Transduction with the antioxidant enzyme catalase protects human T cells against oxidative stress

Journal of Immunology

Volumn 181, Issue 12, 2008, Pages 8382-8390

  Ando, Takashi ^a   Mimura, Kousaku ^a   Johansson, C Christian ^a   Hanson, Mikael G ^a   Mougiakakos, Dimitrios ^a   Larsson, Charlotte ^a   Da Palma, Telma Martins ^a,b   Sakurai, Daiju ^a   Norell, Håkan ^a,b   Li, Mingli ^b   Nishimura, Michael I ^b   Kiessling, Rolf ^a  

^a Cancer Centre Karolinska   (Sweden)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; CATALASE; HYDROGEN PEROXIDE; ANTIOXIDANT; CYTOKINE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL PROTECTION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; GENETIC TRANSDUCTION; GRANULOCYTE; HUMAN; HUMAN CELL; NORMAL HUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; BIOSYNTHESIS; CELL CULTURE; CELL LINE; CELL PROLIFERATION; CYTOLOGY; ENZYMOLOGY; GENE VECTOR; GENETICS; IMMUNOLOGY; METABOLISM; RETROVIRUS;

ANTIOXIDANTS; CATALASE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DEATH; CELL LINE; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; GENETIC VECTORS; HUMANS; HYDROGEN PEROXIDE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RETROVIRIDAE; TRANSDUCTION, GENETIC;

EID: 58849100439     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.12.8382     Document Type: Article

References (75)

1. Baniyash, M. 2006. Chronic inflammation, immunosuppression and cancer: new insights and outlook. Semin. Cancer Biol. 16: 80-88.
2. + T cell tolerance in cancer. Nat. Med. 13: 828-835.
3. Kiessling, R., K. Wasserman, S. Horiguchi, K. Kono, J. Sjoberg, P. Pisa, and M. Petersson. 1999. Tumor-induced immune dysfunction. Cancer Immunol. Immunother. 48: 353-362.
4. Matsuda, M., M. Petersson, R. Lenkei, J. L. Taupin, I. Magnusson, H. Mellstedt, P. Anderson, and R. Kiessling. 1995. Alterations in the signal-transducing molecules of T cells and NK cells in colorectal tumor-infiltrating, gut mucosal and peripheral lymphocytes: correlation with the stage of the disease. Int. J. Cancer 61: 765-772.
5. Schmielau, J., and O. J. Finn. 2001. Activated granulocytes and granulocytederived hydrogen peroxide are the underlying mechanism of suppression of Tcell function in advanced cancer patients. Cancer Res. 61: 4756-4760.
6. Young, R. C., M. P. Corder, H. A. Haynes, and V. T. DeVita. 1972. Delayed hypersensitivity in Hodgkin's disease: a study of 103 untreated patients. Am. J. Med. 52: 63-72.
7. Horiguchi, S., M. Petersson, T. Nakazawa, M. Kanda, A. H. Zea, A. C. Ochoa, and R. Kiessling. 1999. Primary chemically induced tumors induce profound immunosuppression concomitant with apoptosis and alterations in signal transduction in T cells and NK cells. Cancer Res. 59: 2950-2956. (Pubitemid 29283137)
8. Alexander, J. P., S. Kudoh, K. A. Melsop, T. A. Hamilton, M. G. Edinger, R. R. Tubbs, D. Sica, L. Tuason, E. Klein, R. M. Bukowski, et al. 1993. T-cells infiltrating renal cell carcinoma display a poor proliferative response even though they can produce interleukin 2 and express interleukin 2 receptors. Cancer Res. 53: 1380-1387.
9. Heriot, A. G., J. B. Marriott, S. Cookson, D. Kumar, and A. G. Dalgleish. 2000. Reduction in cytokine production in colorectal cancer patients: association with stage and reversal by resection. Br. J. Cancer 82: 1009-1012.
10. Miescher, S., M. Stoeck, L. Qiao, C. Barras, L. Barrelet, and V. von Fliedner. 1988. Preferential clonogenic deficit of CD8-positive T-lymphocytes infiltrating human solid tumors. Cancer Res. 48: 6992-6998.
11. Wang, Q., C. Redovan, R. Tubbs, T. Olencki, E. Klein, S. Kudoh, J. Finke, and R. M. Bukowski. 1995. Selective cytokine gene expression in renal cell carcinoma tumor cells and tumor-infiltrating lymphocytes. Int. J. Cancer 61: 780-785.
