Inhibition of indoleamine 2,3-dioxygenase in mixed lymphocyte reaction affects glucose influx and enzymes involved in aerobic glycolysis and glutaminolysis in alloreactive T-cells

Human Immunology

Volumn 74, Issue 12, 2013, Pages 1501-1509

  Eleftheriadis, Theodoros ^a   Pissas, Georgios ^a   Yiannaki, Efi ^b   Markala, Dimitra ^b   Arampatzis, Spyridon ^a   Antoniadi, Georgia ^a   Liakopoulos, Vassilios ^a   Stefanidis, Ioannis ^a  

^a UNIVERSITY OF THESSALY   (Greece)

^b THEAGENIO CANCER HOSPITAL   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYL DEXTRO LEVO TRYPTOPHAN; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCOSE TRANSPORTER 1; HEXOKINASE; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; LACTATE DEHYDROGENASE; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PYRUVATE DEHYDROGENASE; PYRUVATE KINASE; UNCLASSIFIED DRUG;

ADULT; ALLOIMMUNITY; ARTICLE; CELL PROLIFERATION; CELL SURFACE; CITRIC ACID CYCLE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GLUCOSE INTAKE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUTAMINOLYSIS; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MIXED LYMPHOCYTE REACTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE;

ADULT; CITRIC ACID CYCLE; ENZYME ACTIVATION; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLYCOLYSIS; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE CULTURE TEST, MIXED; MALE; MULTIPROTEIN COMPLEXES; PROTEIN-SERINE-THREONINE KINASES; T-LYMPHOCYTE SUBSETS; TOR SERINE-THREONINE KINASES; TRYPTOPHAN;

EID: 84888202150     PISSN: 01988859     EISSN: 18791166     Source Type: Journal    
DOI: 10.1016/j.humimm.2013.08.268     Document Type: Article

References (43)

