Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation
► Soluble products of T. suis and T. spiralis suppress clinical signs in murine EAE. ► Soluble products of T. suis, T. spiralis and S. mansoni modulate human dendritic cell function. ► Soluble products of T. suis and S. mansoni enhance dendritic cell OX40L expression. ► Soluble products of helminths...
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Veröffentlicht in: | Molecular immunology 2012-06, Vol.51 (2), p.210-218 |
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creator | Kuijk, Loes M. Klaver, Elsenoor J. Kooij, Gijs van der Pol, Susanne M.A. Heijnen, Priscilla Bruijns, Sven C.M. Kringel, Helene Pinelli, Elena Kraal, Georg de Vries, Helga E. Dijkstra, Christine D. Bouma, Gerd van Die, Irma |
description | ► Soluble products of T. suis and T. spiralis suppress clinical signs in murine EAE. ► Soluble products of T. suis, T. spiralis and S. mansoni modulate human dendritic cell function. ► Soluble products of T. suis and S. mansoni enhance dendritic cell OX40L expression. ► Soluble products of helminths differentially suppress dendritic cell cytokine production. ► Dendritic cells primed with helminth soluble products suppress IL-17A secretion.
The increased incidence of auto-inflammatory and autoimmune diseases in the developed countries seems to be caused by an imbalance of the immune system due to the lack of proper regulation. Helminth parasites are well known modulators of the immune system and as such are of great interest for the treatment of these disorders. Clinical studies showed that administration of eggs of the pig nematode Trichuris suis to patients with inflammatory bowel disease reduces the disease severity. Here we demonstrate that treatment with soluble products from the nematodes T. suis and Trichinella spiralis induces significant suppression of symptoms in murine experimental autoimmune encephalomyelitis, a validated animal model for multiple sclerosis. These data show that infection with live nematodes is not a prerequisite for suppression of inflammation. To translate these results to the human system, the effects of soluble products of T. suis, T. spiralis and Schistosoma mansoni on the phenotype and function of human dendritic cells (DCs) were compared. Our data show that soluble products of T. suis, S. mansoni and T. spiralis suppress TNF-α and IL-12 secretion by TLR-activated human DCs, and that T. suis and S. mansoni, but not T. spiralis, strongly enhance expression of OX40L. Furthermore, helminth-primed human DCs differentially suppress the development of Th1 and/or Th17 cells. In conclusion, our data demonstrate that soluble helminth products have strong immunomodulatory capacities, but might exert their effects through different mechanisms. The suppressed secretion of pro-inflammatory cytokines together with an upregulation of OX40L expression on human DCs might contribute to achieve this modulation. |
doi_str_mv | 10.1016/j.molimm.2012.03.020 |
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The increased incidence of auto-inflammatory and autoimmune diseases in the developed countries seems to be caused by an imbalance of the immune system due to the lack of proper regulation. Helminth parasites are well known modulators of the immune system and as such are of great interest for the treatment of these disorders. Clinical studies showed that administration of eggs of the pig nematode Trichuris suis to patients with inflammatory bowel disease reduces the disease severity. Here we demonstrate that treatment with soluble products from the nematodes T. suis and Trichinella spiralis induces significant suppression of symptoms in murine experimental autoimmune encephalomyelitis, a validated animal model for multiple sclerosis. These data show that infection with live nematodes is not a prerequisite for suppression of inflammation. To translate these results to the human system, the effects of soluble products of T. suis, T. spiralis and Schistosoma mansoni on the phenotype and function of human dendritic cells (DCs) were compared. Our data show that soluble products of T. suis, S. mansoni and T. spiralis suppress TNF-α and IL-12 secretion by TLR-activated human DCs, and that T. suis and S. mansoni, but not T. spiralis, strongly enhance expression of OX40L. Furthermore, helminth-primed human DCs differentially suppress the development of Th1 and/or Th17 cells. In conclusion, our data demonstrate that soluble helminth products have strong immunomodulatory capacities, but might exert their effects through different mechanisms. The suppressed secretion of pro-inflammatory cytokines together with an upregulation of OX40L expression on human DCs might contribute to achieve this modulation.