Bradysia (Sciara) coprophila larvae up-regulate DNA repair pathways and down-regulate developmental regulators in response to ionizing radiation

Abstract The level of resistance to radiation and the developmental and molecular responses can vary between species, and even between developmental stages of one species. For flies (order: Diptera), prior studies concluded that the fungus gnat Bradysia (Sciara) coprophila (sub-order: Nematocera) is...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Genetics (Austin) 2024-03, Vol.226 (3)
Hauptverfasser: Urban, John M, Bateman, Jack R, Garza, Kodie R, Borden, Julia, Jain, Jaison, Brown, Alexia, Thach, Bethany J, Bliss, Jacob E, Gerbi, Susan A
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue 3
container_start_page
container_title Genetics (Austin)
container_volume 226
creator Urban, John M
Bateman, Jack R
Garza, Kodie R
Borden, Julia
Jain, Jaison
Brown, Alexia
Thach, Bethany J
Bliss, Jacob E
Gerbi, Susan A
description Abstract The level of resistance to radiation and the developmental and molecular responses can vary between species, and even between developmental stages of one species. For flies (order: Diptera), prior studies concluded that the fungus gnat Bradysia (Sciara) coprophila (sub-order: Nematocera) is more resistant to irradiation-induced mutations that cause visible phenotypes than the fruit fly Drosophila melanogaster (sub-order: Brachycera). Therefore, we characterized the effects of and level of resistance to ionizing radiation on B. coprophila throughout its life cycle. Our data show that B. coprophila embryos are highly sensitive to even low doses of gamma-irradiation, whereas late-stage larvae can tolerate up to 80 Gy (compared to 40 Gy for D. melanogaster) and still retain their ability to develop to adulthood, though with a developmental delay. To survey the genes involved in the early transcriptional response to irradiation of B. coprophila larvae, we compared larval RNA-seq profiles with and without radiation treatment. The up-regulated genes were enriched for DNA damage response genes, including those involved in DNA repair, cell cycle arrest, and apoptosis, whereas the down-regulated genes were enriched for developmental regulators, consistent with the developmental delay of irradiated larvae. Interestingly, members of the PARP and AGO families were highly up-regulated in the B. coprophila radiation response. We compared the transcriptome responses in B. coprophila to the transcriptome responses in D. melanogaster from 3 previous studies: whereas pathway responses are highly conserved, specific gene responses are less so. Our study lays the groundwork for future work on the radiation responses in Diptera.
doi_str_mv 10.1093/genetics/iyad208
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10917502</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/genetics/iyad208</oup_id><sourcerecordid>3113464506</sourcerecordid><originalsourceid>FETCH-LOGICAL-c372t-404b4e0e5be36ac99ee20ef2e342cbe5abca6f6c2b21d27afccd9ef2e889e4793</originalsourceid><addsrcrecordid>eNqFkU1v1DAQhi1ERT_gzglZ4lKEQv2ROMkJlQJtpQoOwNmaOJNdV1nb2MlW21_BT8bVbkvhwskezzPvzPgl5CVn7zhr5ckCHU7WpBO7gV6w5gk54G0pC6Ekf_rovk8OU7pmjKm2ap6RfdkwpRSvD8ivDxH6TbJAj78ZCxHeUOND9GFpR6AjxDUgnUMRcTGPMCH9-OWURgxgIw0wLW9gkyi4nvb-xv2helzj6MMK3QQj3T37mKh1OUrBu4R08tR6Z2-tW9A8hYUph8_J3gBjwhe784j8-Pzp-9lFcfX1_PLs9KowshZTUbKyK5Fh1aFUYNoWUTAcBMpSmA4r6AyoQRnRCd6LGgZj-vYu3zQtlnUrj8j7rW6YuxX2Jk8aYdQh2hXEjfZg9d8ZZ5d64dc6fzyvKyaywvFOIfqfM6ZJr2wyOI7g0M9Ji5aJbICqeEZf_4Ne-zm6vJ-WnMtSlRVTmWJbykSfUsThYRrO7tpKfe-33vmdS1493uKh4N7gDLzdAn4O_5f7Dfd1vjk</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3113464506</pqid></control><display><type>article</type><title>Bradysia (Sciara) coprophila larvae up-regulate DNA repair pathways and down-regulate developmental regulators in response to ionizing radiation</title><source>MEDLINE</source><source>Oxford University Press Journals All Titles (1996-Current)</source><creator>Urban, John M ; Bateman, Jack R ; Garza, Kodie R ; Borden, Julia ; Jain, Jaison ; Brown, Alexia ; Thach, Bethany J ; Bliss, Jacob E ; Gerbi, Susan A</creator><contributor>Calvi, B</contributor><creatorcontrib>Urban, John M ; Bateman, Jack R ; Garza, Kodie R ; Borden, Julia ; Jain, Jaison ; Brown, Alexia ; Thach, Bethany J ; Bliss, Jacob E ; Gerbi, Susan A ; Calvi, B</creatorcontrib><description>Abstract The level of resistance to radiation and the developmental and molecular responses can vary between species, and even between