Dectin-2-mediated initiation of immune responses caused by influenza virus hemagglutinin
Antigen-presenting cells express pattern recognition receptors (PRRs), which sense pathogen-associated molecular patterns from microorganisms and lead to the induction of inflammatory responses. C-type lectin receptors (CLRs), the representative PRRs, bind to microbial polysaccharides, among which D...
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| Veröffentlicht in: | Biomedical Research 2021/04/10, Vol.42(2), pp.53-66 |
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| creator | YAMAMOTO, Hideki TOMIYAMA, Chikako SATO, Ko KASAMATSU, Jun TAKANO, Kazuki UMEKI, Aya NAKAHATA, Nana MIYASAKA, Tomomitsu KANNO, Emi TANNO, Hiromasa YAMASAKI, Sho SAIJO, Shinobu IWAKURA, Yoichiro ISHII, Keiko KAWAKAMI, Kazuyoshi |
| description | Antigen-presenting cells express pattern recognition receptors (PRRs), which sense pathogen-associated molecular patterns from microorganisms and lead to the induction of inflammatory responses. C-type lectin receptors (CLRs), the representative PRRs, bind to microbial polysaccharides, among which Dectin-2 and Mincle recognize mannose-containing polysaccharides. Because influenza virus (IFV) hemagglutinin (HA) is rich in mannose polysaccharides, Dectin-2 or Mincle may contribute to the recognition of HA. In this study, we addressed the possible involvement of Dectin-2 and Mincle in the viral recognition and the initiation of cytokine production. Interleukin (IL)-12p40 and IL-6 production by bone marrow–derived dendritic cells (BM-DCs) upon stimulation with HA was significantly reduced in Dectin-2 knockout (KO) mice compared to wild-type (WT) mice whereas there was no difference between WT mice and Mincle KO mice. BM-DCs that were treated with Syk inhibitor resulted in a significant reduction of cytokine production upon stimulation with HA. The treatment of BM-DCs with methyl-α-D-mannopyranoside (ManP) also led to a significant reduction in cytokine production by BM-DCs that were stimulated with HA, except for the A/H1N1pdm09 subtype. IL-12p40 and IL-6 synthesis by BM-DCs was completely diminished upon stimulation with HA treated with concanavalin A (ConA)-bound sepharose beads. Finally, GFP expression was detected in reporter cells that were transfected with the Dectin-2 gene, but not with the Mincle gene, when stimulated with HA derived from the A/H3N2 subtype. These data suggested that Dectin-2 may be a key molecule as the sensor for IFV to initiate the immune response and regulate the pathogenesis of IFV infection. |
| doi_str_mv | 10.2220/biomedres.42.53 |
| format | Article |
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C-type lectin receptors (CLRs), the representative PRRs, bind to microbial polysaccharides, among which Dectin-2 and Mincle recognize mannose-containing polysaccharides. Because influenza virus (IFV) hemagglutinin (HA) is rich in mannose polysaccharides, Dectin-2 or Mincle may contribute to the recognition of HA. In this study, we addressed the possible involvement of Dectin-2 and Mincle in the viral recognition and the initiation of cytokine production. Interleukin (IL)-12p40 and IL-6 production by bone marrow–derived dendritic cells (BM-DCs) upon stimulation with HA was significantly reduced in Dectin-2 knockout (KO) mice compared to wild-type (WT) mice whereas there was no difference between WT mice and Mincle KO mice. BM-DCs that were treated with Syk inhibitor resulted in a significant reduction of cytokine production upon stimulation with HA. The treatment of BM-DCs with methyl-α-D-mannopyranoside (ManP) also led to a significant reduction in cytokine production by BM-DCs that were stimulated with HA, except for the A/H1N1pdm09 subtype. IL-12p40 and IL-6 synthesis by BM-DCs was completely diminished upon stimulation with HA treated with concanavalin A (ConA)-bound sepharose beads. Finally, GFP expression was detected in reporter cells that were transfected with the Dectin-2 gene, but not with the Mincle gene, when stimulated with HA derived from the A/H3N2 subtype. These data suggested that Dectin-2 may be a key molecule as the sensor for IFV to initiate the immune response and regulate the pathogenesis of IFV infection.