circulation Research · doi:10.1161/01.res.0000135902.99383.6f · Cited by 1,434 · see citing works
Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy
Zappia, E., Casazza, S., Pedemonte, E., Benvenuto, F., Bonanni, I., Gerdoni, E., Giunti, D., Ceravolo, A., Cazzanti, F., Frassoni, F., et al. (2005) · Blood · doi:10.1182/blood-2005-04-1496 · Cited by 1,431 · see citing works
Bernhagen, J., Krohn, R. M., Lue, H., Gregory, J. L., Zernecke, A., Koenen, R. R., Dewor, M., Georgiev, I., Schober, A., Leng, L., et al. (2007) · Nature Medicine · doi:10.1038/nm1567 · Cited by 1,272 · see citing works
Mesenchymal Stem Cells for Treatment of Therapy-Resistant Graft-versus-Host Disease
Ringdén, O. T. H., Uzunel, M., Rasmusson, I., Remberger, M., Sundberg, B., Lönnies, H., Marschall, H., Dlugosz, A., Szakos, A., Hassan, Z., et al. (2006) · Transplantation · doi:10.1097/01.tp.0000214462.63943.14 · Cited by 1,143 · see citing works
Spaggiari, G. M., Capobianco, A., Abdelrazik, H., Becchetti, F., Mingari, M. C., & Moretta, L. (2007) · Blood · doi:10.1182/blood-2007-02-074997 · Cited by 1,139 · see citing works
Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5‐azacytidine
Wakitani, S., Saito, T., & Caplan, A. I. (1995) · Muscle & Nerve · doi:10.1002/mus.880181212 · Cited by 1,081 · see citing works
In Search of the In Vivo Identity of Mesenchymal Stem Cells
da Silva Meirelles, L., Caplan, A. I., & Nardi, N. B. (2008) · Stem Cells · doi:10.1634/stemcells.2007-1122 · Cited by 1,077 · see citing works
Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow
Colter, D. C., Class, R., DiGirolamo, C. M., & Prockop, D. J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3213 · Cited by 1,019 · see citing works
Kolf, C. M., Cho, E., & Tuan, R. S. (2007) · Arthritis Research & Therapy · doi:10.1186/ar2116 · Cited by 951 · see citing works
Macrophage inflammatory protein-1
Maurer, M., & von Stebut, E. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2003.10.019 · Cited by 769 · see citing works
Lee, R. H., Seo, M. J., Reger, R. L., Spees, J. L., Pulin, A. A., Olson, S. D., & Prockop, D. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608249103 · Cited by 711 · see citing works
Wexler, S., Donaldson, C., Denning‐Kendall, P. A., Rice, C. M., Bradley, B. A., & Hows, J. (2003) · British Journal of Haematology · doi:10.1046/j.1365-2141.2003.04284.x · Cited by 643 · see citing works
Keating, A. (2006) · Current Opinion in Hematology · doi:10.1097/01.moh.0000245697.54887.6f · Cited by 626 · see citing works
Raffaghello, L., Bianchi, G., Bertolotto, M. B., Montecucco, F., Busca, A., Dallegri, F., Ottonello, L. C., & Pistoia, V. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0416 · Cited by 518 · see citing works
Zhang, W., Ge, W., Li, C., You, S., Liao, L., Han, Q., Deng, W., & Zhao, R. C. H. (2004) · Stem Cells and Development · doi:10.1089/154732804323099190 · Cited by 492 · see citing works
Liotta, F., Angeli, R., Cosmi, L., Filì, L., Manuelli, C., Frosali, F., Mazzinghi, B., Maggi, L., Pasini, A., Lisi, V., et al. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0454 · Cited by 485 · see citing works
Toll-like receptors and their ligands control mesenchymal stem cell functions
Pevsner‐Fischer, M., Morad, V., Cohen-Sfady, M., Rousso-Noori, L., Zanin‐Zhorov, A., Cohen, S. J., Cohen, I. R., & Zipori, D. (2006) · Blood · doi:10.1182/blood-2006-06-028704 · Cited by 484 · see citing works