developmental stages of one species. For flies (order: Diptera), prior studies concluded that the fungus gnat Bradysia (Sciara) coprophila (sub-order: Nematocera) is more resistant to irradiation-induced mutations that cause visible phenotypes than the fruit fly Drosophila melanogaster (sub-order: Brachycera). Therefore, we characterized the effects of and level of resistance to ionizing radiation on B. coprophila throughout its life cycle. Our data show that B. coprophila embryos are highly sensitive to even low doses of gamma-irradiation, whereas late-stage larvae can tolerate up to 80 Gy (compared to 40 Gy for D. melanogaster) and still retain their ability to develop to adulthood, though with a developmental delay. To survey the genes involved in the early transcriptional response to irradiation of B. coprophila larvae, we compared larval RNA-seq profiles with and without radiation treatment. The up-regulated genes were enriched for DNA damage response genes, including those involved in DNA repair, cell cycle arrest, and apoptosis, whereas the down-regulated genes were enriched for developmental regulators, consistent with the developmental delay of irradiated larvae. Interestingly, members of the PARP and AGO families were highly up-regulated in the B. coprophila radiation response. We compared the transcriptome responses in B. coprophila to the transcriptome responses in D. melanogaster from 3 previous studies: whereas pathway responses are highly conserved, specific gene responses are less so. Our study lays the groundwork for future work on the radiation responses in Diptera.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1093/genetics/iyad208</identifier><identifier>PMID: 38066617</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Animals ; Apoptosis ; Bradysia ; Bradysia coprophila ; Cell cycle ; Deoxyribonucleic acid ; Developmental stages ; Diptera ; Diptera - genetics ; DNA ; DNA damage ; DNA Repair ; Drosophila - genetics ; Drosophila melanogaster - genetics ; Embryos ; Fruit flies ; Gamma irradiation ; Genes ; Humans ; Investigation ; Ionizing radiation ; Irradiation ; Larva - genetics ; Larvae ; Nematocera ; Phenotypes ; Radiation ; Radiation damage ; Radiation tolerance ; Radiation, Ionizing ; Transcriptomes ; γ Radiation</subject><ispartof>Genetics (Austin), 2024-03, Vol.226 (3)</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c372t-404b4e0e5be36ac99ee20ef2e342cbe5abca6f6c2b21d27afccd9ef2e889e4793</cites><orcidid>0000-0001-9270-6569 ; 0000-0002-8782-5958 ; 0000-0003-2148-7180</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38066617$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Calvi, B</contributor><creatorcontrib>Urban, John M</creatorcontrib><creatorcontrib>Bateman, Jack R</creatorcontrib><creatorcontrib>Garza, Kodie R</creatorcontrib><creatorcontrib>Borden, Julia</creatorcontrib><creatorcontrib>Jain, Jaison</creatorcontrib><creatorcontrib>Brown, Alexia</creatorcontrib><creatorcontrib>Thach, Bethany J</creatorcontrib><creatorcontrib>Bliss, Jacob E</creatorcontrib><creatorcontrib>Gerbi, Susan A</creatorcontrib><title>Bradysia (Sciara) coprophila larvae up-regulate DNA repair pathways and down-regulate developmental regulators in response to ionizing radiation</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Abstract The level of resistance to radiation and the developmental and molecular responses can vary between species, and even between developmental stages of one species. For flies (order: Diptera), prior studies concluded that the fungus gnat Bradysia (Sciara) coprophila (sub-order: Nematocera) is more resistant to irradiation-induced mutations that cause visible phenotypes than the fruit fly Drosophila melanogaster (sub-order: Brachycera). Therefore, we characterized the effects of and level of resistance to ionizing radiation on B. coprophila throughout its life cycle. Our data show that B. coprophila embryos are highly sensitive to even low doses of gamma-irradiation, whereas late-stage larvae can tolerate up to 80 Gy (compared to 40 Gy for D. melanogaster) and still retain their ability to develop to adulthood, though with a developmental delay. To survey the genes involved in the early transcriptional response to irradiation of B. coprophila larvae, we compared larval RNA-seq profiles with and without radiation treatment. The up-regulated genes were enriched for DNA damage response genes, including those involved in DNA repair, cell cycle arrest, and apoptosis, whereas the down-regulated genes were enriched for developmental regulators, consistent with the developmental delay of irradiated larvae. Interestingly, members of the PARP and AGO families were highly up-regulated in the B. coprophila radiation response. We compared the transcriptome responses in B. coprophila to the transcriptome responses in D. melanogaster from 3 previous studies: whereas pathway responses are highly conserved, specific gene responses are less so. Our study lays the groundwork for future work on the radiation responses in Diptera.