Succinate: a metabolic signal in inflammation

Janeway, 2002, Innate immune recognition, Annu. Rev. Immunol., 20, 197, 10.1146/annurev.immunol.20.083001.084359 Pearce, 2013, Metabolic pathways in immune cell activation and quiescence, Immunity, 38, 633, 10.1016/j.immuni.2013.04.005 Krawczyk, 2010, Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation, Blood, 115, 4742, 10.1182/blood-2009-10-249540 Tannahill, 2013, Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha, Nature, 496, 238, 10.1038/nature11986 Everts, 2012, Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells, Blood, 120, 1422, 10.1182/blood-2012-03-419747 Warburg, 1956, On the origin of cancer cells, Science, 123, 309, 10.1126/science.123.3191.309 Dang, 2011, Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1, Cell, 146, 772, 10.1016/j.cell.2011.07.033 Rubic, 2008, Triggering the succinate receptor GPR91 on dendritic cells enhances immunity, Nat. Immunol., 9, 1261, 10.1038/ni.1657 McGettrick, 2013, How metabolism generates signals during innate immunity and inflammation, J. Biol. Chem., 288, 22893, 10.1074/jbc.R113.486464 Infantino, 2011, The mitochondrial citrate carrier: a new player in inflammation, Biochem. J., 438, 433, 10.1042/BJ20111275 He, 2012, Mitochondrial sirtuins: regulators of protein acylation and metabolism, Trends Endocrinol. Metab., 23, 467, 10.1016/j.tem.2012.07.004 Liu, 2013, Deacetylation by SIRT1 reprograms inflammation and cancer, Genes Cancer, 4, 135, 10.1177/1947601913476948 Yeung, 2004, Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase, EMBO J., 23, 2369, 10.1038/sj.emboj.7600244 Zhang, 2010, SIRT1 suppresses activator protein-1 transcriptional activity and cyclooxygenase-2 expression in macrophages, J. Biol. Chem., 285, 7097, 10.1074/jbc.M109.038604 Lim, 2010, Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha, Mol. Cell, 38, 864, 10.1016/j.molcel.2010.05.023 Levine, 2011, Autophagy in immunity and inflammation, Nature, 469, 323, 10.1038/nature09782 Jang, 2012, Nicotinamide-induced mitophagy: event mediated by high NAD+/NADH ratio and SIRT1 protein activation, J. Biol. Chem., 287, 19304, 10.1074/jbc.M112.363747 Lee, 2008, A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy, Proc. Natl. Acad. Sci. U.S.A., 105, 3374, 10.1073/pnas.0712145105 Lin, 2005, Metabolic control through the PGC-1 family of transcription coactivators, Cell Metab., 1, 361, 10.1016/j.cmet.2005.05.004 Misawa, 2013, Microtubule-driven spatial arrangement of mitochondria promotes activation of the NLRP3 inflammasome, Nat. Immunol., 14, 454, 10.1038/ni.2550 Schug, 2010, Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress, Mol. Cell. Biol., 30, 4712, 10.1128/MCB.00657-10 Tannahill, 2011, The emerging role of metabolic regulation in the functioning of Toll-like receptors and the NOD-like receptor Nlrp3, FEBS Lett., 585, 1568, 10.1016/j.febslet.2011.05.008 Guzy, 2008, Loss of the SdhB, but not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis, Mol. Cell. Biol., 28, 718, 10.1128/MCB.01338-07 Kietzmann, 2005, Reactive oxygen species in the control of hypoxia-inducible factor-mediated gene expression, Semin. Cell Dev. Biol., 16, 474, 10.1016/j.semcdb.2005.03.010 Hollander, 2001, Expression of hypoxia-inducible factor 1alpha by macrophages in the rheumatoid synovium: implications for targeting of therapeutic genes to the inflamed joint, Arthritis Rheum., 44, 1540, 10.1002/1529-0131(200107)44:7<1540::AID-ART277>3.0.CO;2-7 Wobben, 2013, Role of hypoxia inducible