</description><identifier>ISSN: 0161-5890</identifier><identifier>EISSN: 1872-9142</identifier><identifier>DOI: 10.1016/j.molimm.2012.03.020</identifier><identifier>PMID: 22482518</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Animal models ; Animals ; Autoimmune diseases ; Cell activation ; Coculture Techniques ; Cytokines ; Data processing ; Dendritic cell ; Dendritic cells ; Dendritic Cells - immunology ; Eggs ; Encephalomyelitis, Autoimmune, Experimental - immunology ; Enzyme-Linked Immunosorbent Assay ; Experimental allergic encephalomyelitis ; Experimental autoimmune encephalomyelitis ; Female ; Flow Cytometry ; Helminth ; Helminth Proteins - immunology ; Helper cells ; Humans ; Immune system ; Immunomodulation ; Immunomodulation - immunology ; Infection ; Inflammation ; Inflammatory bowel diseases ; Innate immunity ; Interleukin 12 ; Lymphocyte Activation - immunology ; Lymphocytes T ; Mice ; Mice, Inbred C57BL ; Multiple sclerosis ; Nematoda ; OX40L protein ; Parasites ; Schistosoma mansoni ; Trichinella spiralis ; Tumor necrosis factor- alpha</subject><ispartof>Molecular immunology, 2012-06, Vol.51 (2), p.210-218</ispartof><rights>2012 Elsevier Ltd</rights><rights>Copyright © 2012 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c395t-454583b5e1a44d8b2a9439b021687db0475c7ae8bd5be31708837c82a657a7f73</citedby><cites>FETCH-LOGICAL-c395t-454583b5e1a44d8b2a9439b021687db0475c7ae8bd5be31708837c82a657a7f73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0161589012001964$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22482518$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuijk, Loes M.</creatorcontrib><creatorcontrib>Klaver, Elsenoor J.</creatorcontrib><creatorcontrib>Kooij, Gijs</creatorcontrib><creatorcontrib>van der Pol, Susanne M.A.</creatorcontrib><creatorcontrib>Heijnen, Priscilla</creatorcontrib><creatorcontrib>Bruijns, Sven C.M.</creatorcontrib><creatorcontrib>Kringel, Helene</creatorcontrib><creatorcontrib>Pinelli, Elena</creatorcontrib><creatorcontrib>Kraal, Georg</creatorcontrib><creatorcontrib>de Vries, Helga E.</creatorcontrib><creatorcontrib>Dijkstra, Christine D.</creatorcontrib><creatorcontrib>Bouma, Gerd</creatorcontrib><creatorcontrib>van Die, Irma</creatorcontrib><title>Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation</title><title>Molecular immunology</title><addtitle>Mol Immunol</addtitle><description>► Soluble products of T. suis and T. spiralis suppress clinical signs in murine EAE. ► Soluble products of T. suis, T. spiralis and S. mansoni modulate human dendritic cell function. ► Soluble products of T. suis and S. mansoni enhance dendritic cell OX40L expression. ► Soluble products of helminths differentially suppress dendritic cell cytokine production. ► Dendritic cells primed with helminth soluble products suppress IL-17A secretion.
The increased incidence of auto-inflammatory and autoimmune diseases in the developed countries seems to be caused by an imbalance of the immune system due to the lack of proper regulation. Helminth parasites are well known modulators of the immune system and as such are of great interest for the treatment of these disorders. Clinical studies showed that administration of eggs of the pig nematode Trichuris suis to patients with inflammatory bowel disease reduces the disease severity. Here we demonstrate that treatment with soluble products from the nematodes T. suis and Trichinella spiralis induces significant suppression of symptoms in murine experimental autoimmune encephalomyelitis, a validated animal model for multiple sclerosis. These data show that infection with live nematodes is not a prerequisite for suppression of inflammation. To translate these results to the human system, the effects of soluble products of T. suis, T. spiralis and Schistosoma mansoni on the phenotype and function of human dendritic cells (DCs) were compared. Our data show that soluble products of T. suis, S. mansoni and T. spiralis suppress TNF-α and IL-12 secretion by TLR-activated human DCs, and that T. suis and S. mansoni, but not T. spiralis, strongly enhance expression of OX40L. Furthermore, helminth-primed human DCs differentially suppress the development of Th1 and/or Th17 cells. In conclusion, our data demonstrate that soluble helminth products have strong immunomodulatory capacities, but might exert their effects through different mechanisms. The suppressed secretion of pro-inflammatory cytokines together with an upregulation of OX40L expression on human DCs might contribute to achieve this modulation.