NADPH oxidase-generated reactive oxygen species in mature follicles are essential for Drosophila ovulation
Ovarian reactive oxygen species (ROS) are believed to regulate ovulation in mammals, but the details of ROS production in follicles and the role of ROS in ovulation in other species remain underexplored. In Drosophila ovulation, matrix metalloproteinase 2 (MMP2) is required for follicle rupture by d...
Gespeichert in:
| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2018-07, Vol.115 (30), p.7765-7770 |
|---|---|
| Hauptverfasser: | , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 7770 |
|---|---|
| container_issue | 30 |
| container_start_page | 7765 |
| container_title | Proceedings of the National Academy of Sciences - PNAS |
| container_volume | 115 |
| creator | Li, Wei Young, Jessica F. Sun, Jianjun |
| description | Ovarian reactive oxygen species (ROS) are believed to regulate ovulation in mammals, but the details of ROS production in follicles and the role of ROS in ovulation in other species remain underexplored. In Drosophila ovulation, matrix metalloproteinase 2 (MMP2) is required for follicle rupture by degradation of posterior follicle cells surrounding a mature oocyte. We recently demonstrated that MMP2 activation and follicle rupture are regulated by the neuronal hormone octopamine (OA) and the octopamine receptor in mushroombody (OAMB). In the current study, we investigated the role of the superoxide-generating enzyme NADPH oxidase (NOX) in Drosophila ovulation. We report that Nox is highly enriched in mature follicle cells and that Nox knockdown in these cells leads to a reduction in superoxide and to defective ovulation. Similar to MMP2 activation, NOX enzymatic activity is also controlled by the OA/OAMB-Ca2+ signaling pathway. In addition, we report that extracellular superoxide dismutase 3 (SOD3) is required to convert superoxide to hydrogen peroxide, which acts as the key signaling molecule for follicle rupture, independent of MMP2 activation. Given that Nox homologs are expressed in mammalian follicles, the NOX-dependent hydrogen peroxide signaling pathway that we describe could play a conserved role in regulating ovulation in other species. |
| doi_str_mv | 10.1073/pnas.1800115115 |
| format | Article |
| fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6065002</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26511282</jstor_id><sourcerecordid>26511282</sourcerecordid><originalsourceid>FETCH-LOGICAL-c443t-84f5c023e3acc3b0190a50deadaae32fcba7ef74ecbcaa23a82a2826960029e63</originalsourceid><addsrcrecordid>eNpdkUFv1DAQhS0EokvhzAkUqRcuaSd24sQXpKoFilQBBzhbs86k9cobBztZ0X_PrLa0gGTJ8sznpzfzhHhdwWkFrTqbRsynVQdQVQ2fJ2JVgalKXRt4KlYAsi27WtZH4kXOGwAwTQfPxZE0pmtBtSux-XJ--e2qiL98j5nKGxop4Ux9kQjd7HfErTuuFnki5ykXfiy2OC-JiiGG4F3gGvKLcqZx9hi4norLFHOcbn3AIu6WgLOP40vxbMCQ6dX9fSx-fPzw_eKqvP766fPF-XXp6lrN7HdoHEhFCp1Ta6gMYAM9YY9ISg5ujS0NbU1u7RClwk6i7KQ2msc1pNWxeH_QnZb1lnrHthIGOyW_xXRnI3r7b2f0t_Ym7qwG3bAGC7y7F0jx50J5tlufHYWAI8UlWwm67brGtIrRk__QTVzSyOMxZXjLoLu9o7MD5XgtOdHwYKYCu8_R7nO0jznyj7d_z_DA_wmOgTcHYJPnmB77mr_zNtRvhiCl-Q</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2099980686</pqid></control><display><type>article</type><title>NADPH oxidase-generated reactive oxygen species in mature follicles are essential for Drosophila ovulation</title><source>Jstor Complete Legacy</source><source>MEDLINE</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Li, Wei ; Young, Jessica F. ; Sun, Jianjun</creator><creatorcontrib>Li, Wei ; Young, Jessica F. ; Sun, Jianjun</creatorcontrib><description>Ovarian reactive oxygen species (ROS) are believed to regulate ovulation in mammals, but the details of ROS production in follicles and the role of ROS in ovulation in other species remain underexplored. In Drosophila ovulation, matrix metalloproteinase 2 (MMP2) is required for follicle rupture by degradation of posterior follicle cells surrounding a mature oocyte. We recently demonstrated