</description><identifier>ISSN: 0388-6107</identifier><identifier>EISSN: 1880-313X</identifier><identifier>DOI: 10.2220/biomedres.42.53</identifier><identifier>PMID: 33840686</identifier><language>eng</language><publisher>Japan: Biomedical Research Press</publisher><subject>Animals ; Antigen-presenting cells ; Antigen-Presenting Cells - metabolism ; Antigens ; Beads ; Bone marrow ; Bone Marrow Cells - metabolism ; Concanavalin A ; Concanavalin A - chemistry ; Cytokines ; Cytokines - metabolism ; Dendritic cells ; Disease Models, Animal ; Green Fluorescent Proteins - metabolism ; Hemagglutinin Glycoproteins, Influenza Virus - metabolism ; Hemagglutinins ; Humans ; Immune response ; Immune system ; Immune System - metabolism ; Inflammation ; Influenza ; Influenza, Human - immunology ; Influenza, Human - metabolism ; Interleukin 12 ; Interleukin 6 ; Interleukin-12 Subunit p40 - biosynthesis ; Interleukin-6 - biosynthesis ; Lectins, C-Type - metabolism ; Lectins, C-Type - physiology ; Ligands ; Mannose ; Membrane Proteins - physiology ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Microorganisms ; NFATC Transcription Factors - metabolism ; Pathogenesis ; Pattern recognition ; Pattern recognition receptors ; Polysaccharides ; Receptors ; Saccharides ; Sepharose - chemistry ; Stimulation ; Syk Kinase - metabolism ; Syk protein ; Viruses</subject><ispartof>Biomedical Research, 2021/04/10, Vol.42(2), pp.53-66</ispartof><rights>2021 Biomedical Research Press</rights><rights>Copyright Japan Science and Technology Agency 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c616t-a78eef63e002e169a5def77d9dd12e88a509b199f2f70b43b5f44084da6ba09a3</citedby><cites>FETCH-LOGICAL-c616t-a78eef63e002e169a5def77d9dd12e88a509b199f2f70b43b5f44084da6ba09a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,1883,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33840686$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>YAMAMOTO, Hideki</creatorcontrib><creatorcontrib>TOMIYAMA, Chikako</creatorcontrib><creatorcontrib>SATO, Ko</creatorcontrib><creatorcontrib>KASAMATSU, Jun</creatorcontrib><creatorcontrib>TAKANO, Kazuki</creatorcontrib><creatorcontrib>UMEKI, Aya</creatorcontrib><creatorcontrib>NAKAHATA, Nana</creatorcontrib><creatorcontrib>MIYASAKA, Tomomitsu</creatorcontrib><creatorcontrib>KANNO, Emi</creatorcontrib><creatorcontrib>TANNO, Hiromasa</creatorcontrib><creatorcontrib>YAMASAKI, Sho</creatorcontrib><creatorcontrib>SAIJO, Shinobu</creatorcontrib><creatorcontrib>IWAKURA, Yoichiro</creatorcontrib><creatorcontrib>ISHII, Keiko</creatorcontrib><creatorcontrib>KAWAKAMI, Kazuyoshi</creatorcontrib><title>Dectin-2-mediated initiation of immune responses caused by influenza virus hemagglutinin</title><title>Biomedical Research</title><addtitle>Biomed. Res.