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Bone marrow stromal cells use TGF-β to suppress allergic responses in a mouse model of ragweed-induced asthma
Bone marrow stromal cells [BMSCs; also known as mesenchymal stem cells (MSCs)] effectively suppress inflammatory responses in acute graft-versus-host disease in humans and in a number of disease models in mice. Many of the studies concluded that BMSC-driven immunomodulation is mediated by the suppre...
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| Published in: | Proceedings of the National Academy of Sciences - PNAS 2010-03, Vol.107 (12), p.5652-5657 |
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| creator | Nemeth, Krisztian Keane-Myers, Andrea Brown, Jared M Metcalfe, Dean D Gorham, Jared D Bundoc, Victor G Hodges, Marcus G Jelinek, Ivett Madala, Satish Karpati, Sarolta Mezey, Eva |
| description | Bone marrow stromal cells [BMSCs; also known as mesenchymal stem cells (MSCs)] effectively suppress inflammatory responses in acute graft-versus-host disease in humans and in a number of disease models in mice. Many of the studies concluded that BMSC-driven immunomodulation is mediated by the suppression of proinflammatory Th1 responses while rebalancing the Th1/Th2 ratio toward Th2. In this study, using a ragweed induced mouse asthma model, we studied if BMSCs could be beneficial in an allergic, Th2-dominant environment. When BMSCs were injected i.v. at the time of the antigen challenge, they protected the animals from the majority of asthma-specific pathological changes, including inhibition of eosinophil infiltration and excess mucus production in the lung, decreased levels of Th2 cytokines (IL-4, IL-5, and IL-13) in bronchial lavage, and lowered serum levels of Th2 immunoglobulins (IgG1 and IgE). To explore the mechanism of the effect we used BMSCs isolated from a variety of knockout mice, performed in vivo blocking of cytokines and studied the effect of asthmatic serum and bronchoalveolar lavage from ragweed challenged animals on the BMSCs in vitro. Our results suggest that IL-4 and/or IL-13 activate the STAT6 pathway in the BMSCs resulting in an increase of their TGF-β production, which seems to mediate the beneficial effect, either alone, or together with regulatory T cells, some of which might be recruited by the BMSCs. These data suggest that, in addition to focusing on graft-versus-host disease and autoimmune diseases, allergic conditions--specifically therapy resistant asthma--might also be a likely target of the recently discovered cellular therapy approach using BMSCs. |
| doi_str_mv | 10.1073/pnas.0910720107 |
| format | article |
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Many of the studies concluded that BMSC-driven immunomodulation is mediated by the suppression of proinflammatory Th1 responses while rebalancing the Th1/Th2 ratio toward Th2. In this study, using a ragweed induced mouse asthma model, we studied if BMSCs could be beneficial in an allergic, Th2-dominant environment. When BMSCs were injected i.v. at the time of the antigen challenge, they protected the animals from the majority of asthma-specific pathological changes, including inhibition of eosinophil infiltration and excess mucus production in the lung, decreased levels of Th2 cytokines (IL-4, IL-5, and IL-13) in bronchial lavage, and lowered serum levels of Th2 immunoglobulins (IgG1 and IgE). To explore the mechanism of the effect we used BMSCs isolated from a variety of knockout mice, performed in vivo blocking of cytokines and studied the effect of asthmatic serum and bronchoalveolar lavage from ragweed challenged animals on the BMSCs in vitro. Our results suggest that IL-4 and/or IL-13 activate the STAT6 pathway in the BMSCs resulting in an increase of their TGF-β production, which seems to mediate the beneficial effect, either alone, or together with regulatory T cells, some of which might be recruited by the BMSCs. These data suggest that, in addition to focusing on graft-versus-host disease and autoimmune diseases, allergic conditions--specifically therapy resistant asthma--might also be a likely target of the recently discovered cellular therapy approach using BMSCs.