Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populations

Abstract Metabolic heterogeneity in various cancer cells within a tumor causes resistance to medical therapies and promotes tumor recurrence and metastasis. However, the mechanisms by which tumors acquire metabolic heterogeneity are poorly understood. Here, we revealed that PKCλ-dependent asymmetric...

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Main Authors: Shoma Tamori, Chika Matsuda, Takahiro Kasai, Shigeo Ohno, Kazunori Sasaki, Kazunori Akimoto
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-025-97985-2
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author Shoma Tamori
Chika Matsuda
Takahiro Kasai
Shigeo Ohno
Kazunori Sasaki
Kazunori Akimoto
author_facet Shoma Tamori
Chika Matsuda
Takahiro Kasai
Shigeo Ohno
Kazunori Sasaki
Kazunori Akimoto
author_sort Shoma Tamori
collection DOAJ
description Abstract Metabolic heterogeneity in various cancer cells within a tumor causes resistance to medical therapies and promotes tumor recurrence and metastasis. However, the mechanisms by which tumors acquire metabolic heterogeneity are poorly understood. Here, we revealed that PKCλ-dependent asymmetric division of ALDH1-positive cancer stem cells (CSCs) led to an uneven distribution of glycolytic capacity, which is crucial for understanding metabolic heterogeneity within a tumor. The rate-limiting enzyme PFKP and the metabolic probe CDG in glycolysis codistributed with the ALDH1A3 protein during the post-cell division phase, highlighting a mechanism for acquiring metabolic diversity. PKCλ deficiency reduced the asymmetric distribution of these proteins in ALDH1high cells with high ALDH1 activity, suggesting a fundamental role for PKCλ in metabolic heterogeneity. We identified 28 distinct distribution patterns combining PFKP and CDG distributions, demonstrating the complexity of glycolytic heterogeneity. Furthermore, validation and prediction of cell distribution patterns via a probabilistic model confirmed that PKCλ deficiency diminished glycolytic diversity in individual cells within a cancer cell colony generated from an ALDH1-positive CSC. These findings suggest that PKCλ-dependent asymmetric cell division of ALDH1-positive CSCs is crucial for glycolytic heterogeneity in cancer cells within a tumor, potentially offering new therapeutic targets against tumor resistance and metastasis.
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issn 2045-2322
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spelling doaj-art-15efacefc1e44e7cb290468f31f5db642025-08-20T03:14:09ZengNature PortfolioScientific Reports2045-23222025-04-0115111710.1038/s41598-025-97985-2Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populationsShoma Tamori0Chika Matsuda1Takahiro Kasai2Shigeo Ohno3Kazunori Sasaki4Kazunori Akimoto5Department of Medicinal and Life Sciences, Faculty of Pharmaceutical Sciences, Tokyo University of ScienceDepartment of Medicinal and Life Sciences, Faculty of Pharmaceutical Sciences, Tokyo University of ScienceDepartment of Medicinal and Life Sciences, Faculty of Pharmaceutical Sciences, Tokyo University of ScienceInstitute for Diseases of Old Age, Juntendo University School of MedicineInstitute for Diseases of Old Age, Juntendo University School of MedicineDepartment of Medicinal and Life Sciences, Faculty of Pharmaceutical Sciences, Tokyo University of ScienceAbstract Metabolic heterogeneity in various cancer cells within a tumor causes resistance to medical therapies and promotes tumor recurrence and metastasis. However, the mechanisms by which tumors acquire metabolic heterogeneity are poorly understood. Here, we revealed that PKCλ-dependent asymmetric division of ALDH1-positive cancer stem cells (CSCs) led to an uneven distribution of glycolytic capacity, which is crucial for understanding metabolic heterogeneity within a tumor. The rate-limiting enzyme PFKP and the metabolic probe CDG in glycolysis codistributed with the ALDH1A3 protein during the post-cell division phase, highlighting a mechanism for acquiring metabolic diversity. PKCλ deficiency reduced the asymmetric distribution of these proteins in ALDH1high cells with high ALDH1 activity, suggesting a fundamental role for PKCλ in metabolic heterogeneity. We identified 28 distinct distribution patterns combining PFKP and CDG distributions, demonstrating the complexity of glycolytic heterogeneity. Furthermore, validation and prediction of cell distribution patterns via a probabilistic model confirmed that PKCλ deficiency diminished glycolytic diversity in individual cells within a cancer cell colony generated from an ALDH1-positive CSC. These findings suggest that PKCλ-dependent asymmetric cell division of ALDH1-positive CSCs is crucial for glycolytic heterogeneity in cancer cells within a tumor, potentially offering new therapeutic targets against tumor resistance and metastasis.https://doi.org/10.1038/s41598-025-97985-2
spellingShingle Shoma Tamori
Chika Matsuda
Takahiro Kasai
Shigeo Ohno
Kazunori Sasaki
Kazunori Akimoto
Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populations
Scientific Reports
title Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populations
title_full Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populations
title_fullStr Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populations
title_full_unstemmed Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populations
title_short Asymmetric cell division of ALDH1-positive cancer stem cells generates glycolytic metabolically diverse cell populations
title_sort asymmetric cell division of aldh1 positive cancer stem cells generates glycolytic metabolically diverse cell populations
url https://doi.org/10.1038/s41598-025-97985-2
work_keys_str_mv AT shomatamori asymmetriccelldivisionofaldh1positivecancerstemcellsgeneratesglycolyticmetabolicallydiversecellpopulations
AT chikamatsuda asymmetriccelldivisionofaldh1positivecancerstemcellsgeneratesglycolyticmetabolicallydiversecellpopulations
AT takahirokasai asymmetriccelldivisionofaldh1positivecancerstemcellsgeneratesglycolyticmetabolicallydiversecellpopulations
AT shigeoohno asymmetriccelldivisionofaldh1positivecancerstemcellsgeneratesglycolyticmetabolicallydiversecellpopulations
AT kazunorisasaki asymmetriccelldivisionofaldh1positivecancerstemcellsgeneratesglycolyticmetabolicallydiversecellpopulations
AT kazunoriakimoto asymmetriccelldivisionofaldh1positivecancerstemcellsgeneratesglycolyticmetabolicallydiversecellpopulations