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ROS-associated immune response and metabolism: a mechanistic approach with implication of various diseases

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Abstract

The immune system plays a pivotal role in maintaining the defense mechanism against external agents and also internal danger signals. Metabolic programming of immune cells is required for functioning of different subsets of immune cells under different physiological conditions. The field of immunometabolism has gained ground because of its immense importance in coordination and balance of immune responses. Metabolism is very much related with production of energy and certain by-products. Reactive oxygen species (ROS) are generated as one of the by-products of various metabolic pathways. The amount, localization of ROS and redox status determine transcription of genes, and also influences the metabolism of immune cells. This review discusses ROS, metabolism of immune cells at different cellular conditions and sheds some light on how ROS might regulate immunometabolism.

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References

  • Abdollahi A, Schwager C, Kleeff J et al (2007) Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc Natl Acad Sci 104(31):12890–12895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abo A, Pick E, Hall A, Totty N, Teahan CG, Segal AW (1991) Activation of the NADPH oxidase involves the small GTP-binding protein p21 rac1. Nature 353(6345):668–670

    Article  CAS  PubMed  Google Scholar 

  • Ahmed N, Kansara M, Berridge VM (1997) Acute regulation of glucose transport in a monocyte–macrophage cell line: Glut-3 affinity for glucose is enhanced during the respiratory burst. Biochem J 327(2):369–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmed S, Mahmood Z, Zahid S (2015) Linking insulin with Alzheimer’s disease: emergence as type III diabetes. Neurolog Sci 36(10):1763–1769

    Article  Google Scholar 

  • Ahmed SMU, Luo L, Namani A, Wang XJ (2017) Tang X Nrf2 signaling pathway: pivotal roles in inflammation. Biochimica et Biophysica Acta (BBA)-Mol Basis Dis 1863:585–597

    Article  CAS  Google Scholar 

  • Alberghina L, Gaglio D (2014) Redox control of glutamine utilization in cancer. Cell Death Dis 5(12):e1561–e1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altman BJ, Stine ZE, Dang CV (2016) From Krebs to clinic: glutamine metabolism to cancer therapy. Nat Rev Cancer 16(10):619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amelio I, Cutruzzolá F, Antonov A, Agostini M, Melino G (2014) Serine and glycine metabolism in cancer. Trends Biochem Sci 39(4):191–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amiel E, Everts B, Freitas TC et al (2012) Inhibition of mechanistic target of rapamycin promotes dendritic cell activation and enhances therapeutic autologous vaccination in mice. J Immunol 189(5):2151–2158

    Article  CAS  PubMed  Google Scholar 

  • Angajala A, Lim S, Phillips JB et al (2018) Diverse roles of mitochondria in immune responses: novel insights into immuno-metabolism. Front Immunol 9:1605

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Araujo JA, Zhang M, Yin F (2012) Heme oxygenase-1, oxidation, inflammation, and atherosclerosis. Front Pharmacol 3:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Arrigo A-P (1999) Gene expression and the thiol redox state. Free Radical Biol Med 27(9–10):936–944

    Article  CAS  Google Scholar 

  • Bambouskova M, Gorvel L, Lampropoulou V et al (2018) Electrophilic properties of itaconate and derivatives regulate the IκBζ–ATF3 inflammatory axis. Nature 556(7702):501–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baroja-Mazo A, Martín-Sánchez F, Gomez AI et al (2014) The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol 15(8):738

    Article  CAS  PubMed  Google Scholar 

  • Bartolini D, Dallaglio K, Torquato P, Piroddi M, Galli F (2018) Nrf2-p62 autophagy pathway and its response to oxidative stress in hepatocellular carcinoma. Transl Res 193:54–71

    Article  PubMed  CAS  Google Scholar 

  • Benhar M (2015) Nitric oxide and the thioredoxin system: a complex interplay in redox regulation. Biochimica et Biophysica Acta (BBA)-General Sub 1850(12):2476–2484

    Article  CAS  Google Scholar 

  • Béraud C, Henzel WJ, Baeuerle PA (1999) Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NF-κB activation. Proc Natl Acad Sci 96(2):429–434

    Article  PubMed  PubMed Central  Google Scholar 

  • Berod L, Friedrich C, Nandan A et al (2014) De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nat Med 20(11):1327

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ (1998) Neuronal calcium signaling. Neuron 21(1):13–26

    Article  CAS  PubMed  Google Scholar 

  • Beurel E, Michalek SM, Jope RS (2010) Innate and adaptive immune responses regulated by glycogen synthase kinase-3 (GSK3). Trends Immunol 31(1):24–31

    Article  CAS  PubMed  Google Scholar 

  • Bhandari T, Olson J, Johnson RS, Nizet V (2013) HIF-1α influences myeloid cell antigen presentation and response to subcutaneous OVA vaccination. J Mol Med 91(10):1199–1205

    Article  CAS  PubMed  Google Scholar 

  • Bianchi T, Gasser S, Trumpp A, MacDonald HR (2006) c-Myc acts downstream of IL-15 in the regulation of memory CD8 T-cell homeostasis. Blood 107(10):3992–3999

    Article  CAS  PubMed  Google Scholar 

  • Biswal D, Pramanik NR, Drew MG et al (2019) Synthesis, crystal structure, DFT calculations, protein interaction, anticancer potential and bromoperoxidase mimicking activity of oxidoalkoxidovanadium (V) complexes. New J Chem 43(45):17783–17800

    Article  Google Scholar 

  • Blanco CL, McGill-Vargas LL, Gastaldelli A et al (2015) Peripheral insulin resistance and impaired insulin signaling contribute to abnormal glucose metabolism in preterm baboons. Endocrinology 156(3):813–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaser H, Dostert C, Mak TW, Brenner D (2016) TNF and ROS crosstalk in inflammation. Trends Cell Biol 26(4):249–261

    Article  CAS  PubMed  Google Scholar 

  • Boden G (2011) 45Obesity, insulin resistance and free fatty acids. Curr Opin Endocrinol Diabetes Obes 18(2):139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonello S, Zähringer C, BelAiba RS et al (2007) Reactive oxygen species activate the HIF-1α promoter via a functional NFκB site. Arterioscler Thromb Vasc Biol 27(4):755–761

    Article  CAS  PubMed  Google Scholar 

  • Booth DM, Enyedi B, Geiszt M, Várnai P, Hajnóczky G (2016) Redox nanodomains are induced by and control calcium signaling at the ER-mitochondrial interface. Mol Cell 63(2):240–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bordon Y (2018) Itaconate charges down inflammation. Nat Rev Immunol 18(6):360–361

    Article  CAS  PubMed  Google Scholar 

  • Botman D, Tigchelaar W, Van Noorden CJ (2014) Determination of glutamate dehydrogenase activity and its kinetics in mouse tissues using metabolic mapping (quantitative enzyme histochemistry). J Histochem Cytochem 62(11):802–812

    Article  PubMed  CAS  Google Scholar 

  • Braakman I, Hebert DN (2013) Protein folding in the endoplasmic reticulum. Cold Spring Harbor Perspectives Biol 5(5):a013201

    Article  CAS  Google Scholar 

  • Bresciani G, da Cruz IBM, González-Gallego J (2015) Manganese superoxide dismutase and oxidative stress modulation advances in clinical chemistry. Elsevier, Amsterdam, pp 87–130

