Preventing Allograft Rejection by Targeting Immune Metabolism

Cell Reports

Volumn 13, Issue 4, 2015, Pages 760-770

  Lee, Chen Fang ^a,b   Lo, Ying Chun ^a   Cheng, Chih Hsien ^a,b   Furtmüller, Georg J ^c   Oh, Byoungchol ^c   Andrade Oliveira, Vinicius ^a   Thomas, Ajit G ^c   Bowman, Caitlyn E ^c   Slusher, Barbara S ^c   Wolfgang, Michael J ^c   Brandacher, Gerald ^c   Powell, Jonathan D ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 DIAZO 5 OXONORLEUCINE; DEOXYGLUCOSE; METFORMIN; GLUTAMINE;

ALLOTRANSPLANTATION; AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIMETABOLIC ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL REGENERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG ACTIVITY; EFFECTOR CELL; GLYCOLYSIS; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SKIN TRANSPLANTATION; T LYMPHOCYTE ACTIVATION; ALLOGRAFT; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROCEDURES; TRANSGENIC MOUSE;

ALLOGRAFTS; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DEOXYGLUCOSE; DIAZOOXONORLEUCINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GLUTAMINE; GLYCOLYSIS; GRAFT REJECTION; HEART TRANSPLANTATION; METFORMIN; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; PHOSPHORYLATION; T-LYMPHOCYTES, REGULATORY;

EID: 84945583836     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.09.036     Document Type: Article

References (55)