12. Buggins, A. G., W. J. Hirst, A. Pagliuca, and G. J. Mufti. 1998. Variable expression of CD3-ζ and associated protein tyrosine kinases in lymphocytes from patients with myeloid malignancies. Br. J. Haematol. 100: 784-792.
13. Matsuda, M., A. K. Ulfgren, R. Lenkei, M. Petersson, A. C. Ochoa, S. Lindblad, P. Andersson, L. Klareskog, and R. Kiessling. 1998. Decreased expression of signal-transducing CD3 ζ chains in T cells from the joints and peripheral blood of rheumatoid arthritis patients. Scand. J. Immunol. 47: 254-262. (Pubitemid 28153403)
14. Bukowski, R. M., P. Rayman, R. Uzzo, T. Bloom, K. Sandstrom, D. Peereboom, T. Olencki, G. T. Budd, D. McLain, P. Elson, et al. 1998. Signal transduction abnormalities in T lymphocytes from patients with advanced renal carcinoma: clinical relevance and effects of cytokine therapy. Clin. Cancer Res. 4: 2337-2347.
15. Gunji, Y., S. Hori, T. Aoe, T. Asano, T. Ochiai, K. Isono, and T. Saito. 1994. High frequency of cancer patients with abnormal assembly of the T cell receptor- CD3 complex in peripheral blood T lymphocytes. Jpn. J. Cancer Res. 85: 1189-1192.
16. Kono, K., M. E. Ressing, R. M. Brandt, C. J. Melief, R. K. Potkul, B. Andersson, M. Petersson, W. M. Kast, and R. Kiessling. 1996. Decreased expression of signal-transducing ζ chain in peripheral T cells and natural killer cells in patients with cervical cancer. Clin. Cancer Res. 2: 1825-1828.
17. Ling, W., P. Rayman, R. Uzzo, P. Clark, H. J. Kim, R. Tubbs, A. Novick, R. Bukowski, T. Hamilton, and J. Finke. 1998. Impaired activation of NFκB in T cells from a subset of renal cell carcinoma patients is mediated by inhibition of phosphorylation and degradation of the inhibitor, IκBα. Blood 92: 1334-1341. (Pubitemid 28369047)
18. Rossi, E., E. Matutes, R. Morilla, K. Owusu-Ankomah, A. M. Heffernan, and D. Catovsky. 1996. ζ chain and CD28 are poorly expressed on T lymphocytes from chronic lymphocytic leukemia. Leukemia 10: 494-497.
19. Uzzo, R. G., P. E. Clark, P. Rayman, T. Bloom, L. Rybicki, A. C. Novick, R. M. Bukowski, and J. H. Finke. 1999. Alterations in NFκB activation in T lymphocytes of patients with renal cell carcinoma. J. Natl. Cancer Inst. 91: 718-721.
20. Saito, T., I. Kuss, G. Dworacki, W. Gooding, J. T. Johnson, and T. L. Whiteside. 1999. Spontaneous ex vivo apoptosis of peripheral blood mononuclear cells in patients with head and neck cancer. Clin. Cancer Res. 5: 1263-1273. (Pubitemid 29282928)
21. Kuss, I., T. Saito, J. T. Johnson, and T. L. Whiteside. 1999. Clinical significance of decreased ζ chain expression in peripheral blood lymphocytes of patients with head and neck cancer. Clin. Cancer Res. 5: 329-334. (Pubitemid 29085186)
22. Mulder, W. M., E. Bloemena, M. J. Stukart, J. A. Kummer, J. Wagstaff, and R. J. Scheper. 1997. T cell receptor-ζ and granzyme B expression in mononuclear cell infiltrates in normal colon mucosa and colon carcinoma. Gut 40: 113-119.
23. Reichert, T. E., R. Day, E. M. Wagner, and T. L. Whiteside. 1998. Absent or low expression of the ζ chain in T cells at the tumor site correlates with poor survival in patients with oral carcinoma. Cancer Res. 58: 5344-5347.
24. Gastman, B. R., D. E. Johnson, T. L. Whiteside, and H. Rabinowich. 1999. Caspase-mediated degradation of T-cell receptor ζ-chain. Cancer Res. 59: 1422-1427. (Pubitemid 29160103)
25. Bingisser, R. M., P. A. Tilbrook, P. G. Holt, and U. R. Kees. 1998. Macrophagederived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J. Immunol. 160: 5729-5734.
26. Uzzo, R. G., P. Rayman, V. Kolenko, P. E. Clark, M. K. Cathcart, T. Bloom, A. C. Novick, R. M. Bukowski, T. Hamilton, and J. H. Finke. 1999. Renal cell carcinoma-derived gangliosides suppress nuclear factor-κB activation in T cells. J. Clin. Invest. 104: 769-776.
