Schistosoma mansoni Soluble Egg Antigens Induce Expression of the Negative Regulators SOCS1 and SHP1 in Human Dendritic Cells via Interaction with the Mannose Receptor
Schistosomiasis is a common debilitating human parasitic disease in (sub)tropical areas, however, schistosome infections can also protect against a variety of inflammatory diseases. This has raised broad interest in the mechanisms by which Schistosoma modulate the immune system into an anti-inflamma...
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description | Schistosomiasis is a common debilitating human parasitic disease in (sub)tropical areas, however, schistosome infections can also protect against a variety of inflammatory diseases. This has raised broad interest in the mechanisms by which Schistosoma modulate the immune system into an anti-inflammatory and regulatory state. Human dendritic cells (DCs) show many phenotypic changes upon contact with Schistosoma mansoni soluble egg antigens (SEA). We here show that oxidation of SEA glycans, but not heat-denaturation, abrogates the capacity of SEA to suppress both LPS-induced cytokine secretion and DC proliferation, indicating an important role of SEA glycans in these processes. Remarkably, interaction of SEA glycans with DCs results in a strongly increased expression of Suppressor Of Cytokine Signalling1 (SOCS1) and SH2-containing protein tyrosine Phosphatase-1 (SHP1), important negative regulators of TLR4 signalling. In addition, SEA induces the secretion of transforming growth factor β (TGF-β), and the surface expression of the costimulatory molecules Programmed Death Ligand-1 (PD-L1) and OX40 ligand (OX40L), which are known phenotypic markers for the capacity of DCs to polarize naïve T cells into Th2/Treg cell subsets. Inhibition of mannose receptor (MR)-mediated internalization of SEA into DCs by blocking with allyl α-D-mannoside or anti-MR antibodies, significantly reduced SOCS1 and SHP1 expression. In conclusion, we demonstrate that SEA glycans are essential for induction of enhanced SOCS1 and SHP1 levels in DCs via the MR. Our data provide novel mechanistic evidence for the potential of S. mansoni SEA glycans to modulate human DCs, which may contribute to the capacity of SEA to down-regulate inflammatory responses. |
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This has raised broad interest in the mechanisms by which Schistosoma modulate the immune system into an anti-inflammatory and regulatory state. Human dendritic cells (DCs) show many phenotypic changes upon contact with Schistosoma mansoni soluble egg antigens (SEA). We here show that oxidation of SEA glycans, but not heat-denaturation, abrogates the capacity of SEA to suppress both LPS-induced cytokine secretion and DC proliferation, indicating an important role of SEA glycans in these processes. Remarkably, interaction of SEA glycans with DCs results in a strongly increased expression of Suppressor Of Cytokine Signalling1 (SOCS1) and SH2-containing protein tyrosine Phosphatase-1 (SHP1), important negative regulators of TLR4 signalling. In addition, SEA induces the secretion of transforming growth factor β (TGF-β), and the surface expression of the costimulatory molecules Programmed Death Ligand-1 (PD-L1) and OX40 ligand (OX40L), which are known phenotypic markers for the capacity of DCs to polarize naïve T cells into Th2/Treg cell subsets. Inhibition of mannose receptor (MR)-mediated internalization of SEA into DCs by blocking with allyl α-D-mannoside or anti-MR antibodies, significantly reduced SOCS1 and SHP1 expression. In conclusion, we demonstrate that SEA glycans are essential for induction of enhanced SOCS1 and SHP1 levels in DCs via the MR. Our data provide novel mechanistic evidence for the potential of S. mansoni SEA glycans to modulate human DCs, which may contribute to the capacity of SEA to down-regulate inflammatory responses.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0124089</identifier><identifier>PMID: 25897665</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antibodies ; Antigens ; Antigens, Helminth - immunology ; Apoptosis ; B7-H1 Antigen - genetics ; B7-H1 Antigen - metabolism ; Biology ; Bone morphogenetic proteins ; Cells, Cultured ; Costimulator ; Cytokines ; Denaturation ; Dendritic cells ; Dendritic Cells - metabolism ; Dendritic Cells - parasitology ; Disease ; Down-regulation ; Gene Expression ; Genotype & phenotype ; Health aspects ; Host-Parasite Interactions ; Humans ; Immune system ; Immunology ; Infections ; Inflammatory bowel disease ; Inflammatory diseases ; Internalization ; Lectins ; Lectins, C-Type - metabolism ; Ligands ; Lipopolysaccharides ; Lipopolysaccharides - pharmacology ; Lymphocytes ; Lymphocytes T ; Mannose ; Mannose-Binding Lectins - metabolism ; Monosaccharides ; Multiple sclerosis ; Ovum - immunology ; OX40 Ligand - genetics ; OX40 Ligand - metabolism ; Ox40L protein ; Oxidation ; Parasitic diseases ; PD-L1 protein ; Polysaccharides ; Protein denaturation ; Protein Tyrosine Phosphatase, Non-Receptor Type 6 - genetics ; Protein Tyrosine Phosphatase, Non-Receptor Type 6 - metabolism ; Protein-tyrosine-phosphatase ; Receptors, Cell Surface - metabolism ; Regulation ; Schistosoma mansoni - immunology ; Schistosomiasis ; SHP-1 protein ; Signaling ; SOCS-1 protein ; Suppressor of Cytokine Signaling 1 Protein ; Suppressor of Cytokine Signaling Proteins - genetics ; Suppressor of Cytokine Signaling Proteins - metabolism ; T cells ; TLR4 protein ; Toll-like receptors ; Transcriptional Activation ; Transforming growth factor ; Transforming growth factor-b ; Transforming growth factors ; Tumor necrosis factor ; Tyrosine</subject><ispartof>PloS one, 2015-04, Vol.10 (4), p.e0124089-e0124089</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Klaver et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Klaver et al 2015 Klaver et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-22863a61158b89f3f251eab65d9e13ed23fa842245fc09b8ed041eb7b758afd83</citedby><cites>FETCH-LOGICAL-c692t-22863a61158b89f3f251eab65d9e13ed23fa842245fc09b8ed041eb7b758afd83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4405200/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4405200/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25897665$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gobert, Geoffrey N.</contributor><creatorcontrib>Klaver, Elsenoor J</creatorcontrib><creatorcontrib>Kuijk, Loes M</creatorcontrib><creatorcontrib>Lindhorst, Thisbe K</creatorcontrib><creatorcontrib>Cummings, Richard D</creatorcontrib><creatorcontrib>van Die, Irma</creatorcontrib><title>Schistosoma mansoni Soluble Egg Antigens Induce Expression of the Negative Regulators SOCS1 and SHP1 in Human Dendritic Cells via Interaction with the Mannose Receptor</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Schistosomiasis is a common debilitating human parasitic disease in (sub)tropical areas, however, schistosome infections can also protect against a variety of inflammatory diseases. This has raised broad interest in the mechanisms by which Schistosoma modulate the immune system into an anti-inflammatory and regulatory state. Human dendritic cells (DCs) show many phenotypic changes upon contact with Schistosoma mansoni soluble egg antigens (SEA). We here show that oxidation of SEA glycans, but not heat-denaturation, abrogates the capacity of SEA to suppress both LPS-induced cytokine secretion and DC proliferation, indicating an important role of SEA glycans in these processes. Remarkably, interaction of SEA glycans with DCs results in a strongly increased expression of Suppressor Of Cytokine Signalling1 (SOCS1) and SH2-containing protein tyrosine Phosphatase-1 (SHP1), important negative regulators of TLR4 signalling. In addition, SEA induces the secretion of transforming growth factor β (TGF-β), and the surface expression of the costimulatory molecules Programmed Death Ligand-1 (PD-L1) and OX40 ligand (OX40L), which are known phenotypic markers for the capacity of DCs to polarize naïve T cells into Th2/Treg cell subsets. Inhibition of mannose receptor (MR)-mediated internalization of SEA into DCs by blocking with allyl α-D-mannoside or anti-MR antibodies, significantly reduced SOCS1 and SHP1 expression. In conclusion, we demonstrate that SEA glycans are essential for induction of enhanced SOCS1 and SHP1 levels in DCs via the MR. Our data provide novel mechanistic evidence for the potential of S. mansoni SEA glycans to modulate human DCs, which may contribute to the capacity of SEA to down-regulate inflammatory responses.