HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells
The human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein gp120 is a vaccine immunogen that can signal via several cell surface receptors. To investigate whether receptor biology could influence immune responses to gp120, we studied its interaction with human, monocyte-derived dendritic...
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| Veröffentlicht in: | PLoS pathogens 2007-11, Vol.3 (11), p.e169-e169 |
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| creator | Shan, Meimei Klasse, Per Johan Banerjee, Kaustuv Dey, Antu K Iyer, Sai Prasad N Dionisio, Robert Charles, Dustin Campbell-Gardener, Lila Olson, William C Sanders, Rogier W Moore, John P |
| description | The human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein gp120 is a vaccine immunogen that can signal via several cell surface receptors. To investigate whether receptor biology could influence immune responses to gp120, we studied its interaction with human, monocyte-derived dendritic cells (MDDCs) in vitro. Gp120 from the HIV-1 strain JR-FL induced IL-10 expression in MDDCs from 62% of donors, via a mannose C-type lectin receptor(s) (MCLR). Gp120 from the strain LAI was also an IL-10 inducer, but gp120 from the strain KNH1144 was not. The mannose-binding protein cyanovirin-N, the 2G12 mAb to a mannose-dependent gp120 epitope, and MCLR-specific mAbs inhibited IL-10 expression, as did enzymatic removal of gp120 mannose moieties, whereas inhibitors of signaling via CD4, CCR5, or CXCR4 were ineffective. Gp120-stimulated IL-10 production correlated with DC-SIGN expression on the cells, and involved the ERK signaling pathway. Gp120-treated MDDCs also responded poorly to maturation stimuli by up-regulating activation markers inefficiently and stimulating allogeneic T cell proliferation only weakly. These adverse reactions to gp120 were MCLR-dependent but independent of IL-10 production. Since such mechanisms might suppress immune responses to Env-containing vaccines, demannosylation may be a way to improve the immunogenicity of gp120 or gp140 proteins. |
| doi_str_mv | 10.1371/journal.ppat.0030169 |
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To investigate whether receptor biology could influence immune responses to gp120, we studied its interaction with human, monocyte-derived dendritic cells (MDDCs) in vitro. Gp120 from the HIV-1 strain JR-FL induced IL-10 expression in MDDCs from 62% of donors, via a mannose C-type lectin receptor(s) (MCLR). Gp120 from the strain LAI was also an IL-10 inducer, but gp120 from the strain KNH1144 was not. The mannose-binding protein cyanovirin-N, the 2G12 mAb to a mannose-dependent gp120 epitope, and MCLR-specific mAbs inhibited IL-10 expression, as did enzymatic removal of gp120 mannose moieties, whereas inhibitors of signaling via CD4, CCR5, or CXCR4 were ineffective. Gp120-stimulated IL-10 production correlated with DC-SIGN expression on the cells, and involved the ERK signaling pathway. Gp120-treated MDDCs also responded poorly to maturation stimuli by up-regulating activation markers inefficiently and stimulating allogeneic T cell proliferation only weakly. These adverse reactions to gp120 were MCLR-dependent but independent of IL-10 production. Since such mechanisms might suppress immune responses to Env-containing vaccines, demannosylation may be a way to improve the immunogenicity of gp120 or gp140 proteins.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.0030169</identifier><identifier>PMID: 17983270</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acquired immune deficiency syndrome ; AIDS ; Cell culture ; Cytokines ; Dendritic Cells - immunology ; Dendritic Cells - metabolism ; Enzyme-Linked Immunosorbent Assay ; Experiments ; Extracellular Signal-Regulated MAP Kinases ; HIV Envelope Protein gp120 - chemistry ; HIV Envelope Protein gp120 - immunology ; HIV Envelope Protein gp120 - metabolism ; Human immunodeficiency virus 1 ; Humans ; Immunology ; Interleukin-10 - biosynthesis ; Lectins, C-Type - metabolism ; Lymphocyte Activation - immunology ; Lymphocytes ; Mannose - metabolism ; Proteins ; Reverse Transcriptase Polymerase Chain Reaction ; Signal Transduction - physiology ; T-Lymphocytes - immunology ; Virology ; Viruses</subject><ispartof>PLoS pathogens, 2007-11, Vol.3 (11), p.e169-e169</ispartof><rights>2007 Shan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Shan M, Klasse PJ, Banerjee K, Dey AK, Iyer SPN, et al. (2007) HIV-1 gp120 Mannoses Induce Immunosuppressive Responses from Dendritic Cells. PLoS Pathog 3(11): e169. doi:10.1371/journal.ppat.0030169</rights><rights>2007 Shan et al. 