</description><subject>Animals</subject><subject>Apoptosis</subject><subject>Bradysia</subject><subject>Bradysia coprophila</subject><subject>Cell cycle</subject><subject>Deoxyribonucleic acid</subject><subject>Developmental stages</subject><subject>Diptera</subject><subject>Diptera - genetics</subject><subject>DNA</subject><subject>DNA damage</subject><subject>DNA Repair</subject><subject>Drosophila - genetics</subject><subject>Drosophila melanogaster - genetics</subject><subject>Embryos</subject><subject>Fruit flies</subject><subject>Gamma irradiation</subject><subject>Genes</subject><subject>Humans</subject><subject>Investigation</subject><subject>Ionizing radiation</subject><subject>Irradiation</subject><subject>Larva - genetics</subject><subject>Larvae</subject><subject>Nematocera</subject><subject>Phenotypes</subject><subject>Radiation</subject><subject>Radiation damage</subject><subject>Radiation tolerance</subject><subject>Radiation, Ionizing</subject><subject>Transcriptomes</subject><subject>γ Radiation</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1v1DAQhi1ERT_gzglZ4lKEQv2ROMkJlQJtpQoOwNmaOJNdV1nb2MlW21_BT8bVbkvhwskezzPvzPgl5CVn7zhr5ckCHU7WpBO7gV6w5gk54G0pC6Ekf_rovk8OU7pmjKm2ap6RfdkwpRSvD8ivDxH6TbJAj78ZCxHeUOND9GFpR6AjxDUgnUMRcTGPMCH9-OWURgxgIw0wLW9gkyi4nvb-xv2helzj6MMK3QQj3T37mKh1OUrBu4R08tR6Z2-tW9A8hYUph8_J3gBjwhe784j8-Pzp-9lFcfX1_PLs9KowshZTUbKyK5Fh1aFUYNoWUTAcBMpSmA4r6AyoQRnRCd6LGgZj-vYu3zQtlnUrj8j7rW6YuxX2Jk8aYdQh2hXEjfZg9d8ZZ5d64dc6fzyvKyaywvFOIfqfM6ZJr2wyOI7g0M9Ji5aJbICqeEZf_4Ne-zm6vJ-WnMtSlRVTmWJbykSfUsThYRrO7tpKfe-33vmdS1493uKh4N7gDLzdAn4O_5f7Dfd1vjk</recordid><startdate>20240306</startdate><enddate>20240306</enddate><creator>Urban, John M</creator><creator>Bateman, Jack R</creator><creator>Garza, Kodie R</creator><creator>Borden, Julia</creator><creator>Jain, Jaison</creator><creator>Brown, Alexia</creator><creator>Thach, Bethany J</creator><creator>Bliss, Jacob E</creator><creator>Gerbi, Susan A</creator><general>Oxford University Press</general><general>Genetics Society of America</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>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9270-6569</orcidid><orcidid>https://orcid.org/0000-0002-8782-5958</orcidid><orcidid>https://orcid.org/0000-0003-2148-7180</orcidid></search><sort><creationdate>20240306</creationdate><title>Bradysia (Sciara) coprophila larvae up-regulate DNA repair pathways and down-regulate developmental regulators in response to ionizing radiation</title><author>Urban, John M ; Bateman, Jack R ; Garza, Kodie R ; Borden, Julia ; Jain, Jaison ; Brown, Alexia ; Thach, Bethany J ; Bliss, Jacob E ; Gerbi, Susan A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c372t-404b4e0e5be36ac99ee20ef2e342cbe5abca6f6c2b21d27afccd9ef2e889e4793</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Apoptosis</topic><topic>Bradysia</topic><topic>Bradysia coprophila</topic><topic>Cell cycle</topic><topic>Deoxyribonucleic acid</topic><topic>Developmental stages</topic><topic>Diptera</topic><topic>Diptera - genetics</topic><topic>DNA</topic><topic>DNA damage</topic><topic>DNA Repair</topic><topic>Drosophila - genetics</topic><topic>Drosophila melanogaster - genetics</topic><topic>Embryos</topic><topic>Fruit flies</topic><topic>Gamma irradiation</topic><topic>Genes</topic><topic>Humans</topic><topic>Investigation</topic><topic>Ionizing radiation</topic><topic>Irradiation</topic><topic>Larva - genetics</topic><topic>Larvae</topic><topic>Nematocera</topic><topic>Phenotypes</topic><topic>Radiation</topic><topic>Radiation damage</topic><topic>Radiation tolerance</topic><topic>Radiation, Ionizing</topic><topic>Transcriptomes</topic><topic>γ Radiation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Urban, John M</creatorcontrib><creatorcontrib>Bateman, Jack R</creatorcontrib><creatorcontrib>Garza, Kodie R</creatorcontrib><creatorcontrib>Borden, Julia</creatorcontrib><creatorcontrib>Jain, Jaison</creatorcontrib><creatorcontrib>Brown, Alexia</creatorcontrib><creatorcontrib>Thach, Bethany