Ionizing radiation impairs T cell activation by affecting metabolic reprogramming

International Journal of Biological Sciences

Volumn 11, Issue 7, 2015, Pages 726-736

  Li, Heng Hong ^a,b   Wang, Yi Wen ^a   Chen, Renxiang ^a,b   Zhou, Bin ^c   Ashwell, Jonathan D ^d   Fornace, Albert J ^a,c,e  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF RADIATION MEDICINE   (China)

^c GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Ionizing radiation; Mass spectrometry; Metabolic reprogramming; Metabolomics; TCR activation; UPLC QTOF

Indexed keywords

ANIMALIA;

PRIMER DNA;

ANIMAL; FLOW CYTOMETRY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IMMUNOLOGY; IONIZING RADIATION; LYMPHOCYTE ACTIVATION; MASS SPECTROMETRY; METABOLISM; METABOLOMICS; MOUSE; NUCLEAR REPROGRAMMING; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE;

ANIMALS; CELLULAR REPROGRAMMING; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DNA PRIMERS; FLOW CYTOMETRY; HUMANS; LYMPHOCYTE ACTIVATION; MASS SPECTROMETRY; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MICE; RADIATION, IONIZING; REAL-TIME POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 84933521520     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.12009     Document Type: Article

References (37)

1. Bretscher P, Cohn M. A theory of self-nonself discrimination. Science. 1970;169:1042-49
2. Marelli-Berg FM, Fu H, Mauro C. Molecular mechanisms of metabolic reprogramming in proliferating cells: implications for T-cell-mediated immunity. Immunology. 2012;136:363-69
3. Maciolek JA, Pasternak JA, Wilson HL. Metabolism of activated T lymphocytes. Curr Opin Immunol. 2014;27:60-74
4. Jones RG, Thompson CB. Revving the engine: signal transduction fuels T cell activation. Immunity. 2007;27:173-78
5. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D. et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity. 2011;35:871-82
6. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, Plas DR. et al. The CD28 signaling pathway regulates glucose metabolism. Immunity. 2002;16:769-77
7. Fox CJ, Hammerman PS, Thompson CB. Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol. 2005;5:844-52
8. Pearce EL, Poffenberger MC, Chang CH, Jones RG. Fueling immunity: insights into metabolism and lymphocyte function. Science. 2013;342:124-2454
9. Macintyre AN, Gerriets VA, Nichols AG, Michalek RD, Rudolph MC, Deoliveira D. et al. The glucose transporter Glut1 is selectively essential for CD4 T cell activation and effector function. Cell Metab. 2014;20:61-72
10. Sinclair LV, Rolf J, Emslie E, Shi YB, Taylor PM, Cantrell DA. Control of amino-acid transport by antigen receptors coordinates the metabolic reprogramming essential for T cell differentiation. Nat Immunol. 2013;14:500-08
11. Yang K, Shrestha S, Zeng H, Karmaus PW, Neale G, Vogel P. et al. T cell exit from quiescence and differentiation into Th2 cells depend on Raptor-mTORC1-mediated metabolic reprogramming. Immunity. 2013;39:1043-56
12. Delgoffe GM, Pollizzi KN, Waickman AT, Heikamp E, Meyers DJ, Horton MR. et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol. 2011;12:295-303
13. Radford IR. Radiation response of mouse lymphoid and myeloid cell lines. Part I. Sensitivity to killing by ionizing radiation, rate of loss of viability, and cell type of origin. Int J Radiat Biol. 1994;65:203-15
14. Palayoor ST, Macklis RM, Bump EA, Coleman CN. Modulation of radiation-induced apoptosis and G2/M block in murine T-lymphoma cells. Radiat Res. 1995;141:235-43
15. Kusunoki Y, Hayashi T. Long-lasting alterations of the immune system by ionizing radiation exposure: implications for disease development among atomic bomb survivors. Int J Radiat Biol. 2008;84:1-14
