T cells expanded in presence of IL-15 exhibit increased antioxidant capacity and innate effector molecules

Cytokine

Volumn 55, Issue 2, 2011, Pages 307-317

  Kaur, Navtej ^a   Naga, Osama S ^a   Norell, Håkan ^a   Al Khami, Amir A ^a   Scheffel, Matthew J ^a   Chakraborty, Nitya G ^b   Voelkel Johnson, Christina ^a   Mukherji, Bijay ^b   Mehrotra, Shikhar ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Apoptosis; Cytokine; Thiols

Indexed keywords

GLUTATHIONE; GLUTATHIONE REDUCTASE; GRANZYME A; GRANZYME B; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 2; PEROXIREDOXIN; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; THIOL; THIOREDOXIN; THIOREDOXIN REDUCTASE 1;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL LEVEL; CELL SURFACE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LYMPHOCYTE CULTURE; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; UPREGULATION;

ANTIOXIDANTS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; HUMANS; HYDROGEN PEROXIDE; IMMUNITY, INNATE; INTERLEUKIN-15; INTERLEUKIN-2; MEMBRANE POTENTIAL, MITOCHONDRIAL; NITRIC OXIDE; OXIDANTS; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; T-LYMPHOCYTES;

EID: 79959548281     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2011.04.014     Document Type: Article

References (84)

