p53-dependent programmed necrosis controls germ cell homeostasis during spermatogenesis
The importance of regulated necrosis in pathologies such as cerebral stroke and myocardial infarction is now fully recognized. However, the physiological relevance of regulated necrosis remains unclear. Here, we report a conserved role for p53 in regulating necrosis in Drosophila and mammalian sperm...
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| creator | Napoletano, Francesco Gibert, Benjamin Yacobi-Sharon, Keren Vincent, Stéphane Favrot, Clémentine Mehlen, Patrick Girard, Victor Teil, Margaux Chatelain, Gilles Walter, Ludivine Arama, Eli Mollereau, Bertrand |
| description | The importance of regulated necrosis in pathologies such as cerebral stroke and myocardial infarction is now fully recognized. However, the physiological relevance of regulated necrosis remains unclear. Here, we report a conserved role for p53 in regulating necrosis in Drosophila and mammalian spermatogenesis. We found that Drosophila p53 is required for the programmed necrosis that occurs spontaneously in mitotic germ cells during spermatogenesis. This form of necrosis involved an atypical function of the initiator caspase Dronc/Caspase 9, independent of its catalytic activity. Prevention of p53-dependent necrosis resulted in testicular hyperplasia, which was reversed by restoring necrosis in spermatogonia. In mouse testes, p53 was required for heat-induced germ cell necrosis, indicating that regulation of necrosis is a primordial function of p53 conserved from invertebrates to vertebrates. Drosophila and mouse spermatogenesis will thus be useful models to identify inducers of necrosis to treat cancers that are refractory to apoptosis. |
| doi_str_mv | 10.1371/journal.pgen.1007024 |
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However, the physiological relevance of regulated necrosis remains unclear. Here, we report a conserved role for p53 in regulating necrosis in Drosophila and mammalian spermatogenesis. We found that Drosophila p53 is required for the programmed necrosis that occurs spontaneously in mitotic germ cells during spermatogenesis. This form of necrosis involved an atypical function of the initiator caspase Dronc/Caspase 9, independent of its catalytic activity. Prevention of p53-dependent necrosis resulted in testicular hyperplasia, which was reversed by restoring necrosis in spermatogonia. In mouse testes, p53 was required for heat-induced germ cell necrosis, indicating that regulation of necrosis is a primordial function of p53 conserved from invertebrates to vertebrates. Drosophila and mouse spermatogenesis will thus be useful models to identify inducers of necrosis to treat cancers that are refractory to apoptosis.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1007024</identifier><identifier>PMID: 28945745</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal models ; Animals ; Apoptosis ; Apoptosis - genetics ; Biology ; Biology and Life Sciences ; Cancer ; Caspase ; Caspase 9 - genetics ; Caspase-9 ; Caspases - genetics ; Catalytic activity ; Cell adhesion & migration ; Cell death ; Cellular Biology ; Cerebral infarction ; Disease Models, Animal ; Drosophila ; Drosophila melanogaster - genetics ; Drosophila melanogaster - growth & development ; Drosophila Proteins - genetics ; Fruit flies ; Funding ; Gangrene ; Gene expression ; Genetic aspects ; Germ cells ; Germ Cells - growth & development ; Germ Cells - pathology ; Health aspects ; Homeostasis ; Homeostasis - genetics ; Humans ; Hyperplasia ; Hyperplasia - genetics ; Hyperplasia - pathology ; Inducers ; Infarction ; Insects ; Invertebrates ; Laboratories ; Life Sciences ; Male ; Medicine and Health Sciences ; Mice ; Myocardial infarction ; Necrosis ; Necrosis - genetics ; Necrosis - pathology ; p53 Protein ; Physiology ; Proteins ; Research and Analysis Methods ; Rodents ; Sperm ; Spermatogenesis ; Spermatogenesis - genetics ; Spermatogonia ; Supervision ; Testes ; Testis - growth & development ; Testis - metabolism ; Tumor