27. Taheri, F., J. B. Ochoa, Z. Faghiri, K. Culotta, H. J. Park, M. S. Lan, A. H. Zea, and A. C. Ochoa. 2001. L-Arginine regulates the expression of the T-cell receptor ζ chain (CD3ζ) in Jurkat cells. Clin. Cancer Res. 7: 958s-965s.
28. Muller, A. J., and G. C. Prendergast. 2007. Indoleamine 2,3-dioxygenase in immune suppression and cancer. Curr. Cancer Drug Targets 7: 31-40. (Pubitemid 46345506)
29. Otsuji, M., Y. Kimura, T. Aoe, Y. Okamoto, and T. Saito. 1996. Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 ζ chain of T-cell receptor complex and antigen-specific T-cell responses. Proc. Natl. Acad. Sci. USA 93: 13119-13124.
30. Kono, K., F. Salazar-Onfray, M. Petersson, J. Hansson, G. Masucci, K. Wasserman, T. Nakazawa, P. Anderson, and R. Kiessling. 1996. Hydrogen peroxide secreted by tumor-derived macrophages down-modulates signal-transducing ζ molecules and inhibits tumor-specific T cell-and natural killer cellmediated cytotoxicity. Eur. J. Immunol. 26: 1308-1313. (Pubitemid 126487439)
31. Malmberg, K. J., V. Arulampalam, F. Ichihara, M. Petersson, K. Seki, T. Andersson, R. Lenkei, G. Masucci, S. Pettersson, and R. Kiessling. 2001. Inhibition of activated/memory (CD45RO+) T cells by oxidative stress associated with block of NF-κB activation. J. Immunol. 167: 2595-2601.
32. Bhattacharyya, S., D. Mandal, G. S. Sen, S. Pal, S. Banerjee, L. Lahiry, J. H. Finke, C. S. Tannenbaum, T. Das, and G. Sa. 2007. Tumor-induced oxidative stress perturbs nuclear factor-κB activity-augmenting tumor necrosis factor-α-mediated T-cell death: protection by curcumin. Cancer Res. 67: 362-370.
33. Ghosh, P., A. Sica, H. A. Young, J. Ye, J. L. Franco, R. H. Wiltrout, D. L. Longo, N. R. Rice, and K. L. Komschlies. 1994. Alterations in NFκB/Rel family proteins in splenic T-cells from tumor-bearing mice and reversal following therapy. Cancer Res. 54: 2969-2972.
34. Liu, W., M. Kato, M. Itoigawa, H. Murakami, M. Yajima, J. Wu, N. Ishikawa, and I. Nakashima. 2001. Distinct involvement of NF-κB and p38 mitogen-activated protein kinase pathways in serum deprivation-mediated stimulation of inducible nitric oxide synthase and its inhibition by 4-hydroxynonenal. J. Cell Biochem. 83: 271-280.
35. Hattori, Y., S. Hattori, and K. Kasai. 2001. 4-hydroxynonenal prevents NO production in vascular smooth muscle cells by inhibiting nuclear factor-κB-dependent transcriptional activation of inducible NO synthase. Arterioscler. Thromb. Vascular Biol. 21: 1179-1183. (Pubitemid 34215147)
36. Chrobot, A. M., A. Szaflarska-Szczepanik, and G. Drewa. 2000. Antioxidant defense in children with chronic viral hepatitis B and C. Med. Sci. Monit. 6: 713-718. (Pubitemid 30682608)
37. Staal, F. J., S. W. Ela, M. Roederer, M. T. Anderson, L. A. Herzenberg, and L. A. Herzenberg. 1992. Glutathione deficiency and human immunodeficiency virus infection. Lancet 339: 909-912.
38. Riddell, S. R., and P. D. Greenberg. 1990. The use of anti-CD3 and anti-CD28 monoclonal antibodies to clone and expand human antigen-specific T cells. J. Immunol. Methods 128: 189-201.
39. Werner, E. 2003. Determination of cellular H2O2 production. Sci STKE 2003: PL3.
40. Kusmartsev, S., Y. Nefedova, D. Yoder, and D. I. Gabrilovich. 2004. Antigenspecific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172: 989-999. (Pubitemid 38113758)
41. Kirkman, H. N., and G. F. Gaetani. 2007. Mammalian catalase: a venerable enzyme with new mysteries. Trends Biochem. Sci. 32: 44-50.
