The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line
Wolbachia are obligate intracellular bacteria which commonly infect arthropods. They are maternally inherited and capable of altering host development, sex determination, and reproduction. Reproductive manipulations include feminization, male-killing, parthenogenesis, and cytoplasmic incompatibility...
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| description | Wolbachia are obligate intracellular bacteria which commonly infect arthropods. They are maternally inherited and capable of altering host development, sex determination, and reproduction. Reproductive manipulations include feminization, male-killing, parthenogenesis, and cytoplasmic incompatibility. The mechanism by which Wolbachia avoid destruction by the host immune response is unknown. Generation of antimicrobial peptides (AMPs) and reactive oxygen species (ROS) by the host are among the first lines of traditional antimicrobial defense. Previous work shows no link between a Wolbachia infection and the induction of AMPs. Here we compare the expression of protein in a cell line naturally infected with Wolbachia and an identical cell line cured of the infection through the use of antibiotics. Protein extracts of each cell line were analyzed by two dimensional gel electrophoresis and LC/MS/MS. Our results show the upregulation of host antioxidant proteins, which are active against ROS generated by aerobic cell metabolism and during an immune response. Furthermore, flow cytometric and microscopic analysis demonstrates that ROS production is significantly greater in Wolbachia-infected mosquito cells and is associated with endosymbiont-containing vacuoles located in the host cell cytoplasm. This is the first empirical data supporting an association between Wolbachia and the insect antioxidant system. |
| doi_str_mv | 10.1371/journal.pone.0002083 |
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They are maternally inherited and capable of altering host development, sex determination, and reproduction. Reproductive manipulations include feminization, male-killing, parthenogenesis, and cytoplasmic incompatibility. The mechanism by which Wolbachia avoid destruction by the host immune response is unknown. Generation of antimicrobial peptides (AMPs) and reactive oxygen species (ROS) by the host are among the first lines of traditional antimicrobial defense. Previous work shows no link between a Wolbachia infection and the induction of AMPs. Here we compare the expression of protein in a cell line naturally infected with Wolbachia and an identical cell line cured of the infection through the use of antibiotics. Protein extracts of each cell line were analyzed by two dimensional gel electrophoresis and LC/MS/MS. Our results show the upregulation of host antioxidant proteins, which are active against ROS generated by aerobic cell metabolism and during an immune response. Furthermore, flow cytometric and microscopic analysis demonstrates that ROS production is significantly greater in Wolbachia-infected mosquito cells and is associated with endosymbiont-containing vacuoles located in the host cell cytoplasm. 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This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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They are maternally inherited and capable of altering host development, sex determination, and reproduction. Reproductive manipulations include feminization, male-killing, parthenogenesis, and cytoplasmic incompatibility. The mechanism by which Wolbachia avoid destruction by the host immune response is unknown. Generation of antimicrobial peptides (AMPs) and reactive oxygen species (ROS) by the host are among the first lines of traditional antimicrobial defense. Previous work shows no link between a Wolbachia infection and the induction of AMPs. Here we compare the expression of protein in a cell line naturally infected with Wolbachia and an identical cell line cured of the infection through the use of antibiotics. Protein extracts of each cell line were analyzed by two dimensional gel electrophoresis and LC/MS/MS. Our results show the upregulation of host antioxidant proteins, which are active against ROS generated by aerobic cell metabolism and during an immune response. 