Abolition of mitochondrial substrate‐level phosphorylation by itaconic acid produced by LPS‐induced Irg1 expression in cells of murine macrophage lineage
Abstract
Itaconate is a nonamino organic acid exhibiting antimicrobial effects. It has been recently identified in cells of macrophage lineage as a product of an enzyme encoded by immunoresponsive gene 1 ( Irg1 ), acting on the citric acid cycle intermediate cis‐aconitate. In mitochondria, itaconate can be converted by succinate‐coenzyme A (CoA) ligase to itaconyl‐CoA at the expense of ATP (or GTP), and is also a weak competitive inhibitor of complex II. Here, we investigated specific bioenergetic effects of increased itaconate production mediated by LPS‐induced stimulation of Irg1 in murine bone marrow‐derived macrophages (BMDM) and RAW‐264.7 cells. In rotenone‐treated macrophage cells, stimulation by LPS led to impairment in substrate‐level phosphorylation (SLP) of in situ mitochondria, deduced by a reversal in the directionality of the adenine nucleotide translocase operation. In RAW‐264.7 cells, the LPS‐induced impairment in SLP was reversed by short‐interfering RNA(siRNA)—but not scrambled siRNA—treatment directed against Irg1. LPS dose‐dependently inhibited oxygen consumption rates (61‐91%) and elevated glycolysis rates (>21%) in BMDM but not RAW‐264.7 cells, studied under various metabolic conditions. In isolated mouse liver mitochondria treated with rotenone, itaconate dose‐dependently (0.5‐2 mM) reversed the operation of adenine nucleotide translocase, implying impairment in SLP, an effect that was partially mimicked by malonate. However, malonate yielded greater ADP‐induced depolarizations (3‐19%) than itaconate. We postulate that itaconate abolishes SLP due to 1) a “CoA trap” in the form of itaconyl‐CoA that negatively affects the upstream supply of succinyl‐CoA from the α‐ketoglutarate dehydrogenase complex; 2) depletion of ATP (or GTP), which are required for the thioesterification by succinate‐CoA ligase; and 3) inhibition of complex II leading to a buildup of succinate which shifts succinate‐CoA ligase equilibrium toward ATP (or GTP) utilization. Our results support the notion that Irg1 ‐expressing cells of macrophage lineage lose the capacity of mitochondrial SLP for producing itaconate during mounting of an immune defense.—Németh, B., Doczi, J., Csete, D., Kacso, G., Ravasz, D., Adams, D., Kiss, G., Nagy, A. M., Horvath, G., Tretter, L., Mócsai, A., Csépányi‐Kömi, R., Iordanov, I., Adam‐Vizi, V., Chinopoulos, C. Abolition of mitochondrial substrate‐level phosphorylation by itaconic acid produced by LPS‐induced Irg1 expression in cells of murine macrophage lineage. FASEB J. 30, 286‐300 (2016). www.fasebj.org
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Cites
1 retracted
Garedew, A., Henderson, S. O., & Moncada, S. (2010) · Cell Death and Differentiation · doi:10.1038/cdd.2010.27 · Cited by 124 · see citing works
RetractedUnderstanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197 · see citing works
Succinate is an inflammatory signal that induces IL-1β through HIF-1α
Tannahill, G. M., Curtis, A. M., Adamik, J., Palsson-McDermott, E. M., McGettrick, A. F., Goel, G., Frezza, C., Bernard, N. J., Kelly, B., Foley, N. H., et al. (2013) · Nature · doi:10.1038/nature11986 · Cited by 4,176 · see citing works
A new collection method for the evaluation of nasal mucus proteins
Ruocco, L. A., Fattori, Romanelli, Martelloni, L., Casani, Samolewska, & Rezzonico (1998) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2222.1998.00312.x · Cited by 1,296 · see citing works
Toll-like receptor–induced changes in glycolytic metabolism regulate dendritic cell activation
Krawczyk, C. M., Holowka, T., Sun, J., Blagih, J., Amiel, E., DeBerardinis, R. J., Cross, J. R., Jung, E., Thompson, C. B., Jones, R. G., et al. (2010) · Blood · doi:10.1182/blood-2009-10-249540 · Cited by 1,246 · see citing works
Identification of Lps2 as a key transducer of MyD88-independent TIR signalling
Hoebe, K. H. N., Du, X., Georgel, P., Janssen, E. M., Tabeta, K., Kim, S. O., Goode, J., Lin, P., Mann, N., Mudd, S., et al. (2003) · Nature · doi:10.1038/nature01889 · Cited by 1,232 · see citing works
Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production
Michelucci, A., Cordes, T., Ghelfi, J., Pailot, A., Reiling, N., Goldmann, O., Binz, T., Wegner, A., Tallam, A., Rausell, A., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218599110 · Cited by 1,191 · see citing works
Rodríguez-Prados, J.-C., Través, P. G., Cuenca, J., Rico, D., Aragonés, J., Martín-Sanz, P., Cascante, M., & Boscá, L. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0901698 · Cited by 1,022 · see citing works
Safranine as a probe of the mitochondrial membrane potential
Åkerman, K. E. O., & Wikström, M. K. F. (1976) · FEBS Letters · doi:10.1016/0014-5793(76)80434-6 · Cited by 793 · see citing works