</description><subject>Animal models</subject><subject>Animals</subject><subject>Autoimmune diseases</subject><subject>Cell activation</subject><subject>Coculture Techniques</subject><subject>Cytokines</subject><subject>Data processing</subject><subject>Dendritic cell</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - immunology</subject><subject>Eggs</subject><subject>Encephalomyelitis, Autoimmune, Experimental - immunology</subject><subject>Enzyme-Linked Immunosorbent Assay</subject><subject>Experimental allergic encephalomyelitis</subject><subject>Experimental autoimmune encephalomyelitis</subject><subject>Female</subject><subject>Flow Cytometry</subject><subject>Helminth</subject><subject>Helminth Proteins - immunology</subject><subject>Helper cells</subject><subject>Humans</subject><subject>Immune system</subject><subject>Immunomodulation</subject><subject>Immunomodulation - immunology</subject><subject>Infection</subject><subject>Inflammation</subject><subject>Inflammatory bowel diseases</subject><subject>Innate immunity</subject><subject>Interleukin 12</subject><subject>Lymphocyte Activation - immunology</subject><subject>Lymphocytes T</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Multiple sclerosis</subject><subject>Nematoda</subject><subject>OX40L protein</subject><subject>Parasites</subject><subject>Schistosoma mansoni</subject><subject>Trichinella spiralis</subject><subject>Tumor necrosis factor- alpha</subject><issn>0161-5890</issn><issn>1872-9142</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkcuO1DAQRSMEYpqBP0DISzYJfibOBgmNhoc0EgtgHTl2hXbLdoIfI_pz-FMc9cASsSqp6lTd0r1N85LgjmDSvzl1fnXW-45iQjvMOkzxo-ZA5EDbkXD6uDlUjLRCjviqeZbSCWPc4148ba4o5ZIKIg_Nry-rK7MDdATnbchHtMXVFJ0TSmXbIqSEtLPBauVQst9DQjYgX6INgODnBtF6CLkOVclrfafs_aBhOyq3-jM4m21CKhhk7LJArLBVzp2RrzJO5apcvArIQDCxshppcPWazvZeZbuG582TRbkELx7qdfPt_e3Xm4_t3ecPn27e3bWajSK3XHAh2SyAKM6NnKkaORtnTEkvBzNjPgg9KJCzETMwMmAp2aAlVb0Y1LAM7Lp5fblbDfhRIOXJ27T_ogKsJU3VdE4wGwn5HxT3TAoxVpRfUB3XlCIs01YdU_FcoZ3rp9N0yXHac5wwm2qOde3Vg0KZPZi_S3-Cq8DbCwDVknsLcUra7r4bG0Hnyaz23wq_AZ5OtQQ</recordid><startdate>201206</startdate><enddate>201206</enddate><creator>Kuijk, Loes M.</creator><creator>Klaver, Elsenoor J.</creator><creator>Kooij, Gijs</creator><creator>van der Pol, Susanne M.A.</creator><creator>Heijnen, Priscilla</creator><creator>Bruijns, Sven C.M.</creator><creator>Kringel, Helene</creator><creator>Pinelli, Elena</creator><creator>Kraal, Georg</creator><creator>de Vries, Helga E.</creator><creator>Dijkstra, Christine D.</creator><creator>Bouma, Gerd</creator><creator>van Die, Irma</creator><general>Elsevier Ltd</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>7X8</scope><scope>7T5</scope><scope>7TK</scope><scope>H94</scope></search><sort><creationdate>201206</creationdate><title>Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation</title><author>Kuijk, Loes M. ; Klaver, Elsenoor J. ; Kooij, Gijs ; van der Pol, Susanne M.A. ; Heijnen, Priscilla ; Bruijns, Sven C.M. ; Kringel, Helene ; Pinelli, Elena ; Kraal, Georg ; de Vries, Helga E. ; Dijkstra, Christine D. ; Bouma, Gerd ; van Die, Irma</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c395t-454583b5e1a44d8b2a9439b021687db0475c7ae8bd5be31708837c82a657a7f73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animal models</topic><topic>Animals</topic><topic>Autoimmune diseases</topic><topic>Cell activation</topic><topic>Coculture Techniques</topic><topic>Cytokines</topic><topic>Data processing</topic><topic>Dendritic cell</topic><topic>Dendritic cells</topic><topic>Dendritic Cells - immunology</topic><topic>Eggs</topic><topic>Encephalomyelitis, Autoimmune, Experimental - immunology</topic><topic>Enzyme-Linked Immunosorbent Assay</topic><topic>Experimental allergic encephalomyelitis</topic><topic>Experimental autoimmune encephalomyelitis</topic><topic>Female</topic><topic>Flow Cytometry</topic><topic>Helminth</topic><topic>Helminth Proteins - immunology</topic><topic>Helper cells</topic><topic>Humans</topic><topic>Immune system</topic><topic>Immunomodulation</topic><topic>Immunomodulation - immunology</topic><topic>Infection</topic><topic>Inflammation</topic><topic>Inflammatory bowel diseases</topic><topic>Innate immunity</topic><topic>Interleukin 12</topic><topic>Lymphocyte Activation - immunology</topic><topic>Lymphocytes T</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Multiple sclerosis</topic><topic>Nematoda</topic><topic>OX40L protein</topic><topic>Parasites</topic><topic>Schistosoma mansoni</topic><topic>Trichinella spiralis</topic><topic>Tumor necrosis factor- alpha</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuijk, Loes M.