1. Arnold R., Pussell B.A., Pianta T.J., Lin C.S., Kiernan M.C., Krishnan A.V. Association between calcineurin inhibitor treatment and peripheral nerve dysfunction in renal transplant recipients. Am. J. Transplant. 2013, 13:2426-2432.
2. Bestard O., Cassis L., Cruzado J.M., Torras J., Franquesa M., Gil-Vernet S., Lucia M., Grinyó J.M. Costimulatory blockade with mTor inhibition abrogates effector T-cell responses allowing regulatory T-cell survival in renal transplantation. Transpl. Int. 2011, 24:451-460.
3. Buzzai M., Jones R.G., Amaravadi R.K., Lum J.J., DeBerardinis R.J., Zhao F., Viollet B., Thompson C.B. Systemic treatment with the antidiabetic drug metformin selectively impairs p53-deficient tumor cell growth. Cancer Res. 2007, 67:6745-6752.
4. Carr E.L., Kelman A., Wu G.S., Gopaul R., Senkevitch E., Aghvanyan A., Turay A.M., Frauwirth K.A. Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J. Immunol. 2010, 185:1037-1044.
5. Cham C.M., Gajewski T.F. Glucose availability regulates IFN-gamma production and p70S6 kinase activation in CD8+ effector T cells. J. Immunol. 2005, 174:4670-4677.
6. Cham C.M., Driessens G., O'Keefe J.P., Gajewski T.F. Glucose deprivation inhibits multiple key gene expression events and effector functions in CD8+ T cells. Eur. J. Immunol. 2008, 38:2438-2450.
7. Chambers J.W., Maguire T.G., Alwine J.C. Glutamine metabolism is essential for human cytomegalovirus infection. J. Virol. 2010, 84:1867-1873.
8. Cheng G., Zielonka J., Dranka B.P., McAllister D., Mackinnon A.C., Joseph J., Kalyanaraman B. Mitochondria-targeted drugs synergize with 2-deoxyglucose to trigger breast cancer cell death. Cancer Res. 2012, 72:2634-2644.
9. Cheng G., Zielonka J., McAllister D., Tsai S., Dwinell M.B., Kalyanaraman B. Profiling and targeting of cellular bioenergetics: inhibition of pancreatic cancer cell proliferation. Br. J. Cancer 2014, 111:85-93.
10. Cheong J.H., Park E.S., Liang J., Dennison J.B., Tsavachidou D., Nguyen-Charles C., Wa Cheng K., Hall H., Zhang D., Lu Y., et al. Dual inhibition of tumor energy pathway by 2-deoxyglucose and metformin is effective against a broad spectrum of preclinical cancer models. Mol. Cancer Ther. 2011, 10:2350-2362.
11. Corry R.J., Winn H.J., Russell P.S. Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 1973, 16:343-350.
12. Crutchlow M.F., Bloom R.D. Transplant-associated hyperglycemia: a new look at an old problem. Clin. J. Am. Soc. Nephrol. 2007, 2:343-355.
13. El-Mir M.Y., Nogueira V., Fontaine E., Avéret N., Rigoulet M., Leverve X. Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 2000, 275:223-228.
14. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226:497-509.
15. Franciosi M., Lucisano G., Lapice E., Strippoli G.F., Pellegrini F., Nicolucci A. Metformin therapy and risk of cancer in patients with type 2 diabetes: systematic review. PLoS ONE 2013, 8:e71583.
16. Graham G.G., Punt J., Arora M., Day R.O., Doogue M.P., Duong J.K., Furlong T.J., Greenfield J.R., Greenup L.C., Kirkpatrick C.M., et al. Clinical pharmacokinetics of metformin. Clin. Pharmacokinet. 2011, 50:81-98.
17. Guba M., Graeb C., Jauch K.-W., Geissler E.K. Pro- and anti-cancer effects of immunosuppressive agents used in organ transplantation. Transplantation 2004, 77:1777-1782.
18. Hoorn E.J., Walsh S.B., McCormick J.A., Zietse R., Unwin R.J., Ellison D.H. Pathogenesis of calcineurin inhibitor-induced hypertension. J. Nephrol. 2012, 25:269-275.
19. Huynh A., DuPage M., Priyadharshini B., Sage P.T., Quiros J., Borges C.M., Townamchai N., Gerriets V.A., Rathmell J.C., Sharpe A.H., et al. Control of PI(3) kinase in Treg cells maintains homeostasis and lineage stability. Nat. Immunol. 2015, 16:188-196.
20. Jacobs S.R., Herman C.E., Maciver N.J., Wofford J.A., Wieman H.L., Hammen J.J., Rathmell J.C. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 2008, 180:4476-4486.
21. Jones R.G., Thompson C.B. Revving the engine: signal transduction fuels T cell activation. Immunity 2007, 27:173-178.
22. Lagodzinski Z., Górski A., Wasik M. Effect of FK506 and cyclosporine on primary and secondary skin allograft survival in mice. Immunology 1990, 71:148-150.
23. Lim J.H., Luo C., Vazquez F., Puigserver P. Targeting mitochondrial oxidative metabolism in melanoma causes metabolic compensation through glucose and glutamine utilization. Cancer Res. 2014, 74:3535-3545.
24. Lo Y.C., Lee C.F., Powell J.D. Insight into the role of mTOR and metabolism in T cells reveals new potential approaches to preventing graft rejection. Curr. Opin. Organ Transplant. 2014, 19:363-371.
25. Macintyre A.N., Gerriets V.A., Nichols A.G., Michalek R.D., Rudolph M.C., Deoliveira D., Anderson S.M., Abel E.D., Chen B.J., Hale L.P., Rathmell J.C. The glucose transporter Glut1 is selectively essential for CD4 T cell activation and effector function. Cell Metab. 2014, 20:61-72.
26. MacIver N.J., Michalek R.D., Rathmell J.C. Metabolic regulation of T lymphocytes. Annu. Rev. Immunol. 2013, 31:259-283.
27. Michalek R.D., Gerriets V.A., Jacobs S.R., Macintyre A.N., MacIver N.J., Mason E.F., Sullivan S.A., Nichols A.G., Rathmell J.C. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J. Immunol. 2011, 186:3299-3303.
28. Nakaya M., Xiao Y., Zhou X., Chang J.H., Chang M., Cheng X., Blonska M., Lin X., Sun S.C. Inflammatory T cell responses rely on amino acid transporter ASCT2 facilitation of glutamine uptake and mTORC1 kinase activation. Immunity 2014, 40:692-705.