Succinate: a metabolic signal in inflammation
Mills, E., & O’Neill, L. A. J. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.11.008 · Cited by 741 · see citing works
The ADP and ATP transport in mitochondria and its carrier
Klingenberg, M. (2008) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2008.04.011 · Cited by 613 · see citing works
Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells
Everts, B., Amiel, E., van der Windt, G. J. W., Freitas, T. C., Chott, R., Yarasheski, K. E., Pearce, E. L., & Pearce, E. J. (2012) · Blood · doi:10.1182/blood-2012-03-419747 · Cited by 532 · see citing works
Biotechnological production of itaconic acid
Willke, T., & Vorlop, K. (2001) · Applied Microbiology and Biotechnology · doi:10.1007/s002530100685 · Cited by 507 · see citing works
Biotechnological production of itaconic acid and its biosynthesis in Aspergillus terreus
Okabe, M., Lies, D., Kanamasa, S., & Park, E. Y. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2132-3 · Cited by 488 · see citing works
Cellular Metabolism and Macrophage Functional Polarization
Zhu, L., Zhao, Q., Yang, T., Ding, W., & Zhao, Y. X. (2014) · International Reviews of Immunology · doi:10.3109/08830185.2014.969421 · Cited by 428 · see citing works
Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses
Kimura, A., Naka, T., Nakahama, T., Chinen, I., Masuda, K., Nohara, K., Fujii‐Kuriyama, Y., & Kishimoto, T. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20090560 · Cited by 414 · see citing works
Itaconic acid is a mammalian metabolite induced during macrophage activation
Strelko, C. L., Lu, W., Dufort, F. J., Seyfried, T. N., Chiles, T. C., Rabinowitz, J. D., & Roberts, M. F. (2011) · Journal of the American Chemical Society · doi:10.1021/ja2070889 · Cited by 391 · see citing works
The contributions of respiration and glycolysis to extracellular acid production
Mookerjee, S. A., Goncalves, R. L. S., Gerencser, A. A., Nicholls, D. G., & Brand, M. D. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2014.10.005 · Cited by 347 · see citing works
LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-α
Xaus, J., Comalada, M., Valledor, A. F., Lloberas, J., López-Soriano, F., Argilés, J. M., Bogdan, C., & Celada, A. (2000) · Blood · doi:10.1182/blood.v95.12.3823 · Cited by 331 · see citing works
Haile, D. J., Rouault, T. A., Harford, J. B., Kennedy, M. C., Blondin, G. A., Beinert, H., & Klausner, R. D. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.24.11735 · Cited by 321 · see citing works
Weinberg, J. M., Venkatachalam, M. A., Roeser, N. F., & Nissim, I. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.6.2826 · Cited by 317 · see citing works
Quantitative Microplate-Based Respirometry with Correction for Oxygen Diffusion
Gerencser, A. A., Neilson, A., Choi, S. W., Edman, U., Yadava, N., Oh, R. J., Ferrick, D. A., Nicholls, D. G., & Brand, M. D. (2009) · Analytical Chemistry · doi:10.1021/ac900881z · Cited by 312 · see citing works
Shin, J.-H., Yang, J.-Y., Jeon, B.-Y., Yoon, Y. J., Cho, S.-N., Kang, Y.-H., Ryu, D. H., & Hwang, G.-S. (2011) · Journal of Proteome Research · doi:10.1021/pr101054m · Cited by 247 · see citing works
Itaconate, an isocitrate lyase-directed inhibitor in Pseudomonas indigofera
McFadden, B. A., & Purohit, S. (1977) · Journal of Bacteriology · doi:10.1128/jb.131.1.136-144.1977 · Cited by 220 · see citing works
Mechanisms underlying the loss of mitochondrial membrane potential in glutamate excitotoxicity
Abramov, A. Y., & Duchen, M. R. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.04.017 · Cited by 213 · see citing works
Bochud‐Allemann, N., & Schneider, A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205776200 · Cited by 203 · see citing works
Biochemistry of microbial itaconic acid production
Steiger, M. G., Blumhoff, M. L., Mattanovich, D., & Sauer, M. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00023 · Cited by 185 · see citing works
Itaconic Acid: The Surprising Role of an Industrial Compound as a Mammalian Antimicrobial Metabolite
Cordes, T., Michelucci, A., & Hiller, K. (2015) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071714-034243 · Cited by 183 · see citing works
Hypoxia and hypoxia inducible factors in tumor metabolism
Zeng, W., Liu, P., Pan, W., Singh, S. R., & Wei, Y. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.01.032 · Cited by 170 · see citing works
The role of an astrocytic NADPH oxidase in the neurotoxicity of amyloid beta peptides
Abramov, A. Y., & Duchen, M. R. (2005) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2005.1766 · Cited by 158 · see citing works
The proinflammatory cytokine-induced IRG1 protein associates with mitochondria
Degrandi, D., Hoffmann, R., Beuter-Gunia, C., & Pfeffer, K. (2009) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2008.0013 · Cited by 155 · see citing works
