Time and demand are two critical dimensions of immunometabolism: The process of macrophage activation and the pentose phosphate pathway

Frontiers in Immunology

Volumn 6, Issue APR, 2015, Pages

  Nagy, Csörsz ^a   Haschemi, Arvand ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Immunometabolism; Inflammation; Macrophage activation; Metabolic reprograming; Pentose phosphate pathway; Primary carbohydrate metabolism; Sedoheptulose kinase; Time and demand

Indexed keywords

6 PHOSPHOFRUCTOKINASE; GAMMA INTERFERON; GLUCOSE 6 PHOSPHATE; GLUCOSE TRANSPORTER 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOKINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MONOCARBOXYLATE TRANSPORTER 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STAT6 PROTEIN; TRANSALDOLASE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BONE MARROW DERIVED MACROPHAGE; CARBOHYDRATE METABOLISM; DOWN REGULATION; EVOLUTIONARY ADAPTATION; HUMAN; IMMUNE RESPONSE; IMMUNOMETABOLISM; IMMUNOREGULATION; MACROPHAGE ACTIVATION; NERVE CELL PLASTICITY; OXYGEN CONSUMPTION; PENTOSE PHOSPHATE CYCLE; SIGNAL TRANSDUCTION;

EID: 84934284021     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00164     Document Type: Article

References (87)

1. Levene PA, Meyer GM. The action of leucocytes on glucose. J Biol Chem (1912) 12:361-70.
2. Warburg O. Stoffwechsel der Tumoren. Berlin: Springer (1926).
3. Bakker A. Einige uebereinstimmungen im stoffwechsel der carcinomzellen und exsudatleukocyten. Klin Wochenschr (1927) 6:252-4. doi: 10.1007/BF01710710
4. Fleischmann W, Kubowitz F. Ueber den stoffwechsel der leukocyten. Biochem Ztschr (1927) 181:395.
5. Kempner W, Peschel E. Stoffwechsel der entzuendung. Ztschr f klin Med (1930) 114:439-55.
6. Schade H, Claußen F, Häbler C, Hoff F, Mochizucki N, Birner M. Weitere untersuchungen der molekularpathologie der entzündung: die exsudate. Ztschr f d ges Exp Med (1926) 49(1):334-410. doi:10.1007/BF02622491
7. Dinh PH, Corraza F, Mestdagh K, Kassengera Z, Doyen V, Michel O. Validation of the cantharidin-induced skin blister as an in vivo model of inflammation. Br J Clin Pharmacol (2011) 72(6):912-20. doi:10.1111/j.1365-2125.2011.04020.x
8. Sbarra AJ, Karnovsky ML. The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes. J Biol Chem (1959) 234(6):1355-62.
9. Newsholme P, Curi R, Gordon S, Newsholme EA. Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages. Biochem J (1986) 239(1):121-5.
10. Newsholme P, Newsholme EA. Rates of utilization of glucose, glutamine and oleate and formation of end-products by mouse peritoneal macrophages in culture. Biochem J (1989) 261(1):211-8.
