Bone marrow stromal cells attenuate sepsis via prostaglandin E2–dependent reprogramming of host macrophages to increase their interleukin-10 production
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Sepsis causes over 200,000 deaths yearly in the US; better treatments are urgently needed. Administering bone marrow stromal cells (BMSCs -- also known as mesenchymal stem cells) to mice before or shortly after inducing sepsis by cecal ligation and puncture reduced mortality and improved organ function. The beneficial effect of BMSCs was eliminated by macrophage depletion or pretreatment with antibodies specific for interleukin-10 (IL-10) or IL-10 receptor. Monocytes and/or macrophages from septic lungs made more IL-10 when prepared from mice treated with BMSCs versus untreated mice. Lipopolysaccharide (LPS)-stimulated macrophages produced more IL-10 when cultured with BMSCs, but this effect was eliminated if the BMSCs lacked the genes encoding Toll-like receptor 4, myeloid differentiation primary response gene-88, tumor necrosis factor (TNF) receptor-1a or cyclooxygenase-2. Our results suggest that BMSCs (activated by LPS or TNF-alpha) reprogram macrophages by releasing prostaglandin E(2) that acts on the macrophages through the prostaglandin EP2 and EP4 receptors. Because BMSCs have been successfully given to humans and can easily be cultured and might be used without human leukocyte antigen matching, we suggest that cultured, banked human BMSCs may be effective in treating sepsis in high-risk patient groups.
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In mouse sepsis models, PGE2 secretion of TNF-α-primed BM-MSCs reprograms macrophages to increase IL-10 to attenuate sepsis.
“This was observed in mouse sepsis models, through PGE2 secretion of TNF-α-primed BM-MSCs [70].”
From Mesenchymal stem cell secretome for regenerative medicine: Where do we stand? (2025) · cites this paper as [70]
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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
Le Blanc, K., Rasmusson, I., Sundberg, B., Götherström, C., Hassan, M., Uzunel, M., & Ringdén, O. (2004) · The Lancet · doi:10.1016/s0140-6736(04)16104-7 · Cited by 2,734 · 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
RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement
Shinkai, Y. (1992) · Cell · doi:10.1016/0092-8674(92)90029-c · Cited by 2,651 · see citing works
Chamberlain, G., Fox, J. M., Ashton, B. A., & Middleton, J. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0197 · Cited by 2,376 · see citing works
Bone Marrow Stromal Stem Cells: Nature, Biology, and Potential Applications
Bianco, P., Riminucci, M., Gronthos, S., & Robey, P. G. (2001) · Stem Cells · doi:10.1634/stemcells.19-3-180 · Cited by 1,944 · see citing works
Self-citationMoore, K. W., O’Garra, A., Malefyt, R. D. W., Vieira, P., & Mosmann, T. R. (1993) · Annual Review of Immunology · doi:10.1146/annurev.iy.11.040193.001121 · Cited by 1,883 · 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
Tögel, F., Hu, Z.-M., Weiss, K., Isaac, J., Lange, C., & Westenfelder, C. (2005) · AJP - Renal Physiology · doi:10.1152/ajprenal.00007.2005 · Cited by 1,196 · see citing works
Interactions Between Human Mesenchymal Stem Cells and Natural Killer Cells
Sotiropoulou, P. A., Perez, S. A., Gritzapis, A. D., Baxevanis, C. N., & Papamichail, M. (2006) · Stem Cells · doi:10.1634/stemcells.2004-0359 · Cited by 956 · see citing works
Imai, Y., Ibata, I., Ito, D., Ohsawa, K., & Kohsaka, S. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1112 · Cited by 872 · see citing works
Hata, A. N., & BREYER, R. M. (2004) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2004.06.003 · Cited by 839 · see citing works
Hubbard, W. J., Choudhry, M. A., Schwacha, M. G., Kerby, J. D., Rue, L. W., Bland, K. I., & Chaudry, I. H. (2005) · Shock · doi:10.1097/01.shk.0000191414.94461.7e · Cited by 801 · see citing works
Rougier, P. R., Adenis, A., Ducreux, M. P., Forni, M. D., Bonneterre, J. M., Dembak, M., Clouet, P., Lebecq, A., Baille, P., Lefresne-Soulas, F., et al. (2000) · European Journal of Cancer · doi:10.1016/s0959-8049(00)00072-1 · Cited by 751 · see citing works
Role of neutrophils in ischemia-reperfusion-induced microvascular injury
Hernandez, L. A., Grisham, M. B., Twohig, B., Arfors, K. ‐., Harlan, J. M., & Granger, D. N. (1987) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1987.253.3.h699 · Cited by 699 · see citing works
Jung, Y., Isaacs, J. S., Lee, S., Trepel, J. B., & Neckers, L. (2003) · The FASEB Journal · doi:10.1096/fj.03-0329fje · Cited by 680 · see citing works