42. -) T cells by hydrogen peroxide-induced oxidative stress. J. Immunol. 174: 6080-6087.
43. Thoren, F. B., A. I. Romero, and K. Hellstrand. 2006. Oxygen radicals induce poly(ADP-ribose) polymerase-dependent cell death in cytotoxic lymphocytes. J. Immunol. 176: 7301-7307.
44. Dudley, M. E., and S. A. Rosenberg. 2003. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat. Rev. 3: 666-675.
45. Foster, A. E., and C. M. Rooney. 2006. Improving T cell therapy for cancer. Exp. Opin. Biol. Ther. 6: 215-229.
46. Gustafsson, A., V. Levitsky, J. Z. Zou, T. Frisan, T. Dalianis, P. Ljungman, O. Ringden, J. Winiarski, I. Ernberg, and M. G. Masucci. 2000. Epstein-Barr virus (EBV) load in bone marrow transplant recipients at risk to develop posttransplant lymphoproliferative disease: prophylactic infusion of EBV-specific cytotoxic T cells. Blood 95: 807-814.
47. Cinatl, J., Jr., J. U. Vogel, R. Kotchetkov, M. Scholz, and H. W. Doerr. 1999. Proinflammatory potential of cytomegalovirus infection. specific inhibition of cytomegalovirus immediate-early expression in combination with antioxidants as a novel treatment strategy? Intervirology 42: 419-424.
48. Stehbens, W. E. 2004. Oxidative stress in viral hepatitis and AIDS. Exp. Mol. Pathol. 77: 121-132.
49. Evans, L. S., P. R. Witte, A. L. Feldhaus, B. H. Nelson, S. R. Riddell, P. D. Greenberg, S. D. Lupton, and L. A. Jones. 1999. Expression of chimeric granulocyte-macrophage colony-stimulating factor/interleukin 2 receptors in human cytotoxic T lymphocyte clones results in granulocyte-macrophage colonystimulating factor-dependent growth. Hum. Gene Ther. 10: 1941-1951.
50. + memory effector T cells reconstitutes antigen-induced IL-2 production. J. Exp. Med. 198: 947-955.
51. Rufer, N., M. Migliaccio, J. Antonchuk, R. K. Humphries, E. Roosnek, and P. M. Lansdorp. 2001. Transfer of the human telomerase reverse transcriptase (TERT) gene into T lymphocytes results in extension of replicative potential. Blood 98: 597-603.
52. Clay, T. M., M. C. Custer, J. Sachs, P. Hwu, S. A. Rosenberg, and M. I. Nishimura. 1999. Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J. Immunol. 163: 507-513.
53. Test, S. T., and S. J. Weiss. 1984. Quantitative and temporal characterization of the extracellular H2O2 pool generated by human neutrophils. J. Biol. Chem. 259: 399-405.
54. Danel, C., S. C. Erzurum, P. Prayssac, N. T. Eissa, R. G. Crystal, P. Herve, B. Baudet, M. Mazmanian, and P. Lemarchand. 1998. Gene therapy for oxidant injury-related diseases: adenovirus-mediated transfer of superoxide dismutase and catalase cDNAs protects against hyperoxia but not against ischemia-reperfusion lung injury. Hum. Gene Ther. 9: 1487-1496. (Pubitemid 28379088)
55. Benhamou, P. Y., C. Moriscot, M. J. Richard, O. Beatrix, L. Badet, F. Pattou, J. Kerr-Conte, J. Chroboczek, P. Lemarchand, and S. Halimi. 1998. Adenovirusmediated catalase gene transfer reduces oxidant stress in human, porcine and rat pancreatic islets. Diabetologia 41: 1093-1100. (Pubitemid 28394416)
56. Mann, H., M. T. McCoy, J. Subramaniam, H. Van Remmen, and J. L. Cadet. 1997. Overexpression of superoxide dismutase and catalase in immortalized neural cells: toxic effects of hydrogen peroxide. Brain Res. 770: 163-168. (Pubitemid 27468063)
57. Heslop, H. E., C. Y. Ng, C. Li, C. A. Smith, S. K. Loftin, R. A. Krance, M. K. Brenner, and C. M. Rooney. 1996. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virusspecific T lymphocytes. Nat. Med. 2: 551-555.
58. Rooney, C. M., C. A. Smith, C. Y. Ng, S. K. Loftin, J. W. Sixbey, Y. Gan, D. K. Srivastava, L. C. Bowman, R. A. Krance, M. K. Brenner, and H. E. Heslop. 1998. Infusion of cytotoxic T cells for the prevention and treatment of Epstein- Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 92: 1549-1555.