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0910720107</identifier><identifier>PMID: 20231466</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Allergies ; Ambrosia - adverse effects ; Ambrosia - immunology ; Animals ; Asthma ; Asthma - etiology ; Asthma - immunology ; Asthma - pathology ; Asthma - therapy ; Biological Sciences ; Bronchoalveolar Lavage Fluid - cytology ; Bronchoalveolar Lavage Fluid - immunology ; Cytokines ; Cytokines - deficiency ; Cytokines - genetics ; Cytokines - metabolism ; Disease models ; Disease Models, Animal ; Eosinophils ; Humans ; Immunosuppression ; In Vitro Techniques ; Lung - immunology ; Lung - pathology ; Lungs ; Mast cells ; Mesenchymal Stem Cell Transplantation ; Mesenchymal stem cells ; Mesenchymal Stromal Cells - immunology ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Stromal cells ; T lymphocytes ; Th2 Cells - immunology ; Transforming Growth Factor beta - immunology ; Transplantation, Homologous ; Transplantation, Isogeneic</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2010-03, Vol.107 (12), p.5652-5657</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c494t-2fbb0f550157e61e7adc5ace7033708d1c9f75d23c95e1638e5c92b2d639245c3</citedby><cites>FETCH-LOGICAL-c494t-2fbb0f550157e61e7adc5ace7033708d1c9f75d23c95e1638e5c92b2d639245c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/107/12.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25665035$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25665035$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,53827,53829,58593,58826</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20231466$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nemeth, Krisztian</creatorcontrib><creatorcontrib>Keane-Myers, Andrea</creatorcontrib><creatorcontrib>Brown, Jared M</creatorcontrib><creatorcontrib>Metcalfe, Dean D</creatorcontrib><creatorcontrib>Gorham, Jared D</creatorcontrib><creatorcontrib>Bundoc, Victor G</creatorcontrib><creatorcontrib>Hodges, Marcus G</creatorcontrib><creatorcontrib>Jelinek, Ivett</creatorcontrib><creatorcontrib>Madala, Satish</creatorcontrib><creatorcontrib>Karpati, Sarolta</creatorcontrib><creatorcontrib>Mezey, Eva</creatorcontrib><title>Bone marrow stromal cells use TGF-β to suppress allergic responses in a mouse model of ragweed-induced asthma</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Bone marrow stromal cells [BMSCs; also known as mesenchymal stem cells (MSCs)] effectively suppress inflammatory responses in acute graft-versus-host disease in humans and in a number of disease models in mice. Many of the studies concluded that BMSC-driven immunomodulation is mediated by the suppression of proinflammatory Th1 responses while rebalancing the Th1/Th2 ratio toward Th2. In this study, using a ragweed induced mouse asthma model, we studied if BMSCs could be beneficial in an allergic, Th2-dominant environment. When BMSCs were injected i.v. at the time of the antigen challenge, they protected the animals from the majority of asthma-specific pathological changes, including inhibition of eosinophil infiltration and excess mucus production in the lung, decreased levels of Th2 cytokines (IL-4, IL-5, and IL-13) in bronchial lavage, and lowered serum levels of Th2 immunoglobulins (IgG1 and IgE). To explore the mechanism of the effect we used BMSCs isolated from a variety of knockout mice, performed in vivo blocking of cytokines and studied the effect of asthmatic serum and bronchoalveolar lavage from ragweed challenged animals on the BMSCs in vitro. Our results suggest that IL-4 and/or IL-13 activate the STAT6 pathway in the BMSCs resulting in an increase of their TGF-β production, which seems to mediate the beneficial effect, either alone, or together with regulatory T cells, some of which might be recruited by the BMSCs. These data suggest that, in addition to focusing on graft-versus-host disease and autoimmune diseases, allergic conditions--specifically therapy resistant asthma--might also be a likely target of the recently discovered cellular therapy approach using BMSCs.