Cited by 727Cancer, Hypoxia, and MetabolismMetabolism, Diabetes, and CancerCancer Cells and Metastasis

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MYC/PGC-1α Balance Determines the Metabolic Phenotype and Plasticity of Pancreatic Cancer Stem Cells

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Sancho, Patricia, Burgos-Ramos, Emma, Tavera, Alejandra, Bou Kheir, Tony, Jagust, Petra, Schoenhals, Matthieu, Barneda, David, Sellers, Katherine, Campos-Olivas, Ramon, Graña, Osvaldo, Viera, Catarina R., Yuneva, Mariia, Sainz, Bruno, Heeschen, Christopher·2015·Cell Metabolism

DOI 10.1016/j.cmet.2015.08.015

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Abstract

The anti-diabetic drug metformin targets pancreatic cancer stem cells (CSCs), but not their differentiated progenies (non-CSCs), which may be related to distinct metabolic phenotypes. Here we conclusively demonstrate that while non-CSCs were highly glycolytic, CSCs were dependent on oxidative metabolism (OXPHOS) with very limited metabolic plasticity. Thus, mitochondrial inhibition, e.g., by metformin, translated into energy crisis and apoptosis. However, resistant CSC clones eventually emerged during treatment with metformin due to their intermediate glycolytic/respiratory phenotype. Mechanistically, suppression of MYC and subsequent increase of PGC-1α were identified as key determinants for the OXPHOS dependency of CSCs, which was abolished in resistant CSC clones. Intriguingly, no resistance was observed for the mitochondrial ROS inducer menadione and resistance could also be prevented/reversed for metformin by genetic/pharmacological inhibition of MYC. Thus, the specific metabolic features of pancreatic CSCs are amendable to therapeutic intervention and could provide the basis for developing more effective therapies to combat this lethal cancer.

