Succinate inhibition of α-ketoglutarate-dependent enzymes in a yeast model of paraganglioma

Smith, Emily H.; Janknecht, Ralf; Maher, L. James

doi:10.1093/hmg/ddm275

Cited by 169Cancer, Hypoxia, and MetabolismAdrenal and Paraganglionic TumorsMetabolism and Genetic Disorders

Succinate inhibition of α-ketoglutarate-dependent enzymes in a yeast model of paraganglioma

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Smith, Emily H., Janknecht, Ralf, Maher, L. James·2007·Human Molecular Genetics

DOI 10.1093/hmg/ddm275

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Abstract

The tricarboxylic acid (TCA) cycle enzyme succinate dehydrogenase (SDH) is a tumor suppressor. Heterozygosity for defective SDH subunit genes predisposes to familial paraganglioma (PGL) or pheochromocytoma (PHEO). Models invoking reactive oxygen species (ROS) or succinate accumulation have been proposed to explain the link between TCA cycle dysfunction and oncogenesis. Here we study the biochemical consequences of a common familial PGL-linked mutation, loss of the SDHB subunit, in a yeast model. This strain has increased ROS production but no evidence of mutagenic DNA damage. Because the strain lacks SDH activity, succinate accumulates dramatically and inhibits alpha-ketoglutarate (alphaKG)-dependent enzyme Jlp1, involved in sulfur metabolism, and alphaKG-dependent histone demethylase Jhd1. We show that mammalian JmjC-domain histone demethylases are also vulnerable to succinate inhibition in vitro and in cultured cells. Our results suggest that any alphaKG-dependent enzyme is a potential target of accumulated succinate in oncogenesis. The possible role that inhibition of these enzymes by succinate may have in oncogenesis is discussed.

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Elevated succinate levels can cause epigenetic dysregulation.
“Elevated succinate levels can lead to epigenetic dysregulation (Cervera et al., 2009; Smith et al., 2007).”
From SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways (2013) · cites this paper as Smith et al., 2007
Succinate alters histone demethylase activity in yeast.
“succinate has been shown to alter histone demethylase activity in yeast (Smith et al., 2007)”
From Metabolic Reprogramming: A Cancer Hallmark Even Warburg Did Not Anticipate (2012) · cites this paper as Smith et al., 2007

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Authors: Smith, E. H., Janknecht, R., & Maher, L. J.
Affiliations: Mayo Clinic (US)
Corresponding author: Maher, L. James
ORCID: Janknecht, Ralf
Maher, L. James
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2007-09-19
Volume: 16
Issue: 24
Pages: 3136-3148
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddm275
OpenAlex: W2107911729
Cited by: 169
References: 70
Citations by year: 2026: 2 · 2025: 8 · 2024: 6 · 2023: 5 · 2022: 11 · 2021: 10 · 2020: 6 · 2019: 9 · 2018: 7 · 2017: 7 · 2016: 5 · 2015: 14 · 2014: 12 · 2013: 19 · 2012: 18
FWCI: 2.35
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
Locations: Human Molecular Genetics (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Funders: Mayo Clinic
Fraternal Order of Eagles
Mayo Foundation for Medical Education and Research
University of Minnesota
School of Medicine, University of North Carolina at Chapel Hill
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Health Sciences › Medicine › Surgery › Adrenal and Paraganglionic Tumors
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Metabolism and Genetic Disorders
Keywords: succinic acid, succinate dehydrogenase, SDHB mutation, paraganglioma, pheochromocytoma, succinate accumulation, reactive oxygen species, tumor suppressor, yeast model, sulfur metabolism, carcinogenesis
MeSH terms: Cells, Cultured, Citric Acid Cycle, Enzyme Inhibitors, Humans, Mixed Function Oxygenases, Ketoglutaric Acids, Models, Biological, Oxidoreductases, N-Demethylating, Paraganglioma, Saccharomyces cerevisiae, Succinate Dehydrogenase, Reactive Oxygen Species, Succinic Acid, Protein Subunits, Saccharomyces cerevisiae Proteins, Organisms, Genetically Modified, Dioxygenases, Jumonji Domain-Containing Histone Demethylases

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Succinate inhibition of α-ketoglutarate-dependent enzymes in a yeast model of paraganglioma

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