Suppressor Protein p53 - genetics ; Vertebrates ; Visualization</subject><ispartof>PLoS genetics, 2017-09, Vol.13 (9), p.e1007024-e1007024</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Napoletano F, Gibert B, Yacobi-Sharon K, Vincent S, Favrot C, Mehlen P, et al. (2017) p53-dependent programmed necrosis controls germ cell homeostasis during spermatogenesis. PLoS Genet13(9): e1007024. https://doi.org/10.1371/journal.pgen.1007024</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2017 Napoletano et al 2017 Napoletano et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Napoletano F, Gibert B, Yacobi-Sharon K, Vincent S, Favrot C, Mehlen P, et al. (2017) p53-dependent programmed necrosis controls germ cell homeostasis during spermatogenesis. PLoS Genet13(9): e1007024. https://doi.org/10.1371/journal.pgen.1007024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c789t-b5c2a3d77fc6d540ee28b5c79ee8f8124071c700678c5c575820445d1cb1c3913</citedby><cites>FETCH-LOGICAL-c789t-b5c2a3d77fc6d540ee28b5c79ee8f8124071c700678c5c575820445d1cb1c3913</cites><orcidid>0000-0001-9677-5449 ; 0000-0003-4710-8185 ; 0000-0003-1743-5417 ; 0000-0002-5295-3124</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5629030/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5629030/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28945745$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://inserm.hal.science/inserm-02157622$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Copenhaver, Gregory P.</contributor><creatorcontrib>Napoletano, Francesco</creatorcontrib><creatorcontrib>Gibert, Benjamin</creatorcontrib><creatorcontrib>Yacobi-Sharon, Keren</creatorcontrib><creatorcontrib>Vincent, Stéphane</creatorcontrib><creatorcontrib>Favrot, Clémentine</creatorcontrib><creatorcontrib>Mehlen, Patrick</creatorcontrib><creatorcontrib>Girard, Victor</creatorcontrib><creatorcontrib>Teil, Margaux</creatorcontrib><creatorcontrib>Chatelain, Gilles</creatorcontrib><creatorcontrib>Walter, Ludivine</creatorcontrib><creatorcontrib>Arama, Eli</creatorcontrib><creatorcontrib>Mollereau, Bertrand</creatorcontrib><title>p53-dependent programmed necrosis controls germ cell homeostasis during spermatogenesis</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The importance of regulated necrosis in pathologies such as cerebral stroke and myocardial infarction is now fully recognized. However, the physiological relevance of regulated necrosis remains unclear. Here, we report a conserved role for p53 in regulating necrosis in Drosophila and mammalian spermatogenesis. We found that Drosophila p53 is required for the programmed necrosis that occurs spontaneously in mitotic germ cells during spermatogenesis. This form of necrosis involved an atypical function of the initiator caspase Dronc/Caspase 9, independent of its catalytic activity. Prevention of p53-dependent necrosis resulted in testicular hyperplasia, which was reversed by restoring necrosis in spermatogonia. In mouse testes, p53 was required for heat-induced germ cell necrosis, indicating that regulation of necrosis is a primordial function of p53 conserved from invertebrates to vertebrates. Drosophila and mouse spermatogenesis will thus be useful models to identify inducers of necrosis to treat cancers that are refractory to apoptosis.</description><subject>Animal models</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Apoptosis - genetics</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cancer</subject><subject>Caspase</subject><subject>Caspase 9 - genetics</subject><subject>Caspase-9</subject><subject>Caspases - genetics</subject><subject>Catalytic activity</subject><subject>Cell adhesion & migration</subject><subject>Cell death</subject><subject>Cellular Biology</subject><subject>Cerebral infarction</subject><subject>Disease Models, Animal</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - growth & development</subject><subject>Drosophila Proteins - genetics</subject><subject>Fruit