J</creatorcontrib><creatorcontrib>Bliss, Jacob E</creatorcontrib><creatorcontrib>Gerbi, Susan A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>University Readers</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</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>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Urban, John M</au><au>Bateman, Jack R</au><au>Garza, Kodie R</au><au>Borden, Julia</au><au>Jain, Jaison</au><au>Brown, Alexia</au><au>Thach, Bethany J</au><au>Bliss, Jacob E</au><au>Gerbi, Susan A</au><au>Calvi, B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bradysia (Sciara) coprophila larvae up-regulate DNA repair pathways and down-regulate developmental regulators in response to ionizing radiation</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2024-03-06</date><risdate>2024</risdate><volume>226</volume><issue>3</issue><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><abstract>Abstract The level of resistance to radiation and the developmental and molecular responses can vary between species, and even between developmental stages of one species. For flies (order: Diptera), prior studies concluded that the fungus gnat Bradysia (Sciara) coprophila (sub-order: Nematocera) is more resistant to irradiation-induced mutations that cause visible phenotypes than the fruit fly Drosophila melanogaster (sub-order: Brachycera). Therefore, we characterized the effects of and level of resistance to ionizing radiation on B. coprophila throughout its life cycle. Our data show that B. coprophila embryos are highly sensitive to even low doses of gamma-irradiation, whereas late-stage larvae can tolerate up to 80 Gy (compared to 40 Gy for D. melanogaster) and still retain their ability to develop to adulthood, though with a developmental delay. To survey the genes involved in the early transcriptional response to irradiation of B. coprophila larvae, we compared larval RNA-seq profiles with and without radiation treatment. The up-regulated genes were enriched for DNA damage response genes, including those involved in DNA repair, cell cycle arrest, and apoptosis, whereas the down-regulated genes were enriched for developmental regulators, consistent with the developmental delay of irradiated larvae. Interestingly, members of the PARP and AGO families were highly up-regulated in the B. coprophila radiation response. We compared the transcriptome responses in B. coprophila to the transcriptome responses in D. melanogaster from 3 previous studies: whereas pathway responses are highly conserved, specific gene responses are less so. Our study lays the groundwork for future work on the radiation responses in Diptera.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>38066617</pmid><doi>10.1093/genetics/iyad208</doi><orcidid>https://orcid.org/0000-0001-9270-6569</orcidid><orcidid>https://orcid.org/0000-0002-8782-5958</orcidid><orcidid>https://orcid.org/0000-0003-2148-7180</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 1943-2631
ispartof Genetics (Austin), 2024-03, Vol.226 (3)
issn 1943-2631
0016-6731
1943-2631
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10917502
source MEDLINE; Oxford University Press Journals All Titles (1996-Current)
subjects Animals
Apoptosis
Bradysia
Bradysia coprophila
Cell cycle
Deoxyribonucleic acid
Developmental stages
Diptera
Diptera - genetics
DNA
DNA damage
DNA Repair
Drosophila - genetics
Drosophila melanogaster - genetics
Embryos
Fruit flies
Gamma irradiation
Genes
Humans
Investigation
Ionizing radiation
Irradiation
Larva - genetics
Larvae
Nematocera
Phenotypes
Radiation
Radiation damage
Radiation tolerance
Radiation, Ionizing
Transcriptomes
γ Radiation
title Bradysia (Sciara) coprophila larvae up-regulate DNA repair pathways and down-regulate developmental regulators in response to ionizing radiation
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T21%3A47%3A31IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Bradysia%20(Sciara)%20coprophila%20larvae%20up-regulate%20DNA%20repair%20pathways%20and%20down-regulate%20developmental%20regulators%20in%20response%20to%20ionizing%20radiation&rft.jtitle=Genetics%20(Austin)&rft.au=Urban,%20John%20M&rft.date=2024-03-06&rft.volume=226&rft.issue=3&rft.issn=1943-2631&rft.eissn=1943-2631&rft_id=info:doi/10.1093/genetics/iyad208&rft_dat=%3Cproquest_pubme%3E3113464506%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3113464506&rft_id=info:pmid/38066617&rft_oup_id=10.1093/genetics/iyad208&rfr_iscdi=true