    Google Scholar 

  • Calder PC (2018) Metabolism of polyunsaturated fatty acids by cells of the immune system polyunsaturated fatty acid metabolism. Elsevier, Amsterdam, pp 135–155

    Book  Google Scholar 

  • Caldwell RB, Toque HA, Narayanan SP, Caldwell RW (2015) Arginase: an old enzyme with new tricks. Trends Pharmacol Sci 36(6):395–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campa CC, Ciraolo E, Ghigo A, Germena G, Hirsch E (2015) Crossroads of PI3K and Rac pathways. Small GTPases 6(2):71–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carr EL, Kelman A, Wu GS et al (2010) Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J Immunol 185(2):1037–1044

    Article  CAS  PubMed  Google Scholar 

  • Chandirasegaran G, Elanchezhiyan C, Ghosh K, Sethupathy S (2017) Berberine chloride ameliorates oxidative stress, inflammation and apoptosis in the pancreas of Streptozotocin induced diabetic rats. Biomed Pharmacother 95:175–185

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Chen G, Hong L et al (2013) How does hypoxia inducible factor-1α participate in enhancing the glycolysis activity in cervical cancer? Ann Diag Pathol 17(3):305–311

    Article  Google Scholar 

  • Cheng C, Geng F, Cheng X, Guo D (2018) Lipid metabolism reprogramming and its potential targets in cancer. Cancer Commun 38(1):27

    Article  Google Scholar 

  • Choubey D, Panchanathan R (2016) IFI16, an amplifier of DNA-damage response: role in cellular senescence and aging-associated inflammatory diseases. Ageing Res Rev 28:27–36

    Article  CAS  PubMed  Google Scholar 

  • Chowdhury S, Sinha K, Banerjee S, Sil PC (2016) Taurine protects cisplatin induced cardiotoxicity by modulating inflammatory and endoplasmic reticulum stress responses. BioFactors 42(6):647–664

    Article  CAS  PubMed  Google Scholar 

  • Cleeter M, Cooper J, Darley-Usmar V, Moncada S, Schapira A (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide: implications for neurodegenerative diseases. FEBS Lett 345(1):50–54

    Article  CAS  PubMed  Google Scholar 

  • Clementi E, Brown GC, Feelisch M, Moncada S (1998) Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci 95(13):7631–7636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connolly DJ, Bowie AG (2014) The emerging role of human PYHIN proteins in innate immunity: implications for health and disease. Biochem Pharmacol 92(3):405–414

    Article  CAS  PubMed  Google Scholar 

  • Corbera-Bellalta M, Planas-Rigol E, Lozano E et al (2016) Blocking interferon γ reduces expression of chemokines CXCL9, CXCL10 and CXCL11 and decreases macrophage infiltration in ex vivo cultured arteries from patients with giant cell arteritis. Ann Rheum Dis 75(6):1177–1186

    Article  CAS  PubMed  Google Scholar 

  • Corcoran SE, O’Neill LA (2016) HIF1α and metabolic reprogramming in inflammation. J Clin Investig 126(10):3699–3707

    Article  PubMed  PubMed Central  Google Scholar 

  • Correia SC, Santos RX, Cardoso SM, Santos MS, Oliveira CR, Moreira PI (2012) Cyanide preconditioning protects brain endothelial and NT2 neuron-like cells against glucotoxicity: role of mitochondrial reactive oxygen species and HIF-1α. Neurobiol Dis 45(1):206–218

    Article  CAS  PubMed  Google Scholar 

  • Cotugno N, Finocchi A, Cagigi A et al (2015) Defective B-cell proliferation and maintenance of long-term memory in patients with chronic granulomatous disease. J Allergy Clin Immunol 135(3):753–761

    Article  CAS  PubMed  Google Scholar 

  • Cross CE, Halliwell B, Borish ET et al (1987) Oxygen radicals and human disease. Ann Intern Med 107(4):526–545

    Article  CAS  PubMed  Google Scholar 

  • Csibi A, Lee G, Yoon S-O et al (2014) The mTORC1/S6K1 pathway regulates glutamine metabolism through the eIF4B-dependent control of c-Myc translation. Curr Biol 24(19):2274–2280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Currie E, Schulze A, Zechner R, Walther TC, Farese RV Jr (2013) Cellular fatty acid metabolism and cancer. Cell Metab 18(2):153–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cutler RG, Kelly J, Storie K et al (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc Natl Acad Sci 101(7):2070–2075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dang L, White DW, Gross S et al (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462(7274):739–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das J, Ghosh J, Manna P, Sil PC (2010) Taurine protects acetaminophen-induced oxidative damage in mice kidney through APAP urinary excretion and CYP2E1 inactivation. Toxicology 269(1):24–34

    Article  CAS  PubMed  Google Scholar 

  • Das J, Vasan V, Sil PC (2012) Taurine exerts hypoglycemic effect in alloxan-induced diabetic rats, improves insulin-mediated glucose transport signaling pathway in heart and ameliorates cardiac oxidative stress and apoptosis. Toxicol Appl Pharmacol 258(2):296–308

    Article  CAS  PubMed  Google Scholar 

  • de Araújo EF, Feriotti C, GaldinoNAdL PNW, Calich VLG, Loures FV (2017) The iDO–ahr axis controls Th17/Treg immunity in a pulmonary model of fungal infection. Front Immunol 8:880

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54(9):2325–2340

    Article  CAS  Google Scholar 

  • Doig AJ (2018) Positive feedback loops in Alzheimer’s disease: the Alzheimer’s feedback hypothesis. J Alzheimer's Dis 66(1):25–36

    Article  CAS  Google Scholar 

  • Drapier J, Hibbs J (1988) Differentiation of murine macrophages to express nonspecific cytotoxicity for tumor cells results in L-arginine-dependent inhibition of mitochondrial iron-sulfur enzymes in the macrophage effector cells. J Immunol 140(8):2829–2838

    CAS  PubMed  Google Scholar 

  • Duan Y, Li F, Li Y et al (2016) The role of leucine and its metabolites in protein and energy metabolism. Amino Acids 48(1):41–51

    Article  CAS  PubMed  Google Scholar 

  • Dutta S, Saha S, Mahalanobish S, Sadhukhan P, Sil PC (2018) Melatonin attenuates arsenic induced nephropathy via the regulation of oxidative stress and inflammatory signaling cascades in mice. Food Chem Toxicol 118:303–316

    Article  CAS  PubMed  Google Scholar 

  • Edwards DN, Ngwa VM, Wang S et al (2017) The receptor tyrosine kinase EphA2 promotes glutamine metabolism in tumors by activating the transcriptional coactivators YAP and TAZ. Sci Signal 10(508):eaan4667

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ehrenfeld M, Blank M, Shoenfeld Y, Hidvegi M (2001) Avemar (a new benzoquinone-containing natural product) administration interferes with the Th2 response in experimental SLE and promotes amelioration of the disease. Lupus 10(9):622–627

    Article  CAS  PubMed  Google Scholar 

  • Eleftheriadis T, Pissas G, Liakopoulos V, Stefanidis I (2018) IDO decreases glycolysis and glutaminolysis by activating GCN2K, while it increases fatty acid oxidation by activating AhR, thus preserving CD4+ T-cell survival and proliferation. Int J Mol Med 42(1):557–568

