Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc Cells
The 1-phosphatidylinositol-3-phosphate 5-kinase PIKfyve generates PtdIns3,5P2 on late phagolysosomes, which by recruiting the scission protein Atg18, results in their fragmentation in the normal course of endosome processing. Loss of PIKfyve function causes cellular hypervacuolization in eukaryotes...
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| Language: | English |
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Frontiers Media S.A.
2021-08-01
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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.2021.692473/full |
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| author | Yoko Yamada Yoko Yamada Yoko Yamada Gillian Forbes Qingyou Du Takefumi Kawata Pauline Schaap |
| author_facet | Yoko Yamada Yoko Yamada Yoko Yamada Gillian Forbes Qingyou Du Takefumi Kawata Pauline Schaap |
| author_sort | Yoko Yamada |
| collection | DOAJ |
| description | The 1-phosphatidylinositol-3-phosphate 5-kinase PIKfyve generates PtdIns3,5P2 on late phagolysosomes, which by recruiting the scission protein Atg18, results in their fragmentation in the normal course of endosome processing. Loss of PIKfyve function causes cellular hypervacuolization in eukaryotes and organ failure in humans. We identified pikfyve as the defective gene in a Dictyostelium mutant that failed to form spores. The amoebas normally differentiated into prespore cells and initiated spore coat protein synthesis in Golgi-derived prespore vesicles. However, instead of exocytosing, the prespore vesicles fused into the single vacuole that typifies the stalk and basal disc cells that support the spores. This process was accompanied by stalk wall biosynthesis, loss of spore gene expression and overexpression of ecmB, a basal disc and stalk-specific gene, but not of the stalk-specific genes DDB_G0278745 and DDB_G0277757. Transdifferentiation of prespore into stalk-like cells was previously observed in mutants that lack early autophagy genes, like atg5, atg7, and atg9. However, while autophagy mutants specifically lacked cAMP induction of prespore gene expression, pikfyve− showed normal early autophagy and prespore induction, but increased in vitro induction of ecmB. Combined, the data suggest that the Dictyostelium endosomal system influences cell fate by acting on cell type specific gene expression. |
| first_indexed | 2024-12-22T04:38:48Z |
| format | Article |
| id | doaj.art-14c64f188c034a2d9b7965b525b948b4 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-22T04:38:48Z |
| publishDate | 2021-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-14c64f188c034a2d9b7965b525b948b42022-12-21T18:38:48ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-08-01910.3389/fcell.2021.692473692473Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc CellsYoko Yamada0Yoko Yamada1Yoko Yamada2Gillian Forbes3Qingyou Du4Takefumi Kawata5Pauline Schaap6School of Life Sciences, University of Dundee, Dundee, United KingdomDepartment of Biology, Faculty of Science, Toho University, Funabashi, JapanDepartment of Materials and Life Sciences, Faculty of Science and Technology, Sophia University, Tokyo, JapanSchool of Life Sciences, University of Dundee, Dundee, United KingdomSchool of Life Sciences, University of Dundee, Dundee, United KingdomDepartment of Biology, Faculty of Science, Toho University, Funabashi, JapanSchool of Life Sciences, University of Dundee, Dundee, United KingdomThe 1-phosphatidylinositol-3-phosphate 5-kinase PIKfyve generates PtdIns3,5P2 on late phagolysosomes, which by recruiting the scission protein Atg18, results in their fragmentation in the normal course of endosome processing. Loss of PIKfyve function causes cellular hypervacuolization in eukaryotes and organ failure in humans. We identified pikfyve as the defective gene in a Dictyostelium mutant that failed to form spores. The amoebas normally differentiated into prespore cells and initiated spore coat protein synthesis in Golgi-derived prespore vesicles. However, instead of exocytosing, the prespore vesicles fused into the single vacuole that typifies the stalk and basal disc cells that support the spores. This process was accompanied by stalk wall biosynthesis, loss of spore gene expression and overexpression of ecmB, a basal disc and stalk-specific gene, but not of the stalk-specific genes DDB_G0278745 and DDB_G0277757. Transdifferentiation of prespore into stalk-like cells was previously observed in mutants that lack early autophagy genes, like atg5, atg7, and atg9. However, while autophagy mutants specifically lacked cAMP induction of prespore gene expression, pikfyve− showed normal early autophagy and prespore induction, but increased in vitro induction of ecmB. Combined, the data suggest that the Dictyostelium endosomal system influences cell fate by acting on cell type specific gene expression.https://www.frontiersin.org/articles/10.3389/fcell.2021.692473/full1-phosphatidylinositol-3-phosphate 5-kinaseAtg18Vac14membrane scissionvesicle traffickingcell-type specific gene expression |
| spellingShingle | Yoko Yamada Yoko Yamada Yoko Yamada Gillian Forbes Qingyou Du Takefumi Kawata Pauline Schaap Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc Cells Frontiers in Cell and Developmental Biology 1-phosphatidylinositol-3-phosphate 5-kinase Atg18 Vac14 membrane scission vesicle trafficking cell-type specific gene expression |
| title | Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc Cells |
| title_full | Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc Cells |
| title_fullStr | Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc Cells |
| title_full_unstemmed | Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc Cells |
| title_short | Loss of PIKfyve Causes Transdifferentiation of Dictyostelium Spores Into Basal Disc Cells |
| title_sort | loss of pikfyve causes transdifferentiation of dictyostelium spores into basal disc cells |
| topic | 1-phosphatidylinositol-3-phosphate 5-kinase Atg18 Vac14 membrane scission vesicle trafficking cell-type specific gene expression |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2021.692473/full |
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