1. King N.J., Thomas S.R. Molecules in focus: indoleamine 2,3-dioxygenase. Int J Biochem Cell Biol 2007, 39:2167.
2. Curti A., Trabanelli S., Salvestrini V., Baccarani M., Lemoli R.M. The role of indoleamine 2,3-dioxygenase in the induction of immune tolerance: focus on hematology. Blood 2009, 113:2394.
3. Munn D.H., Sharma M.D., Baban B., Harding H.P., Zhang Y., Ron D., et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 2005, 22:633.
4. Cobbold S.P., Adams E., Farquhar C.A., Nolan K.F., Howie D., Lui K., et al. Infectious tolerance via the consumption of essential amino acids and mTOR signaling. Proc Natl Acad Sci USA 2009, 106:12055.
5. Seo S.K., Choi J.H., Kim Y.H., Kang W.J., Park H.Y., Suh J.H., et al. 4-1BB-mediated immunotherapy of rheumatoid arthritis. Nat Med 2004, 10:1088.
6. Gurtner G.J., Newberry R.D., Schloemann S.R., McDonald K.G., Stenson W.F. Inhibition of indoleamine 2,3-dioxygenase augments trinitrobenzene sulfonic acid colitis in mice. Gastroenterology 2003, 125:1762.
7. Kwidzinski E., Bunse J., Aktas O., Richter D., Mutlu L., Zipp F., et al. Indoleamine 2,3-dioxygenase is expressed in the CNS and down-regulates autoimmune inflammation. FASEB J 2005, 19:1347.
8. Alexander A.M., Crawford M., Bertera S., Rudert W.A., Takikawa O., Robbins P.D., et al. Indoleamine 2,3-dioxygenase expression in transplanted NOD islets prolongs graft survival after adoptive transfer of diabetogenic splenocytes. Diabetes 2002, 51:356.
9. Beutelspacher S.C., Pillai R., Watson M.P., Tan P.H., Tsang J., McClure M.O., et al. Function of indoleamine 2,3-dioxygenase in corneal allograft rejection and prolongation of allograft survival by over-expression. Eur J Immunol 2006, 36:690.
10. Li Y., Tredget E.E., Ghaffari A., Lin X., Kilani R.T., Ghahary A. Local expression of indoleamine 2,3-dioxygenase protects engraftment of xenogeneic skin substitute. J Invest Dermatol 2006, 126:128.
11. Munn D.H., Mellor A.L. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest 2007, 117:1147.
12. Munn D.H., Zhou M., Attwood J.T., Bondarev I., Conway S.J., Marshall B., et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998, 281:1191.
13. Mellor A.L., Sivakumar J., Chandler P., Smith K., Molina H., Mao D., et al. Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol 2001, 2:64.
14. Eleftheriadis T., Liakopoulos V., Antoniadi G., Stefanidis I., Galaktidou G. Indoleamine 2,3-dioxygenase is increased in hemodialysis patients and affects immune response to hepatitis B vaccination. Vaccine 2011, 29:2242.
15. Eleftheriadis T., Yiannaki E., Antoniadi G., Liakopoulos V., Pissas G., Galaktidou G., et al. Plasma indoleamine 2,3-dioxygenase and arginase type I may contribute to decreased blood T-cell count in hemodialysis patients. Ren Fail 2012, 34:1118.
16. Forouzandeh F., Jalili R.B., Germain M., Duronio V., Ghahary A. Differential immunosuppressive effect of indoleamine 2,3-dioxygenase (IDO) on primary human CD4+ and CD8+ T cells. Mol Cell Biochem 2008, 309:1.
17. Fallarino F., Grohmann U., You S., McGrath B.C., Cavener D.R., Vacca C., et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J Immunol 2006, 176:6752.
18. Sharma M.D., Baban B., Chandler P., Hou D.Y., Singh N., Yagita H., et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest 2007, 117:2570.
19. Bozza S., Fallarino F., Pitzurra L., Zelante T., Montagnoli C., Bellocchio S., et al. A crucial role for tryptophan catabolism at the host/Candida albicans interface. J Immunol 2005, 174:2910.
20. Sharma M.D., Hou D.Y., Liu Y., Koni P.A., Metz R., Chandler P., et al. Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 2009, 113:6102.
21. Zhao Z.G., Xu W., Sun L., You Y., Li F., Li Q.B., et al. Immunomodulatory function of regulatory dendritic cells induced by mesenchymal stem cells. Immunol Invest 2012, 41:183.
22. Maciver N.J., Jacobs S.R., Wieman H.L., Wofford J.A., Coloff J.L., Rathmell J.C. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival. J Leukoc Biol 2008, 84:949.
23. Fox C.J., Hammerman P.S., Thompson C.B. Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol 2005, 5:844.
24. Michalek R.D., Gerriets V.A., Jacobs S.R., Macintyre A.N., MacIver N.J., Mason E.F., et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol 2011, 186:3299.
25. Shi L.Z., Wang R., Huang G., Vogel P., Neale G., Green D.R., et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 2011, 208:1367.
26. Wang R., Dillon C.P., Shi L.Z., Milasta S., Carter R., Finkelstein D., et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011, 35:871.
27. Eleftheriadis T., Pissas G., Karioti A., Antoniadi G., Liakopoulos V., Dafopoulou K., et al. The indoleamine 2,3-dioxygenase inhibitor 1-methyl-tryptophan suppresses mitochondrial function, induces aerobic glycolysis and decreases interleukin-10 production in human lymphocytes. Immunol Invest 2012, 41:507.
28. Sato T., Deiwick A., Raddatz G., Koyama K., Schlitt H.J. Interactions of allogeneic human mononuclear cells in the two-way mixed leucocyte culture (MLC): influence of cell numbers, subpopulations and cyclosporin. Clin Exp Immunol 1999, 115:301.
29. Jia L., Schweikart K., Tomaszewski J., Page J.G., Noker P.E., Buhrow S.A., et al. Toxicology and pharmacokinetics of 1-methyl-d-tryptophan: absence of toxicity due to saturating absorption. Food Chem Toxicol 2008, 46:203.
30. Berridge M.V., Herst P.M., Tan A.S. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev 2005, 11:127.
31. Warburg O. On the origin of cancer cells. Science 1956, 123:309.
32. Deval C., Chaveroux C., Maurin A.C., Cherasse Y., Parry L., Carraro V., et al. Amino acid limitation regulates the expression of genes involved in several specific biological processes through GCN2-dependent and GCN2-independent pathways. FEBS J 2009, 276:707.
33. Deberardinis R.J., Sayed N., Ditsworth D., Thompson C.B. Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev 2008, 18:54.
34. Kroemer G., Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008, 13:472.
35. Anastasiou D., Cantley L.C. Breathless cancer cells get fat on glutamine. Cell Res 2012, 22:443.
36. Maciver N.J., Jacobs S.R., Wieman H.L., Wofford J.A., Coloff J.L., Rathmell J.C. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival. J Leukoc Biol 2008, 84:949.
37. Christofk H.R., Vander Heiden M.G., Harris M.H., Ramanathan A., Gerszten R.E., Wei R, et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230.
38. Hitosugi T., Kang S., Vander Heiden M.G., Chung T.W., Elf S, Lythgoe K, et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2009, 2:ra73.
39. Sugden M.C., Holness M.J. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 2003, 284:E855.
40. Fan J., Hitosugi T., Chung T.W., Xie J., Ge Q., Gu T.L., et al. Tyrosine phosphorylation of lactate dehydrogenase A is important for NADH/NAD(+) redox homeostasis in cancer cells. Mol Cell Biol 2011, 31:4938.
41. DeBerardinis R.J., Mancuso A., Daikhin E., Nissim I., Yudkoff M., Wehrli S., et al. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci USA 2007, 104:19345.
42. Metallo C.M., Gameiro P.A., Bell E.L., Mattaini K.R., Yang J., Hiller K., et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 2012, 481:380.
43. Mullen A.R., Wheaton W.W., Jin E.S., Chen P.H., Sullivan L.B., Cheng T., et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 2012, 481:385.