that MMP2 activation and follicle rupture are regulated by the neuronal hormone octopamine (OA) and the octopamine receptor in mushroombody (OAMB). In the current study, we investigated the role of the superoxide-generating enzyme NADPH oxidase (NOX) in Drosophila ovulation. We report that Nox is highly enriched in mature follicle cells and that Nox knockdown in these cells leads to a reduction in superoxide and to defective ovulation. Similar to MMP2 activation, NOX enzymatic activity is also controlled by the OA/OAMB-Ca2+ signaling pathway. In addition, we report that extracellular superoxide dismutase 3 (SOD3) is required to convert superoxide to hydrogen peroxide, which acts as the key signaling molecule for follicle rupture, independent of MMP2 activation. Given that Nox homologs are expressed in mammalian follicles, the NOX-dependent hydrogen peroxide signaling pathway that we describe could play a conserved role in regulating ovulation in other species.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1800115115</identifier><identifier>PMID: 29987037</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Activation ; Animal reproduction ; Animals ; Biological Sciences ; Calcium ions ; Calcium signalling ; Drosophila ; Drosophila melanogaster ; Drosophila Proteins - metabolism ; Enzymatic activity ; Female ; Follicles ; Gelatinase A ; Homology ; Hydrogen peroxide ; Hydrogen Peroxide - metabolism ; Insects ; Mammals ; Matrix ; Matrix metalloproteinase ; Matrix Metalloproteinase 2 - metabolism ; Metalloproteinase ; NAD(P)H oxidase ; NADPH Oxidases - metabolism ; Octopamine ; Ovarian Follicle - metabolism ; Ovulation ; Ovulation - physiology ; Oxygen ; Proteins ; Reactive oxygen species ; Rupturing ; Signal transduction ; Signal Transduction - physiology ; Superoxide dismutase ; Superoxide Dismutase - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2018-07, Vol.115 (30), p.7765-7770</ispartof><rights>Volumes 1–89 and 106–115, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright © 2018 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Jul 24, 2018</rights><rights>Copyright © 2018 the Author(s). Published by PNAS. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-84f5c023e3acc3b0190a50deadaae32fcba7ef74ecbcaa23a82a2826960029e63</citedby><cites>FETCH-LOGICAL-c443t-84f5c023e3acc3b0190a50deadaae32fcba7ef74ecbcaa23a82a2826960029e63</cites><orcidid>0000-0002-6015-738X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26511282$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26511282$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27903,27904,53769,53771,57995,58228</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29987037$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Wei</creatorcontrib><creatorcontrib>Young, Jessica F.</creatorcontrib><creatorcontrib>Sun, Jianjun</creatorcontrib><title>NADPH oxidase-generated reactive oxygen species in mature follicles are essential for Drosophila ovulation</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Ovarian reactive oxygen species (ROS) are believed to regulate ovulation in mammals, but the details of ROS production in follicles and the role of ROS in ovulation in other species remain underexplored. In Drosophila ovulation, matrix metalloproteinase 2 (MMP2) is required for follicle rupture by degradation of posterior follicle cells surrounding a mature oocyte. We recently demonstrated that MMP2 activation and follicle rupture are regulated by the neuronal hormone octopamine (OA) and the octopamine receptor in mushroombody (OAMB). In the current study, we investigated the role of the superoxide-generating enzyme NADPH oxidase (NOX) in Drosophila ovulation. We report that Nox is highly enriched in mature follicle cells and that Nox knockdown in these cells leads to a reduction in superoxide and to defective ovulation. Similar to MMP2 activation, NOX enzymatic activity is also controlled by the OA/OAMB-Ca2+ signaling pathway. In addition, we report that extracellular superoxide dismutase 3 (SOD3) is required to convert superoxide to hydrogen peroxide, which acts as the key signaling molecule for follicle rupture, independent of MMP2 activation. Given that Nox homologs are expressed in mammalian follicles, the NOX-dependent hydrogen peroxide signaling pathway that we describe could play a conserved role in regulating ovulation in other species.