Togel, F. E., Weiss, K., Yang, Y., Hu, Z., Zhang, P., & Westenfelder, C. S. (2007) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00339.2006 · Cited by 642 · 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
Mechanisms of neutrophil-induced parenchymal cell injury
Jaeschke, H., & Smith, C. W. (1997) · Journal of Leukocyte Biology · doi:10.1002/jlb.61.6.647 · Cited by 448 · see citing works
The ‘cytokine profile’: a code for sepsis
Ulloa, L., & Tracey, K. J. (2005) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2004.12.007 · Cited by 438 · see citing works
Habu, S., Fukui, H., Shimamura, K., Kasai, M., Nagai, Y., Okumura, K., & Tamaoki, N. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.127.1.34 · Cited by 426 · see citing works
Lange, C., Togel, F. E., Ittrich, H., Clayton, F. C., Nolte-Ernsting, C. C. A., Zander, A. R., & Westenfelder, C. S. (2005) · Kidney International · doi:10.1111/j.1523-1755.2005.00573.x · Cited by 413 · see citing works
van Rooijen, N., Sanders, A., & van den Berg, T. K. (1996) · Journal of Immunological Methods · doi:10.1016/0022-1759(96)00056-7 · Cited by 408 · see citing works
Immune modulation by mesenchymal stem cells
Rasmusson, I. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.03.019 · Cited by 374 · see citing works
Ajuebor, M. N., Das, A., Virág, L., Flower, R. J., Szabó, C., & Perretti, M. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.3.1685 · Cited by 300 · see citing works
In vivo effect of anti-asialo GM1 antibody on natural killer activity
Kasai, M., Yoneda, T., Habu, S., MARUYAMA, Y., Okumura, K., & Tokunaga, T. (1981) · Nature · doi:10.1038/291334a0 · Cited by 272 · see citing works
Ethyl pyruvate decreases sepsis-induced acute renal failure and multiple organ damage in aged mice
Miyaji, T., Hu, X., Yuen, P. S. T., Muramatsu, Y., Iyer, S. N., Hewitt, S. M., & Star, R. A. (2003) · Kidney International · doi:10.1046/j.1523-1755.2003.00268.x · Cited by 260 · see citing works
Self-citationSimvastatin improves sepsis-induced mortality and acute kidney injury via renal vascular effects.
Yasuda, H., Yuen, P. S. T., Hu, X., Zhou, H., & Star, R. A. (2006) · Kidney International · doi:10.1038/sj.ki.5000300 · Cited by 209 · see citing works
Self-citationPathogenesis of sepsis: new concepts and implications for future treatment
Bochud, P., & Calandra, T. (2003) · BMJ · doi:10.1136/bmj.326.7383.262 · Cited by 208 · see citing works
Ringdén, O. T. H., Uzunel, M., Sundberg, B., Lönnies, L., Nava, S., Gustafsson, J., Henningsohn, L., & Blanc, K. L. (2007) · Leukemia · doi:10.1038/sj.leu.2404833 · Cited by 208 · see citing works
Macrophages are a significant source of type 1 cytokines during mycobacterial infection
Wang, J., Wakeham, J., Harkness, R. E., & Xing, Z. (1999) · Journal of Clinical Investigation · doi:10.1172/jci6224 · Cited by 197 · see citing works
Shinomiya, S., Naraba, H., Ueno, A., Utsunomiya, I., Maruyama, T., Ohuchida, S., Ushikubi, F., Yuki, K., Narumiya, S., Sugimoto, Y., et al. (2001) · Biochemical Pharmacology · doi:10.1016/s0006-2952(01)00586-x · Cited by 172 · see citing works
Nakao, S., Ogtata, Y., Shimizu, E., Yamazaki, M., Furuyama, S., & Sugiya, H. (2002) · Molecular and Cellular Biochemistry · doi:10.1023/a:1019927616000 · Cited by 155 · see citing works
Multipotent mesenchymal stromal cells and immune tolerance
Noël, D., Djouad, F., Bouffi, C., Mrugala, D., & Jørgensen, C. (2007) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428190701361869 · Cited by 141 · see citing works
Crisostomo, P. R., Wang, M., Herring, C. M., Markel, T. A., Meldrum, K. K., Lillemoe, K. D., & Meldrum, D. R. (2006) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2006.09.016 · Cited by 129 · see citing works
Mesenchymal Stem Cells Ameliorate Tissue Damages Triggered by Renal Ischemia and Reperfusion Injury
Semedo, P., Wang, P., Andreucci, T. H., Cenedeze, M. A., Teixeira, V. P. A., dos Reis, M. A., Pacheco‐Silva, Á., & Câmara, N. O. S. (2007) · Transplantation Proceedings · doi:10.1016/j.transproceed.2007.01.036 · Cited by 127 · see citing works
Human mesenchymal stem cells are tolerized by mice and improve skin and spinal cord injuries
Mansilla, E., Marin, G. H., Sturla, F., Drago, H. E., Gil, M. A., Salas, E., Gardiner, M. C., Piccinelli, G., Bossi, S., Salas, E., et al. (2005) · Transplantation Proceedings · doi:10.1016/j.transproceed.2005.01.070 · Cited by 124 · see citing works
Matthijsen, R. A., Huugen, D., Hoebers, N., de Vries, B., Peutz‐Kootstra, C. J., Aratani, Y., Daha, M. R., Tervaert, J. W. C., Buurman, W. A., & Heeringa, P. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.070184 · Cited by 120 · see citing works
Transcriptional regulation of cyclo-oxygenase expression: three pillars of control.