2007</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c555t-a4171705a121d8a576219498e2eb1a507b99118e0a04e491401f56d38215fe93</citedby><cites>FETCH-LOGICAL-c555t-a4171705a121d8a576219498e2eb1a507b99118e0a04e491401f56d38215fe93</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/PMC2048530/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2048530/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23864,27922,27923,53789,53791,79370,79371</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17983270$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Manchester, Marianne</contributor><creatorcontrib>Shan, Meimei</creatorcontrib><creatorcontrib>Klasse, Per Johan</creatorcontrib><creatorcontrib>Banerjee, Kaustuv</creatorcontrib><creatorcontrib>Dey, Antu K</creatorcontrib><creatorcontrib>Iyer, Sai Prasad N</creatorcontrib><creatorcontrib>Dionisio, Robert</creatorcontrib><creatorcontrib>Charles, Dustin</creatorcontrib><creatorcontrib>Campbell-Gardener, Lila</creatorcontrib><creatorcontrib>Olson, William C</creatorcontrib><creatorcontrib>Sanders, Rogier W</creatorcontrib><creatorcontrib>Moore, John P</creatorcontrib><title>HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>The human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein gp120 is a vaccine immunogen that can signal via several cell surface receptors. To investigate whether receptor biology could influence immune responses to gp120, we studied its interaction with human, monocyte-derived dendritic cells (MDDCs) in vitro. Gp120 from the HIV-1 strain JR-FL induced IL-10 expression in MDDCs from 62% of donors, via a mannose C-type lectin receptor(s) (MCLR). Gp120 from the strain LAI was also an IL-10 inducer, but gp120 from the strain KNH1144 was not. The mannose-binding protein cyanovirin-N, the 2G12 mAb to a mannose-dependent gp120 epitope, and MCLR-specific mAbs inhibited IL-10 expression, as did enzymatic removal of gp120 mannose moieties, whereas inhibitors of signaling via CD4, CCR5, or CXCR4 were ineffective. Gp120-stimulated IL-10 production correlated with DC-SIGN expression on the cells, and involved the ERK signaling pathway. Gp120-treated MDDCs also responded poorly to maturation stimuli by up-regulating activation markers inefficiently and stimulating allogeneic T cell proliferation only weakly. These adverse reactions to gp120 were MCLR-dependent but independent of IL-10 production. Since such mechanisms might suppress immune responses to Env-containing vaccines, demannosylation may be a way to improve the immunogenicity of gp120 or gp140 proteins.</description><subject>Acquired immune deficiency syndrome</subject><subject>AIDS</subject><subject>Cell culture</subject><subject>Cytokines</subject><subject>Dendritic Cells - immunology</subject><subject>Dendritic Cells - metabolism</subject><subject>Enzyme-Linked Immunosorbent Assay</subject><subject>Experiments</subject><subject>Extracellular Signal-Regulated MAP Kinases</subject><subject>HIV Envelope Protein gp120 - chemistry</subject><subject>HIV Envelope Protein gp120 - immunology</subject><subject>HIV Envelope Protein gp120 - metabolism</subject><subject>Human immunodeficiency virus 1</subject><subject>Humans</subject><subject>Immunology</subject><subject>Interleukin-10 - biosynthesis</subject><subject>Lectins, C-Type - metabolism</subject><subject>Lymphocyte Activation - immunology</subject><subject>Lymphocytes</subject><subject>Mannose - metabolism</subject><subject>Proteins</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Signal Transduction - physiology</subject><subject>T-Lymphocytes - immunology</subject><subject>Virology</subject><subject>Viruses</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</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>eNqFksFq3DAQhk1padK0b1BaQ6A3b2YsybIuhRLSZmEhl9CrmLXHWy-25Up2IG9fbddJk1LoacTom39Goz9J3iOsUGi82LvZD9StxpGmFYAALMyL5BSVEpkWWr58cj5J3oSwB5AosHidnKA2pcg1nCab6_X3DNPdiDmkPQ2DCxzSdqjnitO27-eYmMfRcwjtHacxjm44II13fVrzUPt2aqu04q4Lb5NXDXWB3y3xLLn9enV7eZ1tbr6tL79sskopNWUkUaMGRZhjXZLSRY5GmpJz3iIp0FtjEEsGAsnSoARsVFGLMkfVsBFnycej7Ni5YJc9BIt5aUCg0ToS6yNRO9rb0bc9-XvrqLW_E87vLPk4dse2kqaAqmqEZpSKtCmIhGJVxwmlFhS1Pi_d5m3PdcXD5Kl7Jvr8Zmh_2J27sznIUgmIAp8WAe9-zhwm27fhsC8a2M3BFib-CxTmv2AOQhkpRATP_wL_vQR5pCrvQvDcPM6MYA8WeqiyBwvZxUKx7MPT9_4pWjwjfgGj9cKx</recordid><startdate>20071101</startdate><enddate>20071101</enddate><creator>Shan, Meimei</creator><creator>Klasse, Per Johan</creator><creator>Banerjee, Kaustuv</creator><creator>Dey, Antu K</creator><creator>Iyer, Sai Prasad N</creator><creator>Dionisio, Robert</creator><creator>Charles, Dustin</creator><creator>Campbell-Gardener, Lila</creator><creator>Olson, William C</creator><creator>Sanders, Rogier W</creator><creator>Moore, John P</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>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7T5</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20071101</creationdate><title>HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells</title><author>Shan, Meimei ; Klasse, Per