Combined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytes

Abstract Drosophila nephrocytes are specialised cells that share critical functional, morphological, and molecular features with mammalian podocytes. Accordingly, nephrocytes represent a preferred invertebrate model for human glomerular disease. Here, we established a method for cell-specific isolat...

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Main Authors: Heiko Meyer, Judith Bossen, Maren Janz, Xenia Müller, Sven Künzel, Thomas Roeder, Achim Paululat
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-07062-z
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author Heiko Meyer
Judith Bossen
Maren Janz
Xenia Müller
Sven Künzel
Thomas Roeder
Achim Paululat
author_facet Heiko Meyer
Judith Bossen
Maren Janz
Xenia Müller
Sven Künzel
Thomas Roeder
Achim Paululat
author_sort Heiko Meyer
collection DOAJ
description Abstract Drosophila nephrocytes are specialised cells that share critical functional, morphological, and molecular features with mammalian podocytes. Accordingly, nephrocytes represent a preferred invertebrate model for human glomerular disease. Here, we established a method for cell-specific isolation of the two types of Drosophila nephrocytes, garland and pericardial cells, from animals of different developmental stages and ages. Mass spectrometry-based proteomics and RNA-Seq-based transcriptomics were applied to characterise the proteome and transcriptome of the respective cells in an integrated and complementary manner. We observed characteristic changes in the proteome and transcriptome due to cellular ageing. Furthermore, functional enrichment analyses suggested that larval and adult nephrocytes, as well as garland and pericardial nephrocytes, fulfil distinct physiological functions. In addition, the pericardial nephrocytes were characterised by transcriptomic and proteomic profiles suggesting an atypical energy metabolism with very low oxidative phosphorylation rates. Moreover, the nephrocytes displayed typical signatures of extensive immune signalling and showed an active antimicrobial response to an infection. Factor-specific comparisons identified novel candidate proteins either expressed and secreted by the nephrocytes or sequestered by them. The data generated in this study represent a valuable basis for a more specific application of the Drosophila model in analysing renal cell function in health and disease.
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spelling doaj-art-769c9ee14c6d4aa09198bc4ce0ae57f42025-08-20T02:18:35ZengNature PortfolioCommunications Biology2399-36422024-11-017111910.1038/s42003-024-07062-zCombined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytesHeiko Meyer0Judith Bossen1Maren Janz2Xenia Müller3Sven Künzel4Thomas Roeder5Achim Paululat6Department of Zoology & Developmental Biology, University of OsnabrückUniversity of Kiel, Zoology, Molecular PhysiologyDepartment of Zoology & Developmental Biology, University of OsnabrückUniversity of Kiel, Zoology, Molecular PhysiologyMax-Planck Institute for Evolutionary BiologyUniversity of Kiel, Zoology, Molecular PhysiologyDepartment of Zoology & Developmental Biology, University of OsnabrückAbstract Drosophila nephrocytes are specialised cells that share critical functional, morphological, and molecular features with mammalian podocytes. Accordingly, nephrocytes represent a preferred invertebrate model for human glomerular disease. Here, we established a method for cell-specific isolation of the two types of Drosophila nephrocytes, garland and pericardial cells, from animals of different developmental stages and ages. Mass spectrometry-based proteomics and RNA-Seq-based transcriptomics were applied to characterise the proteome and transcriptome of the respective cells in an integrated and complementary manner. We observed characteristic changes in the proteome and transcriptome due to cellular ageing. Furthermore, functional enrichment analyses suggested that larval and adult nephrocytes, as well as garland and pericardial nephrocytes, fulfil distinct physiological functions. In addition, the pericardial nephrocytes were characterised by transcriptomic and proteomic profiles suggesting an atypical energy metabolism with very low oxidative phosphorylation rates. Moreover, the nephrocytes displayed typical signatures of extensive immune signalling and showed an active antimicrobial response to an infection. Factor-specific comparisons identified novel candidate proteins either expressed and secreted by the nephrocytes or sequestered by them. The data generated in this study represent a valuable basis for a more specific application of the Drosophila model in analysing renal cell function in health and disease.https://doi.org/10.1038/s42003-024-07062-z
spellingShingle Heiko Meyer
Judith Bossen
Maren Janz
Xenia Müller
Sven Künzel
Thomas Roeder
Achim Paululat
Combined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytes
Communications Biology
title Combined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytes
title_full Combined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytes
title_fullStr Combined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytes
title_full_unstemmed Combined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytes
title_short Combined transcriptome and proteome profiling reveal cell-type-specific functions of Drosophila garland and pericardial nephrocytes
title_sort combined transcriptome and proteome profiling reveal cell type specific functions of drosophila garland and pericardial nephrocytes
url https://doi.org/10.1038/s42003-024-07062-z
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