Ramsay, R. G., Ciznadija, D., Vanevski, M., & Mantamadiotis, T. (2003) · PubMed · Cited by 109 · see citing works
Adult stem cells in the treatment of autoimmune diseases
van Laar, J. M., & Tyndall, A. (2006) · Lara D. Veeken · doi:10.1093/rheumatology/kel158 · Cited by 102 · see citing works
HUMAN MESENCHYMAL STEM CELLS ARE TOLERIZED BY MICE AND IMPROVE SKIN AND SPINAL CORD INJURIES.
Mansilla, E., Drago, H., Sturla, F., Gil, M. A., Marin, G. H., Salas, E., Gardiner, M. C., Iorio, G., Petrelli, L., Salas, E., et al. (2004) · Transplantation · doi:10.1097/00007890-200407271-01182 · Cited by 98 · see citing works
The neutrophil: one of the cellular targets of interleukin-10
Cassatella, M. A. (1998) · International Journal of Clinical & Laboratory Research · doi:10.1007/s005990050036 · Cited by 79 · see citing works
Perretti, M., Szabó, C., & Thiemermann, C. (1995) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1995.tb15061.x · Cited by 63 · see citing works
Leukocytes, the Janus cells in inflammatory disease
Nussler, A. K., Wittel, U. A., Nüssler, N. C., & Beger, H. G. (1999) · Langenbeck s Archives of Surgery · doi:10.1007/s004230050196 · Cited by 57 · see citing works
Kubo, S., Takahashi, H. K., Takei, M., Iwagaki, H., Yoshino, T., Tanaka, N., Mori, S., & Nishibori, M. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.062646 · Cited by 57 · see citing works
Pathogenesis of Septic Shock: Implications for Prevention and Treatment
Calandra, T. (2001) · Journal of Chemotherapy · doi:10.1179/joc.2001.13.supplement-2.173 · Cited by 55 · see citing works
Park, Y.-K., Ahn, D., Oh, M., Tae-Kyoung, L., Yang, E. G., Son, M., & Park, H. (2008) · Molecular Pharmacology · doi:10.1124/mol.108.045278 · Cited by 52 · see citing works
Bal‐Price, A., Gartlon, J., & Brown, G. C. (2005) · Nitric Oxide · doi:10.1016/j.niox.2005.10.002 · Cited by 39 · see citing works
P-Selectin Can Support Both Th1 and Th2 Lymphocyte Rolling in the Intestinal Microvasculature
Bonder, C. S., Norman, M. U., MacRae, T., Mangan, P. R., Weaver, C. T., Bullard, D. C., McCafferty, D., & Kubes, P. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)61248-5 · Cited by 37 · see citing works
Flagged first, then by citations
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Sorted by citations
Mesenchymal stem cell perspective: cell biology to clinical progress
Pittenger, M. F., Discher, D. E., Péault, B. M., Phinney, D. G., Hare, J. M., & Caplan, A. I. (2019) · npj Regenerative Medicine · doi:10.1038/s41536-019-0083-6 · Cited by 2,008 · see citing works
The immunopathology of sepsis and potential therapeutic targets
van der Poll, T., van de Veerdonk, F. L., Scicluna, B. P., & Netea, M. G. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.36 · Cited by 1,957 · see citing works
Mesenchymal Stromal Cells: Clinical Challenges and Therapeutic Opportunities
Galipeau, J., & Sensébé, L. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.05.004 · Cited by 1,819 · see citing works
The acute respiratory distress syndrome
Matthay, M. A., Ware, L. B., & Zimmerman, G. A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60331 · Cited by 1,706 · see citing works
Caplan, A. I., & Correa, D. (2011) · Cell Stem Cell · doi:10.1016/j.stem.2011.06.008 · Cited by 1,682 · see citing works
Islam, M. N., Das, S. R., Emin, M. T., Wei, M., Sun, L., Westphalen, K., Rowlands, D. J., Quadri, S. K., Bhattacharya, S., & Bhattacharya, J. (2012) · Nature Medicine · doi:10.1038/nm.2736 · Cited by 1,585 · see citing works