</description><subject>Allergies</subject><subject>Ambrosia - adverse effects</subject><subject>Ambrosia - immunology</subject><subject>Animals</subject><subject>Asthma</subject><subject>Asthma - etiology</subject><subject>Asthma - immunology</subject><subject>Asthma - pathology</subject><subject>Asthma - therapy</subject><subject>Biological Sciences</subject><subject>Bronchoalveolar Lavage Fluid - cytology</subject><subject>Bronchoalveolar Lavage Fluid - immunology</subject><subject>Cytokines</subject><subject>Cytokines - deficiency</subject><subject>Cytokines - genetics</subject><subject>Cytokines - metabolism</subject><subject>Disease models</subject><subject>Disease Models, Animal</subject><subject>Eosinophils</subject><subject>Humans</subject><subject>Immunosuppression</subject><subject>In Vitro Techniques</subject><subject>Lung - immunology</subject><subject>Lung - pathology</subject><subject>Lungs</subject><subject>Mast cells</subject><subject>Mesenchymal Stem Cell Transplantation</subject><subject>Mesenchymal stem cells</subject><subject>Mesenchymal Stromal Cells - immunology</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Stromal cells</subject><subject>T lymphocytes</subject><subject>Th2 Cells - immunology</subject><subject>Transforming Growth Factor beta - immunology</subject><subject>Transplantation, Homologous</subject><subject>Transplantation, Isogeneic</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><recordid>eNpVkcFu1DAQhi1ERZfCmRPgG6e0Yzu24wtSqWhBqtRD27PldSbbVEkc7ISK1-JB-kx1tEuXXmyP_P3_ePwT8oHBMQMtTsbBpWMw-cwhL6_IiuWqUKWB12QFwHVRlbw8JG9TugcAIyt4Qw45cMFKpVZk-BYGpL2LMTzQNMXQu4567LpE54T05uK8ePxLp0DTPI4RU6Ku6zBuWk9zNYYhYaLtQB3twyLoQ40dDQ2NbvOAWBftUM8ea-rSdNe7d-SgcV3C97v9iNyef785-1FcXl38PDu9LHxpyqngzXoNjZTApEbFULvaS-dRgxAaqpp502hZc-GNRKZEhdIbvua1EoaX0osj8nXrO87rHmuPwxRdZ8fY5lH_2OBa-_JmaO_sJvy2vJJMyyobfNkZxPBrxjTZvk3Lv7gB86BWC1GBBK0yebIlfQwpRWyeuzCwS0h2CcnuQ8qKT_8_7pn_l0oGPu-ARbm305ZxK5Xkmfi4Je7TFOLeQSolQci9Q-OCdZvYJnt7nbsLYBUzRnPxBBi0rS4</recordid><startdate>20100323</startdate><enddate>20100323</enddate><creator>Nemeth, Krisztian</creator><creator>Keane-Myers, Andrea</creator><creator>Brown, Jared M</creator><creator>Metcalfe, Dean D</creator><creator>Gorham, Jared D</creator><creator>Bundoc, Victor G</creator><creator>Hodges, Marcus G</creator><creator>Jelinek, Ivett</creator><creator>Madala, Satish</creator><creator>Karpati, Sarolta</creator><creator>Mezey, Eva</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20100323</creationdate><title>Bone marrow stromal cells use TGF-β to suppress allergic responses in a mouse model of ragweed-induced asthma</title><author>Nemeth, Krisztian ; Keane-Myers, Andrea ; Brown, Jared M ; Metcalfe, Dean D ; Gorham, Jared D ; Bundoc, Victor G ; Hodges, Marcus G ; Jelinek, Ivett ; Madala, Satish ; Karpati, Sarolta ; Mezey, Eva</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c494t-2fbb0f550157e61e7adc5ace7033708d1c9f75d23c95e1638e5c92b2d639245c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Allergies</topic><topic>Ambrosia - adverse effects</topic><topic>Ambrosia - immunology</topic><topic>Animals</topic><topic>Asthma</topic><topic>Asthma - etiology</topic><topic>Asthma - immunology</topic><topic>Asthma - pathology</topic><topic>Asthma - therapy</topic><topic>Biological Sciences</topic><topic>Bronchoalveolar Lavage Fluid - cytology</topic><topic>Bronchoalveolar Lavage Fluid - immunology</topic><topic>Cytokines</topic><topic>Cytokines - deficiency</topic><topic>Cytokines - genetics</topic><topic>Cytokines - metabolism</topic><topic>Disease models</topic><topic>Disease Models, Animal</topic><topic>Eosinophils</topic><topic>Humans</topic><topic>Immunosuppression</topic><topic>In Vitro Techniques</topic><topic>Lung - immunology</topic><topic>Lung - pathology</topic><topic>Lungs</topic><topic>Mast cells</topic><topic>Mesenchymal Stem Cell Transplantation</topic><topic>Mesenchymal stem cells</topic><topic>Mesenchymal Stromal Cells - immunology</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Stromal cells</topic><topic>T lymphocytes</topic><topic>Th2 Cells - immunology</topic><topic>Transforming Growth Factor beta - immunology</topic><topic>Transplantation, Homologous</topic><topic>Transplantation, Isogeneic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nemeth, Krisztian</creatorcontrib><creatorcontrib>Keane-Myers, Andrea</creatorcontrib><creatorcontrib>Brown, Jared M</creatorcontrib><creatorcontrib>Metcalfe, Dean D</creatorcontrib><creatorcontrib>Gorham, Jared D</creatorcontrib><creatorcontrib>Bundoc, Victor