Miao, Z., Jin, J., Chen, L., Zhu, J., Huang, W., Zhao, J., Qian, H., & Zhang, X. (2006) · Cell Biology International · doi:10.1016/j.cellbi.2006.03.009 · Cited by 474 · see citing works
Tomchuck, S. L., Zwezdaryk, K. J., Coffelt, S. B., Waterman, R. S., Danka, E. S., & Scandurro, A. B. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0563 · Cited by 449 · see citing works
One strategy for cell and gene therapy: Harnessing the power of adult stem cells to repair tissues
Prockop, D. J., Gregory, C. A., & Spees, J. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1834138100 · Cited by 416 · see citing works
The role of mesenchymal stem cells in haemopoiesis
Dazzi, F., Ramasamy, R., Glennie, S. J., Jones, S. P., & Roberts, I. A. G. (2005) · Blood Reviews · doi:10.1016/j.blre.2005.11.002 · Cited by 361 · see citing works
Romieu, R., François, M., Boivin, M., Bouchentouf, M., Spaner, D., & Galipeau, J. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803864 · Cited by 299 · see citing works
Opitz, C. A., Litzenburger, U. M., Lutz, C., Lanz, T. V., Tritschler, I., Köppel, A., Tolosa, E., Hoberg, M., Anderl, J., Aicher, W. K., et al. (2009) · Stem Cells · doi:10.1002/stem.7 · Cited by 299 · see citing works
Interferon-γ-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell
Stagg, J., Pommey, S., Eliopoulos, N., & Galipeau, J. (2005) · Blood · doi:10.1182/blood-2005-07-2793 · Cited by 290 · see citing works
Role of Toll‐Like Receptors on Human Adipose‐Derived Stromal Cells
Cho, H. H., Bae, Y. C., & Jung, J. S. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0189 · Cited by 276 · see citing works
Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation
Kolf, C. M., Cho, E., & Tuan, R. S. (2007) · Cited by 238 · see citing works
Immune regulation by mesenchymal stem cells: two sides to the coin
Stagg, J. (2006) · Tissue Antigens · doi:10.1111/j.1399-0039.2006.00739.x · Cited by 189 · see citing works
Mesenchymal Stem Cells in Cancer: Tumor-Associated Fibroblasts and Cell-Based Delivery Vehicles
Hall, B., Dembinski, J., Sasser, A., Studeny, M., Andreeff, M., & Marini, F. (2007) · International Journal of Hematology · doi:10.1532/ijh97.06230 · Cited by 171 · see citing works
Hemeda, H., Jakob, M., Ludwig, A., Giebel, B., Lang, S., & Brandau, S. (2010) · Stem Cells and Development · doi:10.1089/scd.2009.0365 · Cited by 158 · see citing works
Self-citationCell-Based Therapy in the Repair of Osteochondral Defects: A Novel Use for Adipose Tissue
Nathan, S., De, S. D., Thambyah, A., Chen, F., Goh, J., & Lee, E. H. (2003) · Tissue Engineering · doi:10.1089/107632703768247412 · Cited by 148 · see citing works
Lombardo, E., DelaRosa, O., Mancheño‐Corvo, P., Menta, R., Ramírez, C., & Büscher, D. (2008) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0340 · Cited by 146 · see citing works
Phenotypes of stem cells from diverse origin
Tárnok, A., Ulrich, H., & Bocsi, J. (2009) · Cytometry Part A · doi:10.1002/cyto.a.20844 · Cited by 136 · see citing works
Isolation and Characterization of Adult Stem Cells from Human Salivary Glands
Rotter, N., Oder, J., Schlenke, P., Lindner, U., Böhrnsen, F., Kramer, J., Rohwedel, J., Huss, R., Brandau, S., Wollenberg, B., et al. (2008) · Stem Cells and Development · doi:10.1089/scd.2007.0180 · Cited by 130 · see citing works
Self-citationSpaggiari, G. M., Abdelrazik, H., Becchetti, F., Mingari, M. C., & Moretta, L. (2009) · Clinical Immunology · doi:10.1016/j.clim.2009.03.133 · Cited by 81 · see citing works