flies</subject><subject>Funding</subject><subject>Gangrene</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Germ cells</subject><subject>Germ Cells - growth & development</subject><subject>Germ Cells - pathology</subject><subject>Health aspects</subject><subject>Homeostasis</subject><subject>Homeostasis - genetics</subject><subject>Humans</subject><subject>Hyperplasia</subject><subject>Hyperplasia - genetics</subject><subject>Hyperplasia - pathology</subject><subject>Inducers</subject><subject>Infarction</subject><subject>Insects</subject><subject>Invertebrates</subject><subject>Laboratories</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Mice</subject><subject>Myocardial infarction</subject><subject>Necrosis</subject><subject>Necrosis - genetics</subject><subject>Necrosis - pathology</subject><subject>p53 Protein</subject><subject>Physiology</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Rodents</subject><subject>Sperm</subject><subject>Spermatogenesis</subject><subject>Spermatogenesis - genetics</subject><subject>Spermatogonia</subject><subject>Supervision</subject><subject>Testes</subject><subject>Testis - 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However, the physiological relevance of regulated necrosis remains unclear. Here, we report a conserved role for p53 in regulating necrosis in Drosophila and mammalian spermatogenesis. We found that Drosophila p53 is required for the programmed necrosis that occurs spontaneously in mitotic germ cells during spermatogenesis. This form of necrosis involved an atypical function of the initiator caspase Dronc/Caspase 9, independent of its catalytic activity. Prevention of p53-dependent necrosis resulted in testicular hyperplasia, which was reversed by restoring necrosis in spermatogonia. In mouse testes, p53 was required for heat-induced germ cell necrosis, indicating that regulation of necrosis is a primordial function of p53 conserved from invertebrates to vertebrates. 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| ispartof | PLoS genetics, 2017-09, Vol.13 (9), p.e1007024-e1007024 |
| issn | 1553-7404 1553-7390 1553-7404 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Public Library of Science (PLoS) |
| subjects | Animal models Animals Apoptosis Apoptosis - genetics Biology Biology and Life Sciences Cancer Caspase Caspase 9 - genetics Caspase-9 Caspases - genetics Catalytic activity Cell adhesion & migration Cell death Cellular Biology Cerebral infarction Disease Models, Animal Drosophila Drosophila melanogaster - genetics Drosophila melanogaster - growth & development Drosophila Proteins - genetics Fruit flies Funding Gangrene Gene expression Genetic aspects Germ cells Germ Cells - growth & development Germ Cells - pathology Health aspects Homeostasis Homeostasis - genetics Humans Hyperplasia Hyperplasia - genetics Hyperplasia - pathology Inducers Infarction Insects Invertebrates Laboratories Life Sciences Male Medicine and Health Sciences Mice Myocardial infarction Necrosis Necrosis - genetics Necrosis - pathology p53 Protein Physiology Proteins Research and Analysis Methods Rodents Sperm Spermatogenesis Spermatogenesis - genetics Spermatogonia Supervision Testes Testis - growth & development Testis - metabolism Tumor Suppressor Protein p53 - genetics Vertebrates Visualization |
| title | p53-dependent programmed necrosis controls germ cell homeostasis during spermatogenesis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-31T05%3A28%3A24IST&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=p53-dependent%20programmed%20necrosis%20controls%20germ%20cell%20homeostasis%20during%20spermatogenesis&rft.jtitle=PLoS%20genetics&rft.au=Napoletano,%20Francesco&rft.date=2017-09-25&rft.volume=13&rft.issue=9&rft.spage=e1007024&rft.epage=e1007024&rft.pages=e1007024-e1007024&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1007024&rft_dat=%3Cgale_plos_%3EA507384949%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=1951454262&rft_id=info:pmid/28945745&rft_galeid=A507384949&rft_doaj_id=oai_doaj_org_article_4cfaff968de847969b9559035d236637&rfr_iscdi=true |