Cited by 430Mitochondrial Function and PathologyT-cell and B-cell ImmunologyCancer, Hypoxia, and Metabolism

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Mitochondrial Biogenesis and Proteome Remodeling Promote One-Carbon Metabolism for T Cell Activation

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Ron-Harel, Noga, Santos, Daniel, Ghergurovich, Jonathan M., Sage, Peter T., Reddy, Anita, Lovitch, Scott B., Dephoure, Noah, Satterstrom, F. Kyle, Sheffer, Michal, Spinelli, Jessica B., Gygi, Steven, Rabinowitz, Joshua D., Sharpe, Arlene H., Haigis, Marcia C.·2016·Cell Metabolism

DOI 10.1016/j.cmet.2016.06.007PMC PMC5330619

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Abstract

Naive T cell stimulation activates anabolic metabolism to fuel the transition from quiescence to growth and proliferation. Here we show that naive CD4(+) T cell activation induces a unique program of mitochondrial biogenesis and remodeling. Using mass spectrometry, we quantified protein dynamics during T cell activation. We identified substantial remodeling of the mitochondrial proteome over the first 24 hr of T cell activation to generate mitochondria with a distinct metabolic signature, with one-carbon metabolism as the most induced pathway. Salvage pathways and mitochondrial one-carbon metabolism, fed by serine, contribute to purine and thymidine synthesis to enable T cell proliferation and survival. Genetic inhibition of the mitochondrial serine catabolic enzyme SHMT2 impaired T cell survival in culture and antigen-specific T cell abundance in vivo. Thus, during T cell activation, mitochondrial proteome remodeling generates specialized mitochondria with enhanced one-carbon metabolism that is critical for T cell activation and survival.

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Authors: Ron-Harel, N., Santos, D., Ghergurovich, J. M., Sage, P. T., Reddy, A., Lovitch, S. B., Dephoure, N., Satterstrom, F. K., Sheffer, M., Spinelli, J. B., Gygi, S., Rabinowitz, J. D., Sharpe, A. H., & Haigis, M. C.
Affiliations: Harvard University (US)
Princeton University (US)
Brigham and Women's Hospital (US)
Corresponding author: Haigis, Marcia C.
ORCID: Santos, Daniel
Ghergurovich, Jonathan M.
Sage, Peter T.
Reddy, Anita
Lovitch, Scott B.
Dephoure, Noah
Satterstrom, F. Kyle
Sheffer, Michal
Spinelli, Jessica B.
Gygi, Steven
Rabinowitz, Joshua D.
Sharpe, Arlene H.
Haigis, Marcia C.
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2016-07
Volume: 24
Issue: 1
Pages: 104-117
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2016.06.007
PMC: PMC5330619
OpenAlex: W2472560175
Cited by: 429
References: 41
Citations by year: 2026: 41 · 2025: 57 · 2024: 63 · 2023: 42 · 2022: 40 · 2021: 51 · 2020: 47 · 2019: 29 · 2018: 27 · 2017: 25 · 2016: 7
FWCI: 15.25
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, 376 d)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Human Genome Research Institute (T32HG003284)
National Institute of Allergy and Infectious Diseases (HHSN272201100018C)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK103295, T32DK007260)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Keywords: mitochondrial biogenesis, one-carbon metabolism, T cell activation, CD4+ T cells, serine catabolism, SHMT2, purine biosynthesis, thymidine synthesis, T cell proliferation, T cell survival, metabolic reprogramming
MeSH terms: Animals, Epitopes, Organelle Biogenesis, Carbon, Cell Survival, Energy Metabolism, Lymphocyte Activation, Mice, Inbred C57BL, Mitochondria, Pyrimidines, T-Lymphocytes, CD4-Positive T-Lymphocytes, Proteome, Proteomics, Metabolic Networks and Pathways

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Mitochondrial Biogenesis and Proteome Remodeling Promote One-Carbon Metabolism for T Cell Activation

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