</addtitle><description>Antigen-presenting cells express pattern recognition receptors (PRRs), which sense pathogen-associated molecular patterns from microorganisms and lead to the induction of inflammatory responses. C-type lectin receptors (CLRs), the representative PRRs, bind to microbial polysaccharides, among which Dectin-2 and Mincle recognize mannose-containing polysaccharides. Because influenza virus (IFV) hemagglutinin (HA) is rich in mannose polysaccharides, Dectin-2 or Mincle may contribute to the recognition of HA. In this study, we addressed the possible involvement of Dectin-2 and Mincle in the viral recognition and the initiation of cytokine production. Interleukin (IL)-12p40 and IL-6 production by bone marrow–derived dendritic cells (BM-DCs) upon stimulation with HA was significantly reduced in Dectin-2 knockout (KO) mice compared to wild-type (WT) mice whereas there was no difference between WT mice and Mincle KO mice. BM-DCs that were treated with Syk inhibitor resulted in a significant reduction of cytokine production upon stimulation with HA. The treatment of BM-DCs with methyl-α-D-mannopyranoside (ManP) also led to a significant reduction in cytokine production by BM-DCs that were stimulated with HA, except for the A/H1N1pdm09 subtype. IL-12p40 and IL-6 synthesis by BM-DCs was completely diminished upon stimulation with HA treated with concanavalin A (ConA)-bound sepharose beads. Finally, GFP expression was detected in reporter cells that were transfected with the Dectin-2 gene, but not with the Mincle gene, when stimulated with HA derived from the A/H3N2 subtype. These data suggested that Dectin-2 may be a key molecule as the sensor for IFV to initiate the immune response and regulate the pathogenesis of IFV infection.</description><subject>Animals</subject><subject>Antigen-presenting cells</subject><subject>Antigen-Presenting Cells - metabolism</subject><subject>Antigens</subject><subject>Beads</subject><subject>Bone marrow</subject><subject>Bone Marrow Cells - metabolism</subject><subject>Concanavalin A</subject><subject>Concanavalin A - chemistry</subject><subject>Cytokines</subject><subject>Cytokines - metabolism</subject><subject>Dendritic cells</subject><subject>Disease Models, Animal</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Hemagglutinin Glycoproteins, Influenza Virus - metabolism</subject><subject>Hemagglutinins</subject><subject>Humans</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immune System - metabolism</subject><subject>Inflammation</subject><subject>Influenza</subject><subject>Influenza, Human - immunology</subject><subject>Influenza, Human - metabolism</subject><subject>Interleukin 12</subject><subject>Interleukin 6</subject><subject>Interleukin-12 Subunit p40 - biosynthesis</subject><subject>Interleukin-6 - biosynthesis</subject><subject>Lectins, C-Type - metabolism</subject><subject>Lectins, C-Type - physiology</subject><subject>Ligands</subject><subject>Mannose</subject><subject>Membrane Proteins - physiology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Microorganisms</subject><subject>NFATC Transcription Factors - metabolism</subject><subject>Pathogenesis</subject><subject>Pattern recognition</subject><subject>Pattern recognition receptors</subject><subject>Polysaccharides</subject><subject>Receptors</subject><subject>Saccharides</subject><subject>Sepharose - chemistry</subject><subject>Stimulation</subject><subject>Syk Kinase - metabolism</subject><subject>Syk protein</subject><subject>Viruses</subject><issn>0388-6107</issn><issn>1880-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpd0M1LwzAYBvAgipsfZ29S8OKlWz7aND36rTDworBbSNs3M6NNZ9II8683Uh3oKQnvL0_Cg9AZwTNKKZ5Xpu-gceBnGZ3lbA9NiRA4ZYQt99EUMyFSTnAxQUfer3E8E8EO0YQxkWEu-BQtb6EejE1pGnOMGqBJjDVD3JneJr1OTNcFC0l8YtNbDz6pVfBRVdsIdRvAfqrkw7jgkzfo1GrVhphn7Ak60Kr1cPqzHqPX-7uXm8d08fzwdHO1SGtO-JCqQgBozgBjCoSXKm9AF0VTNg2hIITKcVmRstRUF7jKWJXrLMMiaxSvFC4VO0aXY-7G9e8B_CA742toW2WhD17SnBBRFiWnkV78o-s-OBt_FxXFOck4zaOaj6p2vfcOtNw40ym3lQTL79LlrnSZUZmzeOP8JzdUcbDzvy1HcD2CtR_UCnZAucHULfwNpGPqbli_KSfBsi-epZkM</recordid><startdate>20210410</startdate><enddate>20210410</enddate><creator>YAMAMOTO, Hideki</creator><creator>TOMIYAMA, Chikako</creator><creator>SATO, Ko</creator><creator>KASAMATSU, Jun</creator><creator>TAKANO, Kazuki</creator><creator>UMEKI, Aya</creator><creator>NAKAHATA, Nana</creator><creator>MIYASAKA, Tomomitsu</creator><creator>KANNO, Emi</creator><creator>TANNO, Hiromasa</creator><creator>YAMASAKI, Sho</creator><creator>SAIJO, Shinobu</creator><creator>IWAKURA, Yoichiro</creator><creator>ISHII, Keiko</creator><creator>KAWAKAMI, Kazuyoshi</creator><general>Biomedical