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Listeria monocytogenes induces mast cell extracellular traps
Abstract Mast cells play an essential role in different immunological phenomena including allergy and infectious diseases. Several bacteria induce mast cell activation leading to degranulation and the production of several cytokines and chemokines. However, mast cells also have different microbicida...
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| Published in: | Immunobiology (1979) 2017-02, Vol.222 (2), p.432-439 |
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| Main Authors: | , , , , , , , , , , , , , |
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| container_end_page | 439 |
| container_issue | 2 |
| container_start_page | 432 |
| container_title | Immunobiology (1979) |
| container_volume | 222 |
| creator | Campillo-Navarro, Marcia Leyva-Paredes, Kahiry Donis-Maturano, Luis González-Jiménez, Marco Paredes-Vivas, Yuriria Cerbulo-Vázquez, Arturo Serafín-López, Jeanet García-Pérez, Blanca Ullrich, Stephen E Flores-Romo, Leopoldo Pérez-Tapia, Sonia M Estrada-Parra, Sergio Estrada-García, Iris Chacón-Salinas, Rommel |
| description | Abstract Mast cells play an essential role in different immunological phenomena including allergy and infectious diseases. Several bacteria induce mast cell activation leading to degranulation and the production of several cytokines and chemokines. However, mast cells also have different microbicidal activities such as phagocytosis and the release of DNA with embedded granular proteins known as Mast Cell Extracellular Traps (MCETs). Although previous reports indicate that extracellular bacteria are able to induce MCETs little is known if intracellular bacteria can induce these structures. In this work, we evaluated MCETs induction by the intracellular bacteria Listeria monocytogenes . We found that mast cells released DNA after stimulation with L. monocytogenes , and this DNA was complexed to histone and tryptase. Before extracellular DNA release, L. monocytogenes induced modifications to the mast cell nuclear envelope and DNA was detected outside the nucleus. L. monocytogenes stimulated mast cells to produce significant amounts of reactive oxygen species (ROS) and blocking NADPH oxidase diminished DNA release by mast cells. Finally, MCETs showed antimicrobial activity against L. monocytogenes that was partially blocked when β-hexosaminidase activity was inhibited. These results show that L. monocytogenes induces mast cells to produce microbicidal MCETs, suggesting a role for mast cells in containing infection beyond the induction of inflammation. |
| doi_str_mv | 10.1016/j.imbio.2016.08.006 |
| format | article |
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Several bacteria induce mast cell activation leading to degranulation and the production of several cytokines and chemokines. However, mast cells also have different microbicidal activities such as phagocytosis and the release of DNA with embedded granular proteins known as Mast Cell Extracellular Traps (MCETs). Although previous reports indicate that extracellular bacteria are able to induce MCETs little is known if intracellular bacteria can induce these structures. In this work, we evaluated MCETs induction by the intracellular bacteria Listeria monocytogenes . We found that mast cells released DNA after stimulation with L. monocytogenes , and this DNA was complexed to histone and tryptase. Before extracellular DNA release, L. monocytogenes induced modifications to the mast cell nuclear envelope and DNA was detected outside the nucleus. L. monocytogenes stimulated mast cells to produce significant amounts of reactive oxygen species (ROS) and blocking NADPH oxidase diminished DNA release by mast cells. Finally, MCETs showed antimicrobial activity against L. monocytogenes that was partially blocked when β-hexosaminidase activity was inhibited. These results show that L. monocytogenes induces mast cells to produce microbicidal MCETs, suggesting a role for mast cells in containing infection beyond the induction of inflammation.