Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogaster
Cell migration is an important morphogenetic process necessary at different stages of individual development and body functioning. The initiation and maintenance of the cell movement state requires the activation of many factors involved in the regulation of transcription, signal transduction, adhes...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Siberian Branch of the Russian Academy of Sciences, Federal Research Center Institute of Cytology and Genetics, The Vavilov Society of Geneticists and Breeders
2020-08-01
|
| Series: | Вавиловский журнал генетики и селекции |
| Subjects: | |
| Online Access: | https://vavilov.elpub.ru/jour/article/view/2717 |
| _version_ | 1797214003015974912 |
|---|---|
| author | N. V. Dorogova A. S. Khruscheva Iu. A. Galimova D. Yu. Oshchepkov D. E. Maslov E. D. Shvedkina K. A. Akhmetova S. A. Fedorova |
| author_facet | N. V. Dorogova A. S. Khruscheva Iu. A. Galimova D. Yu. Oshchepkov D. E. Maslov E. D. Shvedkina K. A. Akhmetova S. A. Fedorova |
| author_sort | N. V. Dorogova |
| collection | DOAJ |
| description | Cell migration is an important morphogenetic process necessary at different stages of individual development and body functioning. The initiation and maintenance of the cell movement state requires the activation of many factors involved in the regulation of transcription, signal transduction, adhesive interactions, modulation of membranes and the cytoskeleton. However, cell movement depends on the status of both migrating and surrounding cells, interacting with each other during movement. The surrounding cells or cell matrix not only form a substrate for movement, but can also participate in the spatio-temporal regulation of the migration. At present, there is no exact understanding of the genetic mechanisms of this regulation. To determine the role of the cell environment in the regulation of individual cell migration, we studied the migration of primordial germline cells (PGC) during early embryogenesis in Drosophila melanogaster. Normally, PGC are formed at the 3rd stage of embryogenesis at the posterior pole of the embryo. During gastrulation (stages 6–7), PGC as a consolidated cell group passively transfers into the midgut primordium. Further, PGC are individualized, acquire an amoeboid form, and actively move through the midgut epithelium and migrate to the 5–6 abdominal segment of the embryo, where they form paired embryonic gonads. We screened for genes expressed in the epithelium surrounding PGC during early embryogenesis and affecting their migration. We identified the myc, Hph, stat92E, Tre-1, and hop genes, whose RNA interference leads to premature active PGC migration at stages 4–7 of embryogenesis. These genes can be divided into two groups: 1) modulators of JAK/STAT pathway activity inducing PGC migration (stat92E, Tre-1, hop), and 2) myc and Hph involved in epithelial morphogenesis and polarization, i.e. modifying the permeability of the epithelial barrier. Since a depletion of each of these gene products resulted in premature PGC migration, we can conclude that, normally, the somatic environment negatively regulates PGC migration during early Drosophila embryogenesis. |
| first_indexed | 2024-03-07T16:04:58Z |
| format | Article |
| id | doaj.art-50103c1ced1c43e08f879c41a3066323 |
| institution | Directory Open Access Journal |
| issn | 2500-3259 |
| language | English |
| last_indexed | 2024-04-24T11:07:15Z |
| publishDate | 2020-08-01 |
| publisher | Siberian Branch of the Russian Academy of Sciences, Federal Research Center Institute of Cytology and Genetics, The Vavilov Society of Geneticists and Breeders |
| record_format | Article |
| series | Вавиловский журнал генетики и селекции |
| spelling | doaj.art-50103c1ced1c43e08f879c41a30663232024-04-11T15:31:03ZengSiberian Branch of the Russian Academy of Sciences, Federal Research Center Institute of Cytology and Genetics, The Vavilov Society of Geneticists and BreedersВавиловский журнал генетики и селекции2500-32592020-08-0124552553210.18699/VJ20.6441079Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogasterN. V. Dorogova0A. S. Khruscheva1Iu. A. Galimova2D. Yu. Oshchepkov3D. E. Maslov4E. D. Shvedkina5K. A. Akhmetova6S. A. Fedorova7Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of SciencesInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of SciencesInstitute of Molecular and Cellular Biology of Siberian Branch of the Russian Academy of SciencesInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of SciencesNovosibirsk State UniversityNovosibirsk State UniversityInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences; University of Alabama at Birmingham, Department of Biochemistry and Molecular Genetics, School of MedicineInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of SciencesCell migration is an important morphogenetic process necessary at different stages of individual development and body functioning. The initiation and maintenance of the cell movement state requires the activation of many factors involved in the regulation of transcription, signal transduction, adhesive interactions, modulation of membranes and the cytoskeleton. However, cell movement depends on the status of both migrating and surrounding cells, interacting with each other during movement. The surrounding cells or cell matrix not only form a substrate for movement, but can also participate in the spatio-temporal regulation of the migration. At present, there is no exact understanding of the genetic mechanisms of this regulation. To determine the role of the cell environment in the regulation of individual cell migration, we studied the migration of primordial germline cells (PGC) during early embryogenesis in Drosophila melanogaster. Normally, PGC are formed at the 3rd stage of embryogenesis at the posterior pole of the embryo. During gastrulation (stages 6–7), PGC as a consolidated cell group passively transfers into the midgut primordium. Further, PGC are individualized, acquire an amoeboid form, and actively move through the midgut epithelium and migrate to the 5–6 abdominal segment of the embryo, where they form paired embryonic gonads. We screened for genes expressed in the epithelium surrounding PGC during early embryogenesis and affecting their migration. We identified the myc, Hph, stat92E, Tre-1, and hop genes, whose RNA interference leads to premature active PGC migration at stages 4–7 of embryogenesis. These genes can be divided into two groups: 1) modulators of JAK/STAT pathway activity inducing PGC migration (stat92E, Tre-1, hop), and 2) myc and Hph involved in epithelial morphogenesis and polarization, i.e. modifying the permeability of the epithelial barrier. Since a depletion of each of these gene products resulted in premature PGC migration, we can conclude that, normally, the somatic environment negatively regulates PGC migration during early Drosophila embryogenesis.https://vavilov.elpub.ru/jour/article/view/2717drosophila melanogasterembryogenesisgermline cellscell migrationembryonic gonad development |
| spellingShingle | N. V. Dorogova A. S. Khruscheva Iu. A. Galimova D. Yu. Oshchepkov D. E. Maslov E. D. Shvedkina K. A. Akhmetova S. A. Fedorova Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogaster Вавиловский журнал генетики и селекции drosophila melanogaster embryogenesis germline cells cell migration embryonic gonad development |
| title | Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogaster |
| title_full | Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogaster |
| title_fullStr | Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogaster |
| title_full_unstemmed | Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogaster |
| title_short | Migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in Drosophila melanogaster |
| title_sort | migration of primordial germline cells is negatively regulated by surrounding somatic cells during early embryogenesis in drosophila melanogaster |
| topic | drosophila melanogaster embryogenesis germline cells cell migration embryonic gonad development |
| url | https://vavilov.elpub.ru/jour/article/view/2717 |
| work_keys_str_mv | AT nvdorogova migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster AT askhruscheva migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster AT iuagalimova migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster AT dyuoshchepkov migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster AT demaslov migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster AT edshvedkina migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster AT kaakhmetova migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster AT safedorova migrationofprimordialgermlinecellsisnegativelyregulatedbysurroundingsomaticcellsduringearlyembryogenesisindrosophilamelanogaster |