Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migration
Introduction: A key regulator of collective cell migration is prostaglandin (PG) signaling. However, it remains largely unclear whether PGs act within the migratory cells or their microenvironment to promote migration. Here we use Drosophila border cell migration as a model to uncover the cell-speci...
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2023.1257751/full |
| _version_ | 1797356615521796096 |
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| author | Samuel Q. Mellentine Samuel Q. Mellentine Hunter N. Brown Hunter N. Brown Anna S. Ramsey Anna S. Ramsey Jie Li Jie Li Tina L. Tootle Tina L. Tootle |
| author_facet | Samuel Q. Mellentine Samuel Q. Mellentine Hunter N. Brown Hunter N. Brown Anna S. Ramsey Anna S. Ramsey Jie Li Jie Li Tina L. Tootle Tina L. Tootle |
| author_sort | Samuel Q. Mellentine |
| collection | DOAJ |
| description | Introduction: A key regulator of collective cell migration is prostaglandin (PG) signaling. However, it remains largely unclear whether PGs act within the migratory cells or their microenvironment to promote migration. Here we use Drosophila border cell migration as a model to uncover the cell-specific roles of two PGs in collective migration. The border cells undergo a collective and invasive migration between the nurse cells; thus, the nurse cells are the substrate and microenvironment for the border cells. Prior work found PG signaling is required for on-time border cell migration and cluster cohesion.Methods: Confocal microscopy and quantitative image analyses of available mutant alleles and RNAi lines were used to define the roles of the PGE2 and PGF2α synthases in border cell migration.Results: We find that the PGE2 synthase cPGES is required in the substrate, while the PGF2α synthase Akr1B is required in the border cells for on-time migration. Akr1B acts in both the border cells and their substrate to regulate cluster cohesion. One means by which Akr1B may regulate border cell migration and/or cluster cohesion is by promoting integrin-based adhesions. Additionally, Akr1B limits myosin activity, and thereby cellular stiffness, in the border cells, whereas cPGES limits myosin activity in both the border cells and their substrate. Decreasing myosin activity overcomes the migration delays in both akr1B and cPGES mutants, indicating the changes in cellular stiffness contribute to the migration defects.Discussion: Together these data reveal that two PGs, PGE2 and PGF2α, produced in different locations, play key roles in promoting border cell migration. These PGs likely have similar migratory versus microenvironment roles in other collective cell migrations. |
| first_indexed | 2024-03-08T14:29:14Z |
| format | Article |
| id | doaj.art-9c8235328d9b4692886aeb81b6b7c311 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-03-08T14:29:14Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-9c8235328d9b4692886aeb81b6b7c3112024-01-12T12:45:27ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2024-01-011110.3389/fcell.2023.12577511257751Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migrationSamuel Q. Mellentine0Samuel Q. Mellentine1Hunter N. Brown2Hunter N. Brown3Anna S. Ramsey4Anna S. Ramsey5Jie Li6Jie Li7Tina L. Tootle8Tina L. Tootle9Anatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesBiology, University of Iowa, Iowa City, IA, United StatesAnatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesBiology, University of Iowa, Iowa City, IA, United StatesAnatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesBiology, University of Iowa, Iowa City, IA, United StatesAnatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesBiology, University of Iowa, Iowa City, IA, United StatesAnatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesBiology, University of Iowa, Iowa City, IA, United StatesIntroduction: A key regulator of collective cell migration is prostaglandin (PG) signaling. However, it remains largely unclear whether PGs act within the migratory cells or their microenvironment to promote migration. Here we use Drosophila border cell migration as a model to uncover the cell-specific roles of two PGs in collective migration. The border cells undergo a collective and invasive migration between the nurse cells; thus, the nurse cells are the substrate and microenvironment for the border cells. Prior work found PG signaling is required for on-time border cell migration and cluster cohesion.Methods: Confocal microscopy and quantitative image analyses of available mutant alleles and RNAi lines were used to define the roles of the PGE2 and PGF2α synthases in border cell migration.Results: We find that the PGE2 synthase cPGES is required in the substrate, while the PGF2α synthase Akr1B is required in the border cells for on-time migration. Akr1B acts in both the border cells and their substrate to regulate cluster cohesion. One means by which Akr1B may regulate border cell migration and/or cluster cohesion is by promoting integrin-based adhesions. Additionally, Akr1B limits myosin activity, and thereby cellular stiffness, in the border cells, whereas cPGES limits myosin activity in both the border cells and their substrate. Decreasing myosin activity overcomes the migration delays in both akr1B and cPGES mutants, indicating the changes in cellular stiffness contribute to the migration defects.Discussion: Together these data reveal that two PGs, PGE2 and PGF2α, produced in different locations, play key roles in promoting border cell migration. These PGs likely have similar migratory versus microenvironment roles in other collective cell migrations.https://www.frontiersin.org/articles/10.3389/fcell.2023.1257751/fullprostaglandinscell migrationborder cellsDrosophilaPGE2PGF2α |
| spellingShingle | Samuel Q. Mellentine Samuel Q. Mellentine Hunter N. Brown Hunter N. Brown Anna S. Ramsey Anna S. Ramsey Jie Li Jie Li Tina L. Tootle Tina L. Tootle Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migration Frontiers in Cell and Developmental Biology prostaglandins cell migration border cells Drosophila PGE2 PGF2α |
| title | Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migration |
| title_full | Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migration |
| title_fullStr | Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migration |
| title_full_unstemmed | Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migration |
| title_short | Specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote Drosophila border cell migration |
| title_sort | specific prostaglandins are produced in the migratory cells and the surrounding substrate to promote drosophila border cell migration |
| topic | prostaglandins cell migration border cells Drosophila PGE2 PGF2α |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2023.1257751/full |
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