29. Oberhuber R., Cardini B., Kofler M., Ritschl P., Oellinger R., Aigner F., Sucher R., Schneeberger S., Pratschke J., Brandacher G., Maglione M. Murine cervical heart transplantation model using a modified cuff technique. J. Vis. Exp. 2014, 92:e50753.
30. Oderup C., Malm H., Ekberg H., Qi Z., Veress B., Ivars F., Corbascio M. Costimulation blockade-induced cardiac allograft tolerance: inhibition of T cell expansion and accumulation of intragraft cD4(+)Foxp3(+) T cells. Transplantation 2006, 82:1493-1500.
31. Pearce E.L., Poffenberger M.C., Chang C.H., Jones R.G. Fueling immunity: insights into metabolism and lymphocyte function. Science 2013, 342:1242454.
32. Pilon C.B., Petillon S., Naserian S., Martin G.H., Badoual C., Lang P., Azoulay D., Piaggio E., Grimbert P., Cohen J.L. Administration of low doses of IL-2 combined to rapamycin promotes allogeneic skin graft survival in mice. Am. J. Transplant. 2014, 14:2874-2882.
33. Pollizzi K.N., Powell J.D. Integrating canonical and metabolic signalling programmes in the regulation of T cell responses. Nat. Rev. Immunol. 2014, 14:435-446.
34. + T cell differentiation. J. Clin. Invest. 2015, 125:2090-2108.
35. Powell J.D., Zheng Y. Dissecting the mechanism of T-cell anergy with immunophilin ligands. Curr. Opin. Investig. Drugs 2006, 7:1002-1007.
36. Powell J.D., Pollizzi K.N., Heikamp E.B., Horton M.R. Regulation of immune responses by mTOR. Annu. Rev. Immunol. 2012, 30:39-68.
37. Powell J.D., Heikamp E.B., Pollizzi K.N., Waickman A.T. A modified model of T-cell differentiation based on mTOR activity and metabolism. Cold Spring Harb. Symp. Quant. Biol. 2013, 78:125-130.
38. Raez L.E., Papadopoulos K., Ricart A.D., Chiorean E.G., Dipaola R.S., Stein M.N., Rocha Lima C.M., Schlesselman J.J., Tolba K., Langmuir V.K., et al. A phase I dose-escalation trial of 2-deoxy-D-glucose alone or combined with docetaxel in patients with advanced solid tumors. Cancer Chemother. Pharmacol. 2013, 71:523-530.
39. Roodnat J.I., Hilbrands L.B., Hené R.J., de Sévaux R.G., Smak Gregoor P.J., Kal-van Gestel J.A., Konijn C., van Zuilen A., van Gelder T., Hoitsma A.J., Weimar W. 15-year follow-up of a multicenter, randomized, calcineurin inhibitor withdrawal study in kidney transplantation. Transplantation 2014, 98:47-53.
40. Rowe I., Chiaravalli M., Mannella V., Ulisse V., Quilici G., Pema M., Song X.W., Xu H., Mari S., Qian F., et al. Defective glucose metabolism in polycystic kidney disease identifies a new therapeutic strategy. Nat. Med. 2013, 19:488-493.
41. Sayegh M.H., Carpenter C.B. Transplantation 50 years later--progress, challenges, and promises. N. Engl. J. Med. 2004, 351:2761-2766.
42. Shi L.Z., Wang R., Huang G., Vogel P., Neale G., Green D.R., Chi H. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 2011, 208:1367-1376.
43. Sullivan M.P., Nelson J.A., Feldman S., Van Nguyen B. Pharmacokinetic and phase I study of intravenous DON (6-diazo-5-oxo-L-norleucine) in children. Cancer Chemother. Pharmacol. 1988, 21:78-84.
44. Thomas A.G., Rojas C., Tanega C., Shen M., Simeonov A., Boxer M.B., Auld D.S., Ferraris D.V., Tsukamoto T., Slusher B.S. Kinetic characterization of ebselen, chelerythrine and apomorphine as glutaminase inhibitors. Biochem. Biophys. Res. Commun. 2013, 438:243-248.
45. Thomas A.G., O'Driscoll C.M., Bressler J., Kaufmann W., Rojas C.J., Slusher B.S. Small molecule glutaminase inhibitors block glutamate release from stimulated microglia. Biochem. Biophys. Res. Commun. 2014, 443:32-36.
46. Tsilidis K.K., Capothanassi D., Allen N.E., Rizos E.C., Lopez D.S., van Veldhoven K., Sacerdote C., Ashby D., Vineis P., Tzoulaki I., Ioannidis J.P. Metformin does not affect cancer risk: a cohort study in the U.K. Clinical Practice Research Datalink analyzed like an intention-to-treat trial. Diabetes Care 2014, 37:2522-2532.
47. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
48. Waickman A.T., Powell J.D. mTOR, metabolism, and the regulation of T-cell differentiation and function. Immunol. Rev. 2012, 249:43-58.
49. Warburg O. On respiratory impairment in cancer cells. Science 1956, 124:269-270.
50. Warburg O., Gawehn K., Geissler A.W. [Metabolism of leukocytes]. Z. Naturforsch. B 1958, 13B:515-516.
51. Willems L., Jacque N., Jacquel A., Neveux N., Maciel T.T., Lambert M., Schmitt A., Poulain L., Green A.S., Uzunov M., et al. Inhibiting glutamine uptake represents an attractive new strategy for treating acute myeloid leukemia. Blood 2013, 122:3521-3532.
52. Wu T., Zhang L., Xu K., Sun C., Lei T., Peng J., Liu G., Wang R., Zhao Y. Immunosuppressive drugs on inducing Ag-specific CD4(+)CD25(+)Foxp3(+) Treg cells during immune response in vivo. Transpl. Immunol. 2012, 27:30-38.
53. Yamasaki T., Tran T.A., Oz O.K., Raj G.V., Schwarz R.E., Deberardinis R.J., Zhang X., Brugarolas J. Exploring a glycolytic inhibitor for the treatment of an FH-deficient type-2 papillary RCC. Nat. Rev. Urol. 2011, 8:165-171.
54. Yang K., Chi H. mTOR and metabolic pathways in T cell quiescence and functional activation. Semin. Immunol. 2012, 24:421-428.
55. Zheng Y., Delgoffe G.M., Meyer C.F., Chan W., Powell J.D. Anergic T cells are metabolically anergic. J. Immunol. 2009, 183:6095-6101.