Toll-like receptor triggering in cord blood mesenchymal stem cells
van den Berk, L. C. J., Jansen, B., Siebers-Vermeulen, K. G. C., Netea, M. G., Latuhihin, T. E., Bergevoet, S. M., Raymakers, R. A. P., Kögler, G., Figdor, C. G., Adema, G. J., et al. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00653.x · Cited by 74 · see citing works
Human Nasal Mucosa Contains Tissue-Resident Immunologically Responsive Mesenchymal Stromal Cells
Jakob, M., Hemeda, H., Janeschik, S., Bootz, F., Rotter, N., Lang, S., & Brandau, S. (2009) · Stem Cells and Development · doi:10.1089/scd.2009.0245 · Cited by 58 · see citing works
Self-citationProteasome inhibition results in increased poly-ADP-ribosylation: Implications for neuron death
Keller, J. N., & Markesbery, W. R. (2000) · Journal of Neuroscience Research · doi:10.1002/1097-4547(20000815)61:4 · Cited by 54 · see citing works
Conrad, C. H., Göttgens, B., Kinston, S., Ellwart, J. W., & Huss, R. (2002) · Experimental Hematology · doi:10.1016/s0301-472x(02)00865-2 · Cited by 45 · see citing works
Clinical Potential of Adult Vascular Progenitor Cells
Kumar, A. H. S., & Caplice, N. (2010) · Arteriosclerosis, Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.198895 · Cited by 27 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Neutrophils in the activation and regulation of innate and adaptive immunity
Mantovani, A., Cassatella, M. A., Costantini, C., & Jaillon, S. (2011) · Nature reviews. Immunology · doi:10.1038/nri3024 · Cited by 3,044 · see citing works
Mesenchymal Stromal Cells: Sensors and Switchers of Inflammation
Bernardo, M. E., & Fibbe, W. E. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.09.006 · Cited by 1,389 · see citing works
Multipotent mesenchymal stromal cells and the innate immune system
Blanc, K. L., & Mougiakakos, D. (2012) · Nature reviews. Immunology · doi:10.1038/nri3209 · Cited by 1,019 · see citing works
Han, Y., Yang, J., Fang, J., Zhou, Y., Candi, E., Wang, J., Hua, D., Shao, C., & Shi, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00932-0 · Cited by 720 · see citing works
Immune modulation by mesenchymal stem cells
Jiang, W., & Xu, J. (2020) · Cell Proliferation · doi:10.1111/cpr.12712 · Cited by 650 · see citing works
Interactions 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 · see citing works
Regmi, S., Pathak, S., Kim, J. O., Yong, C. S., & Jeong, J. (2019) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2019.04.002 · Cited by 316 · see citing works
Neutrophils in innate and adaptive immunity
Jaillon, S., Galdiero, M. R., Prete, D. D., Cassatella, M. A., Garlanda, C., & Mantovani, A. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0374-8 · Cited by 284 · 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
Cassatella, M. A., Mosna, F., Micheletti, A., Lisi, V., Tamassia, N., Cont, C., Calzetti, F., Pelletier, M., Pizzolo, G., & Krampera, M. (2011) · Stem Cells · doi:10.1002/stem.651 · Cited by 222 · see citing works
Cancer‐related circulating and tumor‐associated neutrophils – subtypes, sources and function
Shaul, M. E., & Fridlender, Z. G. (2018) · FEBS Journal · doi:10.1111/febs.14524 · Cited by 215 · see citing works
Stem Cell Therapy in Heart Diseases – Cell Types, Mechanisms and Improvement Strategies
Müller, P., Lemcke, H., & David, R. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000492704 · Cited by 218 · see citing works
Mesenchymal stem cell secretome for regenerative medicine: Where do we stand?
