Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideum
Glucose metabolism is a key factor characterizing the cellular state during multicellular development. In metazoans, the metabolic state of undifferentiated cells correlates with growth/differentiation transition and cell fate determination. Notably, the cell fate of the Amoebozoa species Dictyostel...
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Frontiers Media S.A.
2025-02-01
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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.2024.1526795/full |
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| author | Kenichi Abe Hidenori Hashimura Haruka Hiraoka Shoko Fujishiro Narufumi Kameya Kazuteru Taoka Satoshi Kuwana Masashi Fukuzawa Satoshi Sawai Satoshi Sawai Satoshi Sawai |
| author_facet | Kenichi Abe Hidenori Hashimura Haruka Hiraoka Shoko Fujishiro Narufumi Kameya Kazuteru Taoka Satoshi Kuwana Masashi Fukuzawa Satoshi Sawai Satoshi Sawai Satoshi Sawai |
| author_sort | Kenichi Abe |
| collection | DOAJ |
| description | Glucose metabolism is a key factor characterizing the cellular state during multicellular development. In metazoans, the metabolic state of undifferentiated cells correlates with growth/differentiation transition and cell fate determination. Notably, the cell fate of the Amoebozoa species Dictyostelium discoideum is biased by the presence of glucose and is also correlated with early differences in intracellular ATP. However, the relationship between early cell–cell heterogeneity, cell differentiation, and the metabolic state is unclear. To address the link between glucose metabolism and cell differentiation in D. discoideum, we studied the role of phosphoenolpyruvate carboxylase (PEPC), a key enzyme in the PEP-oxaloacetate-pyruvate node, a core junction that dictates the metabolic flux of glycolysis, the TCA cycle, and gluconeogenesis. We demonstrate that there is cell–cell heterogeneity in PEPC promoter activity in vegetative cells, which depends on nutrient conditions, and that cells with high PEPC promoter activity differentiate into spores. The PEPC null mutant exhibited an aberrantly high prestalk/prespore ratio, and the spore mass of the fruiting body was glassy and consisted of immature spores. Furthermore, the PEPC null mutant had high ATP levels and low mitochondrial membrane potential. Our results suggest the importance of cell–cell heterogeneity in the levels of metabolic enzymes during early cell fate priming. |
| format | Article |
| id | doaj-art-a52139deffe74366819463c373cd70eb |
| institution | Kabale University |
| issn | 2296-634X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj-art-a52139deffe74366819463c373cd70eb2025-02-04T06:32:01ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2025-02-011210.3389/fcell.2024.15267951526795Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideumKenichi Abe0Hidenori Hashimura1Haruka Hiraoka2Shoko Fujishiro3Narufumi Kameya4Kazuteru Taoka5Satoshi Kuwana6Masashi Fukuzawa7Satoshi Sawai8Satoshi Sawai9Satoshi Sawai10Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyō, JapanDepartment of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Meguro, JapanGraduate School of Frontier Biosciences, Osaka University, Suita, JapanDepartment of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Meguro, JapanDepartment of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, JapanDepartment of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, JapanDepartment of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Meguro, JapanDepartment of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyō, JapanDepartment of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Meguro, JapanResearch Center for Complex Systems Biology, Universal Biology Institute, The University of Tokyo, Meguro, JapanGlucose metabolism is a key factor characterizing the cellular state during multicellular development. In metazoans, the metabolic state of undifferentiated cells correlates with growth/differentiation transition and cell fate determination. Notably, the cell fate of the Amoebozoa species Dictyostelium discoideum is biased by the presence of glucose and is also correlated with early differences in intracellular ATP. However, the relationship between early cell–cell heterogeneity, cell differentiation, and the metabolic state is unclear. To address the link between glucose metabolism and cell differentiation in D. discoideum, we studied the role of phosphoenolpyruvate carboxylase (PEPC), a key enzyme in the PEP-oxaloacetate-pyruvate node, a core junction that dictates the metabolic flux of glycolysis, the TCA cycle, and gluconeogenesis. We demonstrate that there is cell–cell heterogeneity in PEPC promoter activity in vegetative cells, which depends on nutrient conditions, and that cells with high PEPC promoter activity differentiate into spores. The PEPC null mutant exhibited an aberrantly high prestalk/prespore ratio, and the spore mass of the fruiting body was glassy and consisted of immature spores. Furthermore, the PEPC null mutant had high ATP levels and low mitochondrial membrane potential. Our results suggest the importance of cell–cell heterogeneity in the levels of metabolic enzymes during early cell fate priming.https://www.frontiersin.org/articles/10.3389/fcell.2024.1526795/fullPEPCcell fatecell metabolismcell heterogeneitycell differentiationDictyostelium discoideum |
| spellingShingle | Kenichi Abe Hidenori Hashimura Haruka Hiraoka Shoko Fujishiro Narufumi Kameya Kazuteru Taoka Satoshi Kuwana Masashi Fukuzawa Satoshi Sawai Satoshi Sawai Satoshi Sawai Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideum Frontiers in Cell and Developmental Biology PEPC cell fate cell metabolism cell heterogeneity cell differentiation Dictyostelium discoideum |
| title | Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideum |
| title_full | Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideum |
| title_fullStr | Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideum |
| title_full_unstemmed | Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideum |
| title_short | Cell–cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in Dictyostelium discoideum |
| title_sort | cell cell heterogeneity in phosphoenolpyruvate carboxylase biases early cell fate priming in dictyostelium discoideum |
| topic | PEPC cell fate cell metabolism cell heterogeneity cell differentiation Dictyostelium discoideum |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2024.1526795/full |
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