Krzyszczyk, P., Schloss, R. S., Palmer, A. F., & Francois Berthiaume, B. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00419 · Cited by 1,562 · see citing works
Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications
Wang, Y., Chen, X., Cao, W., & Shi, Y. (2014) · Nature Immunology · doi:10.1038/ni.3002 · Cited by 1,452 · see citing works
Mechanisms involved in the therapeutic properties of mesenchymal stem cells
da Silva Meirelles, L., Fontes, A. M., Covas, D. T., & Caplan, A. I. (2009) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.10.002 · Cited by 1,436 · see citing works
Mesenchymal stem cell secretome: toward cell-free therapeutic strategies in regenerative medicine
Vizoso, F., Eiro, N., Cid, S., Schneider, J., & Perez-Fernandez, R. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18091852 · Cited by 1,363 · 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
Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine
Murphy, M. B., Moncivais, K., & Caplan, A. I. (2013) · Experimental & Molecular Medicine · doi:10.1038/emm.2013.94 · Cited by 1,231 · see citing works
Waterman, R. S., Tomchuck, S. L., Henkle, S. L., & Betancourt, A. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010088 · Cited by 1,238 · see citing works
Immunoregulatory mechanisms of mesenchymal stem and stromal cells in inflammatory diseases
Shi, Y., Wang, Y., Li, Q., Liu, K., Hou, J., Shao, C., & Wang, Y. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0023-5 · Cited by 1,223 · see citing works
The Acute Respiratory Distress Syndrome: Pathogenesis and Treatment
Matthay, M. A., & Zemans, R. L. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011110-130158 · Cited by 1,085 · 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
Mesenchymal stem cell-macrophage crosstalk and bone healing
Pajarinen, J., Lin, T., Gibon, E., Kohno, Y., Maruyama, M., Nathan, K., Lu, L. Y., Yao, Z., & Goodman, S. B. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2017.12.025 · Cited by 1,011 · see citing works
Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs
Phinney, D. G., Di Giuseppe, M., Njah, J., Sala, E., Shiva, S., St Croix, C. M., Stolz, D. B., Watkins, S. C., Di, Y. P., Leikauf, G. D., et al. (2015) · Nature Communications · doi:10.1038/ncomms9472 · Cited by 1,007 · see citing works
Mesenchymal Stem Cell Immunomodulation: Mechanisms and Therapeutic Potential
Song, N., Scholtemeijer, M., & Shah, K. (2020) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2020.06.009 · Cited by 1,021 · see citing works
Mesenchymal stem cells: a new trend for cell therapy
Wei, X., Yang, X. F., Han, Z., Qu, F.-F., Shao, L., & Shi, Y. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2013.50 · Cited by 945 · see citing works
Mechanisms of mesenchymal stem/stromal cell function
Spees, J. L., Lee, R. H., & Gregory, C. A. (2016) · Stem Cell Research & Therapy · doi:10.1186/s13287-016-0363-7 · Cited by 893 · see citing works
Krasnodembskaya, A. D., Song, Y., Fang, X., Gupta, N., Serikov, V. B., Lee, J. W., & Matthay, M. A. (2010) · Stem Cells · doi:10.1002/stem.544 · Cited by 851 · see citing works
Mesenchymal Stem/Stromal Cells (MSCs): Role as Guardians of Inflammation
Prockop, D. J., & Youn Oh, J. (2012) · Molecular Therapy · doi:10.1038/mt.2011.211 · Cited by 816 · see citing works
Strioga, M. M., Viswanathan, S., Darinskas, A., Slabý, O., & Michálek, J. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0722 · Cited by 826 · see citing works
Harnessing the Mesenchymal Stem Cell Secretome for the Treatment of Cardiovascular Disease