Research Press</general><general>Japan Science and Technology Agency</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>7QO</scope><scope>7QP</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20210410</creationdate><title>Dectin-2-mediated initiation of immune responses caused by influenza virus hemagglutinin</title><author>YAMAMOTO, Hideki ; TOMIYAMA, Chikako ; SATO, Ko ; KASAMATSU, Jun ; TAKANO, Kazuki ; UMEKI, Aya ; NAKAHATA, Nana ; MIYASAKA, Tomomitsu ; KANNO, Emi ; TANNO, Hiromasa ; YAMASAKI, Sho ; SAIJO, Shinobu ; IWAKURA, Yoichiro ; ISHII, Keiko ; KAWAKAMI, Kazuyoshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c616t-a78eef63e002e169a5def77d9dd12e88a509b199f2f70b43b5f44084da6ba09a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Antigen-presenting cells</topic><topic>Antigen-Presenting Cells - metabolism</topic><topic>Antigens</topic><topic>Beads</topic><topic>Bone marrow</topic><topic>Bone Marrow Cells - metabolism</topic><topic>Concanavalin A</topic><topic>Concanavalin A - chemistry</topic><topic>Cytokines</topic><topic>Cytokines - metabolism</topic><topic>Dendritic cells</topic><topic>Disease Models, Animal</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Hemagglutinin Glycoproteins, Influenza Virus - metabolism</topic><topic>Hemagglutinins</topic><topic>Humans</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immune System - metabolism</topic><topic>Inflammation</topic><topic>Influenza</topic><topic>Influenza, Human - immunology</topic><topic>Influenza, Human - metabolism</topic><topic>Interleukin 12</topic><topic>Interleukin 6</topic><topic>Interleukin-12 Subunit p40 - biosynthesis</topic><topic>Interleukin-6 - biosynthesis</topic><topic>Lectins, C-Type - metabolism</topic><topic>Lectins, C-Type - physiology</topic><topic>Ligands</topic><topic>Mannose</topic><topic>Membrane Proteins - physiology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Microorganisms</topic><topic>NFATC Transcription Factors - metabolism</topic><topic>Pathogenesis</topic><topic>Pattern recognition</topic><topic>Pattern recognition receptors</topic><topic>Polysaccharides</topic><topic>Receptors</topic><topic>Saccharides</topic><topic>Sepharose - chemistry</topic><topic>Stimulation</topic><topic>Syk Kinase - metabolism</topic><topic>Syk protein</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>YAMAMOTO, Hideki</creatorcontrib><creatorcontrib>TOMIYAMA, Chikako</creatorcontrib><creatorcontrib>SATO, Ko</creatorcontrib><creatorcontrib>KASAMATSU, Jun</creatorcontrib><creatorcontrib>TAKANO, Kazuki</creatorcontrib><creatorcontrib>UMEKI, Aya</creatorcontrib><creatorcontrib>NAKAHATA, Nana</creatorcontrib><creatorcontrib>MIYASAKA, Tomomitsu</creatorcontrib><creatorcontrib>KANNO, Emi</creatorcontrib><creatorcontrib>TANNO, Hiromasa</creatorcontrib><creatorcontrib>YAMASAKI, Sho</creatorcontrib><creatorcontrib>SAIJO, Shinobu</creatorcontrib><creatorcontrib>IWAKURA, Yoichiro</creatorcontrib><creatorcontrib>ISHII, Keiko</creatorcontrib><creatorcontrib>KAWAKAMI, Kazuyoshi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Biomedical Research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>YAMAMOTO, Hideki</au><au>TOMIYAMA, Chikako</au><au>SATO, Ko</au><au>KASAMATSU, Jun</au><au>TAKANO, Kazuki</au><au>UMEKI, Aya</au><au>NAKAHATA, Nana</au><au>MIYASAKA, Tomomitsu</au><au>KANNO, Emi</au><au>TANNO, Hiromasa</au><au>YAMASAKI, Sho</au><au>SAIJO, Shinobu</au><au>IWAKURA, Yoichiro</au><au>ISHII, Keiko</au><au>KAWAKAMI, Kazuyoshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dectin-2-mediated initiation of immune responses caused by influenza virus hemagglutinin</atitle><jtitle>Biomedical Research</jtitle><addtitle>Biomed. Res.