Preferential cell death of CD8+ effector memory (CCR7 -CD45RA-) T cells by hydrogen peroxide-induced oxidative stress

Journal of Immunology

Volumn 174, Issue 10, 2005, Pages 6080-6087

  Takahashi, Akihiro ^a   Hanson, Mikael G V ^a   Norell, Håkan R ^a   Havelka, Aleksandra Mandic ^a   Kono, Koji ^b   Malmberg, Karl Johan ^c   Kiessling, Rolf V R ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF YAMANASHI   (Japan)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR7; HYDROGEN PEROXIDE;

ADOPTIVE TRANSFER; ARTICLE; CELL DEATH; CELL POLARITY; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MEMORY CELL; MITOCHONDRIAL RESPIRATION; NORMAL HUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

EID: 18644362802     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.10.6080     Document Type: Article

References (58)

1. 2 production during the respiratory burst in alveolar macrophages. Adv. Exp. Med. Biol. 121: 53-74.
2. Dahlgren, C., and A. Karlsson. 1999. Respiratory burst in human neutrophils. J. Immunol. Methods 232: 3-14.
3. Hohmeier, H. E., V. V. Tran, G. Chen, R. Gasa, and C. B. 2003. Newgard. Inflammatory mechanisms in diabetes: lessons from the β-cell. Int. J. Obes. Relat. Metab. Disord. 27(Suppl. 3): S12-S16.
4. Patel, M., B. J. Day, J. D. Crapo, I. Fridovich, and J. O. McNamara. 1996. Requirement for superoxide in excitotoxic cell death. Neuron 16: 345-355.
5. Buttke, T. M., and P. A. Sandstrom. 1995. Redox regulation of programmed cell death in lymphocytes. Free Radical Res. 11: 389-397.
6. Flescher, E., J. A. Ledbetter, G. L. Schieven, N. Vela-Roch, D. Fossum, H. Dang, N. Ogawa, and N. Talal. 1994. Longitudinal exposure of human T lymphocytes to weak oxidative stress suppresses transmembrane and nuclear signal transduction. J. Immunol. 153: 4880-4889.
7. Flescher, E., H. Tripoli, K. Salnikow, and F. J. Burns. 1998. Oxidative stress suppresses transcription factor activities in stimulated lymphocytes. Clin. Exp. Immunol. 112: 242-247.
8. Lahdenpohja, N., K. Savinainen, and M. Hurme. 1998. Pre-exposure to oxidative stress decreases the nuclear factor-κB-dependent transcription in T lymphocytes. J. Immunol. 160: 1354-1358.
9. +) T cells by oxidative stress associated with block of NF-κB activation. J. Immunol. 167: 2595-2601.
10. Gringhuis, S. I., A. Leow, E. A. Papendrecht-Van Der Voort, P. H. Remans, F. C. Breedveld, and C. L. Verweij. 2000. Displacement of linker for activation of T cells from the plasma membrane due to redox balance alterations results in hyporesponsiveness of synovial fluid T lymphocytes in rheumatoid arthritis. J. Immunol. 164: 2170-2179.
11. Maurice, M. M., A. C. Lankester, A. C. Bezemer, M. F. Geertsma, P. P. Tak, F. C. Breedveld, R. A. van Lier, and C. L. Verweij. 1997. Defective TCR-mediated signaling in synovial T cells in rheumatoid arthritis. J. Immunol. 159: 2973-2978.
12. Verweij, C. L., and S. I. Gringhuis. 2002. Oxidants and tyrosine phosphorylation: role of acute and chronic oxidative stress in T- and B-lymphocyte signaling. Antioxid. Redox Signal. 4: 543-551.
13. Dobmeyer, T. S., S. Findhammer, J. M. Dobmeyer, S. A. Klein, B. Raffel, D. Hoelzer, E. B. Helm, D. Kabelitz, and R. Rossol. 1997. Ex vivo induction of apoptosis in lymphocytes is mediated by oxidative stress: role for lymphocyte loss in HIV infection. Free Radical Biol. Med. 22: 775-785.
14. Schmielau, J., and O. J. Finn. 2001. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res. 61: 4756-4760.
15. Malmberg, K. J. 2004. Effective immunotherapy against cancer: a question of overcoming immune suppression and immune escape? Cancer Immunol. Immunother. 53: 879-892.
16. Aoe, T., Y. Okamoto, and T. Saito. 1995. Activated macrophages induce structural abnormalities of the T cell receptor-CD3 complex. J. Exp. Med. 181: 1881-1886.
17. 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.
18. 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 cell-mediated cytotoxicity. Eur. J. Immunol. 26: 1308-1313.
19. Hansson, M., A. Asea, U. Ersson, S. Hermodsson, and K. Hellstrand. 1996. Induction of apoptosis in NK cells by monocyte-derived reactive oxygen metabolites. J. Immunol. 156: 42-47.
20. Bingisser, R. M., P. A. Tilbrook, P. G. Holt, and U. R. Kees. 1998. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J. Immunol. 160: 5729-5734.
21. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
22. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
23. Hildeman, D. A., T. Mitchell, T. K. Teague, P. Henson, B. J. Day, J. Kappler, and P. C. Marrack. 1999. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10: 735-744.
24. Tran, V. V., G. Chen, C. B. Newgard, and H. E. Hohmeier. 2003. Discrete and complementary mechanisms of protection of β-cells against cytokine-induced and oxidative damage achieved by bcl-2 overexpression and a cytokine selection strategy. Diabetes 52: 1423-1432.
25. Fadeel, B., A. Ahlin, J. I. Henter, S. Orrenius, and M. B. Hampton. 1998. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 92: 4808-4818.