factor-1alpha for interferon synthesis in mouse dendritic cells, Biol. Chem., 394, 495, 10.1515/hsz-2012-0320 He, 2004, Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors, Nature, 429, 188, 10.1038/nature02488 Wittenberger, 2001, An expressed sequence tag (EST) data mining strategy succeeding in the discovery of new G-protein coupled receptors, J. Mol. Biol., 307, 799, 10.1006/jmbi.2001.4520 Ariza, 2012, The succinate receptor as a novel therapeutic target for oxidative and metabolic stress-related conditions, Front. Endocrinol., 3, 22, 10.3389/fendo.2012.00022 Robben, 2009, Localization of the succinate receptor in the distal nephron and its signaling in polarized MDCK cells, Kidney Int., 76, 1258, 10.1038/ki.2009.360 Bhuniya, 2011, Discovery of a potent and selective small molecule hGPR91 antagonist, Bioorg. Med. Chem. Lett., 21, 3596, 10.1016/j.bmcl.2011.04.091 Park, 2013, SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways, Mol. Cell, 50, 919, 10.1016/j.molcel.2013.06.001 Zhang, 2011, Identification of lysine succinylation as a new post-translational modification, Nat. Chem. Biol., 7, 58, 10.1038/nchembio.495 Du, 2011, Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase, Science, 334, 806, 10.1126/science.1207861 Nakagawa, 2009, SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle, Cell, 137, 560, 10.1016/j.cell.2009.02.026 Hawkins, 2010, Mitochondrial complex II prevents hypoxic but not calcium- and proapoptotic Bcl-2 protein-induced mitochondrial membrane potential loss, J. Biol. Chem., 285, 26494, 10.1074/jbc.M110.143164 Wayne, 1982, Glyoxylate metabolism and adaptation of Mycobacterium tuberculosis to survival under anaerobic conditions, Infect. Immun., 37, 1042, 10.1128/IAI.37.3.1042-1049.1982 Eoh, 2013, Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis, Proc. Natl. Acad. Sci. U.S.A., 110, 6554, 10.1073/pnas.1219375110 McKinney, 2000, Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase, Nature, 406, 735, 10.1038/35021074 Cimen, 2010, Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria, Biochemistry, 49, 304, 10.1021/bi901627u McGivney, 1979, Action of bacterial endotoxin and lipid A on mitochondrial enzyme activities of cells in culture and subcellular fractions, Infect. Immun., 25, 664, 10.1128/IAI.25.2.664-671.1979 Wu, 2013, Metabolic changes in cancer: beyond the Warburg effect, Acta Biochim. Biophys. Sin., 45, 18, 10.1093/abbs/gms104 Selak, 2005, Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase, Cancer Cell, 7, 77, 10.1016/j.ccr.2004.11.022 Maxwell, 1999, The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis, Nature, 399, 271, 10.1038/20459 Aguiar, 2010, Succinate modulates Ca2+ transient and cardiomyocyte viability through PKA-dependent pathway, Cell Calcium, 47, 37, 10.1016/j.ceca.2009.11.003 Oeckinghaus, 2011, Crosstalk in NF-kappaB signaling pathways, Nat. Immunol., 12, 695, 10.1038/ni.2065 Toma, 2008, Succinate receptor GPR91 provides a direct link between high glucose levels and renin release in murine and rabbit kidney, J. Clin. Invest., 118, 2526 Ghanem, 2007, Inflammation in high blood pressure: a clinician perspective, J. Am. Soc. Hypertens., 1, 113, 10.1016/j.jash.2007.01.004 Sadagopan, 2007, Circulating succinate is elevated in rodent models of hypertension and metabolic disease, Am. J. Hypertens., 20, 1209 Fukui, 1997, Mucosal blood flow and generation of superoxide in rat experimental colitis induced by succinic acid, J. Gastroenterol., 32, 464, 10.1007/BF02934084