Johan ; Banerjee, Kaustuv ; Dey, Antu K ; Iyer, Sai Prasad N ; Dionisio, Robert ; Charles, Dustin ; Campbell-Gardener, Lila ; Olson, William C ; Sanders, Rogier W ; Moore, John P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c555t-a4171705a121d8a576219498e2eb1a507b99118e0a04e491401f56d38215fe93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Acquired immune deficiency syndrome</topic><topic>AIDS</topic><topic>Cell culture</topic><topic>Cytokines</topic><topic>Dendritic Cells - immunology</topic><topic>Dendritic Cells - metabolism</topic><topic>Enzyme-Linked Immunosorbent Assay</topic><topic>Experiments</topic><topic>Extracellular Signal-Regulated MAP Kinases</topic><topic>HIV Envelope Protein gp120 - chemistry</topic><topic>HIV Envelope Protein gp120 - immunology</topic><topic>HIV Envelope Protein gp120 - metabolism</topic><topic>Human immunodeficiency virus 1</topic><topic>Humans</topic><topic>Immunology</topic><topic>Interleukin-10 - biosynthesis</topic><topic>Lectins, C-Type - metabolism</topic><topic>Lymphocyte Activation - immunology</topic><topic>Lymphocytes</topic><topic>Mannose - metabolism</topic><topic>Proteins</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Signal Transduction - physiology</topic><topic>T-Lymphocytes - immunology</topic><topic>Virology</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shan, Meimei</creatorcontrib><creatorcontrib>Klasse, Per Johan</creatorcontrib><creatorcontrib>Banerjee, Kaustuv</creatorcontrib><creatorcontrib>Dey, Antu K</creatorcontrib><creatorcontrib>Iyer, Sai Prasad N</creatorcontrib><creatorcontrib>Dionisio, Robert</creatorcontrib><creatorcontrib>Charles, Dustin</creatorcontrib><creatorcontrib>Campbell-Gardener, Lila</creatorcontrib><creatorcontrib>Olson, William C</creatorcontrib><creatorcontrib>Sanders, Rogier W</creatorcontrib><creatorcontrib>Moore, John P</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</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>Immunology Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shan, Meimei</au><au>Klasse, Per Johan</au><au>Banerjee, Kaustuv</au><au>Dey, Antu K</au><au>Iyer, Sai Prasad N</au><au>Dionisio, Robert</au><au>Charles, Dustin</au><au>Campbell-Gardener, Lila</au><au>Olson, William C</au><au>Sanders, Rogier W</au><au>Moore, John P</au><au>Manchester, Marianne</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2007-11-01</date><risdate>2007</risdate><volume>3</volume><issue>11</issue><spage>e169</spage><epage>e169</epage><pages>e169-e169</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>The human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein gp120 is a vaccine immunogen that can signal via several cell surface receptors. To investigate whether receptor biology could influence immune responses to gp120, we studied its interaction with human, monocyte-derived dendritic cells (MDDCs) in vitro. Gp120 from the HIV-1 strain JR-FL induced IL-10 expression in MDDCs from 62% of donors, via a mannose C-type lectin receptor(s) (MCLR). Gp120 from the strain LAI was also an IL-10 inducer, but gp120 from the strain KNH1144 was not. The mannose-binding protein cyanovirin-N, the 2G12 mAb to a mannose-dependent gp120 epitope, and MCLR-specific mAbs inhibited IL-10 expression, as did enzymatic removal of gp120 mannose moieties, whereas inhibitors of signaling via CD4, CCR5, or CXCR4 were ineffective. Gp120-stimulated IL-10 production correlated with DC-SIGN expression on the cells, and involved the ERK signaling pathway. Gp120-treated MDDCs also responded poorly to maturation stimuli by up-regulating activation markers inefficiently and stimulating allogeneic T cell proliferation only weakly. These adverse reactions to gp120 were MCLR-dependent but independent of IL-10 production. Since such mechanisms might suppress immune responses to Env-containing vaccines, demannosylation may be a way to improve the immunogenicity of gp120 or gp140 proteins.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>17983270</pmid><doi>10.1371/journal.ppat.0030169</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Acquired immune deficiency syndrome AIDS Cell culture Cytokines Dendritic Cells - immunology Dendritic Cells - metabolism Enzyme-Linked Immunosorbent Assay Experiments Extracellular Signal-Regulated MAP Kinases HIV Envelope Protein gp120 - chemistry HIV Envelope Protein gp120 - immunology HIV Envelope Protein gp120 - metabolism Human immunodeficiency virus 1 Humans Immunology Interleukin-10 - biosynthesis Lectins, C-Type - metabolism Lymphocyte Activation - immunology Lymphocytes Mannose - metabolism Proteins Reverse Transcriptase Polymerase Chain Reaction Signal Transduction - physiology T-Lymphocytes - immunology Virology Viruses |
| title | HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells |
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