Trigo, C. M., Rodrigues, J. S., Camões, S. P., Solá, S., & Miranda, J. P. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2024.05.004 · Cited by 205 · see citing works
Toll-Like Receptors as Modulators of Mesenchymal Stem Cells
DelaRosa, O., Dalemans, W., & Lombardo, E. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00182 · Cited by 186 · see citing works
IL1β Induces Mesenchymal Stem Cells Migration and Leucocyte Chemotaxis Through NF-κB
Carrero, R., Cerrada, I., Lledó, E., Dopazo, J., Garcia‐García, F., Rubio, M., Trigueros, C., Dorronsoro, A., Ruiz‐Saurí, A., Montero, J., et al. (2012) · Stem Cell Reviews and Reports · doi:10.1007/s12015-012-9364-9 · Cited by 184 · see citing works
Alvites, R., Branquinho, M., Sousa, A. C., Lopes, B., Sousa, P., & Maurício, A. C. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14020381 · Cited by 174 · see citing works
Matthay, M. A., Pati, S., & Lee, J. W. (2016) · Stem Cells · doi:10.1002/stem.2551 · Cited by 166 · see citing works
Cell-based Therapy for Acute Organ Injury
Monsel, A., Zhu, Y., Gennai, S., Hao, Q., Liu, J., & Lee, J. W. (2014) · Anesthesiology · doi:10.1097/aln.0000000000000446 · Cited by 156 · see citing works
Planat‐Benard, V., Varin, A., & Casteilla, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.626755 · Cited by 139 · see citing works
Mesenchymal stem cells: From regeneration to cancer
Li, P., Gong, Z., Shultz, L. D., & Ren, G. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.04.005 · Cited by 134 · see citing works
Arrest Functions of the MIF Ligand/Receptor Axes in Atherogenesis
Tillmann, S., Bernhagen, J., & Noels, H. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00115 · Cited by 112 · see citing works
Mesenchymal Stem Cells Augment the Anti-Bacterial Activity of Neutrophil Granulocytes
Brandau, S., Jakob, M., Bruderek, K., Bootz, F., Giebel, B., Radtke, S., Mauel, K., Jäger, M., Flohé, S. B., & Lang, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106903 · Cited by 112 · see citing works
Self-citationThe role of secreted factors in stem cells-mediated immune regulation
Lin, L., & Du, L. (2017) · Cellular Immunology · doi:10.1016/j.cellimm.2017.07.010 · Cited by 106 · see citing works
Isakova, I. A., Lanclos, C., Bruhn, J., Kuroda, M. J., Baker, K. C., Krishnappa, V., & Phinney, D. G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087238 · Cited by 98 · see citing works
TNF‐α and IL‐1β sensitize human MSC for IFN‐γ signaling and enhance neutrophil recruitment
Hackel, A. M., Aksamit, A., Bruderek, K., Lang, S., & Brandau, S. (2020) · European Journal of Immunology · doi:10.1002/eji.201948336 · Cited by 88 · see citing works
Self-citationWeber, B., Emmert, M. Y., Behr, L., Schoenauer, R., Brokopp, C. E., Drögemüller, C., Modregger, P., Stampanoni, M., Vats, D., Rudin, M., et al. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2011.11.087 · Cited by 83 · see citing works
Mesenchymal Stromal Cells for Transplant Tolerance
Podestà, M. A., Remuzzi, G., & Casiraghi, F. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01287 · Cited by 82 · see citing works
Anti-Inflammatory and Immunomodulatory Activities of Stem Cells
Peroni, J. F., & Borjesson, D. L. (2011) · Veterinary Clinics of North America Equine Practice · doi:10.1016/j.cveq.2011.06.003 · Cited by 82 · see citing works
Osteoporosis and the Potential of Cell-Based Therapeutic Strategies
Macías, I., Alcorta-Sevillano, N., Rodrı́guez, C. I., & Infante, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051653 · Cited by 77 · see citing works
Role of the immune system in regeneration and its dynamic interplay with adult stem cells
Abnave, P., & Ghigo, É. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.04.002 · Cited by 78 · see citing works
The role of mesenchymal stem cells in cancer development
Yagi, H., & Kitagawa, Y. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00261 · Cited by 73 · see citing works
Walker, J., Schueller, K., Schäfer, L.-M., Pignitter, M., Esefelder, L., & Somoza, V. (2013) · Food & Function · doi:10.1039/c3fo60236b · Cited by 66 · see citing works
Mahmoudi, M., Taghavi-Farahabadi, M., Rezaei, N., & Hashemi, S. M. (2019) · International Immunopharmacology · doi:10.1016/j.intimp.2019.105689 · Cited by 65 · see citing works
Mesenchymal stromal cells for tolerance induction in organ transplantation