    CAS  PubMed  Google Scholar 

  • Evavold CL, Kagan JC (2019) Inflammasomes: Threat-Assessment Organelles of the Innate Immune System. Immunity 51(4):609–624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Everts B, Amiel E, van der Windt GJ et al (2012) Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells. Blood J Am Soc Hematol 120(7):1422–1431

    CAS  Google Scholar 

  • Everts B, Amiel E, Huang SC-C et al (2014) TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKɛ supports the anabolic demands of dendritic cell activation. Nat Immunol 15(4):323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farooqui T, Farooqui AA (2011) Lipid-mediated oxidative stress and inflammation in the pathogenesis of Parkinson's disease. Parkinson’s Dis 2011:247467

    Google Scholar 

  • Fischer R, Maier O (2015) Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF. Oxidative Med Cel Longevity 2015:610813

    Google Scholar 

  • Foley JF, Yu C-R, Solow R, Yacobucci M, Peden KW, Farber JM (2005) Roles for CXC chemokine ligands 10 and 11 in recruiting CD4+ T cells to HIV-1-infected monocyte-derived macrophages, dendritic cells, and lymph nodes. J Immunol 174(8):4892–4900

    Article  CAS  PubMed  Google Scholar 

  • Franchina DG, Dostert C, Brenner D (2018) Reactive oxygen species: involvement in T cell signaling and metabolism. Trends Immunol 39(6):489–502

    Article  CAS  PubMed  Google Scholar 

  • Freemerman AJ, Johnson AR, Sacks GN et al (2014) Metabolic reprogramming of macrophages glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem 289(11):7884–7896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15(6):1583–1606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fullerton MD, Galic S, Marcinko K et al (2013) Single phosphorylation sites in Acc1 and Acc2 regulate lipid homeostasis and the insulin-sensitizing effects of metformin. Nat Med 19(12):1649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaglio D, Metallo CM, Gameiro PA et al (2011) Oncogenic K-Ras decouples glucose and glutamine metabolism to support cancer cell growth. Mol Syst Biol 7(1):523

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Galván-Peña S, Carroll RG, Newman C et al (2019) Malonylation of GAPDH is an inflammatory signal in macrophages. Nat Commun 10(1):1–11

    Article  CAS  Google Scholar 

  • Gao P, Tchernyshyov I, Chang T-C et al (2009) c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458(7239):762–765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Wang H, Yang JJ, Liu X, Liu Z-R (2012) Pyruvate kinase M2 regulates gene transcription by acting as a protein kinase. Mol Cell 45(5):598–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Wang H, Yang JJ et al (2013) Reciprocal regulation of protein kinase and pyruvate kinase activities of pyruvate kinase M2 by growth signals. J Biol Chem 288(22):15971–15979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardner PR (1997) Superoxide-driven aconitase Fe–S center cycling. Biosci Rep 17(1):33–42

    Article  CAS  PubMed  Google Scholar 

  • Geerlings SE, Hoepelman AI (1999) Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunol Med Microbiol 26(3–4):259–265

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Chowdhury S, Sarkar P, Sil PC (2018) Ameliorative role of ferulic acid against diabetes associated oxidative stress induced spleen damage. Food Chem Toxicol 118:272–286

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Chowdhury S, Das AK, Sil PC (2019) Taurine ameliorates oxidative stress induced inflammation and ER stress mediated testicular damage in STZ-induced diabetic Wistar rats. Food Chem Toxicol 124:64–80

    Article  CAS  PubMed  Google Scholar 

  • Goverse G, Molenaar R, Macia L et al (2017) Diet-derived short chain fatty acids stimulate intestinal epithelial cells to induce mucosal tolerogenic dendritic cells. J Immunol 198(5):2172–2181

    Article  CAS  PubMed  Google Scholar 

  • Groß O, Yazdi AS, Thomas CJ et al (2012) Inflammasome activators induce interleukin-1α secretion via distinct pathways with differential requirement for the protease function of caspase-1. Immunity 36(3):388–400

    Article  PubMed  CAS  Google Scholar 

  • Guo C, Chen S, Liu W et al (2019) Immunometabolism: a new target for improving cancer immunotherapy. Adv Cancer Res 143:195–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez T, Simmen T (2018) Endoplasmic reticulum chaperones tweak the mitochondrial calcium rheostat to control metabolism and cell death. Cell Calcium 70:64–75

    Article  PubMed  CAS  Google Scholar 

  • Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT (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(2):718–731

    Article  CAS  PubMed  Google Scholar 

  • Haas R, Smith J, Rocher-Ros V et al (2015) Lactate regulates metabolic and pro-inflammatory circuits in control of T cell migration and effector functions. PLoS Biol 13(7):e1002202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hagen T (2012) Oxygen versus Reactive Oxygen in the Regulation of HIF-1: The Balance Tips. Biochem Res Int 2012:436981

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Halliwell B, Gutteridge JM (1985) Free radicals in biology and medicine

  • Hannemann N, Cao S, Eriksson D et al (2019) Transcription factor Fra-1 targets arginase-1 to enhance macrophage-mediated inflammation in arthritis. J Clin Invest 129(7):2669–2684

    Article  PubMed  PubMed Central  Google Scholar 

  • Harding HP, Zhang Y, Scheuner D, Chen J-J, Kaufman RJ, Ron D (2009) Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2α) dephosphorylation in mammalian development. Proc Natl Acad Sci 106(6):1832–1837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartai Z, Juhász A, Rimanóczy Á et al (2007) Decreased serum and red blood cell kynurenic acid levels in Alzheimer's disease. Neurochem Int 50(2):308–313

    Article  CAS  PubMed  Google Scholar 

  • Hensley CT, Wasti AT, DeBerardinis RJ (2013) Glutamine and cancer: cell biology, physiology, and clinical opportunities. J Clin Investig 123(9):3678–3684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hooftman A, O’Neill LAJ (2019) The immunomodulatory potential of the metabolite itaconate. Trends Immunol 40(8):687–698

    Article  CAS  PubMed  Google Scholar 

  • Howard BV (1999) Insulin resistance and lipid metabolism. Am J Cardiol 84(1):28–32

    Article  Google Scholar 

  • Huang Y, Tang C, Du J, Jin H (2016) Endogenous sulfur dioxide: a new member of gasotransmitter family in the cardiovascular system. Oxidative Med Cel Longevity 2016:8961951

    Google Scholar 

  • Hurrle S, Hsu WH (2017) The etiology of oxidative stress in insulin resistance. Biomed J 40(5):257–262

    Article  PubMed  PubMed Central  Google Scholar 

  • Ibrahim J, Nguyen AH, Rehman A et al (2012) Dendritic cell populations with different concentrations of lipid regulate tolerance and immunity in mouse and human liver. Gastroenterology 143(4):1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Imamura K, Tanaka T (1982) Pyruvate kinase isozymes from rat Methods in enzymology. Elsevier, Amsterdam, pp 150–165

    Google Scholar 

  • Itoh K, Chiba T, Takahashi S et al (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236(2):313–322

    Article  CAS  PubMed  Google Scholar 

  • Jabłońska J, Tawfik DS (2019) The number and type of oxygen-utilizing enzymes indicates aerobic vs. anaerobic phenotype. Free Radical Biol Med 140:84–92