</description><subject>Activation</subject><subject>Animal reproduction</subject><subject>Animals</subject><subject>Biological Sciences</subject><subject>Calcium ions</subject><subject>Calcium signalling</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila Proteins - metabolism</subject><subject>Enzymatic activity</subject><subject>Female</subject><subject>Follicles</subject><subject>Gelatinase A</subject><subject>Homology</subject><subject>Hydrogen peroxide</subject><subject>Hydrogen Peroxide - metabolism</subject><subject>Insects</subject><subject>Mammals</subject><subject>Matrix</subject><subject>Matrix metalloproteinase</subject><subject>Matrix Metalloproteinase 2 - metabolism</subject><subject>Metalloproteinase</subject><subject>NAD(P)H oxidase</subject><subject>NADPH Oxidases - metabolism</subject><subject>Octopamine</subject><subject>Ovarian Follicle - metabolism</subject><subject>Ovulation</subject><subject>Ovulation - physiology</subject><subject>Oxygen</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>Rupturing</subject><subject>Signal transduction</subject><subject>Signal Transduction - physiology</subject><subject>Superoxide dismutase</subject><subject>Superoxide Dismutase - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUFv1DAQhS0EokvhzAkUqRcuaSd24sQXpKoFilQBBzhbs86k9cobBztZ0X_PrLa0gGTJ8sznpzfzhHhdwWkFrTqbRsynVQdQVQ2fJ2JVgalKXRt4KlYAsi27WtZH4kXOGwAwTQfPxZE0pmtBtSux-XJ--e2qiL98j5nKGxop4Ux9kQjd7HfErTuuFnki5ykXfiy2OC-JiiGG4F3gGvKLcqZx9hi4norLFHOcbn3AIu6WgLOP40vxbMCQ6dX9fSx-fPzw_eKqvP766fPF-XXp6lrN7HdoHEhFCp1Ta6gMYAM9YY9ISg5ujS0NbU1u7RClwk6i7KQ2msc1pNWxeH_QnZb1lnrHthIGOyW_xXRnI3r7b2f0t_Ym7qwG3bAGC7y7F0jx50J5tlufHYWAI8UlWwm67brGtIrRk__QTVzSyOMxZXjLoLu9o7MD5XgtOdHwYKYCu8_R7nO0jznyj7d_z_DA_wmOgTcHYJPnmB77mr_zNtRvhiCl-Q</recordid><startdate>20180724</startdate><enddate>20180724</enddate><creator>Li, Wei</creator><creator>Young, Jessica F.</creator><creator>Sun, Jianjun</creator><general>National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6015-738X</orcidid></search><sort><creationdate>20180724</creationdate><title>NADPH oxidase-generated reactive oxygen species in mature follicles are essential for Drosophila ovulation</title><author>Li, Wei ; Young, Jessica F. ; Sun, Jianjun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c443t-84f5c023e3acc3b0190a50deadaae32fcba7ef74ecbcaa23a82a2826960029e63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Activation</topic><topic>Animal reproduction</topic><topic>Animals</topic><topic>Biological Sciences</topic><topic>Calcium ions</topic><topic>Calcium signalling</topic><topic>Drosophila</topic><topic>Drosophila melanogaster</topic><topic>Drosophila Proteins - metabolism</topic><topic>Enzymatic activity</topic><topic>Female</topic><topic>Follicles</topic><topic>Gelatinase A</topic><topic>Homology</topic><topic>Hydrogen peroxide</topic><topic>Hydrogen Peroxide - metabolism</topic><topic>Insects</topic><topic>Mammals</topic><topic>Matrix</topic><topic>Matrix metalloproteinase</topic><topic>Matrix Metalloproteinase 2 - metabolism</topic><topic>Metalloproteinase</topic><topic>NAD(P)H oxidase</topic><topic>NADPH Oxidases - metabolism</topic><topic>Octopamine</topic><topic>Ovarian Follicle - metabolism</topic><topic>Ovulation</topic><topic>Ovulation - physiology</topic><topic>Oxygen</topic><topic>Proteins</topic><topic>Reactive oxygen species</topic><topic>Rupturing</topic><topic>Signal transduction</topic><topic>Signal Transduction - physiology</topic><topic>Superoxide dismutase</topic><topic>Superoxide Dismutase - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Wei</creatorcontrib><creatorcontrib>Young, Jessica F.