Casiraghi, F., Perico, N., & Remuzzi, G. (2017) · Human Immunology · doi:10.1016/j.humimm.2017.12.008 · Cited by 63 · see citing works
Chen, M., Peng, J., Xie, Q., Xiao, N., Su, X., Mei, H., Lu, Y., Zhou, J., Dai, Y., Wang, S., et al. (2019) · Stem Cells International · doi:10.1155/2019/6961052 · Cited by 63 · see citing works
Ward, C. L., Sánchez, C. J., Pollot, B. E., Romano, D. R., Hardy, S. K., Becerra, S. C., Rathbone, C. R., & Wenke, J. C. (2015) · BMC Microbiology · doi:10.1186/s12866-015-0412-x · Cited by 60 · see citing works
Barley grains for the production of endotoxin-free growth factors
Magnúsdóttir, A., Vidarsson, H., Björnsson, J. M., & Örvar, B. L. (2013) · Trends in biotechnology · doi:10.1016/j.tibtech.2013.06.002 · Cited by 59 · see citing works
Schwarz, S., Huss, R., Schulz‐Siegmund, M., Vogel, B., Brandau, S., Lang, S., & Rotter, N. (2014) · International Journal of Oral Science · doi:10.1038/ijos.2014.23 · Cited by 58 · see citing works
Self-citationZhang, J., Zhang, Y., Lv, H., Yu, Q., Zhou, Z., Zhu, Q., Wang, Z., Cooper, P. R., Smith, A. J., Niu, Z., et al. (2013) · Journal of Endodontics · doi:10.1016/j.joen.2013.07.018 · Cited by 55 · see citing works
Human mesenchymal stem cells protect neutrophils from serum-deprived cell death
Maqbool, M., Vidyadaran, S., George, E., & Ramasamy, R. (2011) · Cell Biology International · doi:10.1042/cbi20110070 · Cited by 53 · see citing works
Immunomodulatory effects of mesenchymal stem cells on leukocytes with emphasis on neutrophils
Salami, F., Tavassoli, A., Mehrzad, J., & Parham, A. (2018) · Immunobiology · doi:10.1016/j.imbio.2018.08.002 · Cited by 52 · see citing works
Yuan, Y., Lin, S., Guo, N., Zhao, C., Shen, S., Bu, X., & Ye, H. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.06.002 · Cited by 51 · see citing works
Naskou, M. C., Sumner, S. M., Chocallo, A. H., Kemelmakher, H., Thoresen, M., Copland, I. B., Galipeau, J., & Peroni, J. F. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0823-3 · Cited by 51 · see citing works
Kim, S. H., Das, A., Chai, J. C., Binas, B., Choi, M., Park, K. S., Lee, Y. S., Jung, K. H., & Chai, Y. G. (2016) · Scientific Reports · doi:10.1038/srep30311 · Cited by 48 · see citing works
Mesenchymal Stem Cell–Immune Cell Interaction and Related Modulations for Bone Tissue Engineering
Chen, R., Hao, Z., Wang, Y., Zhu, H., Hu, Y., Chen, T., Zhang, P., & Li, J. (2022) · Stem Cells International · doi:10.1155/2022/7153584 · Cited by 48 · see citing works
Healing the Broken Heart; The Immunomodulatory Effects of Stem Cell Therapy
Wagner, M. J., Khan, M., & Mohsin, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00639 · Cited by 47 · see citing works
Taghavi-Farahabadi, M., Mahmoudi, M., Rezaei, N., & Hashemi, S. M. (2020) · Immunological Investigations · doi:10.1080/08820139.2020.1801720 · Cited by 46 · see citing works
Dumitru, C. A., Hemeda, H., Jakob, M., Lang, S., & Brandau, S. (2014) · The FASEB Journal · doi:10.1096/fj.14-250159 · Cited by 43 · see citing works
Self-citationDorronsoro, A., Fernández‐Rueda, J., Fechter, K., Ferrin, I., Salcedo, J. M., Jakobsson, E., & Trigueros, C. (2013) · Bone Marrow Research · doi:10.1155/2013/203643 · Cited by 41 · see citing works
Brock, C. K., Hebert, K. L., Artiles, M., Wright, M. K., Cheng, T., Windsor, G. O., Nguyen, K., Alzoubi, M. S., Collins‐Burow, B. M., Martin, E. C., et al. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.751239 · Cited by 40 · see citing works
Interaction between Mesenchymal Stem Cells and Immune Cells during Bone Injury Repair
Xu, W., Yang, Y., Li, N., & Hua, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914484 · Cited by 39 · see citing works
Mesenchymal Stem Cells as Endogenous Regulators of Inflammation
Munir, H., Ward, L. S. C., & McGettrick, H. M. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-78127-3_5 · Cited by 36 · see citing works
Shushtari, N., & Froushani, S. M. A. (2017) · PubMed Central · doi:10.22074/cellj.2017.4364 · Cited by 36 · see citing works
Mahmoudi, M., Taghavi-Farahabadi, M., Namaki, S., Baghaei, K., Rayzan, E., Rezaei, N., & Hashemi, S. M. (2019) · Human Immunology · doi:10.1016/j.humimm.2019.10.006 · Cited by 36 · see citing works
Immunomodulatory functions of mesenchymal stem cells and possible mechanisms.
