Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration
Abstract Background Collective cell migration underlies many essential processes, including sculpting organs during embryogenesis, wound healing in the adult, and metastasis of cancer cells. At mid-oogenesis, Drosophila border cells undergo collective migration. Border cells round up into a small gr...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-12-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-023-09839-8 |
| _version_ | 1797415894337454080 |
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| author | Emily Burghardt Jessica Rakijas Antariksh Tyagi Pralay Majumder Bradley J.S.C. Olson Jocelyn A. McDonald |
| author_facet | Emily Burghardt Jessica Rakijas Antariksh Tyagi Pralay Majumder Bradley J.S.C. Olson Jocelyn A. McDonald |
| author_sort | Emily Burghardt |
| collection | DOAJ |
| description | Abstract Background Collective cell migration underlies many essential processes, including sculpting organs during embryogenesis, wound healing in the adult, and metastasis of cancer cells. At mid-oogenesis, Drosophila border cells undergo collective migration. Border cells round up into a small group at the pre-migration stage, detach from the epithelium and undergo a dynamic and highly regulated migration at the mid-migration stage, and stop at the oocyte, their final destination, at the post-migration stage. While specific genes that promote cell signaling, polarization of the cluster, formation of protrusions, and cell-cell adhesion are known to regulate border cell migration, there may be additional genes that promote these distinct active phases of border cell migration. Therefore, we sought to identify genes whose expression patterns changed during border cell migration. Results We performed RNA-sequencing on border cells isolated at pre-, mid-, and post-migration stages. We report that 1,729 transcripts, in nine co-expression gene clusters, are temporally and differentially expressed across the three migration stages. Gene ontology analyses and constructed protein-protein interaction networks identified genes expected to function in collective migration, such as regulators of the cytoskeleton, adhesion, and tissue morphogenesis, but also uncovered a notable enrichment of genes involved in immune signaling, ribosome biogenesis, and stress responses. Finally, we validated the in vivo expression and function of a subset of identified genes in border cells. Conclusions Overall, our results identified differentially and temporally expressed genetic networks that may facilitate the efficient development and migration of border cells. The genes identified here represent a wealth of new candidates to investigate the molecular nature of dynamic collective cell migrations in developing tissues. |
| first_indexed | 2024-03-09T05:56:03Z |
| format | Article |
| id | doaj.art-330ae78513ab4cc7ac33ec87e178ada5 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-09T05:56:03Z |
| publishDate | 2023-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-330ae78513ab4cc7ac33ec87e178ada52023-12-03T12:13:05ZengBMCBMC Genomics1471-21642023-12-0124112310.1186/s12864-023-09839-8Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migrationEmily Burghardt0Jessica Rakijas1Antariksh Tyagi2Pralay Majumder3Bradley J.S.C. Olson4Jocelyn A. McDonald5Division of Biology, Kansas State UniversityDivision of Biology, Kansas State UniversityDivision of Biology, Kansas State UniversityDepartment of Life Sciences, Presidency UniversityDivision of Biology, Kansas State UniversityDivision of Biology, Kansas State UniversityAbstract Background Collective cell migration underlies many essential processes, including sculpting organs during embryogenesis, wound healing in the adult, and metastasis of cancer cells. At mid-oogenesis, Drosophila border cells undergo collective migration. Border cells round up into a small group at the pre-migration stage, detach from the epithelium and undergo a dynamic and highly regulated migration at the mid-migration stage, and stop at the oocyte, their final destination, at the post-migration stage. While specific genes that promote cell signaling, polarization of the cluster, formation of protrusions, and cell-cell adhesion are known to regulate border cell migration, there may be additional genes that promote these distinct active phases of border cell migration. Therefore, we sought to identify genes whose expression patterns changed during border cell migration. Results We performed RNA-sequencing on border cells isolated at pre-, mid-, and post-migration stages. We report that 1,729 transcripts, in nine co-expression gene clusters, are temporally and differentially expressed across the three migration stages. Gene ontology analyses and constructed protein-protein interaction networks identified genes expected to function in collective migration, such as regulators of the cytoskeleton, adhesion, and tissue morphogenesis, but also uncovered a notable enrichment of genes involved in immune signaling, ribosome biogenesis, and stress responses. Finally, we validated the in vivo expression and function of a subset of identified genes in border cells. Conclusions Overall, our results identified differentially and temporally expressed genetic networks that may facilitate the efficient development and migration of border cells. The genes identified here represent a wealth of new candidates to investigate the molecular nature of dynamic collective cell migrations in developing tissues.https://doi.org/10.1186/s12864-023-09839-8Collective cell migrationOogenesisAdhesionMorphogenesisRibosomeRNA-seq |
| spellingShingle | Emily Burghardt Jessica Rakijas Antariksh Tyagi Pralay Majumder Bradley J.S.C. Olson Jocelyn A. McDonald Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration BMC Genomics Collective cell migration Oogenesis Adhesion Morphogenesis Ribosome RNA-seq |
| title | Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration |
| title_full | Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration |
| title_fullStr | Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration |
| title_full_unstemmed | Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration |
| title_short | Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration |
| title_sort | transcriptome analysis reveals temporally regulated genetic networks during drosophila border cell collective migration |
| topic | Collective cell migration Oogenesis Adhesion Morphogenesis Ribosome RNA-seq |
| url | https://doi.org/10.1186/s12864-023-09839-8 |
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