    Article  CAS  Google Scholar 

  • Jackson SH, Devadas S, Kwon J, Pinto LA, Williams MS (2004) T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol 5(8):818–827

    Article  CAS  PubMed  Google Scholar 

  • Janssen A, Bosman C, Kruidenier L et al (1999) Superoxide dismutases in the human colorectal cancer sequence. J Cancer Res Clin Oncol 125(6):327–335

    Article  CAS  PubMed  Google Scholar 

  • Jantsch J, Chakravortty D, Turza N et al (2008) Hypoxia and hypoxia-inducible factor-1α modulate lipopolysaccharide-induced dendritic cell activation and function. J Immunol 180(7):4697–4705

    Article  CAS  PubMed  Google Scholar 

  • Jeannin P, Delneste Y, Lecoanet-Henchoz S et al (1995) Thiols decrease human interleukin (IL) 4 production and IL-4-induced immunoglobulin synthesis. J Exp Med 182(6):1785–1792

    Article  CAS  PubMed  Google Scholar 

  • Jha JC, Ho F, Dan C, Jandeleit-Dahm K (2018) A causal link between oxidative stress and inflammation in cardiovascular and renal complications of diabetes. Clin Sci 132(16):1811–1836

    Article  CAS  Google Scholar 

  • Jin F, Wu Z, Hu X et al (2019) The PI3K/Akt/GSK-3β/ROS/eIF2B pathway promotes breast cancer growth and metastasis via suppression of NK cell cytotoxicity and tumor cell susceptibility. Cancer Biol Med 16(1):38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson MO, Wolf MM, Madden MZ et al (2018) Distinct regulation of Th17 and Th1 cell differentiation by glutaminase-dependent metabolism. Cell 175(7):1780–1795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamata H, Honda S-i, Maeda S, Chang L, Hirata H, Karin M (2005) Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120(5):649–661

    Article  CAS  PubMed  Google Scholar 

  • Kar S, Kambis TN, Mishra PK (2019) Hydrogen sulfide-mediated regulation of cell death signaling ameliorates adverse cardiac remodeling and diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 316(6):H1237–H1252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller KE, Doctor ZM, Dwyer ZW, Lee Y-S (2014) SAICAR induces protein kinase activity of PKM2 that is necessary for sustained proliferative signaling of cancer cells. Mol Cell 53(5):700–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly B, O'neill LA (2015) Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Res 25(7):771–784

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Keyer K, Imlay JA (1997) Inactivation of dehydratase [4Fe-4S] clusters and disruption of iron homeostasis upon cell exposure to peroxynitrite. J Biol Chem 272(44):27652–27659

    Article  CAS  PubMed  Google Scholar 

  • Khare S, Dorfleutner A, Bryan NB et al (2012) An NLRP7-containing inflammasome mediates recognition of microbial lipopeptides in human macrophages. Immunity 36(3):464–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kizer JR (2013) A tangled threesome: adiponectin, insulin sensitivity, and adiposity: can mendelian randomization sort out causality? Diabetes 62(4):1007–1009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klysz D, Tai X, Robert PA et al (2015) Glutamine-dependent α-ketoglutarate production regulates the balance between T helper 1 cell and regulatory T cell generation. Sci Signal 8(396):97

    Article  CAS  Google Scholar 

  • Krawczyk CM, Holowka T, Sun J et al (2010) Toll-like receptor–induced changes in glycolytic metabolism regulate dendritic cell activation. Blood J Am Soc Hematol 115(23):4742–4749

    CAS  Google Scholar 

  • Krishnamurthy V, Patted AS, Kumar A, Jayaram SK, Magaji BS (2019) Evaluation of serum gamma-glutamyl transferase and highly sensitive C-reactive protein as biomarkers of oxidative stress and inflammation in type 2 diabetes mellitus patients with good and poor glycemic control. Int J Adv Med 6(3):650

    Article  Google Scholar 

  • Kroner Z (2009) The relationship between Alzheimer's disease and diabetes: Type 3 diabetes? Altern Med Rev 14(4):373

    PubMed  Google Scholar 

  • Kumar V, Gabrilovich DI (2014) Hypoxia-inducible factors in regulation of immune responses in tumour microenvironment. Immunology 143(4):512–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lagakos WS (2011) The role of G-protein-coupled receptors in mediating the effect of fatty acids on inflammation and insulin sensitivity. Curr Opin Clin Nutr Metab Care 14(4):322–327

    Article  PubMed  CAS  Google Scholar 

  • Lambeth JD, Neish AS (2014) Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu Rev Pathol 9:119–145

    Article  CAS  PubMed  Google Scholar 

  • LaMonte G, Philip N, Reardon J et al (2012) Translocation of sickle cell erythrocyte microRNAs into plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe 12(2):187–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lampropoulou V, Sergushichev A, Bambouskova M et al (2016) Itaconate links inhibition of succinate dehydrogenase with macrophage metabolic remodeling and regulation of inflammation. Cell Metab 24(1):158–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanis JM, Alexeev EE, Curtis VF et al (2017) Tryptophan metabolite activation of the aryl hydrocarbon receptor regulates IL-10 receptor expression on intestinal epithelia. Mucosal Immunol 10(5):1133–1144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurenti G, Tennant DA (2016) Isocitrate dehydrogenase (IDH), succinate dehydrogenase (SDH), fumarate hydratase (FH): three players for one phenotype in cancer? Biochem Soc Trans 44(4):1111–1116

    Article  CAS  PubMed  Google Scholar 

  • Lee A-H, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23(21):7448–7459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee M-C, Ting KK, Adams S, Brew BJ, Chung R, Guillemin GJ (2010) Characterisation of the expression of NMDA receptors in human astrocytes. PloS one 5(11):e14123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei K, Davis RJ (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci 100(5):2432–2437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levine AJ, Puzio-Kuter AM (2010) The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 330(6009):1340–1344

    Article  CAS  PubMed  Google Scholar 

  • LeWitt PA, Li J, Lu M et al (2013) 3-hydroxykynurenine and other Parkinson's disease biomarkers discovered by metabolomic analysis. Mov Disord 28(12):1653–1660

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Verma IM (2002) NF-κB regulation in the immune system. Nat Rev Immunol 2(10):725–734

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Liu Y, Wang C et al (2018) Succinate induces synovial angiogenesis in rheumatoid arthritis through metabolic remodeling and HIF-1α/VEGF axis. Free Radical Biol Med 126:1–14

    Article  CAS  Google Scholar 

  • Lim S-O, Li C-W, Xia W et al (2016) EGFR signaling enhances aerobic glycolysis in triple-negative breast cancer cells to promote tumor growth and immune escape. Can Res 76(5):1284–1296

    Article  CAS  Google Scholar 

  • Lin S, Hirai S, Yamaguchi Y et al (2013) Taurine improves obesity-induced inflammatory responses and modulates the unbalanced phenotype of adipose tissue macrophages. Mol Nutr Food Res 57(12):2155–2165

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Wang F (2017) Role of neuroinflammation in amyotrophic lateral sclerosis: cellular mechanisms and therapeutic implications. Front Immunol 8:1005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu P-S, Wang H, Li X et al (2017) α-ketoglutarate orchestrates macrophage activation through metabolic and epigenetic reprogramming. Nat Immunol 18(9):985