</description><identifier>ISSN: 0171-2985</identifier><identifier>EISSN: 1878-3279</identifier><identifier>DOI: 10.1016/j.imbio.2016.08.006</identifier><identifier>PMID: 27520114</identifier><language>eng</language><publisher>Netherlands: Elsevier GmbH</publisher><subject>Advanced Basic Science ; Allergy and Immunology ; beta-N-Acetylhexosaminidases - metabolism ; Cell Line ; DNA - metabolism ; Extracellular Traps - immunology ; Extracellular Traps - metabolism ; Histones - metabolism ; Host-Pathogen Interactions - immunology ; Humans ; Listeria monocytogenes ; Listeria monocytogenes - immunology ; Listeriosis ; Mast cell ; Mast cell extracellular trap ; Mast Cells - immunology ; Mast Cells - metabolism ; Mast Cells - ultrastructure ; Nuclear Envelope - ultrastructure ; Phagocytosis - immunology ; Reactive Oxygen Species - metabolism ; β-Hexosaminidase</subject><ispartof>Immunobiology (1979), 2017-02, Vol.222 (2), p.432-439</ispartof><rights>Elsevier GmbH</rights><rights>2016 Elsevier GmbH</rights><rights>Copyright © 2016 Elsevier GmbH. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c414t-6dbb9358174247bc40d421a329c4e0a5615e68d5533d339a2beb2a0435f622323</citedby><cites>FETCH-LOGICAL-c414t-6dbb9358174247bc40d421a329c4e0a5615e68d5533d339a2beb2a0435f622323</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27520114$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Campillo-Navarro, Marcia</creatorcontrib><creatorcontrib>Leyva-Paredes, Kahiry</creatorcontrib><creatorcontrib>Donis-Maturano, Luis</creatorcontrib><creatorcontrib>González-Jiménez, Marco</creatorcontrib><creatorcontrib>Paredes-Vivas, Yuriria</creatorcontrib><creatorcontrib>Cerbulo-Vázquez, Arturo</creatorcontrib><creatorcontrib>Serafín-López, Jeanet</creatorcontrib><creatorcontrib>García-Pérez, Blanca</creatorcontrib><creatorcontrib>Ullrich, Stephen E</creatorcontrib><creatorcontrib>Flores-Romo, Leopoldo</creatorcontrib><creatorcontrib>Pérez-Tapia, Sonia M</creatorcontrib><creatorcontrib>Estrada-Parra, Sergio</creatorcontrib><creatorcontrib>Estrada-García, Iris</creatorcontrib><creatorcontrib>Chacón-Salinas, Rommel</creatorcontrib><title>Listeria monocytogenes induces mast cell extracellular traps</title><title>Immunobiology (1979)</title><addtitle>Immunobiology</addtitle><description>Abstract Mast cells play an essential role in different immunological phenomena including allergy and infectious diseases. Several bacteria induce mast cell activation leading to degranulation and the production of several cytokines and chemokines. However, mast cells also have different microbicidal activities such as phagocytosis and the release of DNA with embedded granular proteins known as Mast Cell Extracellular Traps (MCETs). Although previous reports indicate that extracellular bacteria are able to induce MCETs little is known if intracellular bacteria can induce these structures. In this work, we evaluated MCETs induction by the intracellular bacteria Listeria monocytogenes . We found that mast cells released DNA after stimulation with L. monocytogenes , and this DNA was complexed to histone and tryptase. Before extracellular DNA release, L. monocytogenes induced modifications to the mast cell nuclear envelope and DNA was detected outside the nucleus. L. monocytogenes stimulated mast cells to produce significant amounts of reactive oxygen species (ROS) and blocking NADPH oxidase diminished DNA release by mast cells. Finally, MCETs showed antimicrobial activity against L. monocytogenes that was partially blocked when β-hexosaminidase activity was inhibited. These results show that L. monocytogenes induces mast cells to produce microbicidal MCETs, suggesting a role for mast cells in containing infection beyond the induction of inflammation.