Control of intestinal stem cell function and proliferation by mitochondrial pyruvate metabolism
Open accessAbstract
Most differentiated cells convert glucose to pyruvate in the cytosol through glycolysis, followed by pyruvate oxidation in the mitochondria. These processes are linked by the mitochondrial pyruvate carrier (MPC), which is required for efficient mitochondrial pyruvate uptake. In contrast, proliferative cells, including many cancer and stem cells, perform glycolysis robustly but limit fractional mitochondrial pyruvate oxidation. We sought to understand the role this transition from glycolysis to pyruvate oxidation plays in stem cell maintenance and differentiation. Loss of the MPC in Lgr5-EGFP-positive stem cells, or treatment of intestinal organoids with an MPC inhibitor, increases proliferation and expands the stem cell compartment. Similarly, genetic deletion of the MPC in Drosophila intestinal stem cells also increases proliferation, whereas MPC overexpression suppresses stem cell proliferation. These data demonstrate that limiting mitochondrial pyruvate metabolism is necessary and sufficient to maintain the proliferation of intestinal stem cells.
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Intestinal stem cells express lower levels of MPC than their differentiated progeny, and blocking mitochondrial pyruvate entry via MPC inhibition drives increased ISC numbers and proliferative potential.
“For example, intestinal stem cells (ISCs) express lower levels of MPC than their differentiated progeny, and blocking mitochondrial pyruvate entry via MPC inhibition drives increased ISC numbers and proliferative potential (206).”
From Regulation and function of the mammalian tricarboxylic acid cycle (2023) · cites this paper as [206]
Suppression of MPC accelerates proliferation in intestinal stem cells.
“Suppression of MPC accelerates proliferation in intestinal stem cells,24”
From The multifaceted contributions of mitochondria to cellular metabolism (2018) · cites this paper as [24]
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“For example, intestinal stem cells (ISCs) express lower levels of MPC than their differentiated progeny, and blocking mitochondrial pyruvate entry via MPC inhibition drives increased ISC numbers and proliferative potential (206).”
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- Authors
- Schell, J. C., Wisidagama, D. R., Bensard, C., Zhao, H., Wei, P., Tanner, J., Flores, A., Mohlman, J., Sorensen, L. K., Earl, C. S., Olson, K. A., Miao, R., Waller, T. C., Delker, D., Kanth, P., Jiang, L., DeBerardinis, R. J., Bronner, M. P., Li, D. Y., Cox, J. E., Christofk, H. R., Lowry, W. E., Thummel, C. S., & Rutter, J.
- Affiliations
- University of Utah (US)
- University of California, Los Angeles (US)
- Children's Medical Center (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Rutter, Jared
- ORCID
- Venue
- Nature Cell Biology
- Published
- 2017-08-14
- Volume
- 19
- Issue
- 9
- Pages
- 1027-1036
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC6137334
- OpenAlex
- W2746891430
- Cited by
- 322
- References
- 65
- Citations by year
- 2026: 22 · 2025: 40 · 2024: 34 · 2023: 37 · 2022: 44 · 2021: 38 · 2020: 43 · 2019: 38 · 2018: 21 · 2017: 5
- FWCI
- 11.96
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- University of Utah
- National Institutes of Health (1s10od021505-01)
- National Cancer Institute (P30CA042014)
- National Institute of General Medical Sciences (R01GM094232, R01GM110755)
- National Center for Research Resources (S10RR020883, S10RR026802)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007491)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- intestinal stem cells, mitochondrial pyruvate carrier, pyruvate oxidation, glycolysis, stem cell proliferation, stem cell maintenance, intestinal organoids, Lgr5, stem cell differentiation
- MeSH terms
- Acrylates, Animals, Cell Differentiation, Cells, Cultured, Drosophila melanogaster, Genotype, Glycolysis, Humans, Intestinal Mucosa, Intestines, Mitochondria, Phenotype, Stem Cells, Time Factors, Transfection, Signal Transduction, Mice, Knockout, Pyruvic Acid, Lactic Acid, Mitochondrial Proteins, Anion Transport Proteins, Monocarboxylic Acid Transporters, Drosophila Proteins, Mitochondrial Membrane Transport Proteins, RNA Interference, Receptors, G-Protein-Coupled, Tissue Culture Techniques, Cell Proliferation
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