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Yu H, Gao L et al (2018) The inhibition of GSK-3β promotes the production of reactive oxygen species via β-catenin/C/EBPα signaling in the spleen of zebrafish (Danio rerio). Fish Shellfish Immunol 76:110–120

    Article  CAS  PubMed  Google Scholar 

  • Lu L, Bonham CA, Chambers FG et al (1996) Induction of nitric oxide synthase in mouse dendritic cells by IFN-gamma, endotoxin, and interaction with allogeneic T cells: nitric oxide production is associated with dendritic cell apoptosis. J Immunol 157(8):3577–3586

    CAS  PubMed  Google Scholar 

  • Lugo-Huitrón R, Ugalde Muñiz P, Pineda B, Pedraza-Chaverrí J, Ríos C, Pérez-de la Cruz V (2013) Quinolinic acid: an endogenous neurotoxin with multiple targets. Oxidative Med Cel Longev 2013:104024

    Google Scholar 

  • Lundberg JO, Weitzberg E, Gladwin MT (2008) The nitrate–nitrite–nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discovery 7(2):156–167

    Article  CAS  PubMed  Google Scholar 

  • Lunt SY, Vander Heiden MG (2011) Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27:441–464

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Yu C, Mohamed EM et al (2016) A causal link from ALK to hexokinase II overexpression and hyperactive glycolysis in EML4-ALK-positive lung cancer. Oncogene 35(47):6132–6142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macintyre AN, Rathmell JC (2013) Activated lymphocytes as a metabolic model for carcinogenesis. Cancer Metab 1(1):5

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahalanobish S, Saha S, Dutta S, Sil PC (2019) Matrix metalloproteinase: an upcoming therapeutic approach for idiopathic pulmonary fibrosis. Pharmacol Res 152:104591

    Article  PubMed  CAS  Google Scholar 

  • Maier T, Jenni S, Ban N (2006) Architecture of mammalian fatty acid synthase at 4.5 Å resolution. Science 311(5765):1258–1262

    Article  CAS  PubMed  Google Scholar 

  • Mailloux RJ, Willmore WG (2014) S-glutathionylation reactions in mitochondrial function and disease. Front Cell Dev Biol 2:68

    Article  PubMed  PubMed Central  Google Scholar 

  • Malhotra JD, Kaufman RJ (2007) Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9(12):2277–2294

    Article  CAS  PubMed  Google Scholar 

  • Mason SA, Della Gatta PA, Snow RJ, Russell AP, Wadley GD (2016) Ascorbic acid supplementation improves skeletal muscle oxidative stress and insulin sensitivity in people with type 2 diabetes: findings of a randomized controlled study. Free Radical Biol Med 93:227–238

    Article  CAS  Google Scholar 

  • May MJ, Ghosh S (1997) Rel/NF-κB and IκB proteins: an overview. Seminars in cancer biology. Elsevier, Amsterdam, pp 63–73

    Google Scholar 

  • Mayer CM, Belsham DD (2010) Palmitate attenuates insulin signaling and induces endoplasmic reticulum stress and apoptosis in hypothalamic neurons: rescue of resistance and apoptosis through adenosine 5′ monophosphate-activated protein kinase activation. Endocrinology 151(2):576–585

    Article  CAS  PubMed  Google Scholar 

  • McCoy KD, Ahmed N, Tan AS, Berridge MV (1997) The hemopoietic growth factor, interleukin-3, promotes glucose transport by increasing the specific activity and maintaining the affinity for glucose of plasma membrane glucose transporters. J Biol Chem 272(28):17276–17282

    Article  CAS  PubMed  Google Scholar 

  • McDaniel KL, Restori KH, Dodds JW, Kennett MJ, Ross AC, Cantorna MT (2015) Vitamin A-deficient hosts become nonsymptomatic reservoirs of Escherichia coli-like enteric infections. Infect Immun 83(7):2984–2991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menendez JA, Lupu R (2017) Fatty acid synthase (FASN) as a therapeutic target in breast cancer. Expert Opin Therap Targets 21(11):1001–1016

    Article  CAS  Google Scholar 

  • Miller DM, Thomas SD, Islam A, Muench D, Sedoris K (2012) c-Myc and Cancer Metabolism. Clin Cancer Res 18(20):5546–5553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mills EL, Kelly B, Logan A et al (2016) Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages. Cell 167(2):457–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mills EL, Ryan DG, Prag HA et al (2018) Itaconate is an anti-inflammatory metabolite that activates Nrf2 via alkylation of KEAP1. Nature 556(7699):113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsuishi Y, Taguchi K, Kawatani Y et al (2012) Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 22(1):66–79

    Article  CAS  PubMed  Google Scholar 

  • Moayeri M, Crown D, Newman ZL et al (2010) Inflammasome sensor Nlrp1b-dependent resistance to anthrax is mediated by caspase-1, IL-1 signaling and neutrophil recruitment. PLoS Pathog 6(12):e1001222

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Molteni M, Rossetti C (2017) Neurodegenerative diseases: the immunological perspective. J Neuroimmunol 313:109–115

    Article  CAS  PubMed  Google Scholar 

  • Momeni B, Waite AJ, Shou W (2013) Spatial self-organization favors heterotypic cooperation over cheating. Elife 2:e00960

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moon J-S, Lee S, Park M-A et al (2015) UCP2-induced fatty acid synthase promotes NLRP3 inflammasome activation during sepsis. J Clin Investig 125(2):665–680

    Article  PubMed  PubMed Central  Google Scholar 

  • Moreau K, Dizin E, Ray H et al (2006) BRCA1 affects lipid synthesis through its interaction with acetyl-CoA carboxylase. J Biol Chem 281(6):3172–3181

    Article  CAS  PubMed  Google Scholar 

  • Moretti R, Leger P-L, Besson VC et al (2016) Sildenafil, a cyclic GMP phosphodiesterase inhibitor, induces microglial modulation after focal ischemia in the neonatal mouse brain. J Neuroinflamm 13(1):95

    Article  CAS  Google Scholar 

  • Morgan MJ, Liu Z-g (2011) Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res 21(1):103–115

    Article  CAS  PubMed  Google Scholar 

  • Munn DH, Shafizadeh E, Attwood JT, Bondarev I, Pashine A, Mellor AL (1999) Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med 189(9):1363–1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagai M, Re DB, Nagata T et al (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10(5):615–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa H, Wang L, Cantor H, Kim H-J (2018) New insights into the biology of CD8 regulatory T cells advances in immunology, vol 140. Elsevier, Amster, pp 1–20

    Google Scholar 

  • Nakajima S, Kitamura M (2013) Bidirectional regulation of NF-κB by reactive oxygen species: a role of unfolded protein response. Free Radical Biol Med 65:162–174

    Article  CAS  Google Scholar 

  • Nallu A, Sharma S, Ramezani A, Muralidharan J, Raj D (2017) Gut microbiome in chronic kidney disease: challenges and opportunities. Transl Res 179:24–37

    Article  CAS  PubMed  Google Scholar 

  • Nathan C, Cunningham-Bussel A (2013) Beyond oxidative stress: an immunologist's guide to reactive oxygen species. Nat Rev Immunol 13(5):349–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann AK, Yang J, Biju MP et al (2005) Hypoxia inducible factor 1α regulates T cell receptor signal transduction. Proc Natl Acad Sci 102(47):17071–17076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niki E (2014) Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence. Free Radical Biol Med 66:3–12