Ranganath, S. H., Levy, O., Inamdar, M. S., & Karp, J. M. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.02.005 · Cited by 808 · see citing works
Morrison, T. J., Jackson, M. V., Cunningham, E. K., Kissenpfennig, A., McAuley, D. F., O’Kane, C. M., & Krasnodembskaya, A. D. (2017) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201701-0170oc · Cited by 796 · see citing works
Mesenchymal stem cell–educated macrophages: A novel type of alternatively activated macrophages
Kim, J., & Hematti, P. (2009) · Experimental Hematology · doi:10.1016/j.exphem.2009.09.004 · Cited by 785 · see citing works
Mesenchymal stromal cells: new directions
Keating, A. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.05.015 · Cited by 778 · see citing works
Immunobiology of mesenchymal stem cells
Ma, S., Xie, N., Li, W., Yuan, B., Shi, Y., & Wang, Y. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.158 · Cited by 772 · see citing works
Mesenchymal stem (stromal) cells for treatment of ARDS: a phase 1 clinical trial
Wilson, J. G., Liu, K. D., Zhuo, H., Caballero, L., McMillan, M., Fang, X., Cosgrove, K. M., Vojnik, R., Calfee, C. S., Lee, J. W., et al. (2014) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(14)70291-7 · Cited by 759 · see citing works
Mesenchymal Stem Cells as Therapeutics
Parekkadan, B., & Milwid, J. M. (2010) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-070909-105309 · Cited by 758 · see citing works
Zhang, Q., Shi, S., Liu, Y., Uyanne, J., Shi, Y., Shi, S., & Le, A. D. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0902318 · Cited by 753 · see citing works
Osteoimmunomodulation for the development of advanced bone biomaterials
Chen, Z.-T., Klein, T. J., Murray, R., Crawford, R., Chang, J., Wu, C.-T., & Xiao, Y. (2016) · Materials Today · doi:10.1016/j.mattod.2015.11.004 · Cited by 558 · see citing works
Mei, S. H. J., Haitsma, J. J., dos Santos, C. C., Deng, Y., Lai, P. F. H., Slutsky, A. S., Liles, W. C., & Stewart, D. J. (2010) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201001-0010oc · Cited by 721 · see citing works
Lee, J. W., Fang, X., Gupta, N., Serikov, V. B., & Matthay, M. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907996106 · Cited by 716 · see citing works
Mesenchymal Stem Cells: Mechanisms of Immunomodulation and Homing
Yagi, H., Soto–Gutiérrez, A., Parekkadan, B., Kitagawa, Y., Tompkins, R. G., Kobayashi, N., & Yarmush, M. L. (2010) · Cell Transplantation · doi:10.3727/096368910x508762 · Cited by 699 · see citing works
Weiß, A. R. R., & Dahlke, M. H. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01191 · Cited by 695 · see citing works
François, M., Romieu, R., Li, M., & Galipeau, J. (2011) · Molecular Therapy · doi:10.1038/mt.2011.189 · Cited by 694 · see citing works
Zhu, Y.-G., Feng, X.-M., Abbott, J., Fang, X.-H., Hao, Q., Monsel, A., Qu, J.-M., Matthay, M. A., & Lee, J. W. (2014) · Stem Cells · doi:10.1002/stem.1504 · Cited by 688 · see citing works
Spaggiari, G. M., Abdelrazik, H., Becchetti, F., & Moretta, L. (2009) · Blood · doi:10.1182/blood-2009-02-203943 · Cited by 670 · see citing works
Apoptosis in mesenchymal stromal cells induces in vivo recipient-mediated immunomodulation
Galleu, A., Riffo‐Vasquez, Y., Trento, C., Lomas, C., Dolcetti, L., Cheung, T. S., Bonin, M. V., Barbieri, L., Halai, K., Ward, S., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aam7828 · Cited by 647 · see citing works
Resolution of Inflammation: What Controls Its Onset?