11. Murphy C, Newsholme P. Importance of glutamine metabolism in murine macrophages and human monocytes to l-arginine biosynthesis and rates of nitrite or urea production. Clin Sci (Lond) (1998) 95(4):397-407. doi:10.1042/CS19980194
12. Medzhitov R. Origin and physiological roles of inflammation. Nature (2008) 454(7203):428-35. doi:10.1038/nature07201
13. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci (2008) 13:453-61. doi:10.2741/2692
14. Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep (2014) 6:13. doi:10.12703/P6-13
15. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest (2012) 122(3):787-95. doi:10.1172/JCI59643
16. Mounier R, Theret M, Arnold L, Cuvellier S, Bultot L, Goransson O, et al. AMPKalpha1 regulates macrophage skewing at the time of resolution of inflammation during skeletal muscle regeneration. Cell Metab (2013) 18(2):251-64. doi:10.1016/j.cmet.2013.06.017
17. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol (2008) 8(12):958-69. doi:10.1038/nri2448
18. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature (2007) 447(7147):972-8. doi:10.1038/nature05836
19. Galvan-Pena S, O'Neill LA. Metabolic reprograming in macrophage polarization. Front Immunol (2014) 5:420. doi:10.3389/fimmu.2014.00420
20. Rodriguez-Prados JC, Traves PG, Cuenca J, Rico D, Aragones J, Martin-Sanz P, et al. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J Immunol (2010) 185(1):605-14. doi:10.4049/jimmunol.0901698
21. Haschemi A, Kosma P, Gille L, Evans CR, Burant CF, Starkl P, et al. The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism. Cell Metab (2012) 15(6):813-26. doi:10.1016/j.cmet.2012.04.023
22. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature (2013) 496(7444):238-42. doi:10.1038/nature11986
23. Palsson-McDermott EM, Curtis AM, Goel G, Lauterbach MA, Sheedy FJ, Gleeson LE, et al. Pyruvate kinase M2 regulates Hif-1alpha activity and IL-1beta induction and is a critical determinant of the Warburg effect in LPS-activated macrophages. Cell Metab (2015) 21(1):65-80. doi:10.1016/j.cmet.2014.12.005
24. Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, et al. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab (2006) 4(1):13-24. doi:10.1016/j.cmet.2006.08.006
25. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell (2003) 112(5):645-57. doi:10.1016/S0092-8674(03)00154-5
26. Fukuzumi M, Shinomiya H, Shimizu Y, Ohishi K, Utsumi S. Endotoxin-induced enhancement of glucose influx into murine peritoneal macrophages via GLUT1. Infect Immun (1996) 64(1):108-12.
27. Shulga N, Pastorino JG. Hexokinase II binding to mitochondria is necessary for Kupffer cell activation and is potentiated by ethanol exposure. J Biol Chem (2014) 289(38):26213-25. doi:10.1074/jbc. M114.580175
28. Everts B, Amiel E, Huang SC, Smith AM, Chang CH, Lam WY, et al. TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKvarepsilon supports the anabolic demands of dendritic cell activation. Nat Immunol (2014) 15(4):323-32. doi:10.1038/ni.2833
29. Mathupala SP, Ko YH, Pedersen PL. Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene (2006) 25(34):4777-86. doi:10.1038/sj.onc.1209603
30. Wamelink MM, Struys EA, Jansen EE, Levtchenko EN, Zijlstra FS, Engelke U, et al. Sedoheptulokinase deficiency due to a 57-kb deletion in cystinosis patients causes urinary accumulation of sedoheptulose: elucidation of the CARKL gene. Hum Mutat (2008) 29(4):532-6. doi:10.1002/humu.20685
31. Kardon T, Stroobant V, Veiga-da-Cunha M, Schaftingen EV. Characterization of mammalian sedoheptulokinase and mechanism of formation of erythritol in sedoheptulokinase deficiency. FEBS Lett (2008) 582(23-24):3330-4. doi:10.1016/j.febslet.2008.08.024
32. Touchman JW, Anikster Y, Dietrich NL, Maduro VV, McDowell G, Shotelersuk V, et al. The genomic region encompassing the nephropathic cystinosis gene (CTNS): complete sequencing of a 200-kb segment and discovery of a novel gene within the common cystinosis-causing deletion. Genome Res (2000) 10(2):165-73. doi:10.1101/gr.10.2.165
33. Luo W, Hu H, Chang R, Zhong J, Knabel M, O'Meally R, et al. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell (2011) 145(5):732-44. doi:10.1016/j.cell.2011.03.054
34. Ruiz-Garcia A, Monsalve E, Novellasdemunt L, Navarro-Sabate A, Manzano A, Rivero S, et al. Cooperation of adenosine with macrophage Toll-4 receptor agonists leads to increased glycolytic flux through the enhanced expression of PFKFB3 gene. J Biol Chem (2011) 286(22):19247-58. doi:10.1074/jbc. M110.190298