    Article  CAS  Google Scholar 

  • Nowarski R, Jackson R, Gagliani N et al (2015) Epithelial IL-18 equilibrium controls barrier function in colitis. Cell 163(6):1444–1456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nwafor I, Eze J, Anyanwu C, Ezemba N, Onyia U, Enwerem N (2017) The scope of cardiac surgery at a national cardiothoracic center of excellence (NCTCE) in Nigeria: a 3-year review. J Vasc Med Surg 5(308):2

    Google Scholar 

  • O’Neill LA, Pearce EJ (2016) Immunometabolism governs dendritic cell and macrophage function. J Exp Med 213(1):15–23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Odegaard JI, Chawla A (2011) Alternative macrophage activation and metabolism. Annu Rev Pathol 6:275–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ofengeim D, Mazzitelli S, Ito Y et al (2017) RIPK1 mediates a disease-associated microglial response in Alzheimer’s disease. Proc Natl Acad Sci 114(41):E8788–E8797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa T, Matson W, Beal M et al (1992) Kynurenine pathway abnormalities in Parkinson's disease. Neurology 42(9):1702–1702

    Article  CAS  PubMed  Google Scholar 

  • Oguntibeju OO (2019) Type 2 diabetes mellitus, oxidative stress and inflammation: examining the links. Int J Physiol Pathophysiol Pharmacol 11(3):45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohtani M, Nagai S, Kondo S et al (2008) Mammalian target of rapamycin and glycogen synthase kinase 3 differentially regulate lipopolysaccharide-induced interleukin-12 production in dendritic cells. Blood J Am Soc Hematol 112(3):635–643

    CAS  Google Scholar 

  • Olechnowicz J, Tinkov A, Skalny A, Suliburska J (2018) Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci 68(1):19–31

    Article  CAS  PubMed  Google Scholar 

  • Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183

    Article  CAS  PubMed  Google Scholar 

  • Oxenkrug GF (2007) Genetic and hormonal regulation of tryptophan-kynurenine metabolism: implications for vascular cognitive impairment, major depressive disorder, and aging. Ann NY Acad Sci 1122(1):35–49

    Article  CAS  PubMed  Google Scholar 

  • Oxenkrug GF (2015) Increased plasma levels of xanthurenic and kynurenic acids in type 2 diabetes. Mol Neurobiol 52(2):805–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oxenkrug GF, Turski WA, Zgrajka W, Weinstock JV, Summergrad P (2013) Tryptophan-kynurenine metabolism and insulin resistance in hepatitis C patients. Hepat Res Treat 2013:149247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palazon A, Goldrath AW, Nizet V, Johnson RS (2014) HIF transcription factors, inflammation, and immunity. Immunity 41(4):518–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmieri EM, Menga A, Martín-Pérez R et al (2017) Pharmacologic or genetic targeting of glutamine synthetase skews macrophages toward an M1-like phenotype and inhibits tumor metastasis. Cell Rep 20(7):1654–1666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palsson-McDermott EM, Curtis AM, Goel G et al (2015) Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages. Cell Metab 21(1):65–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park CH, Xu FH, Roh S-S et al (2015a) Astaxanthin and Corni Fructus protect against diabetes-induced oxidative stress, inflammation, and advanced glycation end product in livers of streptozotocin-induced diabetic rats. J Med Food 18(3):337–344

    Article  CAS  PubMed  Google Scholar 

  • Park J, Lee SE, Hur J et al (2015b) M-CSF from cancer cells induces fatty acid synthase and PPARβ/δ activation in tumor myeloid cells, leading to tumor progression. Cell Rep 10(9):1614–1625

    Article  CAS  PubMed  Google Scholar 

  • Paul BD, Snyder SH (2012) H 2 S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13(8):499–507

    Article  CAS  PubMed  Google Scholar 

  • Pavlova NN, Thompson CB (2016) The emerging hallmarks of cancer metabolism. Cell Metab 23(1):27–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perry JS, Russler-Germain EV, Zhou YW et al (2018) Transfer of cell-surface antigens by scavenger receptor CD36 promotes thymic regulatory T cell receptor repertoire development and allo-tolerance. Immunity 48(5):923–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pesce JT, Ramalingam TR, Mentink-Kane MM et al (2009) Arginase-1–expressing macrophages suppress Th2 cytokine–driven inflammation and fibrosis. PLoS Pathog 5(4):e1000371

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pollari E, Goldsteins G, Bart G, Koistinaho J, Giniatullin R (2014) The role of oxidative stress in degeneration of the neuromuscular junction in amyotrophic lateral sclerosis. Front Cel Neurosci 8:131

    Google Scholar 

  • Powers RK, Sullivan KD, Culp-Hill R, et al (2018) Trisomy 21 drives production of neurotoxic tryptophan catabolites via the interferon-inducible kynurenine pathway. bioRxiv:403642

  • Pucino V, Bombardieri M, Pitzalis C, Mauro C (2017) Lactate at the crossroads of metabolism, inflammation, and autoimmunity. Eur J Immunol 47(1):14–21

    Article  CAS  PubMed  Google Scholar 

  • Ransohoff RM (2017) Specks of insight into Alzheimer’s disease. Nature Publishing Group, Berlin

    Book  Google Scholar 

  • Ratajczak W, Rył A, Mizerski A, Walczakiewicz K, Sipak O, Laszczyńska M (2019) Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochim Pol 66(1):1–12

    CAS  PubMed  Google Scholar 

  • Rathinam VA, Fitzgerald KA (2016) Inflammasome complexes: emerging mechanisms and effector functions. Cell 165(4):792–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rathinam VA, Vanaja SK, Fitzgerald KA (2012) Regulation of inflammasome signaling. Nat Immunol 13(4):333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond J, Segrè D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311(5768):1764–1767

    Article  CAS  PubMed  Google Scholar 

  • Read KA, Powell MD, McDonald PW, Oestreich KJ (2016) IL-2, IL-7, and IL-15: multistage regulators of CD4+ T helper cell differentiation. Exp Hematol 44(9):799–808

    Article  CAS  PubMed  Google Scholar 

  • Reczek CR, Chandel NS (2015) ROS-dependent signal transduction. Curr Opin Cell Biol 33:8–13

    Article  CAS  PubMed  Google Scholar 

  • Reyes Ocampo J, Lugo Huitrón R, González-Esquivel D et al (2014) Kynurenines with neuroactive and redox properties: relevance to aging and brain diseases. Oxid Med Cel Long 2014:646909

    Google Scholar 

  • Rice CM, Davies LC, Subleski JJ et al (2018) Tumour-elicited neutrophils engage mitochondrial metabolism to circumvent nutrient limitations and maintain immune suppression. Nat Commun 9(1):1–13

    Article  CAS  Google Scholar 

  • Rizzo MR, Marfella R, Barbieri M et al (2010) Relationships between daily acute glucose fluctuations and cognitive performance among aged type 2 diabetic patients. Diabetes Care 33(10):2169–2174

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriguez AE, Ducker GS, Billingham LK et al (2019) Serine metabolism supports macrophage IL-1β production. Cell Metab 29(4):1003–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rojas-Gutierrez E, Muñoz-Arenas G, Treviño S et al (2017) Alzheimer's disease and metabolic syndrome: a link from oxidative stress and inflammation to neurodegeneration. Synapse 71(10):e21990