Sugimoto, M. A., Sousa, L. P., Pinho, V., Perretti, M., & Teixeira, M. M. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00160 · Cited by 638 · see citing works
Choi, H., Lee, R. H., Bazhanov, N., Oh, J. Y., & Prockop, D. J. (2011) · Blood · doi:10.1182/blood-2010-12-327353 · Cited by 637 · see citing works
How mesenchymal stem cells interact with tissue immune responses
Shi, Y., Su, J., Roberts, A. I., Shou, P., Rabson, A. B., & Ren, G. (2012) · Trends in Immunology · doi:10.1016/j.it.2011.11.004 · Cited by 629 · see citing works
Zhang, Q.-Z., Su, W., Shi, S., Wilder-Smith, P. B. B., Xiang, A. P., Wong, A. K., Nguyen, A. L., Kwon, C. W., & Le, A. D. (2010) · Stem Cells · doi:10.1002/stem.503 · Cited by 620 · see citing works
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
Madrigal, M., Rao, K. S. J., & Riordan, N. H. (2014) · Journal of Translational Medicine · doi:10.1186/s12967-014-0260-8 · Cited by 615 · see citing works
Mesenchymal stem cell therapy: Two steps forward, one step back
Ankrum, J. A., & Karp, J. M. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.02.005 · Cited by 615 · see citing works
Innate immune responses to trauma
Huber-Lang, M. S., Lambris, J. D., & Ward, P. A. (2018) · Nature Immunology · doi:10.1038/s41590-018-0064-8 · Cited by 604 · see citing works
Mesenchymal stromal cell secretome: influencing therapeutic potential by cellular pre-conditioning
Ferreira, J. R., Teixeira, G. Q., Santos, S. G., Barbosa, M. A., Almeida-Porada, G., & Gonçalves, R. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02837 · Cited by 572 · 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
Macrophages as a therapeutic target to promote diabetic wound healing
Sharifiaghdam, M., Shaabani, E., Majidi, R. F., Smedt, S. C. D., Braeckmans, K., & Fraire, J. C. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.07.016 · Cited by 596 · see citing works
Diverse macrophage populations mediate acute lung inflammation and resolution
Aggarwal, N. R., King, L. S., & D’Alessio, F. R. (2014) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00341.2013 · Cited by 583 · see citing works
Jackson, M. V., Morrison, T. J., Doherty, D. F., McAuley, D. F., Matthay, M. A., Kissenpfennig, A., O'Kane, C. M., & Krasnodembskaya, A. D. (2016) · Stem Cells · doi:10.1002/stem.2372 · Cited by 582 · see citing works
Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair
Shi, Y., Hu, G., Su, J., Li, W., Chen, Q., Shou, P., Xu, C., Chen, X., Huang, Y., Zhu, Z., et al. (2010) · Cell Research · doi:10.1038/cr.2010.44 · Cited by 575 · 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
Maggini, J., Mirkin, G. A., Bognanni, I., Holmberg, J., Piazzón, I., Nepomnaschy, I., Costa, H., Cañones, C., Raiden, S., Vermeulen, M. E., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009252 · Cited by 568 · see citing works
Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy
Fan, X., Zhang, Y., Li, X., & Fu, Q. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03454-6 · Cited by 539 · see citing works
Skin tissue engineering: wound healing based on stem-cell-based therapeutic strategies
Dehkordi, A. N., Mirahmadi, F., Chehelgerdi, M., & Dehkordi, S. R. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1212-2 · Cited by 547 · see citing works
de Witte, S. F. H., Luk, F., Sierra Parraga, J. M., Gargesha, M., Merino, A., Korevaar, S. S., Shankar, A. S., O'Flynn, L., Elliman, S. J., Roy, D., et al. (2018) · Stem Cells · doi:10.1002/stem.2779 · Cited by 504 · see citing works
Sepsis and Acute Kidney Injury
Zarjou, A., & Agarwal, A. (2011) · Journal of the American Society of Nephrology · doi:10.1681/asn.2010050484 · Cited by 521 · see citing works
Mechanisms of mesenchymal stromal cell immunomodulation
English, K. (2012) · Immunology and Cell Biology · doi:10.1038/icb.2012.56 · Cited by 524 · see citing works
Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications
Ghannam, S., Bouffi, C., Djouad, F., Jorgensen, C., & Noël, D. (2010) · Stem Cell Research & Therapy · doi:10.1186/scrt2 · Cited by 507 · see citing works
Bone Marrow Stromal Cells Attenuate Lung Injury in a Murine Model of Neonatal Chronic Lung Disease
Aslam, M., Baveja, R., Liang, O. D., Fernandez‐Gonzalez, A., Lee, C., Mitsialis, S. A., & Kourembanas, S. (2009) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200902-0242oc · Cited by 510 · see citing works
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
Mesenchymal Stem Cell-Based Immunomodulation: Properties and Clinical Application