Wang, Q., Ding, G., & Xu, X. (2016) · PubMed · doi:10.14670/hh-11-750 · Cited by 35 · see citing works
BULUT, Ö., & GÜRSEL, İ. (2020) · TURKISH JOURNAL OF BIOLOGY · doi:10.3906/biy-2002-79 · Cited by 34 · see citing works
Dameshghi, S., Hosseini, A. Z., Soudi, S., Shirazi, F. J., Nojehdehi, S., & Hashemi, S. M. (2015) · Immunology Letters · doi:10.1016/j.imlet.2015.12.002 · Cited by 34 · see citing works
Misawa, M. Y. O., Silvério, K. G., Nociti, F. H., Albiero, M. L., Saito, M. T., Stipp, R. N., Condino‐Neto, A., Holzhausen, M., Palombo, H., & Villar, C. C. (2019) · Journal of Periodontology · doi:10.1002/jper.18-0220 · Cited by 32 · see citing works
Marinescu, C. I., Preda, M. B., & Burlacu, A. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02344-3 · Cited by 31 · see citing works
Ahn, S. Y., Maeng, Y., Kim, Y. R., Choe, Y. H., Hwang, H. S., & Hyun, Y. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-1559-4 · Cited by 30 · see citing works
Mesenchymal Stem Cells and Myeloid Derived Suppressor Cells: Common Traits in Immune Regulation
Lyadova, I. V., Sosunova, E., Николаев, А. А., & Nenasheva, T. A. (2016) · Journal of Immunology Research · doi:10.1155/2016/7121580 · Cited by 30 · see citing works
Alipour, R., Adib, M., Karimi, M. M., Hashemibeni, B., & Sereshki, N. (2013) · PubMed · Cited by 29 · see citing works
Kol, A., Walker, N. J., Galuppo, L. D., Clark, K. C., Buerchler, S., BERNANKE, A., & Borjesson, D. L. (2012) · Equine Veterinary Journal · doi:10.1111/j.2042-3306.2012.00600.x · Cited by 29 · see citing works
Meshes in a mess: Mesenchymal stem cell-based therapies for soft tissue reinforcement
Marinaro, F., Sanchez-Margallo, F. M., Álvarez, V., López, E., Tarazona, R., Brun, M. V., Blázquez, R., & Casado, J. G. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.11.042 · Cited by 27 · see citing works
Dubus, M., Varin, J., Papa, S., Rammal, H., Chevrier, J., Maisonneuve, E., Mauprivez, C., Mongaret, C., Gangloff, S. C., Reffuveille, F., et al. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.12.028 · Cited by 27 · see citing works
Park, Y. S., Lim, G.-W., Cho, K., Woo, S., Shin, M., Yoo, E., Ra, J. C., & Ryu, K. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.05.049 · Cited by 27 · see citing works
Thanunchai, M., Kanrai, P., Wiboon-ut, S., Puthavathana, P., Hongeng, S., & Thitithanyanont, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081805 · Cited by 27 · see citing works
Andalib, E., Kashfi, M., Mahmoudvand, G., Rezaei, E., Mahjoor, M., Torki, A., & Afkhami, H. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1251956 · Cited by 27 · see citing works
Brandau, S., Bruderek, K., Hestermann, K., Görtz, G.-E., Horstmann, M., Mattheis, S., Lang, S., Eckstein, A. K., & Berchner‐Pfannschmidt, U. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-16610 · Cited by 26 · see citing works
Self-citationMagne, B., Lataillade, J., & Trouillas, M. (2018) · Stem Cells and Development · doi:10.1089/scd.2018.0094 · Cited by 27 · see citing works
Liu, Y., Zhao, C., Zhang, R., Pang, Y., Li, L., & Feng, S. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03914-x · Cited by 25 · see citing works
Lange-Consiglio, A., Gusmara, C., Manfredi, E., Idda, A., Soggiù, A., Greco, V., Bonizzi, L., Cremonesi, F., & Zecconi, A. (2019) · Frontiers in Veterinary Science · doi:10.3389/fvets.2019.00443 · Cited by 25 · see citing works
Schuler, P. J., Westerkamp, A. M., Kansy, B., Bruderek, K., Dissmann, P. A., Dumitru, C. A., Lang, S., Jackson, E. K., & Brandau, S. (2016) · Immunobiology · doi:10.1016/j.imbio.2016.01.013 · Cited by 24 · see citing works
