Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling
Epithelial cells and their underlying basement membranes (BMs) slide along each other to renew epithelia, shape organs, and enlarge BM openings. How BM sliding is controlled, however, is poorly understood. Using genetic and live cell imaging approaches during uterine-vulval attachment in C. elegans,...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2016-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/17218 |
| _version_ | 1811180442710179840 |
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| author | Shelly TH McClatchey Zheng Wang Lara M Linden Eric L Hastie Lin Wang Wanqing Shen Alan Chen Qiuyi Chi David R Sherwood |
| author_facet | Shelly TH McClatchey Zheng Wang Lara M Linden Eric L Hastie Lin Wang Wanqing Shen Alan Chen Qiuyi Chi David R Sherwood |
| author_sort | Shelly TH McClatchey |
| collection | DOAJ |
| description | Epithelial cells and their underlying basement membranes (BMs) slide along each other to renew epithelia, shape organs, and enlarge BM openings. How BM sliding is controlled, however, is poorly understood. Using genetic and live cell imaging approaches during uterine-vulval attachment in C. elegans, we have discovered that the invasive uterine anchor cell activates Notch signaling in neighboring uterine cells at the boundary of the BM gap through which it invades to promote BM sliding. Through an RNAi screen, we found that Notch activation upregulates expression of ctg-1, which encodes a Sec14-GOLD protein, a member of the Sec14 phosphatidylinositol-transfer protein superfamily that is implicated in vesicle trafficking. Through photobleaching, targeted knockdown, and cell-specific rescue, our results suggest that CTG-1 restricts BM adhesion receptor DGN-1 (dystroglycan) trafficking to the cell-BM interface, which promotes BM sliding. Together, these studies reveal a new morphogenetic signaling pathway that controls BM sliding to remodel tissues. |
| first_indexed | 2024-04-11T09:03:14Z |
| format | Article |
| id | doaj.art-d44a600026ea4b88b0b999bdeeb58cfa |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:03:14Z |
| publishDate | 2016-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-d44a600026ea4b88b0b999bdeeb58cfa2022-12-22T04:32:43ZengeLife Sciences Publications LtdeLife2050-084X2016-09-01510.7554/eLife.17218Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodelingShelly TH McClatchey0Zheng Wang1Lara M Linden2Eric L Hastie3Lin Wang4Wanqing Shen5Alan Chen6Qiuyi Chi7David R Sherwood8https://orcid.org/0000-0003-2245-2334Department of Biology, Duke University, Durham, United StatesCenter for Tissue Engineering and Regenerative Medicine, Union Hospital, Wuhan, China; Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; Department of Gastrointestinal Surgery, Union Hospital, Wuhan, China; Development and Molecular Oncology Laboratory, Union Hospital, Wuhan, ChinaDepartment of Biology, Duke University, Durham, United StatesDepartment of Biology, Duke University, Durham, United StatesCenter for Tissue Engineering and Regenerative Medicine, Union Hospital, Wuhan, China; Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaCenter for Tissue Engineering and Regenerative Medicine, Union Hospital, Wuhan, China; Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Biology, Duke University, Durham, United StatesDepartment of Biology, Duke University, Durham, United StatesDepartment of Biology, Duke University, Durham, United StatesEpithelial cells and their underlying basement membranes (BMs) slide along each other to renew epithelia, shape organs, and enlarge BM openings. How BM sliding is controlled, however, is poorly understood. Using genetic and live cell imaging approaches during uterine-vulval attachment in C. elegans, we have discovered that the invasive uterine anchor cell activates Notch signaling in neighboring uterine cells at the boundary of the BM gap through which it invades to promote BM sliding. Through an RNAi screen, we found that Notch activation upregulates expression of ctg-1, which encodes a Sec14-GOLD protein, a member of the Sec14 phosphatidylinositol-transfer protein superfamily that is implicated in vesicle trafficking. Through photobleaching, targeted knockdown, and cell-specific rescue, our results suggest that CTG-1 restricts BM adhesion receptor DGN-1 (dystroglycan) trafficking to the cell-BM interface, which promotes BM sliding. Together, these studies reveal a new morphogenetic signaling pathway that controls BM sliding to remodel tissues.https://elifesciences.org/articles/17218basement membranemorphogenesisNotch signalingSec14 family phospholipid transfer proteindystroglycanmembrane transport |
| spellingShingle | Shelly TH McClatchey Zheng Wang Lara M Linden Eric L Hastie Lin Wang Wanqing Shen Alan Chen Qiuyi Chi David R Sherwood Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling eLife basement membrane morphogenesis Notch signaling Sec14 family phospholipid transfer protein dystroglycan membrane transport |
| title | Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling |
| title_full | Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling |
| title_fullStr | Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling |
| title_full_unstemmed | Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling |
| title_short | Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling |
| title_sort | boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling |
| topic | basement membrane morphogenesis Notch signaling Sec14 family phospholipid transfer protein dystroglycan membrane transport |
| url | https://elifesciences.org/articles/17218 |
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