Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad
Organogenesis requires the proper production of diverse cell types and their positioning/migration. However, the coordination of these processes during development remains poorly understood. The gonad in C. elegans exhibits a mirror-symmetric structure guided by the migration of distal tip cells (DT...
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eLife Sciences Publications Ltd
2024-11-01
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| Online Access: | https://elifesciences.org/articles/103035 |
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| author | Shuhei So Masayo Asakawa Hitoshi Sawa |
| author_facet | Shuhei So Masayo Asakawa Hitoshi Sawa |
| author_sort | Shuhei So |
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| description | Organogenesis requires the proper production of diverse cell types and their positioning/migration. However, the coordination of these processes during development remains poorly understood. The gonad in C. elegans exhibits a mirror-symmetric structure guided by the migration of distal tip cells (DTCs), which result from asymmetric divisions of somatic gonadal precursors (SGPs; Z1 and Z4). We found that the polarity of Z1 and Z4, which possess mirror-symmetric orientation, is controlled by the redundant functions of the LIN-17/Frizzled receptor and three Wnt proteins (CWN-1, CWN-2, and EGL-20) with distinct functions. In lin-17 mutants, CWN-2 promotes normal polarity in both Z1 and Z4, while CWN-1 promotes reverse and normal polarity in Z1 and Z4, respectively. In contrast, EGL-20 inhibits the polarization of both Z1 and Z4. In lin-17 egl-20 cwn-2 triple mutants with a polarity reversal of Z1, DTCs from Z1 frequently miss-migrate to the posterior side. Our further analysis demonstrates that the mis-positioning of DTCs in the gonad due to the polarity reversal of Z1 leads to mis-migration. Similar mis-migration was also observed in cki-1(RNAi) animals producing ectopic DTCs. These results highlight the role of Wnt signaling in coordinating the production and migration of DTCs to establish a mirror-symmetric organ. |
| format | Article |
| id | doaj-art-343da4e03e3e4d8596f3b22970f8cf47 |
| institution | OA Journals |
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| language | English |
| publishDate | 2024-11-01 |
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| spelling | doaj-art-343da4e03e3e4d8596f3b22970f8cf472025-08-20T02:31:24ZengeLife Sciences Publications LtdeLife2050-084X2024-11-011310.7554/eLife.103035Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonadShuhei So0https://orcid.org/0000-0002-1730-6693Masayo Asakawa1Hitoshi Sawa2https://orcid.org/0000-0001-9774-7976Multicellular Organization Laboratory, Department of Gene Function and Phenomics, National Institute of Genetics, Research Organization of Information and Systems (ROIS), Mishima, JapanMulticellular Organization Laboratory, Department of Gene Function and Phenomics, National Institute of Genetics, Research Organization of Information and Systems (ROIS), Mishima, JapanMulticellular Organization Laboratory, Department of Gene Function and Phenomics, National Institute of Genetics, Research Organization of Information and Systems (ROIS), Mishima, Japan; Department of Genetics, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Mishima, JapanOrganogenesis requires the proper production of diverse cell types and their positioning/migration. However, the coordination of these processes during development remains poorly understood. The gonad in C. elegans exhibits a mirror-symmetric structure guided by the migration of distal tip cells (DTCs), which result from asymmetric divisions of somatic gonadal precursors (SGPs; Z1 and Z4). We found that the polarity of Z1 and Z4, which possess mirror-symmetric orientation, is controlled by the redundant functions of the LIN-17/Frizzled receptor and three Wnt proteins (CWN-1, CWN-2, and EGL-20) with distinct functions. In lin-17 mutants, CWN-2 promotes normal polarity in both Z1 and Z4, while CWN-1 promotes reverse and normal polarity in Z1 and Z4, respectively. In contrast, EGL-20 inhibits the polarization of both Z1 and Z4. In lin-17 egl-20 cwn-2 triple mutants with a polarity reversal of Z1, DTCs from Z1 frequently miss-migrate to the posterior side. Our further analysis demonstrates that the mis-positioning of DTCs in the gonad due to the polarity reversal of Z1 leads to mis-migration. Similar mis-migration was also observed in cki-1(RNAi) animals producing ectopic DTCs. These results highlight the role of Wnt signaling in coordinating the production and migration of DTCs to establish a mirror-symmetric organ.https://elifesciences.org/articles/103035Wntcell polaritycell migrationorganogenesis |
| spellingShingle | Shuhei So Masayo Asakawa Hitoshi Sawa Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad eLife Wnt cell polarity cell migration organogenesis |
| title | Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad |
| title_full | Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad |
| title_fullStr | Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad |
| title_full_unstemmed | Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad |
| title_short | Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad |
| title_sort | distinct functions of three wnt proteins control mirror symmetric organogenesis in the c elegans gonad |
| topic | Wnt cell polarity cell migration organogenesis |
| url | https://elifesciences.org/articles/103035 |
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