Self-citationAbbasi, A., Rahmani-Kukia, N., Froushani, S. M. A., & Hashemi, S. M. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.03.009 · Cited by 24 · see citing works
Mesenchymal Stem Cells in the Treatment of Amyotrophic Lateral Sclerosis
Hajivalili, M., Pourgholi, F., Kafil, H. S., Jadidi‐Niaragh, F., & Yousefi, M. (2016) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x10666150902095031 · Cited by 23 · see citing works
Taghavi-Farahabadi, M., Mahmoudi, M., Hashemi, S. M., & Rezaei, N. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106463 · Cited by 23 · see citing works
Khezri, S., Froushani, S. M. A., & Shahmoradi, M. (2017) · Immunological Investigations · doi:10.1080/08820139.2017.1391841 · Cited by 22 · see citing works
Mesenchymal Stem Cells and Tuberculosis: Clinical Challenges and Opportunities
Zhang, X., Xie, Q., Ye, Z., Li, Y., Che, Z., Huang, M., & Zeng, J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.695278 · Cited by 22 · see citing works
Periodontal ligament stem cells regulate apoptosis of neutrophils
Wang, Q., Ding, G., & Xu, X. (2017) · Open Medicine · doi:10.1515/med-2017-0004 · Cited by 22 · see citing works
Krajewska–Włodarczyk, M., Owczarczyk-Saczonek, A. B., Placek, W. J., Osowski, A., Engelgardt, P., & Wojtkiewicz, J. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms19010080 · Cited by 22 · see citing works
Involvement of Mesenchymal Stem Cells in Oral Mucosal Bacterial Immunotherapy
Vázquez, A., Fernández-Sevilla, L. M., Jiménez, E., Pérez-Cabrera, D., Yañez, R., Subiza, J. L., Varas, A., Valencia, J., & Vicente, Á. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.567391 · Cited by 21 · see citing works
Fast-tracking regenerative medicine for traumatic brain injury
Bonsack, B., Heyck, M., Kingsbury, C., Cozene, B., Sadanandan, N., Lee, J.-Y., & Borlongan, C. V. (2020) · Neural Regeneration Research · doi:10.4103/1673-5374.270294 · Cited by 20 · see citing works
Revolutionizing bone defect healing: the power of mesenchymal stem cells as seeds
Zhang, Y., Fan, M., & Zhang, Y. (2024) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2024.1421674 · Cited by 19 · see citing works
Evaluation of Immunomodulatory Properties of Feline Mesenchymal Stem Cells
Parys, M., Kruger, J. M., & Yuzbasiyan‐Gurkan, V. (2017) · Stem Cells and Development · doi:10.1089/scd.2016.0041 · Cited by 19 · see citing works
Caffeine alters the effects of bone marrow-derived mesenchymal stem cells on neutrophils
Abbasi, A., Froushani, S. M. A., Delirezh, N., & Mostafaei, A. (2018) · Advances in Clinical and Experimental Medicine · doi:10.17219/acem/78557 · Cited by 18 · see citing works
Taghavi-Farahabadi, M., Mahmoudi, M., Mahdaviani, S. A., Baghaei, K., Rayzan, E., Hashemi, S. M., & Rezaei, N. (2020) · Human Immunology · doi:10.1016/j.humimm.2020.05.009 · Cited by 18 · see citing works
Chen, H., Liu, Z., Yue, K., Ding, J., & He, Y. (2023) · Cell and Tissue Research · doi:10.1007/s00441-023-03743-z · Cited by 17 · see citing works
Henriques‐Pons, A., Beghini, D. G., Silva, V. S., Horita, S. I. M., & da Silva, F. A. B. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.780900 · Cited by 17 · see citing works
Zheng, Z., Xu, Y., Shi, Y., & Shao, C. (2022) · Cellular Immunology · doi:10.1016/j.cellimm.2022.104576 · Cited by 16 · see citing works
Improving the Wound Healing Process: Pivotal role of Mesenchymal stromal/stem Cells and Immune Cells