[11] The preparation of heart mitochondria from laboratory animals
Tyler, D. D., & Gonze, J. (1967) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(67)10014-1 · Cited by 151 · see citing works
STAT3 regulates NF-κB recruitment to the IL-12p40 promoter in dendritic cells
Hoentjen, F., Sartor, R. B., Ozaki, M., & Jobin, C. (2004) · Blood · doi:10.1182/blood-2004-04-1309 · Cited by 143 · see citing works
Highly Sensitive GC/MS/MS Method for Quantitation of Amino and Nonamino Organic Acids
Kvitvang, H. F. N., Andreassen, T., Adam, T., Villas-Bôas, S. G., & Bruheim, P. (2011) · Analytical Chemistry · doi:10.1021/ac103245b · Cited by 136 · see citing works
Studies on succinate dehydrogenase
Dervartanian, D. V., & Veeger, C. (1964) · Biochimica et Biophysica Acta (BBA) - Specialized Section on Enzymological Subjects · doi:10.1016/0926-6569(64)90182-8 · Cited by 130 · see citing works
Tavakoli, S., Zamora, D. A., Ullevig, S. L., & Asmis, R. (2013) · Journal of Nuclear Medicine · doi:10.2967/jnumed.112.119099 · Cited by 109 · see citing works
Chinopoulos, C., Gerencser, A. A., Mandi, M., Mathe, K., Töröcsik, B., Doczi, J., Turiak, L., Kiss, G., Konràd, C., Vajda, S., et al. (2010) · The FASEB Journal · doi:10.1096/fj.09-149898 · Cited by 103 · see citing works
Self-citationMetabolomic Patterns in Glioblastoma and Changes during Radiotherapy: A Clinical Microdialysis Study
Wibom, C., Surowiec, I., Mörén, L., Bergström, P., Johansson, M., Antti, H., & Bergenheim, A. T. (2010) · Journal of Proteome Research · doi:10.1021/pr901088r · Cited by 101 · see citing works
A Novel Kinetic Assay of Mitochondrial ATP-ADP Exchange Rate Mediated by the ANT
Chinopoulos, C., Vajda, S., Csanády, L., Mándi, M., Mathe, K., & Ádám‐Vizi, V. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2008.12.3915 · Cited by 100 · see citing works
Self-citationHypoxia-mediated regulation of macrophage functions in pathophysiology
Riboldi, E., Porta, C., Morlacchi, S., Viola, A., Mantovani, A., & Sica, A. (2012) · International Immunology · doi:10.1093/intimm/dxs110 · Cited by 97 · see citing works
Non-targeted metabolite profiling in activated macrophage secretion
Sugimoto, M., Sakagami, H., Yokote, Y., Onuma, H., Kaneko, M., Mori, M., Sakaguchi, Y., Soga, T., & Tomita, M. (2012) · Metabolomics · doi:10.1007/s11306-011-0353-9 · Cited by 95 · see citing works
THE METABOLISM OF ITACONIC ACID BY LIVER MITOCHONDRIA
Adler, J., Wang, S., & Lardy, H. A. (1957) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)63691-4 · Cited by 88 · see citing works
Coenzyme A and its derivatives: renaissance of a textbook classic
Theodoulou, F. L., Sibon, O. C. M., Jackowski, S., & Gout, I. T. (2014) · Biochemical Society Transactions · doi:10.1042/bst20140176 · Cited by 88 · see citing works
Través, P. G., de Atauri, P., Marín, S., Pimentel-Santillana, M., Rodríguez‐Prados, J., de Mas, I. M., Selivanov, V. A., Martín‐Sanz, P., Boscá, L., & Cascante, M. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101781 · Cited by 83 · see citing works
Mitochondrial consumption of cytosolic ATP: Not so fast
Chinopoulos, C. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.004 · Cited by 79 · see citing works
Self-citationThe Pathway of Itaconate Metabolism by Liver Mitochondria
Wang, S., Adler, J., & Lardy, H. A. (1961) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)64421-7 · Cited by 75 · see citing works
Berg, I. A., Filatova, L. V., & Ivanovsky, R. N. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11413.x · Cited by 71 · see citing works
Naringin inhibits chemokine production in an LPS-induced RAW 264.7 macrophage cell line
Liu, Y., Su, W., WANG, S., & Li, P. (2012) · Molecular Medicine Reports · doi:10.3892/mmr.2012.1072 · Cited by 71 · see citing works
Hillier, S., & Charnetzky, W. T. (1981) · Journal of Bacteriology · doi:10.1128/jb.145.1.452-458.1981 · Cited by 68 · see citing works
Itaconate reduces visceral fat by inhibiting fructose 2,6-bisphosphate synthesis in rat liver
Sakai, A., Kusumoto, A., Kiso, Y., & Furuya, E. (2004) · Nutrition · doi:10.1016/j.nut.2004.08.007 · Cited by 66 · see citing works
Kiss, G., Konrad, C., Doczi, J., Starkov, A., Kawamata, H., Manfredi, G., Zhang, S. F., Gibson, G. E., Beal, M., Ádám-Vizi, V., et al. (2013) · The FASEB Journal · doi:10.1096/fj.12-220202 · Cited by 64 · see citing works
Self-citationSanadi, D. R., Gibson, D. M., & Ayengar, P. (1954) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(54)90205-x · Cited by 62 · see citing works
The role of succinyl-CoA synthetase in the control of heme biosynthesis.
Labbe, R. E., Kurumada, T., & Onisawa, J. (1965) · Biochimica et Biophysica Acta · doi:10.1016/0304-4165(65)90050-4 · Cited by 61 · see citing works
Lee, Y., Sohn, W., Kim, D., & Kwon, H. (2004) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.2004.04011.x · Cited by 60 · see citing works
Succinic thiokinase and metabolic control.