16. Hayashi T, Kusunoki Y, Hakoda M, Morishita Y, Kubo Y, Maki M. et al. Radiation dose-dependent increases in inflammatory response markers in A-bomb survivors. Int J Radiat Biol. 2003;79:129-36
17. Neriishi K, Nakashima E, Delongchamp RR. Persistent subclinical inflammation among A-bomb survivors. Int J Radiat Biol. 2001;77:475-82
18. Neriishi K, Akiba S, Amano T, Ogino T, Kodama K. Prevalence of hepatitis B surface antigen, hepatitis B e antigen and antibody, and antigen subtypes in atomic bomb survivors. Radiat Res. 1995;144:215-21
19. Dainiak N. Hematologic consequences of exposure to ionizing radiation. Exp Hematol. 2002;30:513-28
20. Schaue D, McBride WH. T lymphocytes and normal tissue responses to radiation. Front Oncol. 2012;2:119
21. Hernandez-Godoy J, Planelles D, Balsalobre B. Immediate and short-, midand long-term effects of in vivo ionizing radiation exposure in BALB/c mice: II. activation of phorbol myristate acetate and/or calcium ionophore on lymphocyte proliferation. In Vivo. 2013;27:67-76
22. Li HH, Tyburski JB, Wang YW, Strawn S, Moon BH, Kallakury BV. et al. Modulation of fatty acid and bile acid metabolism by peroxisome proliferator-activated receptor alpha protects against alcoholic liver disease. Alcohol Clin Exp Res. 2014;38:1520-31
23. Xia J, Psychogios N, Young N, Wishart DS. MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 2009;37:W652-60
24. Mak TD, Laiakis EC, Goudarzi M, Fornace AJ, Jr. MetaboLyzer: a novel statistical workflow for analyzing Postprocessed LC-MS metabolomics data. Anal Chem. 2014;86:506-13
25. Svensson C, Petrini B. Changes of gamma/delta T cells in blood after radiation therapy for prostatic cancer. Cancer Lett. 1993;72:175-78
26. Seki H, Kanegane H, Iwai K, Konno A, Ohta K, Yachie A. et al. Ionizing radiation induces apoptotic cell death in human TcR-gamma/delta+ T and natural killer cells without detectable p53 protein. Eur J Immunol. 1994;24:2914-17
27. Zheng Y, Delgoffe GM, Meyer CF, Chan W, Powell JD. Anergic T cells are metabolically anergic. J Immunol. 2009;183:6095-101
28. Fathman CG, Lineberry NB. Molecular mechanisms of CD4+ T-cell anergy. Nat Rev Immunol. 2007;7:599-609
29. Kusunoki Y, Yamaoka M, Kubo Y, Hayashi T, Kasagi F, Douple EB. et al. T-cell immunosenescence and inflammatory response in atomic bomb survivors. Radiat Res. 2010;174:870-76
30. Hernandez-Godoy J, Silvestre DP, Hernandez BB. Immediate and short-, midand long-term effects of in vivo ionizing radiation exposure in BALB/c mice: I. Activation of lymphocytes and subpopulations. In Vivo. 2010;24:719-26
31. Shklovskaya E, Fazekas de StGroth B. Severely impaired clonal deletion of CD4+ T cells in low-dose irradiated mice: role of T cell antigen receptor and IL-7 receptor signals. J Immunol. 2006;177:8320-30
32. Liu SZ, Jin SZ, Liu XD, Sun YM. Role of CD28/B7 costimulation and IL-12/IL-10 interaction in the radiation-induced immune changes. BMC Immunol. 2001;2:8
33. Quill H, Schwartz RH. Stimulation of normal inducer T cell clones with antigen presented by purified Ia molecules in planar lipid membranes: specific induction of a long-lived state of proliferative nonresponsiveness. J Immunol. 1987;138:3704-12
34. Jenkins MK, Chen CA, Jung G, Mueller DL, Schwartz RH. Inhibition of antigen-specific proliferation of type 1 murine T cell clones after stimulation with immobilized anti-CD3 monoclonal antibody. J Immunol. 1990;144:16-22
35. Linsley PS, Ledbetter JA. The role of the CD28 receptor during T cell responses to antigen. Annu Rev Immunol. 1993;11:191-212
36. Stillwell R, Bierer BE. T cell signal transduction and the role of CD7 in costimulation. Immunol Res. 2001;24:31-52
37. Calvisi DF, Wang C, Ho C, Ladu S, Lee SA, Mattu S. et al. Increased lipogenesis, induced by AKT-mTORC1-RPS6 signaling, promotes development of human hepatocellular carcinoma. Gastroenterology. 2011;140:1071-83.