Extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate Ciona
Abstract Apoptosis is a regulated cell death ubiquitous in animals defined by morphological features depending on caspases. Two regulation pathways are described, currently named the intrinsic and the extrinsic apoptosis. While intrinsic apoptosis is well studied and considered ancestral among metaz...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-03-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-48411-y |
| _version_ | 1797266779297284096 |
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| author | Gabriel Krasovec Cécile Renaud Éric Quéinnec Yasunori Sasakura Jean-Philippe Chambon |
| author_facet | Gabriel Krasovec Cécile Renaud Éric Quéinnec Yasunori Sasakura Jean-Philippe Chambon |
| author_sort | Gabriel Krasovec |
| collection | DOAJ |
| description | Abstract Apoptosis is a regulated cell death ubiquitous in animals defined by morphological features depending on caspases. Two regulation pathways are described, currently named the intrinsic and the extrinsic apoptosis. While intrinsic apoptosis is well studied and considered ancestral among metazoans, extrinsic apoptosis is poorly studied outside mammals. Here, we address extrinsic apoptosis in the urochordates Ciona, belonging to the sister group of vertebrates. During metamorphosis, Ciona larvae undergo a tail regression depending on tissue contraction, migration and apoptosis. Apoptosis begin at the tail tip and propagates towards the trunk as a polarized wave. We identified Ci-caspase 8/10 by phylogenetic analysis as homolog to vertebrate caspases 8 and 10 that are the specific initiator of extrinsic apoptosis. We detected Ci-caspase 8/10 expression in Ciona larvae, especially at the tail tip. We showed that chemical inhibition of Ci-caspase 8/10 leads to a delay of tail regression, and Ci-caspase 8/10 loss of function induced an incomplete tail regression. The specificity between apoptotic pathways and initiator caspase suggests that extrinsic apoptosis regulates cell death during the tail regression. Our study presents rare in vivo work on extrinsic apoptosis outside mammals, and contribute to the discussion on its evolutionary history in animals. |
| first_indexed | 2024-04-25T01:06:07Z |
| format | Article |
| id | doaj.art-8c395c1a498c4862a0dc3a6ebd21c5ea |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-25T01:06:07Z |
| publishDate | 2024-03-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-8c395c1a498c4862a0dc3a6ebd21c5ea2024-03-10T12:13:38ZengNature PortfolioScientific Reports2045-23222024-03-0114111010.1038/s41598-023-48411-yExtrinsic apoptosis participates to tail regression during the metamorphosis of the chordate CionaGabriel Krasovec0Cécile Renaud1Éric Quéinnec2Yasunori Sasakura3Jean-Philippe Chambon4Institut de Systématique, Evolution, Biodiversité, Sorbonne Université, Muséum National d’Histoire Naturelle, CNRS, EPHEInstitut de Systématique, Evolution, Biodiversité, Sorbonne Université, Muséum National d’Histoire Naturelle, CNRS, EPHEInstitut de Systématique, Evolution, Biodiversité, Sorbonne Université, Muséum National d’Histoire Naturelle, CNRS, EPHEShimoda Marine Research Center, University of TsukubaCRBM, Université de Montpellier, CNRSAbstract Apoptosis is a regulated cell death ubiquitous in animals defined by morphological features depending on caspases. Two regulation pathways are described, currently named the intrinsic and the extrinsic apoptosis. While intrinsic apoptosis is well studied and considered ancestral among metazoans, extrinsic apoptosis is poorly studied outside mammals. Here, we address extrinsic apoptosis in the urochordates Ciona, belonging to the sister group of vertebrates. During metamorphosis, Ciona larvae undergo a tail regression depending on tissue contraction, migration and apoptosis. Apoptosis begin at the tail tip and propagates towards the trunk as a polarized wave. We identified Ci-caspase 8/10 by phylogenetic analysis as homolog to vertebrate caspases 8 and 10 that are the specific initiator of extrinsic apoptosis. We detected Ci-caspase 8/10 expression in Ciona larvae, especially at the tail tip. We showed that chemical inhibition of Ci-caspase 8/10 leads to a delay of tail regression, and Ci-caspase 8/10 loss of function induced an incomplete tail regression. The specificity between apoptotic pathways and initiator caspase suggests that extrinsic apoptosis regulates cell death during the tail regression. Our study presents rare in vivo work on extrinsic apoptosis outside mammals, and contribute to the discussion on its evolutionary history in animals.https://doi.org/10.1038/s41598-023-48411-y |
| spellingShingle | Gabriel Krasovec Cécile Renaud Éric Quéinnec Yasunori Sasakura Jean-Philippe Chambon Extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate Ciona Scientific Reports |
| title | Extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate Ciona |
| title_full | Extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate Ciona |
| title_fullStr | Extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate Ciona |
| title_full_unstemmed | Extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate Ciona |
| title_short | Extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate Ciona |
| title_sort | extrinsic apoptosis participates to tail regression during the metamorphosis of the chordate ciona |
| url | https://doi.org/10.1038/s41598-023-48411-y |
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