</description><subject>Advanced Basic Science</subject><subject>Allergy and Immunology</subject><subject>beta-N-Acetylhexosaminidases - metabolism</subject><subject>Cell Line</subject><subject>DNA - metabolism</subject><subject>Extracellular Traps - immunology</subject><subject>Extracellular Traps - metabolism</subject><subject>Histones - metabolism</subject><subject>Host-Pathogen Interactions - immunology</subject><subject>Humans</subject><subject>Listeria monocytogenes</subject><subject>Listeria monocytogenes - immunology</subject><subject>Listeriosis</subject><subject>Mast cell</subject><subject>Mast cell extracellular trap</subject><subject>Mast Cells - immunology</subject><subject>Mast Cells - metabolism</subject><subject>Mast Cells - ultrastructure</subject><subject>Nuclear Envelope - ultrastructure</subject><subject>Phagocytosis - immunology</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>β-Hexosaminidase</subject><issn>0171-2985</issn><issn>1878-3279</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNqFkUtLxDAQx4Mo7vr4BIL06KU1zzYFFWTxBQse1HNI01nJ2jZr0or77U3d1YMXTzMD__88foPQCcEZwSQ_X2a2razLaCwyLDOM8x00JbKQKaNFuYummBQkpaUUE3QQwhJjUtJC7qMJLUR0ET5FF3MbevBWJ63rnFn37hU6CInt6sHE2OrQJwaaJoHP3usxGxrtk5ivwhHaW-gmwPE2HqKX25vn2X06f7x7mF3PU8MJ79O8rqqSCUkKTnlRGY5rTolmtDQcsBY5EZDLWgjGasZKTSuoqMaciUVOKaPsEJ1t-q68ex8g9Kq1YVxFd-CGoIgUNBdclCxK2UZqvAvBw0KtvG21XyuC1YhNLdU3NjViU1iqiC26TrcDhqqF-tfzwykKLjcCiGd-WPAqGAudgdp6ML2qnf1nwNUfv2lsZ41u3mANYekG30WCiqhAFVZP4-fGx5GcYcYLxr4AhjCS8A</recordid><startdate>20170201</startdate><enddate>20170201</enddate><creator>Campillo-Navarro, Marcia</creator><creator>Leyva-Paredes, Kahiry</creator><creator>Donis-Maturano, Luis</creator><creator>González-Jiménez, Marco</creator><creator>Paredes-Vivas, Yuriria</creator><creator>Cerbulo-Vázquez, Arturo</creator><creator>Serafín-López, Jeanet</creator><creator>García-Pérez, Blanca</creator><creator>Ullrich, Stephen E</creator><creator>Flores-Romo, Leopoldo</creator><creator>Pérez-Tapia, Sonia M</creator><creator>Estrada-Parra, Sergio</creator><creator>Estrada-García, Iris</creator><creator>Chacón-Salinas, Rommel</creator><general>Elsevier GmbH</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></search><sort><creationdate>20170201</creationdate><title>Listeria monocytogenes induces mast cell extracellular traps</title><author>Campillo-Navarro, Marcia ; 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Several bacteria induce mast cell activation leading to degranulation and the production of several cytokines and chemokines. However, mast cells also have different microbicidal activities such as phagocytosis and the release of DNA with embedded granular proteins known as Mast Cell Extracellular Traps (MCETs). Although previous reports indicate that extracellular bacteria are able to induce MCETs little is known if intracellular bacteria can induce these structures. In this work, we evaluated MCETs induction by the intracellular bacteria Listeria monocytogenes . We found that mast cells released DNA after stimulation with L. monocytogenes , and this DNA was complexed to histone and tryptase. Before extracellular DNA release, L. monocytogenes induced modifications to the mast cell nuclear envelope and DNA was detected outside the nucleus. L. monocytogenes stimulated mast cells to produce significant amounts of reactive oxygen species (ROS) and blocking NADPH oxidase diminished DNA release by mast cells. Finally, MCETs showed antimicrobial activity against L. monocytogenes that was partially blocked when β-hexosaminidase activity was inhibited. These results show that L. monocytogenes induces mast cells to produce microbicidal MCETs, suggesting a role for mast cells in containing infection beyond the induction of inflammation.</abstract><cop>Netherlands</cop><pub>Elsevier GmbH</pub><pmid>27520114</pmid><doi>10.1016/j.imbio.2016.08.006</doi><tpages>8</tpages></addata></record> |
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| subjects | Advanced Basic Science Allergy and Immunology beta-N-Acetylhexosaminidases - metabolism Cell Line DNA - metabolism Extracellular Traps - immunology Extracellular Traps - metabolism Histones - metabolism Host-Pathogen Interactions - immunology Humans Listeria monocytogenes Listeria monocytogenes - immunology Listeriosis Mast cell Mast cell extracellular trap Mast Cells - immunology Mast Cells - metabolism Mast Cells - ultrastructure Nuclear Envelope - ultrastructure Phagocytosis - immunology Reactive Oxygen Species - metabolism β-Hexosaminidase |
| title | Listeria monocytogenes induces mast cell extracellular traps |
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