Ottaway, J., Mcclellan, J. A., & Saunderson, C. (1981) · International Journal of Biochemistry · doi:10.1016/0020-711x(81)90111-7 · Cited by 48 · see citing works
Caenorhabditis elegans and Ascaris suum: inhibition of isocitrate lyase by itaconate
Patel, T. R., & McFadden, B. A. (1978) · Experimental Parasitology · doi:10.1016/0014-4894(78)90107-8 · Cited by 46 · see citing works
Xu, L., Shen, S., Ma, Y., Kim, J. K., Rodríguez‐Agudo, D., Heuman, D. M., Hylemon, P. B., Pandak, W. M., & Ren, S. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00337.2011 · Cited by 45 · see citing works
The inhibitory effects of itaconic acid in vitro and in vivo
Booth, A. N., Taylor, J., Wilson, R. H., & DeEds, F. (1952) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)55778-1 · Cited by 42 · see citing works
The “B Space” of mitochondrial phosphorylation
Chinopoulos, C. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22659 · Cited by 39 · see citing works
Self-citationKiss, G., Konrad, C., Pour-Ghaz, I., Mansour, J. J., Németh, B., Starkov, A., Ádám-Vizi, V., & Chinopoulos, C. (2014) · The FASEB Journal · doi:10.1096/fj.13-243030 · Cited by 39 · see citing works
Self-citationNolte, J., Schürmann, M., Schepers, C.-L., Vogel, E., Wübbeler, J. H., & Steinbüchel, A. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.03075-13 · Cited by 32 · see citing works
[Methylglutaconase, a new hydrase participating in the metabolism of various carboxylic acids].
Hilz, H., Knappe, J., Ringelmann, E., & Lynen, F. (1958) · PubMed · Cited by 24 · see citing works
Xiao, W., Wang, L., Xiao, R., Wu, M., Tan, J., & He, Y. (2011) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-011-0784-7 · Cited by 13 · see citing works
Hunger‐Glaser, I., Brun, R., Linder, M., & Seebeck, T. (1999) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(99)00032-8 · Cited by 10 · see citing works
Franke, W., Mitarbeit, E. H. U., & Taschen, G. (1957) · Justus Liebig s Annalen der Chemie · doi:10.1002/jlac.19576080115 · Cited by 10 · see citing works
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O'Neill, L., & Pearce, E. (2016) · Journal of Experimental Medicine · doi:10.1084/jem.20151570 · Cited by 1,641 · see citing works
Lampropoulou, V., Sergushichev, A., Bambousková, M., Nair, S., Vincent, E. E., Loginicheva, E., Cervantes‐Barragán, L., Ma, X., Huang, S. C., Griss, T., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.06.004 · Cited by 1,547 · see citing works
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HIF1α and metabolic reprogramming in inflammation
Corcoran, S. E., & O'Neill, L. A. J. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84431 · Cited by 789 · see citing works
Glycolysis – a key player in the inflammatory response
Soto‐Heredero, G., Heras, M. M. G. D. L., Gabandé‐Rodríguez, E., Oller, J., & Mittelbrunn, M. (2020) · FEBS Journal · doi:10.1111/febs.15327 · Cited by 645 · see citing works
Itaconate: the poster child of metabolic reprogramming in macrophage function
O'Neill, L. A. J., & Artyomov, M. N. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0128-5 · Cited by 624 · see citing works
Metabolic Regulation of Macrophage Polarization in Cancer
Mehla, K., & Singh, P. K. (2019) · Trends in cancer · doi:10.1016/j.trecan.2019.10.007 · Cited by 617 · see citing works
Williams, N. C., & O'Neill, L. A. J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00141 · Cited by 569 · see citing works
Succinate, an intermediate in metabolism, signal transduction, ROS, hypoxia, and tumorigenesis.
Tretter, L., Patócs, A., & Chinopoulos, C. (2016) · Biochimica et Biophysica Acta · doi:10.1016/j.bbabio.2016.03.012 · Cited by 502 · see citing works
Self-citationCordes, T., Wallace, M., Michelucci, A., Divakaruni, A. S., Sapcariu, S. C., Sousa, C., Koseki, H., Cabrales, P., Murphy, A. N., Hiller, K., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.685792 · Cited by 526 · see citing works
Palmieri, E. M., Gonzalez-Cotto, M., Baseler, W. A., Davies, L. C., Ghesquière, B., Maio, N., Rice, C. M., Rouault, T. A., Cassel, T., Higashi, R. M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14433-7 · Cited by 472 · see citing works
Krebs cycle Reborn in macrophage immunometabolism
Ryan, D. G., & O'Neill, L. A. J. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-081619-104850 · Cited by 444 · see citing works
Coupling Krebs cycle metabolites to signalling in immunity and cancer
Ryan, D. G., Murphy, M. P., Frezza, C., Prag, H. A., Chouchani, E. T., O’Neill, L. A., & Mills, E. L. (2018) · Nature Metabolism · doi:10.1038/s42255-018-0014-7 · Cited by 398 · see citing works
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Belizário, J. E., Faintuch, J., & Garay-Malpartida, M. (2018) · Mediators of Inflammation · doi:10.1155/2018/2037838 · Cited by 341 · see citing works
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Diskin, C., & Pålsson‐McDermott, E. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00270 · Cited by 292 · see citing works
Papathanassiu, A. E., Ko, J., Imprialou, M., Bagnati, M., Srivastava, P. K., Vu, H., Cucchi, D., McAdoo, S. P., Ananieva, E. A., Mauro, C., et al. (2017) · Nature Communications · doi:10.1038/ncomms16040 · Cited by 250 · see citing works
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Hooftman, A., & O'Neill, L. A. J. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.05.007 · Cited by 232 · see citing works
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Wu, R., Chen, F., Wang, N., Tang, D., & Kang, R. (2020) · Cellular and Molecular Immunology · doi:10.1038/s41423-020-0489-5 · Cited by 217 · see citing works
Fleetwood, A. J., Lee, M. K. S., Singleton, W., Achuthan, A. A., Lee, M.-C., O’brien-simpson, N. M., Cook, A. D., Murphy, A. J., Dashper, S. G., Reynolds, E. C., et al. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00351 · Cited by 206 · see citing works