    Article  PubMed  CAS  Google Scholar 

  • Ron D, Hubbard SR (2008) How IRE1 reacts to ER stress. Cell 132(1):24–26

    Article  CAS  PubMed  Google Scholar 

  • Rooks MG, Garrett WS (2016) Gut microbiota, metabolites and host immunity. Nat Rev Immunol 16(6):341–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross AC, Chen Q, Ma Y (2011) Vitamin A and retinoic acid in the regulation of B-cell development and antibody production Vitamins and Hormones, vol 86. Elsevier, Amsterdam, pp 103–126

    Google Scholar 

  • Rubinsztein DC (2017) RIPK1 promotes inflammation and β-amyloid accumulation in Alzheimer’s disease. Proc Natl Acad Sci 114(41):10813–10814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sachdev S, Davies KJ (2008) Production, detection, and adaptive responses to free radicals in exercise. Free Radical Biol Med 44(2):215–223

    Article  CAS  Google Scholar 

  • Saini R, Singh S (2019) Inducible nitric oxide synthase: an asset to neutrophils. J Leukoc Biol 105(1):49–61

    Article  CAS  PubMed  Google Scholar 

  • Salzano S, Checconi P, Hanschmann E-M et al (2014) Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal. Proc Natl Acad Sci 111(33):12157–12162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Lopez E, Zhong Z, Stubelius A et al (2019) Choline uptake and metabolism modulate macrophage IL-1β and IL-18 production. Cell Met 29(6):1350–1362

    Article  CAS  Google Scholar 

  • Sa-nguanmoo P, Tanajak P, Kerdphoo S et al (2017) SGLT2-inhibitor and DPP-4 inhibitor improve brain function via attenuating mitochondrial dysfunction, insulin resistance, inflammation, and apoptosis in HFD-induced obese rats. Toxicol Appl Pharmacol 333:43–50

    Article  CAS  PubMed  Google Scholar 

  • Sarsour EH, Venkataraman S, Kalen AL, Oberley LW, Goswami PC (2008) Manganese superoxide dismutase activity regulates transitions between quiescent and proliferative growth. Aging Cell 7(3):405–417

    Article  CAS  PubMed  Google Scholar 

  • Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24(10):R453–R462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroder K, Tschopp J (2010) The inflammasomes. Cell 140(6):821–832

    Article  CAS  PubMed  Google Scholar 

  • Schwarz MJ, Guillemin GJ, Teipel SJ, Buerger K, Hampel H (2013) Increased 3-hydroxykynurenine serum concentrations differentiate Alzheimer’s disease patients from controls. Eur Arch Psychiatry Clin Neurosci 263(4):345–352

    Article  PubMed  Google Scholar 

  • Selak MA, Armour SM, MacKenzie ED et al (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase. Cancer Cell 7(1):77–85

    Article  CAS  PubMed  Google Scholar 

  • Shadel GS, Horvath TL (2015) Mitochondrial ROS signaling in organismal homeostasis. Cell 163(3):560–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shamim A, Mahmood T, Ahsan F, Kumar A, Bagga P (2018) Lipids: an insight into the neurodegenerative disorders. Clin Nutr Exper 20:1–19

    Article  Google Scholar 

  • Sharma A (2018) The innate effector programmes of invariant natural killer T-cells. The University of Wisconsin-Madison, Madison

    Google Scholar 

  • Shehzad A, Iqbal W, Shehzad O, Lee YS (2012) Adiponectin: regulation of its production and its role in human diseases. Hormones 11(1):8–20

    Article  PubMed  Google Scholar 

  • Shimada K, Crother TR, Karlin J et al (2012) Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 36(3):401–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva Júnior WSd, Godoy-Matos AFd, Kraemer-Aguiar LG (2015) Dipeptidyl peptidase 4: a new link between diabetes mellitus and atherosclerosis? BioMed Res Int 2015:816164

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sinha K, Das J, Pal PB, Sil PC (2013) Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87(7):1157–1180

    Article  CAS  PubMed  Google Scholar 

  • Sivandzade F, Prasad S, Bhalerao A, Cucullo L (2019) NRF2 and NF-қB interplay in cerebrovascular and neurodegenerative disorders: molecular mechanisms and possible therapeutic approaches. Redox Biol 21:101059

    Article  CAS  PubMed  Google Scholar 

  • Smith M, Wilkinson S (2017) ER homeostasis and autophagy. Essays Biochem 61(6):625–635

    Article  PubMed  PubMed Central  Google Scholar 

  • Sosa V, Moliné T, Somoza R, Paciucci R, Kondoh LLeonart HME (2013) Oxidative stress and cancer: an overview. Ageing Res Rev 12(1):376–390

    Article  CAS  PubMed  Google Scholar 

  • Spirig R, Djafarzadeh S, Regueira T et al (2010) Effects of TLR agonists on the hypoxia-regulated transcription factor HIF-1α and dendritic cell maturation under normoxic conditions. PloS One 5(6):e10983

    Article  PubMed Central  CAS  Google Scholar 

  • Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S (2010) Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Can Res 70(1):68–77

    Article  CAS  Google Scholar 

  • Stephensen CB, Jiang X, Freytag T (2004) Vitamin A deficiency increases the in vivo development of IL-10–positive Th2 cells and decreases development of Th1 cells in mice. J Nutr 134(10):2660–2666

    Article  CAS  PubMed  Google Scholar 

  • Su X, Yu Y, Zhong Y et al (2015) Interferon-γ regulates cellular metabolism and mRNA translation to potentiate macrophage activation. Nat Immunol 16(8):838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Furio L, Mecheri R et al (2015) Pancreatic β-cells limit autoimmune diabetes via an immunoregulatory antimicrobial peptide expressed under the influence of the gut microbiota. Immunity 43(2):304–317

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Ou Z, Chen R et al (2016) Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology 63(1):173–184

    Article  CAS  PubMed  Google Scholar 

  • Suzanne M (2009) Insulin resistance and Alzheimer’s disease. BMB Rep 42(8):475

    Article  Google Scholar 

  • Talbot K, Wang H-Y, Kazi H et al (2012) Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Investig 122(4):1316–1338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan H-Y, Wang N, Li S, Hong M, Wang X, Feng Y (2016) The Reactive Oxygen Species in Macrophage Polarization: Reflecting Its Dual Role in Progression and Treatment of Human Diseases. Oxid Med Cell Long 2016:2795090

    Google Scholar 

  • Tangvarasittichai S (2015) Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes 6(3):456

    Article  PubMed  PubMed Central  Google Scholar 

  • Tannahill G, Curtis A, Adamik J et al (2013) Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 496(7444):238–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tansey MG, Romero-Ramos M (2019) Immune system responses in Parkinson's disease: early and dynamic. Eur J Neurosci 49(3):364–383

    PubMed  Google Scholar 

  • Tao J-H, Barbi J, Pan F (2015) Hypoxia-inducible factors in T lymphocyte differentiation and function. A review in the theme: cellular responses to hypoxia. Am J Physiol Cell Physiol 309(9):C580–C589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tefera TW, Borges K (2017) Metabolic dysfunctions in amyotrophic lateral sclerosis pathogenesis and potential metabolic treatments. Front Neurosci 10:611