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genetics</subject><subject>Health aspects</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Incompatibility</subject><subject>Infection</subject><subject>Infections</subject><subject>Insect Proteins - genetics</subject><subject>Insect Proteins - isolation & purification</subject><subject>Insects</subject><subject>Killing</subject><subject>Metabolism</subject><subject>Microbiology/Cellular Microbiology and Pathogenesis</subject><subject>Microbiology/Immunity to Infections</subject><subject>Microscopic analysis</subject><subject>Molecular Biology/Translational Regulation</subject><subject>Morphology</subject><subject>Mosquitoes</subject><subject>Oxidative stress</subject><subject>Oxygen</subject><subject>Parthenogenesis</subject><subject>Peptides</subject><subject>Phosphorylation</subject><subject>Polymerase Chain Reaction</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Reproduction (biology)</subject><subject>Ribosomal DNA</subject><subject>Rifampin - pharmacology</subject><subject>Sex determination</subject><subject>Superoxide Dismutase - genetics</subject><subject>Symbiosis</subject><subject>Two dimensional analysis</subject><subject>Vacuoles</subject><subject>Wolbachia</subject><subject>Wolbachia - drug effects</subject><subject>Wolbachia - genetics</subject><subject>Wolbachia - physiology</subject><subject>Wolbachia pipientis</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</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>eNqNkl2L1DAUhoso7jr6D0QLwoIXM-ajTdMbYVj8GFhY0FUvw2lyOpOh03SbVGb-valTdUa8kFwknDzvOcnLmyTPKVlQXtA3Wzf0LTSLzrW4IIQwIvmD5JKWnM0FI_zhyfkieeL9lpCcSyEeJxdUZoJSll0mh7sNptga5w-7yro2pN9cU4HeWEg721lsg_Wpbc2g0adhhPddj95HNnV1unE-pBAht7cm7mnXu4C2HTWxni7RRB00leusDoNPNTZN2tgWnyaPamg8Ppv2WfLl_bu764_zm9sPq-vlzVwXTIZ5ltFMFgC55JjnNQEklRBQV6aqhSEInCGWwHMq8qwCAcRUwHSVsQpFIUo-S14e-3aN82pyzSvKKWOy4JJGYnUkjIOt6nq7g_6gHFj1s-D6tYI-WN2gyoUsClqUYAqZ5dpUZZxRFNJwjZJpjL3eTtOGaodGR_96aM6ant-0dqPW7rtinGW0HJ97NTXo3f2APqid9aNp0KIbvBIllVJQEsFXf4H__tviSK0hPt-2tYtTdVwGd1bH6NQ21pdZwUTOeAzILHl9JohMwH1Yw-C9Wn3-9P_s7ddz9uqE3SA0YeNdM8TktP4czI6g7p33Pda_zaNEjcn_9U81Jl9NyY-yF6fG_xFNUec_AJFSAX0</recordid><startdate>20080507</startdate><enddate>20080507</enddate><creator>Brennan, Lesley J</creator><creator>Keddie, B Andrew</creator><creator>Braig, Henk R</creator><creator>Harris, Harriet L</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20080507</creationdate><title>The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line</title><author>Brennan, Lesley J ; Keddie, B Andrew ; Braig, Henk R ; Harris, Harriet L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c728t-441487aa583e55f0ae0b66afbdbf6d0ea32ee9a351654ba6a0dba2cb42be67693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Aedes - microbiology</topic><topic>Aedes - physiology</topic><topic>Aedes albopictus</topic><topic>Analysis</topic><topic>Animals</topic><topic>Anopheles</topic><topic>Antibiotics</topic><topic>Antiinfectives and antibacterials</topic><topic>Antimicrobial agents</topic><topic>Antimicrobial peptides</topic><topic>Antioxidants</topic><topic>Antioxidants (Nutrients)</topic><topic>Apoptosis</topic><topic>Aquatic insects</topic><topic>Arthropods</topic><topic>Asian tiger mosquito</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - isolation & purification</topic><topic>Biochemistry/Protein Chemistry</topic><topic>Cell Biology/Gene Expression</topic><topic>Cell Line</topic><topic>Cytoplasm</topic><topic>Cytoplasmic incompatibility</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Drosophila</topic><topic>Electrophoresis, Gel, Two-Dimensional</topic><topic>Empirical analysis</topic><topic>Environmental science</topic><topic>Flow Cytometry</topic><topic>Gel electrophoresis</topic><topic>Gene Expression Regulation</topic><topic>Genomes</topic><topic>Glutathione Peroxidase - genetics</topic><topic>Health aspects</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Incompatibility</topic><topic>Infection</topic><topic>Infections</topic><topic>Insect Proteins - genetics</topic><topic>Insect Proteins - isolation & purification</topic><topic>Insects</topic><topic>Killing</topic><topic>Metabolism</topic><topic>Microbiology/Cellular Microbiology and Pathogenesis</topic><topic>Microbiology/Immunity to Infections</topic><topic>Microscopic analysis</topic><topic>Molecular Biology/Translational Regulation</topic><topic>Morphology</topic><topic>Mosquitoes</topic><topic>Oxidative stress</topic><topic>Oxygen</topic><topic>Parthenogenesis</topic><topic>Peptides</topic><topic>Phosphorylation</topic><topic>Polymerase Chain Reaction</topic><topic>Proteins</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Reproduction (biology)</topic><topic>Ribosomal DNA</topic><topic>Rifampin - pharmacology</topic><topic>Sex determination</topic><topic>Superoxide Dismutase - genetics</topic><topic>Symbiosis</topic><topic>Two dimensional analysis</topic><topic>Vacuoles</topic><topic>Wolbachia</topic><topic>Wolbachia - drug effects</topic><topic>Wolbachia - genetics</topic><topic>Wolbachia - physiology</topic><topic>Wolbachia pipientis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brennan, Lesley J</creatorcontrib><creatorcontrib>Keddie, B Andrew</creatorcontrib><creatorcontrib>Braig, Henk R</creatorcontrib><creatorcontrib>Harris, Harriet L</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology 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>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</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>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brennan, Lesley J</au><au>Keddie, B Andrew</au><au>Braig, Henk R</au><au>Harris, Harriet L</au><au>Alspaugh, Andy</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2008-05-07</date><risdate>2008</risdate><volume>3</volume><issue>5</issue><spage>e2083</spage><epage>e2083</epage><pages>e2083-e2083</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Wolbachia are obligate intracellular bacteria which commonly infect arthropods. They are maternally inherited and capable of altering host development, sex determination, and reproduction. Reproductive manipulations include feminization, male-killing, parthenogenesis, and cytoplasmic incompatibility. The mechanism by which Wolbachia avoid destruction by the host immune response is unknown. Generation of antimicrobial peptides (AMPs) and reactive oxygen species (ROS) by the host are among the first lines of traditional antimicrobial defense. Previous work shows no link between a Wolbachia infection and the induction of AMPs. Here we compare the expression of protein in a cell line naturally infected with Wolbachia and an identical cell line cured of the infection through the use of antibiotics. Protein extracts of each cell line were analyzed by two dimensional gel electrophoresis and LC/MS/MS. Our results show the upregulation of host antioxidant proteins, which are active against ROS generated by aerobic cell metabolism and during an immune response. Furthermore, flow cytometric and microscopic analysis demonstrates that ROS production is significantly greater in Wolbachia-infected mosquito cells and is associated with endosymbiont-containing vacuoles located in the host cell cytoplasm. This is the first empirical data supporting an association between Wolbachia and the insect antioxidant system.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>18461124</pmid><doi>10.1371/journal.pone.0002083</doi><tpages>e2083</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Aedes - microbiology Aedes - physiology Aedes albopictus Analysis Animals Anopheles Antibiotics Antiinfectives and antibacterials Antimicrobial agents Antimicrobial peptides Antioxidants Antioxidants (Nutrients) Apoptosis Aquatic insects Arthropods Asian tiger mosquito Bacteria Bacterial Proteins - genetics Bacterial Proteins - isolation & purification Biochemistry/Protein Chemistry Cell Biology/Gene Expression Cell Line Cytoplasm Cytoplasmic incompatibility Deoxyribonucleic acid DNA Drosophila Electrophoresis, Gel, Two-Dimensional Empirical analysis Environmental science Flow Cytometry Gel electrophoresis Gene Expression Regulation Genomes Glutathione Peroxidase - genetics Health aspects Immune response Immune system Incompatibility Infection Infections Insect Proteins - genetics Insect Proteins - isolation & purification Insects Killing Metabolism Microbiology/Cellular Microbiology and Pathogenesis Microbiology/Immunity to Infections Microscopic analysis Molecular Biology/Translational Regulation Morphology Mosquitoes Oxidative stress Oxygen Parthenogenesis Peptides Phosphorylation Polymerase Chain Reaction Proteins Reactive oxygen species Reactive Oxygen Species - metabolism Reproduction (biology) Ribosomal DNA Rifampin - pharmacology Sex determination Superoxide Dismutase - genetics Symbiosis Two dimensional analysis Vacuoles Wolbachia Wolbachia - drug effects Wolbachia - genetics Wolbachia - physiology Wolbachia pipientis |
| title | The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-21T05%3A17%3A40IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20endosymbiont%20Wolbachia%20pipientis%20induces%20the%20expression%20of%20host%20antioxidant%20proteins%20in%20an%20Aedes%20albopictus%20cell%20line&rft.jtitle=PloS%20one&rft.au=Brennan,%20Lesley%20J&rft.date=2008-05-07&rft.volume=3&rft.issue=5&rft.spage=e2083&rft.epage=e2083&rft.pages=e2083-e2083&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0002083&rft_dat=%3Cgale_plos_%3EA472652305%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1312287381&rft_id=info:pmid/18461124&rft_galeid=A472652305&rft_doaj_id=oai_doaj_org_article_56877179ad7845cdb9676778d3ce82ce&rfr_iscdi=true |