35. Jurica MS, Mesecar A, Heath PJ, Shi W, Nowak T, Stoddard BL. The allosteric regulation of pyruvate kinase by fructose-1,6-bisphosphate. Structure (1998) 6(2):195-210. doi:10.1016/S0969-2126(98)00021-5
36. Tan Z, Xie N, Banerjee S, Cui H, Fu M, Thannickal VJ, et al. The monocarboxylate transporter 4 is required for glycolytic reprogramming and inflammatory response in macrophages. J Biol Chem (2015) 290(1):46-55. doi:10.1074/jbc. M114.603589
37. Costa Leite T, Da Silva D, Guimaraes Coelho R, Zancan P, Sola-Penna M. Lactate favours the dissociation of skeletal muscle 6-phosphofructo-1-kinase tetramers down-regulating the enzyme and muscle glycolysis. Biochem J (2007) 408(1):123-30. doi:10.1042/BJ20070687
38. Du J, Zhou Y, Su X, Yu JJ, Khan S, Jiang H, et al. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science (2011) 334(6057):806-9. doi:10.1126/science.1207861
39. Im SS, Yousef L, Blaschitz C, Liu JZ, Edwards RA, Young SG, et al. Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a. Cell Metab (2011) 13(5):540-9. doi:10.1016/j.cmet.2011.04.001
40. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol (2006) 177(10):7303-11. doi:10.4049/jimmunol.177.10.7303
41. Tornatore L, Thotakura AK, Bennett J, Moretti M, Franzoso G. The nuclear factor kappa B signaling pathway: integrating metabolism with inflammation. Trends Cell Biol (2012) 22(11):557-66. doi:10.1016/j.tcb.2012.08.001
42. Imtiyaz HZ, Simon MC. Hypoxia-inducible factors as essential regulators of inflammation. Curr Top Microbiol Immunol (2010) 345:105-20. doi:10.1007/82_2010_74
43. Huang SC, Everts B, Ivanova Y, O'Sullivan D, Nascimento M, Smith AM, et al. Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat Immunol (2014) 15(9):846-55. doi:10.1038/ni.2956
44. O'Neill LA, Hardie DG. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature (2013) 493(7432):346-55. doi:10.1038/nature11862
45. Pearce EL, Pearce EJ. Metabolic pathways in immune cell activation and quiescence. Immunity (2013) 38(4):633-43. doi:10.1016/j.immuni.2013.04.005
46. Odegaard JI, Chawla A. Alternative macrophage activation and metabolism. Annu Rev Pathol (2011) 6:275-97. doi:10.1146/annurev-pathol-011110-130138
47. Board M, Humm S, Newsholme EA. Maximum activities of key enzymes of glycolysis, glutaminolysis, pentose phosphate pathway and tricarboxylic acid cycle in normal, neoplastic and suppressed cells. Biochem J (1990) 265(2):503-9.
48. Stincone A, Prigione A, Cramer T, Wamelink MM, Campbell K, Cheung E, et al. The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biol Rev Camb Philos Soc (2014). doi:10.1111/brv.12140
49. Kruger NJ, von Schaewen A. The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol (2003) 6(3):236-46. doi:10.1016/S1369-5266(03)00039-6
50. Wamelink MM, Struys EA, Jakobs C. The biochemistry, metabolism and inherited defects of the pentose phosphate pathway: a review. J Inherit Metab Dis (2008) 31(6):703-17. doi:10.1007/s10545-008-1015-6
51. Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal (2012) 24(5):981-90. doi:10.1016/j.cellsig.2012.01.008
52. Pollak N, Dolle C, Ziegler M. The power to reduce: pyridine nucleotides-small molecules with a multitude of functions. Biochem J (2007) 402(2):205-18. doi:10.1042/BJ20061638
53. Nishi T, Shimizu N, Hiramoto M, Sato I, Yamaguchi Y, Hasegawa M, et al. Spatial redox regulation of a critical cysteine residue of NF-kappa B in vivo. J Biol Chem (2002) 277(46):44548-56. doi:10.1074/jbc. M202970200
54. Chandel NS, Trzyna WC, McClintock DS, Schumacker PT. Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol (2000) 165(2):1013-21. doi:10.4049/jimmunol.165.2.1013
55. Perl A, Gergely P Jr, Puskas F, Banki K. Metabolic switches of T-cell activation and apoptosis. Antioxid Redox Signal (2002) 4(3):427-43. doi:10.1089/15230860260196227
56. Kazama H, Ricci JE, Herndon JM, Hoppe G, Green DR, Ferguson TA. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity (2008) 29(1):21-32. doi:10.1016/j.immuni.2008.05.013
57. Kumar S, Rabson AB, Gelinas C. The RxxRxRxxC motif conserved in all Rel/kappa B proteins is essential for the DNA-binding activity and redox regulation of the v-Rel oncoprotein. Mol Cell Biol (1992) 12(7):3094-106.