    Article  PubMed  PubMed Central  Google Scholar 

  • Tian Y, Pate C, Andreolotti A et al (2008) Cytokine secretion requires phosphatidylcholine synthesis. J Cell Biol 181(6):945–957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Truax AD, Chen L, Tam JW et al (2018) The inhibitory innate immune sensor NLRP12 maintains a threshold against obesity by regulating gut microbiota homeostasis. Cell Host Microbe 24(3):364–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tweedell RE, Qi L, Sun Z, Dinglasan RR (2018) Kupffer cells survive Plasmodium berghei sporozoite exposure and respond with a rapid cytokine release. Pathogens 7(4):91

    Article  CAS  PubMed Central  Google Scholar 

  • Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266(1–2):37–56

    Article  CAS  PubMed  Google Scholar 

  • van Diepen JA, Berbée JF, Havekes LM, Rensen PC (2013) Interactions between inflammation and lipid metabolism: relevance for efficacy of anti-inflammatory drugs in the treatment of atherosclerosis. Atherosclerosis 228(2):306–315

    Article  PubMed  CAS  Google Scholar 

  • Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324(5930):1029–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandoorne T, De Bock K, Van Den Bosch L (2018) Energy metabolism in ALS: an underappreciated opportunity? Acta Neuropathol 135(4):489–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vats D, Mukundan L, Odegaard JI et al (2006) Oxidative metabolism and PGC-1β attenuate macrophage-mediated inflammation. Cell Metab 4(1):13–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venegas C, Kumar S, Franklin BS et al (2017) Microglia-derived ASC specks cross-seed amyloid-β in Alzheimer’s disease. Nature 552(7685):355–361

    Article  CAS  PubMed  Google Scholar 

  • Venegas DP, Marjorie K, Landskron G et al (2019) Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 10:277

    Article  CAS  Google Scholar 

  • Vickers NJ (2017) Animal communication: when i’m calling you, will you answer too? Curr Biol 27(14):R713–R715

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Rajput S, Watabe K, Liao D-F, Cao D (2010) Acetyl-CoA carboxylase-alpha as a novel target for cancer therapy. Front Biosci 2:15–26

    Google Scholar 

  • Wang Y, Huang G, Zeng H, Yang K, Lamb RF, Chi H (2013) Tuberous sclerosis 1 (Tsc1)-dependent metabolic checkpoint controls development of dendritic cells. Proc Natl Acad Sci 110(50):E4894–E4903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X-B, Du J-B, Cui H (2015) Signal pathways involved in the biological effects of sulfur dioxide. Eur J Pharmacol 764:94–99

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Wang K, Xu W et al (2017a) SIRT5 desuccinylates and activates pyruvate kinase M2 to block macrophage IL-1β production and to prevent DSS-induced colitis in mice. Cell Rep 19(11):2331–2344

    Article  CAS  PubMed  Google Scholar 

  • Wang XB, Cui H, Liu X, Du JB (2017b) Sulfur dioxide: foe or friend for life? Histol Histopathol 32(12):1231–1238

    CAS  PubMed  Google Scholar 

  • Warburg OH (1926) Uber den stoffwechsel der tumoren.

  • Wei X, Song H, Yin L et al (2016) Fatty acid synthesis configures the plasma membrane for inflammation in diabetes. Nature 539(7628):294–298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weinberg SE, Sena LA, Chandel NS (2015) Mitochondria in the regulation of innate and adaptive immunity. Immunity 42(3):406–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welbourne T (1979) Ammonia production and glutamine incorporation into glutathione in the functioning rat kidney. Can J Biochem 57(3):233–237

    Article  CAS  PubMed  Google Scholar 

  • Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Investig 115(5):1111–1119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West KP Jr (2866S) Extent of vitamin A deficiency among preschool children and women of reproductive age. J Nutr 132(9):2857S–2866S

    Article  CAS  PubMed  Google Scholar 

  • Widner B, Leblhuber F, Walli J, Tilz G, Demel U, Fuchs D (2000) Tryptophan degradation and immune activation in Alzheimer's disease. J Neural Trans 107(3):343–353

    Article  CAS  Google Scholar 

  • Wise DR, Thompson CB (2010) Glutamine addiction: a new therapeutic target in cancer. Trends Biochem Sci 35(8):427–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wlodarska M, Thaiss CA, Nowarski R et al (2014) NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 156(5):1045–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496(7446):445–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie J, Méndez JD, Méndez-Valenzuela V, Aguilar-Hernández MM (2013) Cellular signalling of the receptor for advanced glycation end products (RAGE). Cell Signal 25(11):2185–2197

    Article  CAS  PubMed  Google Scholar 

  • Xie M, Yu Y, Kang R et al (2016) PKM2-dependent glycolysis promotes NLRP3 and AIM2 inflammasome activation. Nat Commun 7(1):1–13

    CAS  Google Scholar 

  • Xu T, Stewart KM, Wang X et al (2017) Metabolic control of T H 17 and induced T reg cell balance by an epigenetic mechanism. Nature 548(7666):228–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi H, Wang H-G (2004) CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem 279(44):45495–45502

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Sudderth J, Dang T, Bachoo RG, McDonald JG, DeBerardinis RJ (2009) Glioblastoma cells require glutamate dehydrogenase to survive impairments of glucose metabolism or Akt signaling. Can Res 69(20):7986–7993

    Article  CAS  Google Scholar 

  • Yang M, Soga T, Pollard PJ (2013) Oncometabolites: linking altered metabolism with cancer. J Clin Investig 123(9):3652–3658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang R, Qu C, Zhou Y et al (2015) Hydrogen sulfide promotes Tet1-and Tet2-mediated Foxp3 demethylation to drive regulatory T cell differentiation and maintain immune homeostasis. Immunity 43(2):251–263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu X, Du Y, Cai C et al (2018) Inflammasome activation negatively regulates MyD88-IRF7 type I IFN signaling and anti-malaria immunity. Nat Commun 9(1):1–12

    Article  CAS  Google Scholar 

  • Zhang DD, Hannink M (2003) Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 23(22):8137–8151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Wang L, Chu Y (2019) Reactive oxygen species: the signal regulator of B cell. Free Radical Biol Med 142:16–22

    Article  CAS  Google Scholar 

  • Zhao Y, Yang J, Shi J et al (2011) The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477(7366):596–600

    Article  CAS  PubMed  Google Scholar 

  • Zhdanov AV, Waters AH, Golubeva AV, Papkovsky DB (2015) Differential contribution of key metabolic substrates and cellular oxygen in HIF signalling. Exp Cell Res 330(1):13–28

    Article  CAS  PubMed  Google Scholar 

  • Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11(2):136

    Article  CAS  PubMed  Google Scholar 

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  1. Division of Molecular Medicine, Bose Institute, P-1/12, CIT Scheme VII M, Kolkata, West Bengal, 700054, India

    Sharmistha Banerjee, Sumit Ghosh, Ankita Mandal, Noyel Ghosh & Parames C. Sil

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  1. Sharmistha Banerjee
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Banerjee, S., Ghosh, S., Mandal, A. et al. ROS-associated immune response and metabolism: a mechanistic approach with implication of various diseases. Arch Toxicol 94, 2293–2317 (2020). https://doi.org/10.1007/s00204-020-02801-7

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