Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium
Abstract Background How stem cell populations are organized and regulated within adult tissues is important for understanding cancer origins and for developing cell replacement strategies. Paradigms such as mammalian gut stem cells and Drosophila ovarian follicle stem cells (FSC) are characterized b...
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| Format: | Article |
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BMC
2023-06-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01636-9 |
| _version_ | 1797795519164055552 |
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| author | Zhi Dong Lan Pang Zhiguo Liu Yifeng Sheng Xiaoping Li Xavier Thibault Amy Reilein Daniel Kalderon Jianhua Huang |
| author_facet | Zhi Dong Lan Pang Zhiguo Liu Yifeng Sheng Xiaoping Li Xavier Thibault Amy Reilein Daniel Kalderon Jianhua Huang |
| author_sort | Zhi Dong |
| collection | DOAJ |
| description | Abstract Background How stem cell populations are organized and regulated within adult tissues is important for understanding cancer origins and for developing cell replacement strategies. Paradigms such as mammalian gut stem cells and Drosophila ovarian follicle stem cells (FSC) are characterized by population asymmetry, in which stem cell division and differentiation are separately regulated processes. These stem cells behave stochastically regarding their contributions to derivative cells and also exhibit dynamic spatial heterogeneity. Drosophila FSCs provide an excellent model for understanding how a community of active stem cells maintained by population asymmetry is regulated. Here, we use single-cell RNA sequencing to profile the gene expression patterns of FSCs and their immediate derivatives to investigate heterogeneity within the stem cell population and changes associated with differentiation. Results We describe single-cell RNA sequencing studies of a pre-sorted population of cells that include FSCs and the neighboring cell types, escort cells (ECs) and follicle cells (FCs), which they support. Cell-type assignment relies on anterior–posterior (AP) location within the germarium. We clarify the previously determined location of FSCs and use spatially targeted lineage studies as further confirmation. The scRNA profiles among four clusters are consistent with an AP progression from anterior ECs through posterior ECs and then FSCs, to early FCs. The relative proportion of EC and FSC clusters are in good agreement with the prevalence of those cell types in a germarium. Several genes with graded profiles from ECs to FCs are highlighted as candidate effectors of the inverse gradients of the two principal signaling pathways, Wnt and JAK-STAT, that guide FSC differentiation and division. Conclusions Our data establishes an important resource of scRNA-seq profiles for FSCs and their immediate derivatives that is based on precise spatial location and functionally established stem cell identity, and facilitates future genetic investigation of regulatory interactions guiding FSC behavior. |
| first_indexed | 2024-03-13T03:19:12Z |
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| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-13T03:19:12Z |
| publishDate | 2023-06-01 |
| publisher | BMC |
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| series | BMC Biology |
| spelling | doaj.art-7cb3fb8860874c14bba1f736654f5fe82023-06-25T11:27:35ZengBMCBMC Biology1741-70072023-06-0121112310.1186/s12915-023-01636-9Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germariumZhi Dong0Lan Pang1Zhiguo Liu2Yifeng Sheng3Xiaoping Li4Xavier Thibault5Amy Reilein6Daniel Kalderon7Jianhua Huang8Institute of Insect Sciences, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, College of Agriculture and Biotechnology, Zhejiang UniversityInstitute of Insect Sciences, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, College of Agriculture and Biotechnology, Zhejiang UniversityInstitute of Insect Sciences, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, College of Agriculture and Biotechnology, Zhejiang UniversityInstitute of Insect Sciences, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, College of Agriculture and Biotechnology, Zhejiang UniversityDepartment of Hepatic Surgery and Liver Transplantation Center of the Third Affiliated Hospital, Organ Transplantation Institute, Sun Yat-Sen UniversityDepartment of Biological Sciences, Columbia UniversityDepartment of Biological Sciences, Columbia UniversityDepartment of Biological Sciences, Columbia UniversityInstitute of Insect Sciences, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, College of Agriculture and Biotechnology, Zhejiang UniversityAbstract Background How stem cell populations are organized and regulated within adult tissues is important for understanding cancer origins and for developing cell replacement strategies. Paradigms such as mammalian gut stem cells and Drosophila ovarian follicle stem cells (FSC) are characterized by population asymmetry, in which stem cell division and differentiation are separately regulated processes. These stem cells behave stochastically regarding their contributions to derivative cells and also exhibit dynamic spatial heterogeneity. Drosophila FSCs provide an excellent model for understanding how a community of active stem cells maintained by population asymmetry is regulated. Here, we use single-cell RNA sequencing to profile the gene expression patterns of FSCs and their immediate derivatives to investigate heterogeneity within the stem cell population and changes associated with differentiation. Results We describe single-cell RNA sequencing studies of a pre-sorted population of cells that include FSCs and the neighboring cell types, escort cells (ECs) and follicle cells (FCs), which they support. Cell-type assignment relies on anterior–posterior (AP) location within the germarium. We clarify the previously determined location of FSCs and use spatially targeted lineage studies as further confirmation. The scRNA profiles among four clusters are consistent with an AP progression from anterior ECs through posterior ECs and then FSCs, to early FCs. The relative proportion of EC and FSC clusters are in good agreement with the prevalence of those cell types in a germarium. Several genes with graded profiles from ECs to FCs are highlighted as candidate effectors of the inverse gradients of the two principal signaling pathways, Wnt and JAK-STAT, that guide FSC differentiation and division. Conclusions Our data establishes an important resource of scRNA-seq profiles for FSCs and their immediate derivatives that is based on precise spatial location and functionally established stem cell identity, and facilitates future genetic investigation of regulatory interactions guiding FSC behavior.https://doi.org/10.1186/s12915-023-01636-9DrosophilaAdult stem cellsFollicle stem cellsOvarySingle-cell RNA sequencing |
| spellingShingle | Zhi Dong Lan Pang Zhiguo Liu Yifeng Sheng Xiaoping Li Xavier Thibault Amy Reilein Daniel Kalderon Jianhua Huang Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium BMC Biology Drosophila Adult stem cells Follicle stem cells Ovary Single-cell RNA sequencing |
| title | Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium |
| title_full | Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium |
| title_fullStr | Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium |
| title_full_unstemmed | Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium |
| title_short | Single-cell expression profile of Drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium |
| title_sort | single cell expression profile of drosophila ovarian follicle stem cells illuminates spatial differentiation in the germarium |
| topic | Drosophila Adult stem cells Follicle stem cells Ovary Single-cell RNA sequencing |
| url | https://doi.org/10.1186/s12915-023-01636-9 |
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