1. Rosenberg S.A., Restifo N.P., Yang J.C., Morgan R.A., Dudley M.E. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008, 8:299-308.
2. Hinrichs C.S., Gattinoni L., Restifo N.P. Programming CD8+ T cells for effective immunotherapy. Curr Opin Immunol 2006, 18:363-370.
3. Paulos C.M., Kaiser A., Wrzesinski C., Hinrichs C.S., Cassard L., Boni A., et al. Toll-like receptors in tumor immunotherapy. Clin Cancer Res 2007, 13:5280-5289.
4. Gattinoni L., Powell D.J., Rosenberg S.A., Restifo N.P. Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol 2006, 6:383-393.
5. Gattinoni L., Klebanoff C.A., Restifo N.P. Pharmacologic induction of CD8+ T cell memory: better living through chemistry. Sci Transl Med 2009, 1:11-12.
6. Vaglio A., Alberici F., Maggiore U., Buti S., Potenzoni D., Passalacqua R., et al. Chronically administered immunotherapy with low-dose IL-2 and IFN-alpha in metastatic renal cell carcinoma: a feasible option for patients with a good prognostic profile. Oncology 2009, 76:69-76.
7. Waldmann T.A. The IL-2/IL-15 receptor systems: targets for immunotherapy. J Clin Immunol 2002, 22:51-56.
8. Arienti F., Belli F., Rivoltini L., Gambacorti-Passerini C., Furlan L., Mascheroni L., et al. Adoptive immunotherapy of advanced melanoma patients with interleukin-2 (IL-2) and tumor-infiltrating lymphocytes selected in vitro with low doses of IL-2. Cancer Immunol Immunother 1993, 36:315-322.
9. Berger C., Berger M., Hackman R.C., Gough M., Elliott C., Jensen M.C., et al. Safety and immunologic effects of IL-15 administration in nonhuman primates. Blood 2009, 114:2417-2426.
10. Waldmann T.A., Dubois S., Tagaya Y. Contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for immunotherapy. Immunity 2001, 14:105-110.
11. Klebanoff C.A., Finkelstein S.E., Surman D.R., Lichtman M.K., Gattinoni L., Theoret M.R., et al. IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc Natl Acad Sci U S A 2004, 101:1969-1974.
12. Zeng R., Spolski R., Finkelstein S.E., Oh S., Kovanen P.E., Hinrichs C.S., et al. Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J Exp Med 2005, 201:139-148.
13. Kutzler M.A., Robinson T.M., Chattergoon M.A., Choo D.K., Choo A.Y., Choe P.Y., et al. Coimmunization with an optimized IL-15 plasmid results in enhanced function and longevity of CD8 T cells that are partially independent of CD4 T cell help. J Immunol 2005, 175:112-123.
14. Oh S., Perera L.P., Terabe M., Ni L., Waldmann T.A., Berzofsky J.A. IL-15 as a mediator of CD4+ help for CD8+ T cell longevity and avoidance of TRAIL-mediated apoptosis. Proc Natl Acad Sci U S A 2008, 105:5201-5206.
15. Waldmann T. The contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for the immunotherapy of rheumatological diseases. Arthritis Res 2002, 4(Suppl. 3):S161-167.
16. Marks-Konczalik J., Dubois S., Losi J.M., Sabzevari H., Yamada N., Feigenbaum L., et al. IL-2-induced activation-induced cell death is inhibited in IL-15 transgenic mice. Proc Natl Acad Sci U S A 2000, 97:11445-11450.
17. Tang C., Yamada H., Shibata K., Yoshida S., Wajjwalku W., Yoshikai Y. IL-15 protects antigen-specific CD8+ T cell contraction after Mycobacterium bovis bacillus Calmette-Guerin infection. J Leukoc Biol 2009, 86:187-194.
18. Shrikant P., Mescher M.F. Opposing effects of IL-2 in tumor immunotherapy: promoting CD8 T cell growth and inducing apoptosis. J Immunol 2002, 169:1753-1759.
19. Berard M., Brandt K., Bulfone-Paus S., Tough D.F. IL-15 promotes the survival of naive and memory phenotype CD8+ T cells. J Immunol 2003, 170:5018-5026.
20. Takahashi A., Hanson M.G., Norell H.R., Havelka A.M., Kono K., Malmberg K.J., et al. Preferential cell death of CD8+ effector memory (CCR7-CD45RA-) T cells by hydrogen peroxide-induced oxidative stress. J Immunol 2005, 174:6080-6087.
21. White-Gilbertson S., Mullen T., Senkal C., Lu P., Ogretmen B., Obeid L., et al. Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells. Oncogene 2009, 28:1132-1141.