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Additional file 1 of Polyamine and EIF5A hypusination downstream of c-Myc confers targeted therapy resistance in BRAF mutant melanoma
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Additional file 1 of A novel lncRNA ROPM-mediated lipid metabolism governs breast cancer stem cell properties
Liu, S., Sun, Y., Hou, Y., Yang, L., Wan, X., Qin, Y., Liu, Y., Wang, R., Zhu, P., Teng, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16907570
Additional file 4 of Insights into gemcitabine resistance in pancreatic cancer: association with metabolic reprogramming and TP53 pathogenicity in patient derived xenografts
Konaté, M. M., Krushkal, J., Li, M.-C., Chen, L., Kotliarov, Y., Palmisano, A., Pauly, R., Xie, Q., Williams, P. M., McShane, L. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757838
Additional file 2 of Three-dimensional environment sensitizes pancreatic cancer cells to the anti-proliferative effect of budesonide by reprogramming energy metabolism
Ibello, E., Saracino, F., Delle Cave, D., Buonaiuto, S., Amoroso, F., Andolfi, G., Corona, M., Guardiola, O., Colonna, V., Sainz Jr, B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26043787
Additional file 3 of Three-dimensional environment sensitizes pancreatic cancer cells to the anti-proliferative effect of budesonide by reprogramming energy metabolism
Ibello, E., Saracino, F., Delle Cave, D., Buonaiuto, S., Amoroso, F., Andolfi, G., Corona, M., Guardiola, O., Colonna, V., Sainz Jr, B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26733777
Additional file 6 of Insights into gemcitabine resistance in pancreatic cancer: association with metabolic reprogramming and TP53 pathogenicity in patient derived xenografts
Konaté, M. M., Krushkal, J., Li, M.-C., Chen, L., Kotliarov, Y., Palmisano, A., Pauly, R., Xie, Q., Williams, P. M., McShane, L. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757844
Additional file 1 of Insights into gemcitabine resistance in pancreatic cancer: association with metabolic reprogramming and TP53 pathogenicity in patient derived xenografts
Konaté, M. M., Krushkal, J., Li, M.-C., Chen, L., Kotliarov, Y., Palmisano, A., Pauly, R., Xie, Q., Williams, P. M., McShane, L. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26500349
Additional file 2 of IL20RB signaling enhances stemness and chemotherapy resistance in pancreatic cancer
Li, X.-H., Huang, G., Xu, Z.-L., Zhao, C.-Y., Dong, X.-Y., 崔伯康, & Lin, X. (2024) · Figshare · doi:10.6084/m9.figshare.26654296
Additional file 3 of Insights into gemcitabine resistance in pancreatic cancer: association with metabolic reprogramming and TP53 pathogenicity in patient derived xenografts
Konaté, M. M., Krushkal, J., Li, M.-C., Chen, L., Kotliarov, Y., Palmisano, A., Pauly, R., Xie, Q., Williams, P. M., McShane, L. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757835
Additional file 5 of Insights into gemcitabine resistance in pancreatic cancer: association with metabolic reprogramming and TP53 pathogenicity in patient derived xenografts
Konaté, M. M., Krushkal, J., Li, M.-C., Chen, L., Kotliarov, Y., Palmisano, A., Pauly, R., Xie, Q., Williams, P. M., McShane, L. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757841
Additional file 2 of A novel lncRNA ROPM-mediated lipid metabolism governs breast cancer stem cell properties
Liu, S., Sun, Y., Hou, Y., Yang, L., Wan, X., Qin, Y., Liu, Y., Wang, R., Zhu, P., Teng, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16907573
Additional file 1 of IL20RB signaling enhances stemness and chemotherapy resistance in pancreatic cancer
Li, X.-H., Huang, G., Xu, Z.-L., Zhao, C.-Y., Dong, X.-Y., 崔伯康, & Lin, X. (2024) · Figshare · doi:10.6084/m9.figshare.26654293
Additional file 2 of Polyamine and EIF5A hypusination downstream of c-Myc confers targeted therapy resistance in BRAF mutant melanoma
Park, B.-S., Jeon, H., Kim, Y., Kwon, H., Choi, G.-E., Chi, S.-G., Park, H.-M., Lee, H., & Kim, T. (2024) · Figshare · doi:10.6084/m9.figshare.26182309
Additional file 2 of Inhibiting NR5A2 targets stemness in pancreatic cancer by disrupting SOX2/MYC signaling and restoring chemosensitivity
Zheng, Q., Tang, J., Aicher, A., Bou Kheir, T., Šabanović, B., Ananthanarayanan, P., Reina, C., Chen, M., Gu, J.-M., He, B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.24647366
Self-citation
Additional file 1 of Three-dimensional environment sensitizes pancreatic cancer cells to the anti-proliferative effect of budesonide by reprogramming energy metabolism
Ibello, E., Saracino, F., Delle Cave, D., Buonaiuto, S., Amoroso, F., Andolfi, G., Corona, M., Guardiola, O., Colonna, V., Sainz Jr, B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26043710
Additional file 1 of Exploring the safety and efficacy of phytomedicine Petiveria alliacea extract (Esperanza) in patients with metastatic gastrointestinal tumors and acute leukemias: study protocol for a phase Ib/randomized double blind phase II trial (PA001)
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Additional file 1 of Targeting cancer stem cell OXPHOS with tailored ruthenium complexes as a new anti-cancer strategy
Alcalá, S., Villarino, L., Ruiz-Cañas, L., Couceiro, J. R., Martínez‐Calvo, M., Palencia‐Campos, A., Navarro, D., Cabezas‐Sainz, P., Rodríguez-Arabaolaza, I., Barreal, A. C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25097312
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Authors: Sancho, P., Burgos-Ramos, E., Tavera, A., Bou Kheir, T., Jagust, P., Schoenhals, M., Barneda, D., Sellers, K., Campos-Olivas, R., Graña, O., Viera, C. R., Yuneva, M., Sainz, B., & Heeschen, C.
Affiliations: Queen Mary University of London (GB)
Spanish National Cancer Research Centre (ES)
Corresponding author: Sancho, Patricia
Heeschen, Christopher
ORCID: Sancho, Patricia
Schoenhals, Matthieu
Barneda, David
Yuneva, Mariia
Heeschen, Christopher
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2015-10
Volume: 22
Issue: 4
Pages: 590-605
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2015.08.015
OpenAlex: W1892036645
Cited by: 722
References: 44
Citations by year: 2026: 36 · 2025: 51 · 2024: 60 · 2023: 72 · 2022: 79 · 2021: 88 · 2020: 94 · 2019: 79 · 2018: 65 · 2017: 51 · 2016: 41 · 2015: 5
FWCI: 17.80
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 371 d)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
RUIdeRA - Institutional University Repository (University of Castilla-La Mancha) (submittedVersion, other-oa)
Funders: Francis Crick Institute (10223)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: pancreatic cancer stem cells, c-Myc, PGC-1α, metformin, oxidative phosphorylation, glycolysis, metabolic plasticity, drug resistance, mitochondrial reactive oxygen species, menadione, apoptosis, energy crisis, cancer metabolism
MeSH terms: Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, AC133 Antigen, Animals, Antineoplastic Agents, Glycoproteins, Humans, Metformin, Mice, Nude, Mitochondria, Oxidative Phosphorylation, Pancreatic Neoplasms, Peptides, Phenotype, Transcription Factors, Tumor Cells, Cultured, Neoplastic Stem Cells, Antigens, CD, Gene Library, Proto-Oncogene Proteins c-myc, Reactive Oxygen Species, Drug Resistance, Neoplasm, Vitamin K 3, RNA Interference, Mice

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MYC/PGC-1α Balance Determines the Metabolic Phenotype and Plasticity of Pancreatic Cancer Stem Cells

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