58. Toledano MB, Leonard WJ. Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci U S A (1991) 88(10):4328-32. doi:10.1073/pnas.88.10.4328
59. Wang F, Wang LY, Wright D, Parmely MJ. Redox imbalance differentially inhibits lipopolysaccharide-induced macrophage activation in the mouse liver. Infect Immun (1999) 67(10):5409-16.
60. Kindzelskii AL, Zhou MJ, Haugland RP, Boxer LA, Petty HR. Oscillatory pericellular proteolysis and oxidant deposition during neutrophil locomotion. Biophys J (1998) 74(1):90-7. doi:10.1016/S0006-3495(98)77770-7
61. Olsen LF, Kummer U, Kindzelskii AL, Petty HR. A model of the oscillatory metabolism of activated neutrophils. Biophys J (2003) 84(1):69-81. doi:10.1016/S0006-3495(03)74833-4
62. Kindzelskii AL, Huang JB, Chaiworapongsa T, Fahmy RM, Kim YM, Romero R, et al. Pregnancy alters glucose-6-phosphate dehydrogenase trafficking, cell metabolism, and oxidant release of maternal neutrophils. J Clin Invest (2002) 110(12):1801-11. doi:10.1172/JCI200215973
63. Adachi Y, Kindzelskii AL, Ohno N, Yadomae T, Petty HR. Amplitude and frequency modulation of metabolic signals in leukocytes: synergistic role of IFN-gamma in IL-6-and IL-2-mediated cell activation. J Immunol (1999) 163(8):4367-74.
64. Petty HR, Kindzelskii AL, Chaiworapongsa T, Petty AR, Romero R. Oxidant release is dramatically increased by elevated glucose concentrations in neutrophils from pregnant women. J Matern Fetal Neonatal Med (2005) 18(6):397-404. doi:10.1080/14767050500361679
65. Slaby O, Lebiedz D. Oscillatory NAD(P)H waves and calcium oscillations in neutrophils? A modeling study of feasibility. Biophys J (2009) 96(2):417-28. doi:10.1016/j.bpj.2008.09.044
66. Cooper MR, DeChatelet LR, McCall CE, LaVia MF, Spurr CL, Baehner RL. Complete deficiency of leukocyte glucose-6-phosphate dehydrogenase with defective bactericidal activity. J Clin Invest (1972) 51(4):769-78. doi:10.1172/JCI106871
67. Roos D, van Zwieten R, Wijnen JT, Gomez-Gallego F, de Boer M, Stevens D, et al. Molecular basis and enzymatic properties of glucose 6-phosphate dehydrogenase volendam, leading to chronic nonspherocytic anemia, granulocyte dysfunction, and increased susceptibility to infections. Blood (1999) 94(9):2955-62.
68. van Bruggen R, Bautista JM, Petropoulou T, de Boer M, van Zwieten R, Gomez-Gallego F, et al. Deletion of leucine 61 in glucose-6-phosphate dehydrogenase leads to chronic nonspherocytic anemia, granulocyte dysfunction, and increased susceptibility to infections. Blood (2002) 100(3):1026-30. doi:10.1182/blood. V100.3.1026
69. Efferth T, Fabry U, Osieka R. DNA damage and apoptosis in mononuclear cells from glucose-6-phosphate dehydrogenase-deficient patients (G6PD Aachen variant) after UV irradiation. J Leukoc Biol (2001) 69(3):340-2.