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Namba, T., Dóczi, J., Pinson, A., Xing, L., Kalebic, N., Wilsch‐Bräuninger, M., Long, K. R., Vaid, S., Lauer, J. L., Bogdanova, A. I., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.11.027 · Cited by 157 · see citing works
Self-citationItaconate modulates tricarboxylic acid and redox metabolism to mitigate reperfusion injury
Cordes, T., Lucas, A., Divakaruni, A. S., Murphy, A. N., Cabrales, P., & Metallo, C. M. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.11.019 · Cited by 153 · see citing works
Krebs cycle rewired for macrophage and dendritic cell effector functions
Ryan, D. G., & O'Neill, L. A. J. (2017) · FEBS Letters · doi:10.1002/1873-3468.12744 · Cited by 150 · see citing works
Role of Macrophages in Wound HealingPreprint
Willenborg, S., Injarabian, L., & Eming, S. A. (2022) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041216 · Cited by 147 · see citing works
Mitochondrial metabolites: undercover signalling molecules
Frezza, C. (2017) · Interface Focus · doi:10.1098/rsfs.2016.0100 · Cited by 136 · see citing works
Effects of Interferons and Viruses on Metabolism
Fritsch, S. D., & Weichhart, T. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00630 · Cited by 134 · see citing works
Huang, H., Li, G., He, Y., Chen, J., Yan, J., Zhang, Q., Li, L., & Cai, X. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1404441 · Cited by 141 · see citing works
Mesaconate is synthesized from itaconate and exerts immunomodulatory effects in macrophages
He, W., Henne, A., Lauterbach, M., Geißmar, E., Nikolka, F., Kho, C., Heinz, A., Dostert, C., Grusdat, M., Cordes, T., et al. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00565-1 · Cited by 99 · see citing works
Biochemistry of proinflammatory macrophage activation
Nonnenmacher, Y., & Hiller, K. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2784-1 · Cited by 110 · see citing works
G Protein–Coupled Receptors Targeting Insulin Resistance, Obesity, and Type 2 Diabetes Mellitus
Riddy, D. M., Delerive, P., Summers, R. J., Sexton, P. M., & Langmead, C. J. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.014373 · Cited by 108 · see citing works
Vitamin D endocrinology on the cross-road between immunity and metabolism
Vanherwegen, A.-S., Gysemans, C. A., & Mathieu, C. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.04.018 · Cited by 105 · see citing works
Zhu, X., Guo, Y., Liu, Z., Yang, J., Tang, H., & Wang, Y. (2021) · Scientific Reports · doi:10.1038/s41598-021-97352-x · Cited by 101 · see citing works
Weiss, J. M., Palmieri, E. M., Gonzalez-Cotto, M., Bettencourt, I. A., Megill, E., Snyder, N. W., & McVicar, D. W. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00801-2 · Cited by 97 · see citing works
Burch, J. S., Marcero, J. R., Maschek, J. A., Cox, J. E., Jackson, L. K., Medlock, A. E., Phillips, J. D., & Dailey, H. A. (2018) · Blood · doi:10.1182/blood-2018-01-829036 · Cited by 92 · see citing works
Immunometabolism of Macrophages in Bacterial Infections
Galli, G., & Saleh, M. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.607650 · Cited by 92 · see citing works
The Role of Tricarboxylic Acid Cycle Metabolites in Viral Infections
Sánchez‐García, F. J., Pérez-Hernández, C. A., Rodríguez-Murillo, M., & Moreno‐Altamirano, M. M. B. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.725043 · Cited by 90 · see citing works
Press-pulse: a novel therapeutic strategy for the metabolic management of cancer
Seyfried, T. N., Yu, G. W., Maroon, J. C., & D’Agostino, D. P. (2017) · Nutrition & Metabolism · doi:10.1186/s12986-017-0178-2 · Cited by 86 · see citing works
Metabolic Reprogramming in Mitochondria of Myeloid Cells
Zuo, H., & Wan, Y. (2019) · Cells · doi:10.3390/cells9010005 · Cited by 81 · see citing works
Cordes, T., & Metallo, C. M. (2021) · Metabolites · doi:10.3390/metabo11020117 · Cited by 76 · see citing works
Macrophage Responses to Environmental Stimuli During Homeostasis and Disease
Rasheed, A., & Rayner, K. J. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnab004 · Cited by 79 · see citing works
Li, L., & Tian, Y. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114504 · Cited by 73 · see citing works
TCA cycle signalling and the evolution of eukaryotes
Ryan, D. G., Frezza, C., & O'Neill, L. A. J. (2020) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2020.09.014 · Cited by 69 · see citing works
Aguilar‐López, B. A., Moreno‐Altamirano, M. M. B., Dockrell, H. M., Duchen, M. R., & Sánchez‐García, F. J. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00051 · Cited by 71 · see citing works
Saborano, R., Wongpinyochit, T., Totten, J. D., Johnston, B. F., Seib, F. P., & Duarte, I. F. (2017) · Advanced Healthcare Materials · doi:10.1002/adhm.201601240 · Cited by 68 · see citing works
Young, T., Kesarcodi-Watson, A., Alfaro, A. C., Mérien, F., Nguyen, T. V., Mae, H., Le, D. V., & Villas-Bôas, S. G. (2017) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2017.03.025 · Cited by 61 · see citing works
Mitochondrial ACOD1/IRG1 in infection and sterile inflammation
Wu, R., Kang, R., & Tang, D. (2022) · Journal of Intensive Medicine · doi:10.1016/j.jointm.2022.01.001 · Cited by 58 · see citing works
PEGylation-Dependent Metabolic Rewiring of Macrophages with Silk Fibroin Nanoparticles
Totten, J. D., Wongpinyochit, T., Carrola, J., Duarte, I. F., & Seib, F. P. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.8b18716 · Cited by 59 · see citing works
Distinct metabolic patterns during microglial remodeling by oleate and palmitate
Chausse, B., Kakimoto, P. A., Caldeira-da-Silva, C. C., Chaves-Filho, A. B., Yoshinaga, M. Y., da Silva, R. P., Miyamoto, S., & Kowaltowski, A. J. (2019) · Bioscience Reports · doi:10.1042/bsr20190072 · Cited by 59 · see citing works
Succinate in ischemia: where does it come from?