</creatorcontrib><creatorcontrib>Klaver, Elsenoor J.</creatorcontrib><creatorcontrib>Kooij, Gijs</creatorcontrib><creatorcontrib>van der Pol, Susanne M.A.</creatorcontrib><creatorcontrib>Heijnen, Priscilla</creatorcontrib><creatorcontrib>Bruijns, Sven C.M.</creatorcontrib><creatorcontrib>Kringel, Helene</creatorcontrib><creatorcontrib>Pinelli, Elena</creatorcontrib><creatorcontrib>Kraal, Georg</creatorcontrib><creatorcontrib>de Vries, Helga E.</creatorcontrib><creatorcontrib>Dijkstra, Christine D.</creatorcontrib><creatorcontrib>Bouma, Gerd</creatorcontrib><creatorcontrib>van Die, Irma</creatorcontrib><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>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><jtitle>Molecular immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuijk, Loes M.</au><au>Klaver, Elsenoor J.</au><au>Kooij, Gijs</au><au>van der Pol, Susanne M.A.</au><au>Heijnen, Priscilla</au><au>Bruijns, Sven C.M.</au><au>Kringel, Helene</au><au>Pinelli, Elena</au><au>Kraal, Georg</au><au>de Vries, Helga E.</au><au>Dijkstra, Christine D.</au><au>Bouma, Gerd</au><au>van Die, Irma</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation</atitle><jtitle>Molecular immunology</jtitle><addtitle>Mol Immunol</addtitle><date>2012-06</date><risdate>2012</risdate><volume>51</volume><issue>2</issue><spage>210</spage><epage>218</epage><pages>210-218</pages><issn>0161-5890</issn><eissn>1872-9142</eissn><abstract>► Soluble products of T. suis and T. spiralis suppress clinical signs in murine EAE. ► Soluble products of T. suis, T. spiralis and S. mansoni modulate human dendritic cell function. ► Soluble products of T. suis and S. mansoni enhance dendritic cell OX40L expression. ► Soluble products of helminths differentially suppress dendritic cell cytokine production. ► Dendritic cells primed with helminth soluble products suppress IL-17A secretion.
The increased incidence of auto-inflammatory and autoimmune diseases in the developed countries seems to be caused by an imbalance of the immune system due to the lack of proper regulation. Helminth parasites are well known modulators of the immune system and as such are of great interest for the treatment of these disorders. Clinical studies showed that administration of eggs of the pig nematode Trichuris suis to patients with inflammatory bowel disease reduces the disease severity. Here we demonstrate that treatment with soluble products from the nematodes T. suis and Trichinella spiralis induces significant suppression of symptoms in murine experimental autoimmune encephalomyelitis, a validated animal model for multiple sclerosis. These data show that infection with live nematodes is not a prerequisite for suppression of inflammation. To translate these results to the human system, the effects of soluble products of T. suis, T. spiralis and Schistosoma mansoni on the phenotype and function of human dendritic cells (DCs) were compared. Our data show that soluble products of T. suis, S. mansoni and T. spiralis suppress TNF-α and IL-12 secretion by TLR-activated human DCs, and that T. suis and S. mansoni, but not T. spiralis, strongly enhance expression of OX40L. Furthermore, helminth-primed human DCs differentially suppress the development of Th1 and/or Th17 cells. In conclusion, our data demonstrate that soluble helminth products have strong immunomodulatory capacities, but might exert their effects through different mechanisms. The suppressed secretion of pro-inflammatory cytokines together with an upregulation of OX40L expression on human DCs might contribute to achieve this modulation.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>22482518</pmid><doi>10.1016/j.molimm.2012.03.020</doi><tpages>9</tpages></addata></record> |
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subjects | Animal models Animals Autoimmune diseases Cell activation Coculture Techniques Cytokines Data processing Dendritic cell Dendritic cells Dendritic Cells - immunology Eggs Encephalomyelitis, Autoimmune, Experimental - immunology Enzyme-Linked Immunosorbent Assay Experimental allergic encephalomyelitis Experimental autoimmune encephalomyelitis Female Flow Cytometry Helminth Helminth Proteins - immunology Helper cells Humans Immune system Immunomodulation Immunomodulation - immunology Infection Inflammation Inflammatory bowel diseases Innate immunity Interleukin 12 Lymphocyte Activation - immunology Lymphocytes T Mice Mice, Inbred C57BL Multiple sclerosis Nematoda OX40L protein Parasites Schistosoma mansoni Trichinella spiralis Tumor necrosis factor- alpha |
title | Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation |
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