</addtitle><date>2021-04-10</date><risdate>2021</risdate><volume>42</volume><issue>2</issue><spage>53</spage><epage>66</epage><pages>53-66</pages><issn>0388-6107</issn><eissn>1880-313X</eissn><abstract>Antigen-presenting cells express pattern recognition receptors (PRRs), which sense pathogen-associated molecular patterns from microorganisms and lead to the induction of inflammatory responses. C-type lectin receptors (CLRs), the representative PRRs, bind to microbial polysaccharides, among which Dectin-2 and Mincle recognize mannose-containing polysaccharides. Because influenza virus (IFV) hemagglutinin (HA) is rich in mannose polysaccharides, Dectin-2 or Mincle may contribute to the recognition of HA. In this study, we addressed the possible involvement of Dectin-2 and Mincle in the viral recognition and the initiation of cytokine production. Interleukin (IL)-12p40 and IL-6 production by bone marrow–derived dendritic cells (BM-DCs) upon stimulation with HA was significantly reduced in Dectin-2 knockout (KO) mice compared to wild-type (WT) mice whereas there was no difference between WT mice and Mincle KO mice. BM-DCs that were treated with Syk inhibitor resulted in a significant reduction of cytokine production upon stimulation with HA. The treatment of BM-DCs with methyl-α-D-mannopyranoside (ManP) also led to a significant reduction in cytokine production by BM-DCs that were stimulated with HA, except for the A/H1N1pdm09 subtype. IL-12p40 and IL-6 synthesis by BM-DCs was completely diminished upon stimulation with HA treated with concanavalin A (ConA)-bound sepharose beads. Finally, GFP expression was detected in reporter cells that were transfected with the Dectin-2 gene, but not with the Mincle gene, when stimulated with HA derived from the A/H3N2 subtype. These data suggested that Dectin-2 may be a key molecule as the sensor for IFV to initiate the immune response and regulate the pathogenesis of IFV infection.</abstract><cop>Japan</cop><pub>Biomedical Research Press</pub><pmid>33840686</pmid><doi>10.2220/biomedres.42.53</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; J-STAGE (Japan Science & Technology Information Aggregator, Electronic) Freely Available Titles - Japanese; EZB-FREE-00999 freely available EZB journals |
| subjects | Animals Antigen-presenting cells Antigen-Presenting Cells - metabolism Antigens Beads Bone marrow Bone Marrow Cells - metabolism Concanavalin A Concanavalin A - chemistry Cytokines Cytokines - metabolism Dendritic cells Disease Models, Animal Green Fluorescent Proteins - metabolism Hemagglutinin Glycoproteins, Influenza Virus - metabolism Hemagglutinins Humans Immune response Immune system Immune System - metabolism Inflammation Influenza Influenza, Human - immunology Influenza, Human - metabolism Interleukin 12 Interleukin 6 Interleukin-12 Subunit p40 - biosynthesis Interleukin-6 - biosynthesis Lectins, C-Type - metabolism Lectins, C-Type - physiology Ligands Mannose Membrane Proteins - physiology Mice Mice, Inbred C57BL Mice, Knockout Microorganisms NFATC Transcription Factors - metabolism Pathogenesis Pattern recognition Pattern recognition receptors Polysaccharides Receptors Saccharides Sepharose - chemistry Stimulation Syk Kinase - metabolism Syk protein Viruses |
| title | Dectin-2-mediated initiation of immune responses caused by influenza virus hemagglutinin |
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