Chinopoulos, C. (2019) · International Journal of Biochemistry and Cell Biology · doi:10.1016/j.biocel.2019.105580 · Cited by 55 · see citing works
Self-citationControl of immune cell signaling by the immuno-metabolite itaconate
Lang, R., & Siddique, M. N. A. A. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1352165 · Cited by 53 · see citing works
Versatility of microglial bioenergetic machinery under starving conditions
Nagy, Á., Fekete, R., Horváth, G., Koncsos, G., Kriston, C., Sebestyén, A. R., Giricz, Z., Környei, Z., Madarász, E., & Tretter, L. (2017) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2017.12.002 · Cited by 52 · see citing works
Self-citationCrosstalk Between Staphylococcus aureus and Innate Immunity: Focus on Immunometabolism
Horn, C. M., & Kielian, T. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.621750 · Cited by 51 · see citing works
Titz, B., Szostak, J., Sewer, A., Phillips, B. W., Nury, C., Schneider, T. L., Dijon, S., Lavrynenko, O., Elamin, A., Guedj, E., et al. (2020) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2020.04.011 · Cited by 49 · see citing works
HIF1α-Dependent Metabolic Signals Control the Differentiation of Follicular Helper T Cells
Dong, L., He, Y., Zhou, S., Cao, Y., Li, Y., Bi, Y., & Liu, G. (2019) · Cells · doi:10.3390/cells8111450 · Cited by 46 · see citing works
Rattigan, K. M., Pountain, A. W., Regnault, C., Achcar, F., Vincent, I. M., Goodyear, C. S., & Barrett, M. P. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194126 · Cited by 44 · see citing works
Yu, S., Ding, L., Liang, D., & Luo, L. (2018) · Molecular Oral Microbiology · doi:10.1111/omi.12241 · Cited by 45 · see citing works
Yaker, L., Tebani, A., Lesueur, C., Dias, C., Jung, V. A., Bekri, S., Guerrera, I. C., Kamel, S., Ausseil, J., & Boullier, A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.823450 · Cited by 44 · see citing works
The promise and peril of targeting cell metabolism for cancer therapy
Weiss, J. M. (2019) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-019-02432-7 · Cited by 42 · see citing works
Spontaneous hydrolysis and spurious metabolic properties of α-ketoglutarate esters
Parker, S. J., Encarnación-Rosado, J., Hollinshead, K. E. R., Hollinshead, D. M., Ash, L. J., Rossi, J. A. K., Lin, E. Y., Sohn, A. S. W., Philips, M. R., Jones, D. R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25228-9 · Cited by 42 · see citing works
Yakupova, E. I., Maleev, G. V., Krivtsov, A. V., & Plotnikov, E. Y. (2022) · Experimental Biology and Medicine · doi:10.1177/15353702221080130 · Cited by 37 · see citing works
Hujber, Z., Horváth, G., Petővári, G., Krencz, I., Dankó, T., Mészáros, K. V., Rajnai, H., Szoboszlai, N., Leenders, W. P. J., Jeney, A., et al. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-0946-5 · Cited by 38 · see citing works
Self-citationBelosludtsev, K. N., Belosludtseva, N. V., Kosareva, E. A., Talanov, E. Y., Gudkov, S. V., & Dubinin, M. V. (2020) · Biochimie · doi:10.1016/j.biochi.2020.07.011 · Cited by 37 · see citing works
Process engineering of pH tolerant Ustilago cynodontis for efficient itaconic acid production
Tehrani, H. H., Saur, K. M., Tharmasothirajan, A., Blank, L. M., & Wierckx, N. J. P. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1266-y · Cited by 37 · see citing works
Proline Oxidation Supports Mitochondrial ATP Production When Complex I Is Inhibited
Pallag, G., Nazarian, S., Ravasz, D., Bui, D., Komlódi, T., Doerrier, C., Gnaiger, E., Seyfried, T. N., & Chinopoulos, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23095111 · Cited by 34 · see citing works
Self-citationTanaka, A., To, J., O’Brien, B. A., Donnelly, S., & Lund, M. E. (2017) · BMC Immunology · doi:10.1186/s12865-017-0223-y · Cited by 33 · see citing works
New Avenues of Heme Synthesis Regulation
Medlock, A. E., & Dailey, H. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137467 · Cited by 33 · see citing works
Ohm, M., Hosseini, S., Lonnemann, N., He, W., More, T. H., Goldmann, O., Medina, E., Hiller, K., & Körte, M. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03188-3 · Cited by 33 · see citing works
Liu, X., Wu, X., Zhu, X., Li, T., & Liu, Y. (2017) · International Immunopharmacology · doi:10.1016/j.intimp.2017.04.012 · Cited by 31 · see citing works
McGettrick, A. F., & O'Neill, L. A. J. (2022) · Current Opinion in Immunology · doi:10.1016/j.coi.2022.102268 · Cited by 32 · see citing works