Sadeghi, M., Moghaddam, A., Amiri, A. M., Charoghdoozi, K., Mohammadi, M., Dehnavi, S., & Orazizadeh, M. (2025) · Stem Cell Reviews and Reports · doi:10.1007/s12015-025-10849-0 · Cited by 17 · see citing works
Mesenchymal Stem Cells in the Treatment of COVID-19, a Promising Future
Beghini, D. G., Horita, S. I. M., & Henriques‐Pons, A. (2021) · Cells · doi:10.3390/cells10102588 · Cited by 14 · see citing works
Ghaleh, H. E. G., Froushani, S. M. A., Ahangaran, N. A., & Hadai, S. N. (2018) · Immunological Investigations · doi:10.1080/08820139.2018.1458108 · Cited by 16 · see citing works
Kriebel, K., Hieke, C., Engelmann, R., Potempa, J., Müller‐Hilke, B., Lang, H., & Kreikemeyer, B. (2018) · Journal of Innate Immunity · doi:10.1159/000489020 · Cited by 15 · see citing works
Nicotine can modulate the effects of the mesenchymal stem cells on neutrophils
Pourtayeb, S., & Froushani, S. M. A. (2017) · Advances in Medical Sciences · doi:10.1016/j.advms.2016.07.006 · Cited by 15 · see citing works
Mesenchymal stem cell-derived extracellular vesicles, osteoimmunology and orthopedic diseases
Ma, M., Cui, G.-F., Liu, Y.-W., Tang, Y.-F., Lu, X.-S., Yue, C., & Zhang, X. (2023) · PeerJ · doi:10.7717/peerj.14677 · Cited by 13 · see citing works
Ghaleh, H. E. G., Delirezh, N., Froushani, S. M. A., & Ahangaran, N. A. (2014) · TURKISH JOURNAL OF BIOLOGY · doi:10.3906/biy-1310-40 · Cited by 14 · see citing works
Wang, C., Ge, F., Ge, F., Xu, Z., & Jiang, J. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04290-w · Cited by 13 · see citing works
Anti‐apoptotic effects of human gingival mesenchymal stromal cells on polymorphonuclear leucocytes
Blufstein, A., Behm, C., Kubin, B., Gahn, J., Moritz, A., Rausch‐Fan, X., & Andrukhov, O. (2021) · Oral Diseases · doi:10.1111/odi.13768 · Cited by 12 · see citing works
Even, K. M., Gaesser, A. M., Ciamillo, S. A., Linardi, R. L., & Ortved, K. F. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.958724 · Cited by 11 · see citing works
Mesenchymal Stem Cells: Immunology and Therapeutic Benefits
El, N. (2011) · InTech eBooks · doi:10.5772/21933 · Cited by 11 · see citing works
- Authors
- Brandau, S., Jakob, M., Hemeda, H., Bruderek, K., Janeschik, S., Bootz, F., & Lang, S.
- Affiliations
- Essen University Hospital (DE)
- University Hospital Bonn (DE)
- Corresponding author
- Brandau, Sven
- Venue
- Journal of Leukocyte Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-08-03
- Volume
- 88
- Issue
- 5
- Pages
- 1005-1015
- ISSN
- 0741-5400 (ISSN-L)
- 1938-3673
- OpenAlex
- W2112271653
- Cited by
- 155
- References
- 48
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 7 · 2022: 12 · 2021: 11 · 2020: 15 · 2019: 15 · 2018: 14 · 2017: 11 · 2016: 10 · 2015: 8 · 2014: 9 · 2013: 15 · 2012: 10
- FWCI
- 4.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Leukocyte Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Else-Kröner Fresenius Stiftung
- German Israeli Foundation
- Bartling Stiftung
- Topics
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- neutrophils, bacterial endotoxin, lipopolysaccharide, interleukin-8, macrophage migration inhibitory factor, chemokine receptor expression, neutrophil recruitment, inflammatory cytokines, neutrophil lifespan, innate immunity
- MeSH terms
- Bacterial Infections, Cell Movement, Chemotaxis, Leukocyte, Flow Cytometry, Humans, Inflammation, Lipopolysaccharides, Lymphocyte Activation, Neutrophils, Parotid Gland, Salivary Gland Diseases, T-Lymphocytes, Cytokines, Receptors, Chemokine, Reverse Transcriptase Polymerase Chain Reaction, 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