Wang, M., Yuan, Q., & Xie, L. (2018) · Stem Cells International · doi:10.1155/2018/3057624 · Cited by 506 · see citing works
Clinical applications of mesenchymal stem cells
Wang, S., Qu, X., & Zhao, R. C. (2012) · Journal of Hematology & Oncology · doi:10.1186/1756-8722-5-19 · Cited by 491 · see citing works
Song, Y., Dou, H., Li, X., Zhao, X., Li, Y., Liu, D., Ji, J., Liu, F., Ding, L., Ni, Y., et al. (2017) · Stem Cells · doi:10.1002/stem.2564 · Cited by 490 · see citing works
Krampera, M., Galipeau, J., Shi, Y., Tarte, K., & Sensebé, L. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.02.010 · Cited by 465 · see citing works
Frenette, P. S., Pinho, S., Lucas, D., & Scheiermann, C. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095919 · Cited by 462 · see citing works
Pathogenesis of Acute Respiratory Distress Syndrome
Huppert, L. A., Matthay, M. A., & Ware, L. B. (2019) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0039-1683996 · Cited by 459 · see citing works
Tumour-associated mesenchymal stem/stromal cells: emerging therapeutic targets
Shi, Y.-F., Du, L., Lin, L.-Y., & Wang, Y. (2016) · Nature reviews. Drug discovery · doi:10.1038/nrd.2016.193 · Cited by 409 · see citing works
Therapeutic Effects of Human Mesenchymal Stem Cell–derived Microvesicles in Severe Pneumonia in Mice
Monsel, A., Zhu, Y., Gennai, S., Qi, H., Hu, S., Rouby, J., Rosenzwajg, M., Matthay, M. A., & Lee, J. W. (2015) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201410-1765oc · Cited by 458 · see citing works
Anti‐inflammatory hydrogel dressings and skin wound healing
Huang, C., Dong, L., Zhao, B., Lu, Y., Huang, S., Yuan, Z., Luo, G., Xu, Y. X., & Qian, W. (2022) · Clinical and Translational Medicine · doi:10.1002/ctm2.1094 · Cited by 452 · see citing works
Xiao, L., Liu, L., Yang, J., Yu, Y., Chai, J., Wang, L., Ma, L., & Yin, H. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.04.030 · Cited by 451 · see citing works
The Life and Fate of Mesenchymal Stem Cells
Eggenhofer, E., Luk, F., Dahlke, M. H., & Hoogduijn, M. J. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00148 · Cited by 446 · see citing works
Concise Review: Mesenchymal Stem Cells for Acute Lung Injury: Role of Paracrine Soluble Factors
Lee, J. W., Fang, X., Krasnodembskaya, A. D., Howard, J. P., & Matthay, M. A. (2011) · Stem Cells · doi:10.1002/stem.643 · Cited by 430 · see citing works
YlÖstalo, J. H., Bartosh, T. J., Coble, K., & Prockop, D. J. (2012) · STEM CELLS · doi:10.1002/stem.1191 · Cited by 427 · see citing works
Articular fibrocartilage - Why does hyaline cartilage fail to repair?
Armiento, A. R., Alini, M., & Stoddart, M. J. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.12.015 · Cited by 413 · see citing works
Németh, K., Keane‐Myers, A., Brown, J. M., Metcalfe, D. D., Gorham, J. D., Bundoc, V., Hodges, M. G., Jelinek, I., Madala, S. K., Kárpáti, S., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910720107 · Cited by 407 · see citing works
Self-citationVasandan, A., Jahnavi, S., Shashank, C., Prasad, P., Kumar, A., & Prasanna, S. (2016) · Scientific Reports · doi:10.1038/srep38308 · Cited by 336 · see citing works
Tailoring Materials for Modulation of Macrophage Fate
Li, J., Jiang, X., Li, H., Gelinsky, M., & Gu, Z. (2021) · Advanced Materials · doi:10.1002/adma.202004172 · Cited by 402 · see citing works
Brennan, M. Á., Layrolle, P., & Mooney, D. J. (2020) · Advanced Functional Materials · doi:10.1002/adfm.201909125 · Cited by 397 · see citing works
Zhang, R., Liu, Y., Yan, K., Chen, L., Chen, X.-R., Li, P., Chen, F.-F., & Jiang, X.-D. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-106 · Cited by 377 · see citing works
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
Mesenchymal stromal cell therapies: immunomodulatory properties and clinical progress
Wu, X., Jiang, J., Gu, Z., Zhang, J., Chen, Y., & Liu, X. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01855-9 · Cited by 343 · see citing works
Biodistribution, migration and homing of systemically applied mesenchymal stem/stromal cells
Leibacher, J., & Henschler, R. (2016) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0271-2 · Cited by 368 · see citing works
ter Huurne, M., Schelbergen, R., Blattes, R., Blom, A., de Munter, W., Grevers, L., Jeanson, J., Noël, D., Casteilla, L., Jorgensen, C., et al. (2012) · Arthritis & Rheumatism · doi:10.1002/art.34626 · Cited by 369 · see citing works
Are Therapeutic Human Mesenchymal Stromal Cells Compatible with Human Blood?