Kacsó, G., Ravasz, D., Doczi, J., Németh, B., Madgar, O., Saada, A., Ilin, P., Miller, C., Ostergaard, E., Iordanov, I., et al. (2016) · Biochemical Journal · doi:10.1042/bcj20160594 · Cited by 27 · see citing works
Self-citationFlores, R. E., Brown, A. K., Taus, L. J., Khoury, J., Glover, F., Kami, K., Sarangarajan, R., Walshe, T. E., Narain, N. R., Kiebish, M. A., et al. (2018) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2018.03.012 · Cited by 30 · see citing works
Self-citationMarcero, J. R., Cox, J. E., Bergonia, H. A., Medlock, A. E., Phillips, J. D., & Dailey, H. A. (2021) · Blood Advances · doi:10.1182/bloodadvances.2021004750 · Cited by 29 · see citing works
Roles of Mitochondrial Respiratory Complexes during Infection
Escoll, P., Platon, L., & Buchrieser, C. (2019) · Immunometabolism · doi:10.20900/immunometab20190011 · Cited by 25 · see citing works
The evolutionary tug-of-war of macrophage metabolism during bacterial infection
Almeida, L., Dhillon-LaBrooy, A., & Sparwasser, T. D. (2023) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2023.11.002 · Cited by 25 · see citing works
Reprogramming immunity with itaconate: metabolic mechanisms and therapeutic perspectives
Gao, H., Ding, M., Liu, Y., Wang, Y., Zhao, S., Chen, J., Chen, Z., & Wang, G. (2025) · Inflammation Research · doi:10.1007/s00011-025-02087-4 · Cited by 26 · see citing works
Han, W., Fessel, J. P., Sherrill, T. P., Kocurek, E. G., Yull, F. E., & Blackwell, T. S. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1900820 · Cited by 25 · see citing works
Glutaminases as a Novel Target for SDHB-Associated Pheochromocytomas/Paragangliomas
Sarkadi, B., Meszaros, K., Krencz, I., Canu, L., Krokker, L., Zakarias, S., Barna, G., Sebestyen, A., Papay, J., Hujber, Z., et al. (2020) · Cancers · doi:10.3390/cancers12030599 · Cited by 23 · see citing works
Self-citationChinopoulos, C. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.543564 · Cited by 23 · see citing works
Self-citationIn vivo itaconate tracing reveals degradation pathway and turnover kinetics
Willenbockel, H. F., Williams, A. T., Lucas, A., Reynolds, M. B., Joulia, E., Ruchhoeft, M. L., Dowerg, B., Cabrales, P., Metallo, C. M., & Cordes, T. (2025) · Nature Metabolism · doi:10.1038/s42255-025-01363-1 · Cited by 21 · see citing works
Basic Mechanisms of Immunometabolites in Shaping the Immune Response
Ryan, D. G., Peace, C. G., & Hooftman, A. (2023) · Journal of Innate Immunity · doi:10.1159/000535452 · Cited by 22 · see citing works
Mitoimmunity—when mitochondria dictates macrophage function
Corrêa‐da‐Silva, F., Pereira, J. A. D. S., de Aguiar, C. F., & Moraes‐Vieira, P. M. (2017) · Cell Biology International · doi:10.1002/cbin.10921 · Cited by 22 · see citing works
Monocyte glycolysis determines CD8+ T cell functionality in human Chagas disease
Sanmarco, L. M., Eberhardt, N., Bergero, G., Palacio, L. P. Q., Adami, P. V. M., Visconti, L. M., Minguez, Á. R., Hernández-Vásquez, Y., Silva, E. A. C., Morelli, L., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.123490 · Cited by 21 · see citing works
Itaconate or how I learned to stop avoiding the study of immunometabolism
Coelho, C. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010361 · Cited by 21 · see citing works
Itaconic Acid – An Emerging Building Block
Steiger, M. G., Wierckx, N. J. P., Blank, L. M., Mattanovich, D., & Sauer, M. (2016) · Industrial Biotechnology · doi:10.1002/9783527807833.ch15 · Cited by 19 · see citing works
Birajdar, M. S., Cho, H., Seo, Y., Choi, J. H., & Park, H. (2017) · Applied Surface Science · doi:10.1016/j.apsusc.2017.12.125 · Cited by 18 · see citing works
Exploring the evolutionary roots and physiological function of itaconate
Cordes, T., & Metallo, C. M. (2020) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2020.11.005 · Cited by 18 · see citing works
Molecular Mechanisms of Iron Metabolism and Overload
Tayal, A., Kaur, J., Sadeghi, P., & Maitta, R. W. (2025) · Biomedicines · doi:10.3390/biomedicines13092067 · Cited by 21 · see citing works
Itaconate and Its Derivatives Repress Early Myogenesis In Vitro and In Vivo
Oh, T. S., Hutchins, D. C., Mainali, R., Goslen, K. H., & Quinn, M. A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.748375 · Cited by 15 · see citing works
Tracing insights into human metabolism using chemical engineering approaches
Cordes, T., & Metallo, C. M. (2016) · Current Opinion in Chemical Engineering · doi:10.1016/j.coche.2016.08.019 · Cited by 14 · see citing works
IRG1/Itaconate induces metabolic reprogramming to suppress ER-positive breast cancer cell growth.
