Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testes

The tight interaction between somatic and germline cells is conserved in animal spermatogenesis. The testes of Drosophila melanogaster are the model of choice to identify processes responsible for mature gamete production. However, processes of differentiation and soma-germline interactions occurrin...

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Main Authors: Vladimir E. Adashev, Sergei S. Bazylev, Daria M. Potashnikova, Baira K. Godneeva, Aleksei S. Shatskikh, Oxana M. Olenkina, Ludmila V. Olenina, Alexei A. Kotov
Format: Article
Language:English
Published: Elsevier 2022-06-01
Series:European Journal of Cell Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S0171933522000498
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author Vladimir E. Adashev
Sergei S. Bazylev
Daria M. Potashnikova
Baira K. Godneeva
Aleksei S. Shatskikh
Oxana M. Olenkina
Ludmila V. Olenina
Alexei A. Kotov
author_facet Vladimir E. Adashev
Sergei S. Bazylev
Daria M. Potashnikova
Baira K. Godneeva
Aleksei S. Shatskikh
Oxana M. Olenkina
Ludmila V. Olenina
Alexei A. Kotov
author_sort Vladimir E. Adashev
collection DOAJ
description The tight interaction between somatic and germline cells is conserved in animal spermatogenesis. The testes of Drosophila melanogaster are the model of choice to identify processes responsible for mature gamete production. However, processes of differentiation and soma-germline interactions occurring in somatic cyst cells are currently understudied. Here we focused on the comparison of transcriptome expression patterns of early and mature somatic cyst cells to find out the developmental changes taking place in them. We employed a FACS-based approach for the isolation of early and mature somatic cyst cells from fly testes, subsequent preparation of RNA-Seq libraries, and analysis of gene differential expression in the sorted cells. We found increased expression of genes involved in cell cycle-related processes in early cyst cells, which is necessary for the proliferation and self-renewal of a crucial population of early cyst cells, cyst stem cells. Genes proposedly required for lamellipodium-like projection organization for proper cyst formation were also detected among the upregulated ones in early cyst cells. Gene Ontology and interactome analyses of upregulated genes in mature cyst cells revealed a striking over-representation of gene categories responsible for metabolic and catabolic cellular processes, as well as genes supporting the energetic state of the cells provided by oxidative phosphorylation that is carried out in mitochondria. Our comparative analyses of differentially expressed genes revealed major peculiarities in early and mature cyst cells and provide novel insight into their regulation, which is important for male fertility.
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spelling doaj.art-9c606ea434b241efac0d22319f0886032022-12-22T02:48:25ZengElsevierEuropean Journal of Cell Biology0171-93352022-06-011013151246Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testesVladimir E. Adashev0Sergei S. Bazylev1Daria M. Potashnikova2Baira K. Godneeva3Aleksei S. Shatskikh4Oxana M. Olenkina5Ludmila V. Olenina6Alexei A. Kotov7Institute of Molecular Genetics of National Research Center ''Kurchatov Institute'', 2 Kurchatov Sq., Moscow 123182, RussiaInstitute of Molecular Genetics of National Research Center ''Kurchatov Institute'', 2 Kurchatov Sq., Moscow 123182, RussiaLomonosov Moscow State University, School of Biology, Department of Cell Biology and Histology, Moscow 119234, RussiaInstitute of Molecular Genetics of National Research Center ''Kurchatov Institute'', 2 Kurchatov Sq., Moscow 123182, RussiaInstitute of Molecular Genetics of National Research Center ''Kurchatov Institute'', 2 Kurchatov Sq., Moscow 123182, RussiaInstitute of Molecular Genetics of National Research Center ''Kurchatov Institute'', 2 Kurchatov Sq., Moscow 123182, RussiaInstitute of Molecular Genetics of National Research Center ''Kurchatov Institute'', 2 Kurchatov Sq., Moscow 123182, Russia; Corresponding authors.Institute of Molecular Genetics of National Research Center ''Kurchatov Institute'', 2 Kurchatov Sq., Moscow 123182, Russia; Corresponding authors.The tight interaction between somatic and germline cells is conserved in animal spermatogenesis. The testes of Drosophila melanogaster are the model of choice to identify processes responsible for mature gamete production. However, processes of differentiation and soma-germline interactions occurring in somatic cyst cells are currently understudied. Here we focused on the comparison of transcriptome expression patterns of early and mature somatic cyst cells to find out the developmental changes taking place in them. We employed a FACS-based approach for the isolation of early and mature somatic cyst cells from fly testes, subsequent preparation of RNA-Seq libraries, and analysis of gene differential expression in the sorted cells. We found increased expression of genes involved in cell cycle-related processes in early cyst cells, which is necessary for the proliferation and self-renewal of a crucial population of early cyst cells, cyst stem cells. Genes proposedly required for lamellipodium-like projection organization for proper cyst formation were also detected among the upregulated ones in early cyst cells. Gene Ontology and interactome analyses of upregulated genes in mature cyst cells revealed a striking over-representation of gene categories responsible for metabolic and catabolic cellular processes, as well as genes supporting the energetic state of the cells provided by oxidative phosphorylation that is carried out in mitochondria. Our comparative analyses of differentially expressed genes revealed major peculiarities in early and mature cyst cells and provide novel insight into their regulation, which is important for male fertility.http://www.sciencedirect.com/science/article/pii/S0171933522000498DrosophilaSpermatogenesisSomatic cyst cellsTranscriptome analysisInteraction networks
spellingShingle Vladimir E. Adashev
Sergei S. Bazylev
Daria M. Potashnikova
Baira K. Godneeva
Aleksei S. Shatskikh
Oxana M. Olenkina
Ludmila V. Olenina
Alexei A. Kotov
Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testes
European Journal of Cell Biology
Drosophila
Spermatogenesis
Somatic cyst cells
Transcriptome analysis
Interaction networks
title Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testes
title_full Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testes
title_fullStr Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testes
title_full_unstemmed Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testes
title_short Comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of Drosophila testes
title_sort comparative transcriptional analysis uncovers molecular processes in early and mature somatic cyst cells of drosophila testes
topic Drosophila
Spermatogenesis
Somatic cyst cells
Transcriptome analysis
Interaction networks
url http://www.sciencedirect.com/science/article/pii/S0171933522000498
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