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The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism

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Wellen, Kathryn E., Lu, Chao, Mancuso, Anthony, Lemons, Johanna M.S., Ryczko, Michael, Dennis, James W., Rabinowitz, Joshua D., Coller, Hilary A., Thompson, Craig B.·2010·Genes & Development

DOI 10.1101/gad.1985910PMC PMC3003197

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Abstract

Glucose and glutamine serve as the two primary carbon sources in proliferating cells, and uptake of both nutrients is directed by growth factor signaling. Although either glucose or glutamine can potentially support mitochondrial tricarboxylic acid (TCA) cycle integrity and ATP production, we found that glucose deprivation led to a marked reduction in glutamine uptake and progressive cellular atrophy in multiple mammalian cell types. Despite the continuous presence of growth factor and an abundant supply of extracellular glutamine, interleukin-3 (IL-3)-dependent cells were unable to maintain TCA cycle metabolite pools or receptor-dependent signal transduction when deprived of glucose. This was due at least in part to down-regulation of IL-3 receptor α (IL-3Rα) surface expression in the absence of glucose. Treatment of glucose-starved cells with N-acetylglucosamine (GlcNAc) to maintain hexosamine biosynthesis restored mitochondrial metabolism and cell growth by promoting IL-3-dependent glutamine uptake and metabolism. Thus, glucose metabolism through the hexosamine biosynthetic pathway is required to sustain sufficient growth factor signaling and glutamine uptake to support cell growth and survival.

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Authors: Wellen, K. E., Lu, C., Mancuso, A., Lemons, J. M. S., Ryczko, M., Dennis, J. W., Rabinowitz, J. D., Coller, H. A., & Thompson, C. B.
Affiliations: University of Pennsylvania (US)
Princeton University (US)
Mount Sinai Hospital (CA)
ORCID: Wellen, Kathryn E.
Lemons, Johanna M.S.
Dennis, James W.
Rabinowitz, Joshua D.
Coller, Hilary A.
Thompson, Craig B.
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2010-11-24
Volume: 24
Issue: 24
Pages: 2784-2799
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.1985910
PMC: PMC3003197
OpenAlex: W2034586537
Cited by: 377
References: 55
Citations by year: 2026: 14 · 2025: 15 · 2024: 14 · 2023: 15 · 2022: 29 · 2021: 25 · 2020: 17 · 2019: 24 · 2018: 36 · 2017: 24 · 2016: 28 · 2015: 29 · 2014: 34 · 2013: 26 · 2012: 35
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Genes & Development (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Damon Runyon Cancer Research Foundation
National Institutes of Health
National Cancer Institute (P01CA104838, R01CA105463)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: hexosamine biosynthetic pathway, glutamine uptake, glucose metabolism, interleukin-3, CD123, N-acetylglucosamine, TCA cycle, mitochondrial metabolism, glucose deprivation, cell growth, growth factor signaling, receptor down-regulation
MeSH terms: Acetylglucosamine, Animals, Atrophy, Biological Transport, Cell Survival, Citric Acid Cycle, Glucose, Glutamine, Hexosamines, Interleukin-3, Signal Transduction, Intercellular Signaling Peptides and Proteins, Mice, Metabolic Networks and Pathways

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The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism

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