Wang, H., Chang, W., Lee, D., Li, X., & Hung, M. (2023) · PubMed Central · Cited by 11 · see citing works
Mikulás, K., Komlódi, T., Földes, A., Sváb, G., Horváth, G., Nagy, Á., Ambrus, A., Gyulai-Gaál, S., Gera, I., Hermann, P., et al. (2020) · Materials · doi:10.3390/ma13163472 · Cited by 11 · see citing works
Self-citationThe itaconate family of immunomodulators grows
McGettrick, A. F., & O'Neill, L. A. J. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00578-w · Cited by 11 · see citing works
Khailova, L. S., Kirsanov, R. S., Rokitskaya, T. I., Krasnov, V. S., Korshunova, G. A., Kotova, Е. А., & Antonenko, Y. N. (2024) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2024.149506 · Cited by 10 · see citing works
The role and therapeutic potential of itaconate in lung disease
He, R., Zuo, Y., Yi, K., Liu, B., Song, C., Li, N., & Geng, Q. (2024) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-024-00642-1 · Cited by 10 · see citing works
Mancebo, C., Fernández, J. J., Herrero-Sánchez, C., Álvarez, Y., Alonso, S., Sandoval, T. A., Cubillos‐Ruiz, J. R., Montero, O., Fernández, N., & Crespo, M. S. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2100666 · Cited by 10 · see citing works
Krebs Cycle Rewired: Driver of Atherosclerosis Progression?
Liang, Y., Chen, Y., Lü, L., Zhang, S., Xiao, J., & Wei, D. (2021) · Current Medicinal Chemistry · doi:10.2174/0929867328666210806105246 · Cited by 10 · see citing works
Yu, X., Xing, Y., Liu, H., Chang, Y.-M., You, Y., Dou, Y., Liu, B., Wang, Q., Ma, D., Chen, L., et al. (2022) · Nutrients · doi:10.3390/nu14091901 · Cited by 9 · see citing works
Glucose Metabolic Reprogramming of Macrophages Against Mycobacterium tuberculosis Infection
Liu, T., Yang, Z., Tong, J., Gao, M., & Pang, Y. (2025) · ImmunoTargets and Therapy · doi:10.2147/itt.s552746 · Cited by 9 · see citing works
Metabolic Adaptations and Functional Activity of Macrophages in Homeostasis and Inflammation
Yurakova, T. R., Gorshkova, E. A., Nosenko, M. A., & Drutskaya, M. S. (2024) · Biochemistry (Moscow) · doi:10.1134/s0006297924050043 · Cited by 7 · see citing works
- Authors
- Németh, B., Doczi, J., Csete, D., Kacso, G., Ravasz, D., Adams, D., Kiss, G., Nagy, A. M., Horvath, G., Tretter, L., Mócsai, A., Csépáinyi‐Kömi, R., Iordanov, I., Adam‐Vizi, V., & Chinopoulos, C.
- Affiliations
- Department of Medical Biochemistry Semmelweis University Budapest Hungary
- Department of Physiology Semmelweis University Budapest Hungary
- Semmelweis University (HU)
- Corresponding author
- Chinopoulos, Christos
- Venue
- The FASEB Journal
- Publisher
- Wiley
- Published
- 2015-09-10
- Volume
- 30
- Issue
- 1
- Pages
- 286-300
- ISSN
- 0892-6638 (ISSN-L)
- 1530-6860
- OpenAlex
- W2232390838
- Cited by
- 136
- References
- 65
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 9 · 2023: 7 · 2022: 20 · 2021: 14 · 2020: 15 · 2019: 15 · 2018: 11 · 2017: 15 · 2016: 9 · 2015: 1
- FWCI
- 5.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The FASEB Journal (publishedVersion)
- PubMed (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Semmelweis University Repository (Semmelweis University) (submittedVersion)
- Funders
- Magyar Tudományos Akadémia (02001)
- Hungarian Scientific Research Fund (K 100918)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- itaconic acid, IRG1, substrate-level phosphorylation, macrophages, LPS, complex II inhibition, succinic acid, adenine nucleotide translocase, mitochondrial bioenergetics, glycolysis, rotenone, malonate, alpha-ketoglutarate dehydrogenase complex, succinyl-CoA, ATP depletion, bone marrow-derived macrophages, RAW 264.7 macrophages
- MeSH terms
- Mitochondrial ADP, ATP Translocases, Animals, Cell Line, Chlorocebus aethiops, Female, Glycolysis, Hydro-Lyases, Lipopolysaccharides, Macrophages, Male, Malonates, Mice, Inbred C57BL, Mitochondria, Liver, Oxidative Phosphorylation, Rotenone, Succinates, Succinate-CoA Ligases, COS Cells, Mice, Membrane Potential, Mitochondrial
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