Glutaminolysis Epigenetically Regulates Antiapoptotic Gene Expression in Idiopathic Pulmonary Fibrosis Fibroblasts
Open accessAbstract
Fibrotic responses involve multiple cellular processes, including epigenetic changes. Epigenetic changes are sensitive to alterations in the tissue microenvironment such as the flux of tricarboxylic acid (TCA) cycle metabolites. TCA metabolites directly regulate epigenetic states, in part by regulating histone modification–related enzymes. Glutaminolysis is a critical metabolic process by which glutamine is converted to glutamate by glutaminase and then to α-ketoglutarate (α-KG), a TCA cycle metabolite. Idiopathic pulmonary fibrosis (IPF) is a disease characterized by aberrant metabolism, including enhanced glutaminolysis. IPF fibroblasts are apoptosis resistant. In this study, we explored the relationship between glutaminolysis and the resistance to apoptosis of IPF fibroblasts. Inhibition of glutaminolysis decreased expression of XIAP and survivin, members of the inhibitor of apoptosis protein (IAP) family. α-KG is a cofactor for JMJD3 histone demethylase, which targets H3K27me3. In the absence of glutamine, JMJD3 activity in fibroblasts is significantly decreased, whereas H3K27me3 levels are increased. Chromatin immunoprecipitation assays confirmed that JMJD3 directly interacts with XIAP and survivin promoter regions in a glutamine-dependent manner. Exogenous α-KG partially restores JMJD3 function and its interaction with the XIAP and survivin promoter regions under glutamine-deficient conditions. Interestingly, α-KG upregulates XIAP, but not survivin, suggesting differential α-KG–dependent and –independent mechanisms by which glutamine regulates these IAPs. Our data demonstrate a novel mechanism of metabolic regulation in which glutaminolysis promotes apoptosis resistance of IPF fibroblasts through epigenetic regulation of XIAP and survivin.
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- Authors
- Bai, L., Bernard, K., Tang, X., Hu, M., Horowitz, J. C., Thannickal, V. J., & Sanders, Y. Y.
- Affiliations
- Central South University (CN)
- University of Alabama at Birmingham (US)
- University of Michigan (US)
- Corresponding author
- Sanders, Yan Y.
- Venue
- American Journal of Respiratory Cell and Molecular Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2019-01-01
- Volume
- 60
- Issue
- 1
- Pages
- 49-57
- ISSN
- 1044-1549 (ISSN-L)
- 1535-4989
- PMC
- PMC6348715
- OpenAlex
- W2888261125
- Cited by
- 88
- References
- 64
- Citations by year
- 2026: 12 · 2025: 8 · 2024: 18 · 2023: 13 · 2022: 11 · 2021: 9 · 2020: 10 · 2019: 5 · 2018: 2
- FWCI
- 4.90
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Respiratory Cell and Molecular Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 BX003056)
- National Institute on Aging (R01AG050567, R01AG046210)
- National Heart, Lung, and Blood Institute (R01HL141195, P01HL114470)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Interstitial Lung Diseases and Idiopathic Pulmonary Fibrosis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- idiopathic pulmonary fibrosis, glutaminolysis, apoptosis resistance, epigenetic regulation, fibroblasts, alpha-ketoglutarate, JMJD3, H3K27me3, histone demethylation, XIAP, survivin, inhibitor of apoptosis proteins, glutamine metabolism, TCA cycle metabolites, glutamine deprivation
- MeSH terms
- Survivin, Cells, Cultured, Fibroblasts, Gene Expression Regulation, Glutaminase, Glutamine, Humans, Apoptosis, Epigenesis, Genetic, X-Linked Inhibitor of Apoptosis Protein, Idiopathic Pulmonary Fibrosis
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