JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutants
Summary: Robust tissue growth is orchestrated by the precise coordination of cell death and cell proliferation. In the developing wing pouches of Drosophila Minute/+ animals, both cell death and compensatory cell proliferation are increased, thereby contributing to robust growth of mutant tissue. He...
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Elsevier
2025-06-01
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| Series: | iScience |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S258900422500848X |
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| author | Nanami Akai Yoshimasa Yagi Tatsushi Igaki Shizue Ohsawa |
| author_facet | Nanami Akai Yoshimasa Yagi Tatsushi Igaki Shizue Ohsawa |
| author_sort | Nanami Akai |
| collection | DOAJ |
| description | Summary: Robust tissue growth is orchestrated by the precise coordination of cell death and cell proliferation. In the developing wing pouches of Drosophila Minute/+ animals, both cell death and compensatory cell proliferation are increased, thereby contributing to robust growth of mutant tissue. Here, we show that JNK-mediated elevation of exocytosis in dying cells is crucial for triggering cell turnover in M/+ wing morphogenesis. Mechanistically, elevated JNK signaling in dying cells upregulates exocytosis-related genes and Wingless (Wg), leading to enhanced Wg secretion. Notably, increased exocytosis promotes caspase activation via an exocytosis-Dronc amplification loop, sustaining apoptotic signaling while reinforcing Wg secretion through Dronc activation. Furthermore, this exocytosis-mediated Wg secretion and apoptotic feedback loop universally occurs downstream of JNK signaling, regardless of the genetic background. Overall, our findings provide mechanistic insights into robust tissue growth through the orchestration of cell turnover, primarily via JNK-mediated exocytosis during Drosophila Minute/+ wing morphogenesis. |
| format | Article |
| id | doaj-art-e64a1f50c8c64c42b442d2fce8264639 |
| institution | DOAJ |
| issn | 2589-0042 |
| language | English |
| publishDate | 2025-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj-art-e64a1f50c8c64c42b442d2fce82646392025-08-20T03:13:00ZengElsevieriScience2589-00422025-06-0128611258710.1016/j.isci.2025.112587JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutantsNanami Akai0Yoshimasa Yagi1Tatsushi Igaki2Shizue Ohsawa3Group of Genetics, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8602, JapanGroup of Genetics, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8602, JapanLaboratory of Genetics, Graduate School of Biostudies, Kyoto University, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, JapanGroup of Genetics, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8602, Japan; Corresponding authorSummary: Robust tissue growth is orchestrated by the precise coordination of cell death and cell proliferation. In the developing wing pouches of Drosophila Minute/+ animals, both cell death and compensatory cell proliferation are increased, thereby contributing to robust growth of mutant tissue. Here, we show that JNK-mediated elevation of exocytosis in dying cells is crucial for triggering cell turnover in M/+ wing morphogenesis. Mechanistically, elevated JNK signaling in dying cells upregulates exocytosis-related genes and Wingless (Wg), leading to enhanced Wg secretion. Notably, increased exocytosis promotes caspase activation via an exocytosis-Dronc amplification loop, sustaining apoptotic signaling while reinforcing Wg secretion through Dronc activation. Furthermore, this exocytosis-mediated Wg secretion and apoptotic feedback loop universally occurs downstream of JNK signaling, regardless of the genetic background. Overall, our findings provide mechanistic insights into robust tissue growth through the orchestration of cell turnover, primarily via JNK-mediated exocytosis during Drosophila Minute/+ wing morphogenesis.http://www.sciencedirect.com/science/article/pii/S258900422500848XCell biologyFunctional aspects of cell biologyDevelopmental biology |
| spellingShingle | Nanami Akai Yoshimasa Yagi Tatsushi Igaki Shizue Ohsawa JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutants iScience Cell biology Functional aspects of cell biology Developmental biology |
| title | JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutants |
| title_full | JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutants |
| title_fullStr | JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutants |
| title_full_unstemmed | JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutants |
| title_short | JNK signaling coordinates epithelial cell turnover through exocytosis in Drosophila ribosomal protein mutants |
| title_sort | jnk signaling coordinates epithelial cell turnover through exocytosis in drosophila ribosomal protein mutants |
| topic | Cell biology Functional aspects of cell biology Developmental biology |
| url | http://www.sciencedirect.com/science/article/pii/S258900422500848X |
| work_keys_str_mv | AT nanamiakai jnksignalingcoordinatesepithelialcellturnoverthroughexocytosisindrosophilaribosomalproteinmutants AT yoshimasayagi jnksignalingcoordinatesepithelialcellturnoverthroughexocytosisindrosophilaribosomalproteinmutants AT tatsushiigaki jnksignalingcoordinatesepithelialcellturnoverthroughexocytosisindrosophilaribosomalproteinmutants AT shizueohsawa jnksignalingcoordinatesepithelialcellturnoverthroughexocytosisindrosophilaribosomalproteinmutants |