59. Dudley, M. E., J. R. Wunderlich, P. F. Robbins, J. C. Yang, P. Hwu, D. J. Schwartzentruber, S. L. Topalian, R. Sherry, N. P. Restifo, A. M. Hubicki, et al. 2002. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854.
60. Sznol, M., J. P. Dutcher, M. B. Atkins, A. R. Rayner, K. A. Margolin, E. R. Gaynor, G. R. Weiss, F. Aronson, D. R. Parkinson, and M. J. Hawkins. 1989. Review of interleukin-2 alone and interleukin-2/LAK clinical trials in metastatic malignant melanoma. Cancer Treat. Rev. 16(Suppl. A): 29-38. (Pubitemid 19231450)
61. June, C. H. 2007. Principles of adoptive T cell cancer therapy. J. Clin. Invest. 117: 1204-1212. (Pubitemid 46718405)
62. June, C. H. 2007. Adoptive T cell therapy for cancer in the clinic. J. Clin. Invest. 117: 1466-1476.
63. Rabinovich, G. A., D. Gabrilovich, and E. M. Sotomayor. 2007. Immunosuppressive strategies that are mediated by tumor cells. Ann. Rev. Immunol. 25: 267-296.
64. Brune, M., S. Castaigne, J. Catalano, K. Gehlsen, A. D. Ho, W. K. Hofmann, D. E. Hogge, B. Nilsson, R. Or, A. I. Romero, et al. 2006. Improved leukemiafree survival after postconsolidation immunotherapy with histamine dihydrochloride and interleukin-2 in acute myeloid leukemia: results of a randomized phase 3 trial. Blood 108: 88-96. (Pubitemid 43996626)
65. Hellstrand, K., A. Asea, C. Dahlgren, and S. Hermodsson. 1994. Histaminergic regulation of NK cells: tole of monocyte-derived reactive oxygen metabolites. J. Immunol. 153: 4940-4947. (Pubitemid 24356125)
66. Gallina, G., L. Dolcetti, P. Serafini, C. De Santo, I. Marigo, M. P. Colombo, G. Basso, F. Brombacher, I. Borrello, P. Zanovello, et al. 2006. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 116: 2777-2790. (Pubitemid 44511641)
67. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5: 641-654. (Pubitemid 41113195)
68. Bronte, V., P. Serafini, C. De Santo, I. Marigo, V. Tosello, A. Mazzoni, D. M. Segal, C. Staib, M. Lowel, G. Sutter, et al. 2003. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J. Immunol. 170: 270-278. (Pubitemid 36026149)
69. De Santo, C., P. Serafini, I. Marigo, L. Dolcetti, M. Bolla, P. Del Soldato, C. Melani, C. Guiducci, M. P. Colombo, M. Iezzi, et al. 2005. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc. Natl. Acad. Sci. USA 102: 4185-4190. (Pubitemid 40388577)
70. Kusmartsev, S., and D. I. Gabrilovich. 2005. STAT1 signaling regulates tumorassociated macrophage-mediated T cell deletion. J. Immunol. 174: 4880-4891.
71. Brys, L., A. Beschin, G. Raes, G. H. Ghassabeh, W. Noel, J. Brandt, F. Brombacher, and P. De Baetselier. 2005. Reactive oxygen species and 12/15- lipoxygenase contribute to the antiproliferative capacity of alternatively activated myeloid cells elicited during helminth infection. J. Immunol. 174: 6095-6104. (Pubitemid 40663798)
72. Hanson, M. G., V. Ozenci, M. C. Carlsten, B. L. Glimelius, J. E. Frodin, G. Masucci, K. J. Malmberg, and R. V. Kiessling. 2007. A short-term dietary supplementation with high doses of vitamin E increases NK cell cytolytic activity in advanced colorectal cancer patients. Cancer Immunol. Immunother. 56: 973-984.
73. Malmberg, K. J., R. Lenkei, M. Petersson, T. Ohlum, F. Ichihara, B. Glimelius, J. E. Frodin, G. Masucci, and R. Kiessling. 2002. A short-term dietary supplementation of high doses of vitamin E increases T helper 1 cytokine production in patients with advanced colorectal cancer. Clin. Cancer Res. 8: 1772-1778.
74. Gattinoni, L., D. J. Powell, Jr., S. A. Rosenberg, and N. P. Restifo. 2006. Adoptive immunotherapy for cancer: building on success. Nat. Rev. Immunol. 6: 383-393.
75. + tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105: 241-250.