22. Sahaf B., Heydari K., Herzenberg L.A. Lymphocyte surface thiol levels. Proc Natl Acad Sci U S A 2003, 100:4001-4005.
23. Sahaf B., Heydari K., Herzenberg L.A. The extracellular microenvironment plays a key role in regulating the redox status of cell surface proteins in HIV-infected subjects. Arch Biochem Biophys 2005, 434:26-32.
24. Banki K., Hutter E., Gonchoroff N.J., Perl A. Elevation of mitochondrial transmembrane potential and reactive oxygen intermediate levels are early events and occur independently from activation of caspases in Fas signaling. J Immunol 1999, 162:1466-1479.
25. Rappl G., Abken H., Hasselmann D.O., Tilgen W., Ugurel S., Reinhold U. The CD7(-) subset of CD4(+) memory T cells is prone to accelerated apoptosis that is prevented by interleukin-15 (IL-15). Cell Death Differ 2001, 8:395-402.
26. Mueller Y.M., Makar V., Bojczuk P.M., Witek J., Katsikis P.D. IL-15 enhances the function and inhibits CD95/Fas-induced apoptosis of human CD4+ and CD8+ effector-memory T cells. Int Immunol 2003, 15:49-58.
27. Demirci G., Li X.C. IL-2 and IL-15 exhibit opposing effects on Fas mediated apoptosis. Cell Mol Immunol 2004, 1:123-128.
28. Gelderman K.A., Hultqvist M., Holmberg J., Olofsson P., Holmdahl R. T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc Natl Acad Sci U S A 2006, 103:12831-12836.
29. Sahaf B., Heydari K., Herzenberg L.A., Herzenberg L.A. Lymphocyte surface thiol levels. Proc Natl Acad Sci U S A 2003, 100:4001-4005.
30. Sahaf B., Heydari K., Herzenberg L.A., Herzenberg L.A. The extracellular microenvironment plays a key role in regulating the redox status of cell surface proteins in HIV-infected subjects. Arch Biochem Biophys 2005, 434:26-32.
31. Franco R., Panayiotidis M.I., Cidlowski J.A. Glutathione depletion is necessary for apoptosis in lymphoid cells independent of reactive oxygen species formation. J Biol Chem 2007, 282:30452-30465.
32. Malamut G., El Machhour R., Montcuquet N., Martin-Lanneree S., Dusanter-Fourt I., Verkarre V., et al. IL-15 triggers an antiapoptotic pathway in human intraepithelial lymphocytes that is a potential new target in celiac disease-associated inflammation and lymphomagenesis. J Clin Invest 2010, 120:2131-2143.
33. Szabo S.J., Sullivan B.M., Stemmann C., Satoskar A.R., Sleckman B.P., Glimcher L.H. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 2002, 295:338-342.
34. Baaten B.J., Li C.R., Deiro M.F., Lin M.M., Linton P.J., Bradley L.M. CD44 regulates survival and memory development in Th1 cells. Immunity 2010, 32:104-115.
35. Focosi D., Bestagno M., Burrone O., Petrini M. CD57+ T lymphocytes and functional immune deficiency. J Leukoc Biol 2010, 87:107-116.
36. Liebenberg L.J., Adedeji A.L., Martin D.P., Gumbi P.P., Denny L., Passmore J.A. CD57 expression by T cells in the female genital tract of HIV-zx1 infected women. Clin Immunol 2010, 135:137-145.
37. Liu K., Catalfamo M., Li Y., Henkart P.A., Weng N.P. IL-15 mimics T cell receptor crosslinking in the induction of cellular proliferation, gene expression, and cytotoxicity in CD8+ memory T cells. Proc Natl Acad Sci U S A 2002, 99:6192-6197.
38. Lu J., Giuntoli R.L., Omiya R., Kobayashi H., Kennedy R., Celis E. Interleukin 15 promotes antigen-independent in vitro expansion and long-term survival of antitumor cytotoxic T lymphocytes. Clin Cancer Res 2002, 8:3877-3884.
39. Tamang D.L., Redelman D., Alves B.N., Vollger L., Bethley C., Hudig D. Induction of granzyme B and T cell cytotoxic capacity by IL-2 or IL-15 without antigens: multiclonal responses that are extremely lytic if triggered and short-lived after cytokine withdrawal. Cytokine 2006, 36:148-159.
40. Davies E., Reid S., Medina M.F., Lichty B., Ashkar A.A. IL-15 has innate anti-tumor activity independent of NK and CD8 T cells. J Leukoc Biol 2010, 88:529-536.
