Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary.
The signaling environment, or niche, often governs the initial difference in behavior of an adult stem cell and a derivative that initiates a path towards differentiation. The transition between an instructive stem cell niche and differentiation niche must generally have single-cell resolution, sugg...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2024-03-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3002515 |
| _version_ | 1797220490874454016 |
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| author | Jiani Chen Chaosqun Li Yifeng Sheng Junwei Zhang Lan Pang Zhi Dong Zhiwei Wu Yueqi Lu Zhiguo Liu Qichao Zhang Xueying Guan Xuexin Chen Jianhua Huang |
| author_facet | Jiani Chen Chaosqun Li Yifeng Sheng Junwei Zhang Lan Pang Zhi Dong Zhiwei Wu Yueqi Lu Zhiguo Liu Qichao Zhang Xueying Guan Xuexin Chen Jianhua Huang |
| author_sort | Jiani Chen |
| collection | DOAJ |
| description | The signaling environment, or niche, often governs the initial difference in behavior of an adult stem cell and a derivative that initiates a path towards differentiation. The transition between an instructive stem cell niche and differentiation niche must generally have single-cell resolution, suggesting that multiple mechanisms might be necessary to sharpen the transition. Here, we examined the Drosophila ovary and found that Cap cells, which are key constituents of the germline stem cell (GSC) niche, express a conserved microRNA (miR-124). Surprisingly, loss of miR-124 activity in Cap cells leads to a defect in differentiation of GSC derivatives. We present evidence that the direct functional target of miR-124 in Cap cells is the epidermal growth factor receptor (EGFR) and that failure to limit EGFR expression leads to the ectopic expression of a key anti-differentiation BMP signal in neighboring somatic escort cells (ECs), which constitute a differentiation niche. We further found that Notch signaling connects EFGR activity in Cap cells to BMP expression in ECs. We deduce that the stem cell niche communicates with the differentiation niche through a mechanism that begins with the selective expression of a specific microRNA and culminates in the suppression of the major anti-differentiation signal in neighboring cells, with the functionally important overall role of sharpening the spatial distinction between self-renewal and differentiation environments. |
| first_indexed | 2024-04-24T12:50:23Z |
| format | Article |
| id | doaj.art-c527c6001d2f40b79c5070ebbbfa995f |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-24T12:50:23Z |
| publishDate | 2024-03-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-c527c6001d2f40b79c5070ebbbfa995f2024-04-06T05:31:15ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852024-03-01223e300251510.1371/journal.pbio.3002515Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary.Jiani ChenChaosqun LiYifeng ShengJunwei ZhangLan PangZhi DongZhiwei WuYueqi LuZhiguo LiuQichao ZhangXueying GuanXuexin ChenJianhua HuangThe signaling environment, or niche, often governs the initial difference in behavior of an adult stem cell and a derivative that initiates a path towards differentiation. The transition between an instructive stem cell niche and differentiation niche must generally have single-cell resolution, suggesting that multiple mechanisms might be necessary to sharpen the transition. Here, we examined the Drosophila ovary and found that Cap cells, which are key constituents of the germline stem cell (GSC) niche, express a conserved microRNA (miR-124). Surprisingly, loss of miR-124 activity in Cap cells leads to a defect in differentiation of GSC derivatives. We present evidence that the direct functional target of miR-124 in Cap cells is the epidermal growth factor receptor (EGFR) and that failure to limit EGFR expression leads to the ectopic expression of a key anti-differentiation BMP signal in neighboring somatic escort cells (ECs), which constitute a differentiation niche. We further found that Notch signaling connects EFGR activity in Cap cells to BMP expression in ECs. We deduce that the stem cell niche communicates with the differentiation niche through a mechanism that begins with the selective expression of a specific microRNA and culminates in the suppression of the major anti-differentiation signal in neighboring cells, with the functionally important overall role of sharpening the spatial distinction between self-renewal and differentiation environments.https://doi.org/10.1371/journal.pbio.3002515 |
| spellingShingle | Jiani Chen Chaosqun Li Yifeng Sheng Junwei Zhang Lan Pang Zhi Dong Zhiwei Wu Yueqi Lu Zhiguo Liu Qichao Zhang Xueying Guan Xuexin Chen Jianhua Huang Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary. PLoS Biology |
| title | Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary. |
| title_full | Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary. |
| title_fullStr | Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary. |
| title_full_unstemmed | Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary. |
| title_short | Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary. |
| title_sort | communication between the stem cell niche and an adjacent differentiation niche through mirna and egfr signaling orchestrates exit from the stem cell state in the drosophila ovary |
| url | https://doi.org/10.1371/journal.pbio.3002515 |
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