G</creatorcontrib><creatorcontrib>Hodges, Marcus G</creatorcontrib><creatorcontrib>Jelinek, Ivett</creatorcontrib><creatorcontrib>Madala, Satish</creatorcontrib><creatorcontrib>Karpati, Sarolta</creatorcontrib><creatorcontrib>Mezey, Eva</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nemeth, Krisztian</au><au>Keane-Myers, Andrea</au><au>Brown, Jared M</au><au>Metcalfe, Dean D</au><au>Gorham, Jared D</au><au>Bundoc, Victor G</au><au>Hodges, Marcus G</au><au>Jelinek, Ivett</au><au>Madala, Satish</au><au>Karpati, Sarolta</au><au>Mezey, Eva</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bone marrow stromal cells use TGF-β to suppress allergic responses in a mouse model of ragweed-induced asthma</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2010-03-23</date><risdate>2010</risdate><volume>107</volume><issue>12</issue><spage>5652</spage><epage>5657</epage><pages>5652-5657</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Edited* by Susan E. Leeman, Boston University School of Medicine, Boston, MA, and approved January 22, 2010 (received for review September 18, 2009)</notes><notes>Author contributions: K.N., A.K.-M., D.D.M., and E.M. designed research; K.N., A.K.-M., J.M.B., V.G.B., S.M., and M.G.H. performed research; D.D.M., J.D.G., and I.J. contributed new reagents/analytic tools; K.N., A.K.-M., J.M.B., I.J., S.K., and E.M. analyzed data; and K.N. and E.M. wrote the paper.</notes><abstract>Bone marrow stromal cells [BMSCs; also known as mesenchymal stem cells (MSCs)] effectively suppress inflammatory responses in acute graft-versus-host disease in humans and in a number of disease models in mice. Many of the studies concluded that BMSC-driven immunomodulation is mediated by the suppression of proinflammatory Th1 responses while rebalancing the Th1/Th2 ratio toward Th2. In this study, using a ragweed induced mouse asthma model, we studied if BMSCs could be beneficial in an allergic, Th2-dominant environment. When BMSCs were injected i.v. at the time of the antigen challenge, they protected the animals from the majority of asthma-specific pathological changes, including inhibition of eosinophil infiltration and excess mucus production in the lung, decreased levels of Th2 cytokines (IL-4, IL-5, and IL-13) in bronchial lavage, and lowered serum levels of Th2 immunoglobulins (IgG1 and IgE). To explore the mechanism of the effect we used BMSCs isolated from a variety of knockout mice, performed in vivo blocking of cytokines and studied the effect of asthmatic serum and bronchoalveolar lavage from ragweed challenged animals on the BMSCs in vitro. Our results suggest that IL-4 and/or IL-13 activate the STAT6 pathway in the BMSCs resulting in an increase of their TGF-β production, which seems to mediate the beneficial effect, either alone, or together with regulatory T cells, some of which might be recruited by the BMSCs. These data suggest that, in addition to focusing on graft-versus-host disease and autoimmune diseases, allergic conditions--specifically therapy resistant asthma--might also be a likely target of the recently discovered cellular therapy approach using BMSCs.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>20231466</pmid><doi>10.1073/pnas.0910720107</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| source | PubMed (Medline); JSTOR |
| subjects | Allergies Ambrosia - adverse effects Ambrosia - immunology Animals Asthma Asthma - etiology Asthma - immunology Asthma - pathology Asthma - therapy Biological Sciences Bronchoalveolar Lavage Fluid - cytology Bronchoalveolar Lavage Fluid - immunology Cytokines Cytokines - deficiency Cytokines - genetics Cytokines - metabolism Disease models Disease Models, Animal Eosinophils Humans Immunosuppression In Vitro Techniques Lung - immunology Lung - pathology Lungs Mast cells Mesenchymal Stem Cell Transplantation Mesenchymal stem cells Mesenchymal Stromal Cells - immunology Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout Stromal cells T lymphocytes Th2 Cells - immunology Transforming Growth Factor beta - immunology Transplantation, Homologous Transplantation, Isogeneic |
| title | Bone marrow stromal cells use TGF-β to suppress allergic responses in a mouse model of ragweed-induced asthma |
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