41. Kohchi C., Inagawa H., Nishizawa T., Soma G. ROS and innate immunity. Anticancer Res 2009, 29:817-821.
42. Thoren F.B., Romero A.I., Hermodsson S., Hellstrand K. The CD16-/CD56bright subset of NK cells is resistant to oxidant-induced cell death. J Immunol 2007, 179:781-785.
43. Franco R., Cidlowski J.A. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ 2009, 16:1303-1314.
44. Meister A. Glutathione metabolism and its selective modification. J Biol Chem 1988, 263:17205-17208.
45. Qiao M., Kisgati M., Cholewa J.M., Zhu W., Smart E.J., Sulistio M.S., et al. Increased expression of glutathione reductase in macrophages decreases atherosclerotic lesion formation in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 2007, 27:1375-1382.
46. Masutani H. S. Ueda and J. Yodoi, The thioredoxin system in retroviral infection and apoptosis. Cell Death Differ 2005, 12(Suppl 1):991-998.
47. Bouzar A.B., Boxus M., Florins A., Francois C., Reichert M., Willems L. Reduced levels of reactive oxygen species correlate with inhibition of apoptosis, rise in thioredoxin expression and increased bovine leukemia virus proviral loads. Retrovirology 2009, 6:102.
48. Tanaka T., Hosoi F., Yamaguchi-Iwai Y., Nakamura H., Masutani H., Ueda S., et al. Thioredoxin-2 (TRX-2) is an essential gene regulating mitochondria-dependent apoptosis. EMBO J 2002, 21:1695-1703.
49. Mustacich D., Powis G. Thioredoxin reductase. Biochem J 2000, 346(Pt 1):1-8.
50. Bishopric N.H., Webster K.A. Preventing apoptosis with thioredoxin: ASK me how. Circ Res 2002, 90:1237-1239.
51. Fujino G., Noguchi T., Takeda K., Ichijo H. Thioredoxin and protein kinases in redox signaling. Semin Cancer Biol 2006, 16:427-435.
52. Sakumi K., Furuichi M., Tsuzuki T., Kakuma T., Kawabata S., Maki H., et al. Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-dGTP, a mutagenic substrate for DNA synthesis. J Biol Chem 1993, 268:23524-23530.
53. Callera G.E., Tostes R.C., Yogi A., Montezano A.C., Touyz R.M. Endothelin-1-induced oxidative stress in DOCA-salt hypertension involves NADPH-oxidase-independent mechanisms. Clin Sci (Lond) 2006, 110:243-253.
54. Zhang Y.L., Dong C. MAP kinases in immune responses. Cell Mol Immunol 2005, 2:20-27.
55. Odobasic D., Kitching A.R., Semple T.J., Holdsworth S.R. Endogenous myeloperoxidase promotes neutrophil-mediated renal injury, but attenuates T cell immunity inducing crescentic glomerulonephritis. J Am Soc Nephrol 2007, 18:760-770.
56. Heslop C.L., Frohlich J.J., Hill J.S. Myeloperoxidase and C-reactive protein have combined utility for long-term prediction of cardiovascular mortality after coronary angiography. J Am Coll Cardiol 2010, 55:1102-1109.
57. R.L. Hengel, V. Thaker, R.A. Lempicki, H.C. Lane, Effector CD4 T-cell Myeloperoxidase expression: evidence of innate-type immune molecules in T-cell pools, Antivir Ther 8 (2003) abstract no-382.
58. Klebanoff C.A., Gattinoni L., Torabi-Parizi P., Kerstann K., Cardones A.R., Finkelstein S.E., et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci U S A 2005, 102:9571-9576.
59. Fisfalen M.E., Palmer E.M., Van Seventer G.A., Soltani K., Sawai Y., Kaplan E., et al. Thyrotropin-receptor and thyroid peroxidase-specific T cell clones and their cytokine profile in autoimmune thyroid disease. J Clin Endocrinol Metab 1997, 82:3655-3663.
60. Figueroa-Vega N., Alfonso-Perez M., Benedicto I., Sanchez-Madrid F., Gonzalez-Amaro R., Marazuela M. Increased circulating pro-inflammatory cytokines and Th17 lymphocytes in Hashimoto's thyroiditis. J Clin Endocrinol Metab 2010, 95:953-962.
61. Ohiro Y., Garkavtsev I., Kobayashi S., Sreekumar K.R., Nantz R., Higashikubo B.T., et al. encodes a homologue of the apoptosis-inducing factor (AIF). FEBS Lett 2002, 524:163-171.
62. Muchmore S.W., Sattler M., Liang H., Meadows R.P., Harlan J.E., Yoon H.S., et al. an inhibitor of programmed cell death. Nature 1996, 381:335-341.