</description><subject>Animals</subject><subject>Antibodies</subject><subject>Antigens</subject><subject>Antigens, Helminth - immunology</subject><subject>Apoptosis</subject><subject>B7-H1 Antigen - genetics</subject><subject>B7-H1 Antigen - metabolism</subject><subject>Biology</subject><subject>Bone morphogenetic proteins</subject><subject>Cells, Cultured</subject><subject>Costimulator</subject><subject>Cytokines</subject><subject>Denaturation</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - metabolism</subject><subject>Dendritic Cells - parasitology</subject><subject>Disease</subject><subject>Down-regulation</subject><subject>Gene Expression</subject><subject>Genotype & phenotype</subject><subject>Health aspects</subject><subject>Host-Parasite Interactions</subject><subject>Humans</subject><subject>Immune system</subject><subject>Immunology</subject><subject>Infections</subject><subject>Inflammatory bowel disease</subject><subject>Inflammatory diseases</subject><subject>Internalization</subject><subject>Lectins</subject><subject>Lectins, C-Type - metabolism</subject><subject>Ligands</subject><subject>Lipopolysaccharides</subject><subject>Lipopolysaccharides - pharmacology</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Mannose</subject><subject>Mannose-Binding Lectins - metabolism</subject><subject>Monosaccharides</subject><subject>Multiple sclerosis</subject><subject>Ovum - immunology</subject><subject>OX40 Ligand - genetics</subject><subject>OX40 Ligand - metabolism</subject><subject>Ox40L protein</subject><subject>Oxidation</subject><subject>Parasitic diseases</subject><subject>PD-L1 protein</subject><subject>Polysaccharides</subject><subject>Protein denaturation</subject><subject>Protein Tyrosine Phosphatase, Non-Receptor Type 6 - genetics</subject><subject>Protein Tyrosine Phosphatase, Non-Receptor Type 6 - metabolism</subject><subject>Protein-tyrosine-phosphatase</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>Regulation</subject><subject>Schistosoma mansoni - immunology</subject><subject>Schistosomiasis</subject><subject>SHP-1 protein</subject><subject>Signaling</subject><subject>SOCS-1 protein</subject><subject>Suppressor of Cytokine Signaling 1 Protein</subject><subject>Suppressor of Cytokine Signaling Proteins - genetics</subject><subject>Suppressor of Cytokine Signaling Proteins - metabolism</subject><subject>T cells</subject><subject>TLR4 protein</subject><subject>Toll-like receptors</subject><subject>Transcriptional Activation</subject><subject>Transforming growth factor</subject><subject>Transforming growth factor-b</subject><subject>Transforming growth factors</subject><subject>Tumor necrosis factor</subject><subject>Tyrosine</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk19v0zAQwCMEYmPwDRBYQkLw0OI_ieO8IFVl0EqDoRV4tRznkrpK7WI7Y3wiviZu100r2gPKQ6LL737OXe6y7DnBY8JK8m7lBm9VP944C2NMaI5F9SA7JhWjI04xe3jn-Sh7EsIK44IJzh9nR7QQVcl5cZz9WeilCdEFt1ZorWxw1qCF64e6B3TadWhio-nABjS3zaBT7GrjIQTjLHItiktAX6BT0VwCuoBu6FV0PqDF-XRBkLINWsy-EmQsmg3Jjj6AbbyJRqMp9H1Al0YlcQSvdNwqf5m43Ek_K2td2Do1bJLyafaoVX2AZ_v7Sfb94-m36Wx0dv5pPp2cjTSvaBxRKjhTnJBC1KJqWUsLAqrmRVMBYdBQ1iqRU5oXrcZVLaDBOYG6rMtCqLYR7CR7ee3d9C7IfY-DJLzMuWBFRRMxvyYap1Zy481a-d_SKSN3Aec7qXyqsAcJOYgWq9TrhuZQU8V5jTG0guQ5ZkQn1_v9aUO9hkaDjV71B9LDN9YsZecuZcovKMZJ8GYv8O7nACHKtQk6tVZZcMPuuwtRYlKwhL76B72_uj3VqVSAsa1L5-qtVE5S30rGSUkSNb6HSlcDa6PTQLYmxQ8S3h4kJCbCVezUEIKcLy7-nz3_cci-vsMuQfVxGdL0bocpHIL5Nai9C8FDe9tkguV2n266Ibf7JPf7lNJe3P1Bt0k3C8T-AjcIG7Y</recordid><startdate>20150421</startdate><enddate>20150421</enddate><creator>Klaver, Elsenoor J</creator><creator>Kuijk, Loes M</creator><creator>Lindhorst, Thisbe K</creator><creator>Cummings, Richard D</creator><creator>van Die, Irma</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150421</creationdate><title>Schistosoma mansoni Soluble Egg Antigens Induce Expression of the Negative Regulators SOCS1 and SHP1 in Human Dendritic Cells via Interaction with the Mannose Receptor</title><author>Klaver, Elsenoor J ; Kuijk, Loes M ; Lindhorst, Thisbe K ; Cummings, Richard D ; van Die, Irma</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-22863a61158b89f3f251eab65d9e13ed23fa842245fc09b8ed041eb7b758afd83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Antibodies</topic><topic>Antigens</topic><topic>Antigens, Helminth - immunology</topic><topic>Apoptosis</topic><topic>B7-H1 Antigen - genetics</topic><topic>B7-H1 Antigen - metabolism</topic><topic>Biology</topic><topic>Bone morphogenetic proteins</topic><topic>Cells, Cultured</topic><topic>Costimulator</topic><topic>Cytokines</topic><topic>Denaturation</topic><topic>Dendritic cells</topic><topic>Dendritic Cells - metabolism</topic><topic>Dendritic Cells - parasitology</topic><topic>Disease</topic><topic>Down-regulation</topic><topic>Gene Expression</topic><topic>Genotype & phenotype</topic><topic>Health aspects</topic><topic>Host-Parasite Interactions</topic><topic>Humans</topic><topic>Immune system</topic><topic>Immunology</topic><topic>Infections</topic><topic>Inflammatory bowel disease</topic><topic>Inflammatory diseases</topic><topic>Internalization</topic><topic>Lectins</topic><topic>Lectins, C-Type - metabolism</topic><topic>Ligands</topic><topic>Lipopolysaccharides</topic><topic>Lipopolysaccharides - pharmacology</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Mannose</topic><topic>Mannose-Binding Lectins - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Klaver, Elsenoor J</au><au>Kuijk, Loes M</au><au>Lindhorst, Thisbe K</au><au>Cummings, Richard D</au><au>van Die, Irma</au><au>Gobert, Geoffrey N.