An in vitro model of antibody-enhanced killing of the intracellular parasite Leishmania amazonensis
Footpad infection of C3HeB/FeJ mice with Leishmania amazonensis leads to chronic lesions accompanied by large parasite loads. Co-infecting these animals with L. major leads to induction of an effective Th1 immune response that can resolve these lesions. This cross-protection can be recapitulated in...
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| description | Footpad infection of C3HeB/FeJ mice with Leishmania amazonensis leads to chronic lesions accompanied by large parasite loads. Co-infecting these animals with L. major leads to induction of an effective Th1 immune response that can resolve these lesions. This cross-protection can be recapitulated in vitro by using immune cells from L. major-infected animals to effectively activate L. amazonensis-infected macrophages to kill the parasite. We have shown previously that the B cell population and their IgG2a antibodies are required for effective cross-protection. Here we demonstrate that, in contrast to L. major, killing L. amazonensis parasites is dependent upon FcRγ common-chain and NADPH oxidase-generated superoxide from infected macrophages. Superoxide production coincided with killing of L. amazonensis at five days post-activation, suggesting that opsonization of the parasites was not a likely mechanism of the antibody response. Therefore we tested the hypothesis that non-specific immune complexes could provide a mechanism of FcRγ common-chain/NADPH oxidase dependent parasite killing. Macrophage activation in response to soluble IgG2a immune complexes, IFN-γ and parasite antigen was effective in significantly reducing the percentage of macrophages infected with L. amazonensis. These results define a host protection mechanism effective during Leishmania infection and demonstrate for the first time a novel means by which IgG antibodies can enhance killing of an intracellular pathogen. |
| doi_str_mv | 10.1371/journal.pone.0106426 |
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Co-infecting these animals with L. major leads to induction of an effective Th1 immune response that can resolve these lesions. This cross-protection can be recapitulated in vitro by using immune cells from L. major-infected animals to effectively activate L. amazonensis-infected macrophages to kill the parasite. We have shown previously that the B cell population and their IgG2a antibodies are required for effective cross-protection. Here we demonstrate that, in contrast to L. major, killing L. amazonensis parasites is dependent upon FcRγ common-chain and NADPH oxidase-generated superoxide from infected macrophages. Superoxide production coincided with killing of L. amazonensis at five days post-activation, suggesting that opsonization of the parasites was not a likely mechanism of the antibody response. Therefore we tested the hypothesis that non-specific immune complexes could provide a mechanism of FcRγ common-chain/NADPH oxidase dependent parasite killing. Macrophage activation in response to soluble IgG2a immune complexes, IFN-γ and parasite antigen was effective in significantly reducing the percentage of macrophages infected with L. amazonensis. These results define a host protection mechanism effective during Leishmania infection and demonstrate for the first time a novel means by which IgG antibodies can enhance killing of an intracellular pathogen.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0106426</identifier><identifier>PMID: 25191842</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antibodies ; Antibodies, Protozoan - immunology ; Antibody response ; Antibody-Dependent Cell Cytotoxicity - immunology ; Antigen-Antibody Complex - immunology ; Antigen-antibody complexes ; Antigens ; Biology and Life Sciences ; Cell activation ; Chains ; Chronic infection ; Cross-protection ; Cytokines ; Disease Models, Animal ; Disease prevention ; Enzymes ; Female ; Immune response ; Immune system ; Immunoglobulin G ; Immunoglobulin G - immunology ; In Vitro Techniques ; Infections ; Interferon ; Intracellular ; Killing ; Leishmania ; Leishmania major ; Leishmania mexicana - immunology ; Leishmaniasis, Cutaneous - immunology ; Leishmaniasis, Cutaneous - parasitology ; Lesions ; Lymphocytes B ; Lymphocytes T ; Macrophage Activation ; Macrophages ; Macrophages - immunology ; Macrophages - metabolism ; Macrophages - parasitology ; Mice ; Mice, Knockout ; NAD(P)H oxidase ; NADPH Oxidases - metabolism ; Nitric oxide ; Opsonization ; Oxidase ; Parasites ; Parasitic diseases ; Pathogens ; Pathology ; Phosphatidylinositol 3-Kinases ; Preventive medicine ; Receptors, IgG - metabolism ; Signal Transduction ; Superoxide ; Superoxides - metabolism ; Veterinary colleges ; Veterinary medicine ; γ-Interferon</subject><ispartof>PloS one, 2014-09, Vol.9 (9), p.e106426</ispartof><rights>2014 Gibson-Corley 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. 