63. Aritomi M., Kunishima N., Inohara N., Ishibashi Y., Ohta S., Morikawa K., et al. J Biol Chem 1997, 272:27886-27892.
64. Lee M., Hyun D.H., Marshall K.A., Ellerby L.M., Bredesen D.E., Jenner P., et al. Effect of overexpression of BCL-2 on cellular oxidative damage, nitric oxide production, antioxidant defenses, and the proteasome. Free Radic Biol Med 2001, 31:1550-1559.
65. Voehringer D.W., Meyn R.E. Redox aspects of Bcl-2 function. Antioxid Redox Signal 2000, 2:537-550.
66. Voehringer D.W. BCL-2 and glutathione: alterations in cellular redox state that regulate apoptosis sensitivity. Free Radic Biol Med 1999, 27:945-950.
67. Voehringer D.W., McConkey D.J., McDonnell T.J., Brisbay S., Meyn R.E. Bcl-2 expression causes redistribution of glutathione to the nucleus. Proc Natl Acad Sci U S A 1998, 95:2956-2960.
68. Bojes H.K., Datta K., Xu J., Chin A., Simonian P., Nunez G., et al. Biochem J 1997, 325(Pt 2):315-319.
69. Mueller Y.M., Bojczuk P.M., Halstead E.S., Kim A.H., Witek J., Altman J.D., et al. IL-15 enhances survival and function of HIV-specific CD8+ T cells. Blood 2003, 101:1024-1029.
70. Petrovas C., Mueller Y.M., Dimitriou I.D., Bojczuk P.M., Mounzer K.C., Witek J., et al. HIV-specific CD8+ T cells exhibit markedly reduced levels of Bcl-2 and Bcl-xL. J Immunol 2004, 172:4444-4453.
71. C. Dong and R. A. Flavell, Control of T helper cell differentiation--in search of master genes, Sci STKE 2000 (2000) pe1.
72. Green D., Kroemer G. The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol 1998, 8:267-271.
73. Hildeman D.A., Mitchell T., Teague T.K., Henson P., Day B.J., Kappler J., et al. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 1999, 10:735-744.
74. Rothe G., Valet G. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine 2',7'-dichlorofluorescin. J Leukoc Biol 1990, 47:440-448.
75. Pouw N., Treffers-Westerlaken E., Kraan J., Wittink F., Ten Hagen T., Verweij J., et al. Combination of IL-21 and IL-15 enhances tumour-specific cytotoxicity and cytokine production of TCR-transduced primary T cells. Cancer Immunol Immunother 2010, 59:921-931.
76. Yang L. TGFbeta, a potent regulator of tumor microenvironment host immune response, implication for therapy. Curr Mol Med 2010, 10:374-380.
77. Yan Z., Banerjee R. Redox remodeling as an immunoregulatory strategy. Biochemistry 2010, 49:1059-1066.
78. Checker R., Sharma D., Sandur S.K., Subrahmanyam G., Krishnan S., Poduval T.B., et al. Plumbagin inhibits proliferative and inflammatory responses of T cells independent of ROS generation but by modulating intracellular thiols. J Cell Biochem 2010, 110:1082-1093.
79. Hoffmann F.W., Hashimoto A.C., Shafer L.A., Dow S., Berry M.J., Hoffmann P.R. Dietary selenium modulates activation and differentiation of CD4+ T cells in mice through a mechanism involving cellular free thiols. J Nutr 2010, 140:1155-1161.
80. Haddad J.J., Fahlman C.S. Redox-oxidant-mediated regulation of interleukin-10: ananti-inflammatory, antioxidant cytokine?. Biochem Biophys Res Commun 2002, 297:163-176.
81. Hellstrand K., Brune M., Dahlgren C., Hansson M., Hermodsson S., Lindner P., et al. Alleviating oxidative stress in cancer immunotherapy: a role for histamine?. Med Oncol 2000, 17:258-269.
82. Li-Weber M., Weigand M.A., Giaisi M., Suss D., Treiber M.K., Baumann S., et al. Vitamin E inhibits CD95 ligand expression and protects T cells from activation-induced cell death. J Clin Invest 2002, 110:681-690.
83. Jariwalla R.J., Lalezari J., Cenko D., Mansour S.E., Kumar A., Gangapurkar B., et al. Restoration of blood total glutathione status and lymphocyte function following alpha-lipoic acid supplementation in patients with HIV infection. J Altern Complement Med 2008, 14:139-146.
84. Trachootham D., Lu W., Ogasawara M.A., Nilsa R.D., Huang P. Redox regulation of cell survival. Antioxid Redox Signal 2008, 10:1343-1374.