Moll, G., Rasmusson‐Duprez, I., von Bahr, L., Connolly-Andersen, A.-M., Elgue, G., Funke, L., Hamad, O., Lönnies, H., Magnusson, P., Sánchez, J., et al. (2012) · Stem Cells · doi:10.1002/stem.1111 · Cited by 338 · see citing works
Abumaree, M., Jumah, M. A., Kalionis, B., Jawdat, D. M., Al-Khaldi, A., Abomaray, F., Fatani, A., Chamley, L., & Knawy, B. A. (2013) · Stem Cell Reviews and Reports · doi:10.1007/s12015-013-9455-2 · Cited by 354 · see citing works
MicroRNA Fingerprints Identify miR-150 as a Plasma Prognostic Marker in Patients with Sepsis
Vasilescu, C., Rossi, S., Shimizu, M., Tudor, Ș., Veronese, A., Ferracin, M., Nicoloso, M. S., Barbarotto, E., Popa, M., Stănciulea, O., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007405 · Cited by 354 · see citing works
Lee, J. W., Krasnodembskaya, A. D., McKenna, D. H., Song, Y., Abbott, J. A., & Matthay, M. A. (2013) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201206-0990oc · Cited by 353 · see citing works
Angele, M. K., Pratschke, S., Hubbard, W. J., & Chaudry, I. H. (2013) · Virulence · doi:10.4161/viru.26982 · Cited by 345 · see citing works
Manufacturing of primed mesenchymal stromal cells for therapy
Yin, J. Q., Zhu, J., & Ankrum, J. A. (2019) · Nature Biomedical Engineering · doi:10.1038/s41551-018-0325-8 · Cited by 345 · see citing works
Regulation and Repair of the Alveolar-Capillary Barrier in Acute Lung Injury
Bhattacharya, J., & Matthay, M. A. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-030212-183756 · Cited by 340 · see citing works
Wang, L., Ting, C.-H., Yen, M., Liu, K., Sytwu, H., Wu, K. K., & Yen, B. L. (2016) · Journal of Biomedical Science · doi:10.1186/s12929-016-0289-5 · Cited by 344 · see citing works
Immunomodulatory Biomaterials for Tissue Repair
Whitaker, R. C., Hernaez‐Estrada, B., Hernández, R. M., Santos‐Vizcaíno, E., & Spiller, K. L. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.0c00895 · Cited by 345 · see citing works
The Role of Stromal Stem Cells in Tissue Regeneration and Wound Repair
Stappenbeck, T. S., & Miyoshi, H. (2009) · Science · doi:10.1126/science.1172687 · Cited by 339 · see citing works
Khatri, M., Richardson, L. A., & Meulia, T. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0774-8 · Cited by 339 · 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
- Authors
- Németh, K., Leelahavanichkul, A., Yuen, P. S. T., Mayer, B., Parmelee, A., Doi, K., Robey, P. G., Leelahavanichkul, K., Koller, B. H., Brown, J. M., Hu, X., Jelinek, I., Star, R. A., & Mezey, É.
- Affiliations
- National Institutes of Health (US)
- National Institute of Diabetes and Digestive and Kidney Diseases (US)
- National Institute of Dental and Craniofacial Research (US)
- University of North Carolina at Chapel Hill (US)
- East Carolina University (US)
- Corresponding author
- Mezey, Éva
- ORCID
- Venue
- Nature Medicine
- Published
- 2008-11-21
- Volume
- 15
- Issue
- 1
- Pages
- 42-49
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC2706487
- OpenAlex
- W2111727066
- Cited by
- 2,364
- References
- 49
- Citations by year
- 2026: 52 · 2025: 60 · 2024: 82 · 2023: 131 · 2022: 138 · 2021: 167 · 2020: 186 · 2019: 171 · 2018: 176 · 2017: 148 · 2016: 201 · 2015: 167 · 2014: 172 · 2013: 148 · 2012: 144
- FWCI
- 32.25
- Type
- journal article
- Language
- en
- Update notices
- erratum (2009-04-01)
- Open access
- bronze
- doi.org
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- The Scholarship East Carolina University's Institutional Repository (East Carolina University) (submittedVersion)
- UNC Libraries
- Funders
- National Institutes of Health
- National Cancer Institute
- National Institute of Allergy and Infectious Diseases
- National Institute of Diabetes and Digestive and Kidney Diseases
- National Institute of Dental and Craniofacial Research (Z01DE000714)
- Topics
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Epidemiology › Sepsis Diagnosis and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- sepsis, mesenchymal stem cells, macrophage reprogramming, IL-10, prostaglandin E2, TLR4, MyD88, TNF receptor 1, cyclooxygenase-2, innate immunity, cecal ligation and puncture, immunomodulation
- MeSH terms
- Animals, Bone Marrow Cells, Cecal Diseases, Cecum, Humans, Macrophages, Male, Mice, Inbred BALB C, Mice, Inbred C57BL, Models, Biological, Transplantation, Wounds, Penetrating, Dinoprostone, Survival Analysis, Bone Marrow Transplantation, Interleukin-10, Stromal Cells, Sepsis, Mice, Cellular Reprogramming
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