70. Wilmanski J, Siddiqi M, Deitch EA, Spolarics Z. Augmented IL-10 production and redox-dependent signaling pathways in glucose-6-phosphate dehydrogenase-deficient mouse peritoneal macrophages. J Leukoc Biol (2005) 78(1):85-94. doi:10.1189/jlb.0105010
71. Wilmanski J, Villanueva E, Deitch EA, Spolarics Z. Glucose-6-phosphate dehydrogenase deficiency and the inflammatory response to endotoxin and polymicrobial sepsis. Crit Care Med (2007) 35(2):510-8. doi:10.1097/01.CCM.0000254337.50361.2E
72. Sanna F, Bonatesta RR, Frongia B, Uda S, Banni S, Melis MP, et al. Production of inflammatory molecules in peripheral blood mononuclear cells from severely glucose-6-phosphate dehydrogenase-deficient subjects. J Vasc Res (2007) 44(4):253-63. doi:10.1159/000100903
73. Ham M, Lee JW, Choi AH, Jang H, Choi G, Park J, et al. Macrophage glucose-6-phosphate dehydrogenase stimulates proinflammatory responses with oxidative stress. Mol Cell Biol (2013) 33(12):2425-35. doi:10.1128/MCB.01260-12
74. Suzuki M, O'Dea JD, Suzuki T, Agar NS. 2-Deoxyglucose as a substrate for glutathione regeneration in human and ruminant red blood cells. Comp Biochem Physiol B (1983) 75(2):195-7. doi:10.1016/0305-0491(83)90312-7
75. Zhao J, Zhong CJ. A review on research progress of transketolase. Neurosci Bull (2009) 25(2):94-9. doi:10.1007/s12264-009-1113-y
76. Samland AK, Sprenger GA. Transaldolase: from biochemistry to human disease. Int J Biochem Cell Biol (2009) 41(7):1482-94. doi:10.1016/j.biocel.2009.02.001
77. Bar-Even A, Flamholz A, Noor E, Milo R. Thermodynamic constraints shape the structure of carbon fixation pathways. Biochim Biophys Acta (2012) 1817(9):1646-59. doi:10.1016/j.bbabio.2012.05.002
78. Nagy C, Haschemi A. Sedoheptulose kinase regulates cellular carbohydrate metabolism by sedoheptulose 7-phosphate supply. Biochem Soc Trans (2013) 41(2):674-80. doi:10.1042/BST20120354
79. Price NE, Cook PF. Kinetic and chemical mechanisms of the sheep liver 6-phosphogluconate dehydrogenase. Arch Biochem Biophys (1996) 336(2):215-23. doi:10.1006/abbi.1996.0551
80. Karadsheh NS, Tejwani GA, Ramaiah A. Sedoheptulose-7-phosphate kinase activity of phosphofructokinase from the different tissues of rabbit. Biochim Biophys Acta (1973) 327(1):66-81. doi:10.1016/0005-2744(73)90104-6
81. Venkataraman R, Racker E. Mechanism of action of transaldolase. I. Crystalization and properties of yeast enzyme. J Biol Chem (1961) 236:1876-82.
82. Lassen N, Black WJ, Estey T, Vasiliou V. The role of corneal crystallins in the cellular defense mechanisms against oxidative stress. Semin Cell Dev Biol (2008) 19(2):100-12. doi:10.1016/j.semcdb.2007.10.004
83. Xue M, Qian Q, Adaikalakoteswari A, Rabbani N, Babaei-Jadidi R, Thornalley PJ. Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease. Diabetes (2008) 57(10):2809-17. doi:10.2337/db06-1003
84. Hanczko R, Fernandez DR, Doherty E, Qian Y, Vas G, Niland B, et al. Prevention of hepatocarcinogenesis and increased susceptibility to acetaminophen-induced liver failure in transaldolase-deficient mice by N-acetylcysteine. J Clin Invest (2009) 119(6):1546-57. doi:10.1172/JCI35722
85. Clasquin MF, Melamud E, Singer A, Gooding JR, Xu X, Dong A, et al. Riboneogenesis in yeast. Cell (2011) 145(6):969-80. doi:10.1016/j.cell.2011.05.022
86. Blackmore PF, Shuman EA. Regulation of hepatic altro heptulose 1,7-bisphosphate levels and control of flux through the pentose pathway by fructose 2,6-bisphosphate. FEBS Lett (1982) 142(2):255-9. doi:10.1016/0014-5793(82)80147-6
87. Belyaeva NF, Golubev MA, Grigorovich JA, Dubinsky ZV, Semenova NA, Pitkanen E, et al. The involvement of fructose 2,6-bisphosphate in substrate cycle control in the nonoxidative stage of the pentose phosphate pathway. A phosphorus magnetic resonance spectroscopy study. Experientia (1994) 50(8):780-4. doi:10.1007/BF01919382