</creatorcontrib><creatorcontrib>Sun, Jianjun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Wei</au><au>Young, Jessica F.</au><au>Sun, Jianjun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>NADPH oxidase-generated reactive oxygen species in mature follicles are essential for Drosophila ovulation</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2018-07-24</date><risdate>2018</risdate><volume>115</volume><issue>30</issue><spage>7765</spage><epage>7770</epage><pages>7765-7770</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Ovarian reactive oxygen species (ROS) are believed to regulate ovulation in mammals, but the details of ROS production in follicles and the role of ROS in ovulation in other species remain underexplored. In Drosophila ovulation, matrix metalloproteinase 2 (MMP2) is required for follicle rupture by degradation of posterior follicle cells surrounding a mature oocyte. We recently demonstrated that MMP2 activation and follicle rupture are regulated by the neuronal hormone octopamine (OA) and the octopamine receptor in mushroombody (OAMB). In the current study, we investigated the role of the superoxide-generating enzyme NADPH oxidase (NOX) in Drosophila ovulation. We report that Nox is highly enriched in mature follicle cells and that Nox knockdown in these cells leads to a reduction in superoxide and to defective ovulation. Similar to MMP2 activation, NOX enzymatic activity is also controlled by the OA/OAMB-Ca2+ signaling pathway. In addition, we report that extracellular superoxide dismutase 3 (SOD3) is required to convert superoxide to hydrogen peroxide, which acts as the key signaling molecule for follicle rupture, independent of MMP2 activation. Given that Nox homologs are expressed in mammalian follicles, the NOX-dependent hydrogen peroxide signaling pathway that we describe could play a conserved role in regulating ovulation in other species.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>29987037</pmid><doi>10.1073/pnas.1800115115</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0002-6015-738X</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0027-8424 |
| ispartof | Proceedings of the National Academy of Sciences - PNAS, 2018-07, Vol.115 (30), p.7765-7770 |
| issn | 0027-8424 1091-6490 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6065002 |
| source | Jstor Complete Legacy; MEDLINE; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | Activation Animal reproduction Animals Biological Sciences Calcium ions Calcium signalling Drosophila Drosophila melanogaster Drosophila Proteins - metabolism Enzymatic activity Female Follicles Gelatinase A Homology Hydrogen peroxide Hydrogen Peroxide - metabolism Insects Mammals Matrix Matrix metalloproteinase Matrix Metalloproteinase 2 - metabolism Metalloproteinase NAD(P)H oxidase NADPH Oxidases - metabolism Octopamine Ovarian Follicle - metabolism Ovulation Ovulation - physiology Oxygen Proteins Reactive oxygen species Rupturing Signal transduction Signal Transduction - physiology Superoxide dismutase Superoxide Dismutase - metabolism |
| title | NADPH oxidase-generated reactive oxygen species in mature follicles are essential for Drosophila ovulation |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-28T03%3A42%3A11IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=NADPH%20oxidase-generated%20reactive%20oxygen%20species%20in%20mature%20follicles%20are%20essential%20for%20Drosophila%20ovulation&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Li,%20Wei&rft.date=2018-07-24&rft.volume=115&rft.issue=30&rft.spage=7765&rft.epage=7770&rft.pages=7765-7770&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1800115115&rft_dat=%3Cjstor_pubme%3E26511282%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2099980686&rft_id=info:pmid/29987037&rft_jstor_id=26511282&rfr_iscdi=true |