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Schistosoma mansoni Soluble Egg Antigens Induce Expression of the Negative Regulators SOCS1 and SHP1 in Human Dendritic Cells via Interaction with the Mannose Receptor</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-04-21</date><risdate>2015</risdate><volume>10</volume><issue>4</issue><spage>e0124089</spage><epage>e0124089</epage><pages>e0124089-e0124089</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Schistosomiasis is a common debilitating human parasitic disease in (sub)tropical areas, however, schistosome infections can also protect against a variety of inflammatory diseases. This has raised broad interest in the mechanisms by which Schistosoma modulate the immune system into an anti-inflammatory and regulatory state. Human dendritic cells (DCs) show many phenotypic changes upon contact with Schistosoma mansoni soluble egg antigens (SEA). We here show that oxidation of SEA glycans, but not heat-denaturation, abrogates the capacity of SEA to suppress both LPS-induced cytokine secretion and DC proliferation, indicating an important role of SEA glycans in these processes. Remarkably, interaction of SEA glycans with DCs results in a strongly increased expression of Suppressor Of Cytokine Signalling1 (SOCS1) and SH2-containing protein tyrosine Phosphatase-1 (SHP1), important negative regulators of TLR4 signalling. In addition, SEA induces the secretion of transforming growth factor β (TGF-β), and the surface expression of the costimulatory molecules Programmed Death Ligand-1 (PD-L1) and OX40 ligand (OX40L), which are known phenotypic markers for the capacity of DCs to polarize naïve T cells into Th2/Treg cell subsets. Inhibition of mannose receptor (MR)-mediated internalization of SEA into DCs by blocking with allyl α-D-mannoside or anti-MR antibodies, significantly reduced SOCS1 and SHP1 expression. In conclusion, we demonstrate that SEA glycans are essential for induction of enhanced SOCS1 and SHP1 levels in DCs via the MR. Our data provide novel mechanistic evidence for the potential of S. mansoni SEA glycans to modulate human DCs, which may contribute to the capacity of SEA to down-regulate inflammatory responses.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25897665</pmid><doi>10.1371/journal.pone.0124089</doi><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2015-04, Vol.10 (4), p.e0124089-e0124089 |
issn | 1932-6203 1932-6203 |
language | eng |
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source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Animals Antibodies Antigens Antigens, Helminth - immunology Apoptosis B7-H1 Antigen - genetics B7-H1 Antigen - metabolism Biology Bone morphogenetic proteins Cells, Cultured Costimulator Cytokines Denaturation Dendritic cells Dendritic Cells - metabolism Dendritic Cells - parasitology Disease Down-regulation Gene Expression Genotype & phenotype Health aspects Host-Parasite Interactions Humans Immune system Immunology Infections Inflammatory bowel disease Inflammatory diseases Internalization Lectins Lectins, C-Type - metabolism Ligands Lipopolysaccharides Lipopolysaccharides - pharmacology Lymphocytes Lymphocytes T Mannose Mannose-Binding Lectins - metabolism Monosaccharides Multiple sclerosis Ovum - immunology OX40 Ligand - genetics OX40 Ligand - metabolism Ox40L protein Oxidation Parasitic diseases PD-L1 protein Polysaccharides Protein denaturation Protein Tyrosine Phosphatase, Non-Receptor Type 6 - genetics Protein Tyrosine Phosphatase, Non-Receptor Type 6 - metabolism Protein-tyrosine-phosphatase Receptors, Cell Surface - metabolism Regulation Schistosoma mansoni - immunology Schistosomiasis SHP-1 protein Signaling SOCS-1 protein Suppressor of Cytokine Signaling 1 Protein Suppressor of Cytokine Signaling Proteins - genetics Suppressor of Cytokine Signaling Proteins - metabolism T cells TLR4 protein Toll-like receptors Transcriptional Activation Transforming growth factor Transforming growth factor-b Transforming growth factors Tumor necrosis factor Tyrosine |
title | Schistosoma mansoni Soluble Egg Antigens Induce Expression of the Negative Regulators SOCS1 and SHP1 in Human Dendritic Cells via Interaction with the Mannose Receptor |
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