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Macrophage activation in response to soluble IgG2a immune complexes, IFN-γ and parasite antigen was effective in significantly reducing the percentage of macrophages infected with L. amazonensis. 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Co-infecting these animals with L. major leads to induction of an effective Th1 immune response that can resolve these lesions. This cross-protection can be recapitulated in vitro by using immune cells from L. major-infected animals to effectively activate L. amazonensis-infected macrophages to kill the parasite. We have shown previously that the B cell population and their IgG2a antibodies are required for effective cross-protection. Here we demonstrate that, in contrast to L. major, killing L. amazonensis parasites is dependent upon FcRγ common-chain and NADPH oxidase-generated superoxide from infected macrophages. Superoxide production coincided with killing of L. amazonensis at five days post-activation, suggesting that opsonization of the parasites was not a likely mechanism of the antibody response. Therefore we tested the hypothesis that non-specific immune complexes could provide a mechanism of FcRγ common-chain/NADPH oxidase dependent parasite killing. Macrophage activation in response to soluble IgG2a immune complexes, IFN-γ and parasite antigen was effective in significantly reducing the percentage of macrophages infected with L. amazonensis. These results define a host protection mechanism effective during Leishmania infection and demonstrate for the first time a novel means by which IgG antibodies can enhance killing of an intracellular pathogen.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25191842</pmid><doi>10.1371/journal.pone.0106426</doi><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2014-09, Vol.9 (9), p.e106426 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1560368801 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Animals Antibodies Antibodies, Protozoan - immunology Antibody response Antibody-Dependent Cell Cytotoxicity - immunology Antigen-Antibody Complex - immunology Antigen-antibody complexes Antigens Biology and Life Sciences Cell activation Chains Chronic infection Cross-protection Cytokines Disease Models, Animal Disease prevention Enzymes Female Immune response Immune system Immunoglobulin G Immunoglobulin G - immunology In Vitro Techniques Infections Interferon Intracellular Killing Leishmania Leishmania major Leishmania mexicana - immunology Leishmaniasis, Cutaneous - immunology Leishmaniasis, Cutaneous - parasitology Lesions Lymphocytes B Lymphocytes T Macrophage Activation Macrophages Macrophages - immunology Macrophages - metabolism Macrophages - parasitology Mice Mice, Knockout NAD(P)H oxidase NADPH Oxidases - metabolism Nitric oxide Opsonization Oxidase Parasites Parasitic diseases Pathogens Pathology Phosphatidylinositol 3-Kinases Preventive medicine Receptors, IgG - metabolism Signal Transduction Superoxide Superoxides - metabolism Veterinary colleges Veterinary medicine γ-Interferon |
| title | An in vitro model of antibody-enhanced killing of the intracellular parasite Leishmania amazonensis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-13T03%3A59%3A08IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=An%20in%20vitro%20model%20of%20antibody-enhanced%20killing%20of%20the%20intracellular%20parasite%20Leishmania%20amazonensis&rft.jtitle=PloS%20one&rft.au=Gibson-Corley,%20Katherine%20N&rft.date=2014-09-05&rft.volume=9&rft.issue=9&rft.spage=e106426&rft.pages=e106426-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0106426&rft_dat=%3Cproquest_plos_%3E3424179061%3C/proquest_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1560368801&rft_id=info:pmid/25191842&rft_doaj_id=oai_doaj_org_article_3f5d39b1152c4f2c8e1e155c221c4cde&rfr_iscdi=true |