26. Hampton, M. B., and S. Orrenius. 1997. Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett. 414: 552-556.
27. Duraont, A., S. P. Hehner, T. G. Hofmann, M. Ueffing, W. Droge, and M. L. Schmitz. 1999. Hydrogen peroxide-induced apoptosis is CD95-independent, requires the release of mitochondria-derived reactive oxygen species and the activation of NF-κB. Oncogene 18: 747-757.
28. Stridh, H., M. Kimland, D. P. Jones, S. Orrenius, and M. B. Hampton. 1998. Cytochrome c release and caspase activation in hydrogen peroxide- and tributyltin-induced apoptosis. FEBS Lett. 429: 351-355.
29. Zoratti, M., and I. Szabo. 1995. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241: 139-176.
30. Sade, H., and A. Sarin. 2004. Reactive oxygen species regulate quiescent T-cell apoptosis via the BH3-only proapoptotic protein BIM. Cell Death Differ. 11: 416-423.
31. Yokoyama, T., M. Tanahashi, Y. Kobayashi, Y. Yamakawa, M. Maeda, T. Inaba, M. Kiriyama, I. Fukai, and Y. Fujii. 2002. The expression of Bcl-2 family proteins (Bcl-2, Bcl-x, Bax, Bak and Bim) in human lymphocytes. Immunol. Lett. 81: 107-113.
32. Akbar, A. N., N. Borthwick, M. Salmon, W. Gombert, M. Bofill, N. Shamsadeen, D. Pilling, S. Pett, J. E. Grundy, and G. Janossy. 1993. The significance of low bcl-2 expression by CD45RO T cells in normal individuals and patients with acute viral infections: the role of apoptosis in T cell memory. J. Exp. Med. 178: 427-438.
33. Hildeman, D. A., Y. Zhu, T. C. Mitchell, P. Bouillet, A. Strasser, J. Kappler, and P. Marrack. 2002. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 16: 759-767.
34. Salmon, M., D. Pilling, N. J. Borthwick, N. Viner, G. Janossy, P. A. Bacon, and A. N. Akbar. 1994. The progressive differentiation of primed T cells is associated with an increasing susceptibility to apoptosis. Eur. J. Immunol. 24: 892-899.
35. Mitchell, T., J. Kappler, and P. Marrack. 1999. Bystander virus infection prolongs activated T cell survival. J. Immunol. 162: 4527-4535.
36. + T cells. J. Immunol. 164: 3950-3954.
37. L. Mol. Cell. Biol. 20: 2687-2695.
38. Grumont, R. J., I. J. Rourke, and S. Gerondakis. 1999. Rel-dependent induction of A1 transcription is required to protect B cells from antigen receptor ligation-induced apoptosis. Genes Dev. 13: 400-411.
39. + lymphocytes. J. Immunol. 165: 1743-1754.
40. Wang, C. Y., D. C. Guttridge, M. W. Mayo, and A. S. Baldwin, Jr. 1999. NF-κB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 19: 5923-5929.
41. Zong, W. X., L. C. Edelstein, C. Chen, J. Bash, and C. Gelinas. 1999. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-κB that blocks TNFα-induced apoptosis. Genes Dev. 13: 382-387.
42. Zea, A. H., M. T. Ochoa, P. Ghosh, D. L. Longo, W. G. Alvord, L. Valderrama, R, Falabella, L. K. Harvey, N. Saravia, L. H. Moreno, and A. C. Ochoa. 1998. Changes in expression of signal transduction proteins in T lymphocytes of patients with leprosy. Infect. Immun. 66: 499-504.
43. Trimble, L. A., and J. Lieberman. 1998. Circulating CD8 T lymphocytes in human immunodeficiency virus-infected individuals have impaired function and downmodulate CD3 ζ, the signaling chain of the T-cell receptor complex. Blood 91: 585-594.
44. Nakagomi, H., M. Petersson, I. Magnusson, C. Juhlin, M. Matsuda, H. Mellstedt, J. L. Taupin, E. Vivier, P. Anderson, and R. Kiessling. 1993. Decreased expression of the signal-transducing ζ chains in tumor-infiltrating T-cells and NK cells of patients with colorectal carcinoma. Cancer Res. 53: 5610-5612.
45. 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.
46. Lai, P., H. Rabinowich, P. A. Crowley-Nowick, M. C. Bell, G. Mantovani, and T. L. Whiteside. 1996. Alterations in expression and function of signal-transducing proteins in tumor-associated T and natural killer cells in patients with ovarian carcinoma. Clin. Cancer Res. 2: 161-173.
47. 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.
48. Kurt, R. A., W. J. Urba, J. W. Smith, and D. D. Schoof. 1998. Peripheral T lymphocytes from women with breast cancer exhibit abnormal protein expression of several signaling molecules. Int. J. Cancer 78: 16-20.
49. 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.
50. + T cells of patients with squamous cell carcinoma of the head and neck. Clin. Cancer Res. 10: 5101-5110.
51. + T lymphocytes in peripheral blood of patients with advanced melanoma. Clin. Cancer Res. 6: 1351-1364.
52. 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.
53. Bronstein-Sitton, N., L. Cohen-Daniel, I. Vaknin, A. V. Ezernitchi, B. Leshem, A. Halabi, Y. Houri-Hadad, E. Greenbaum, Z. Zakay-Rones, L. Shapira, and M. Baniyash. 2003. Sustained exposure to bacterial antigen induces interferon-γ-independent T cell receptor γ down-regulation and impaired T cell function. Nat. Immunol. 4: 957-964.
54. + T cells. Blood 96: 3838-3846.
55. Almand, B., J. I. Clark, E. Nikitina, J. van Beynen, N. R. English, S. C. Knight, D. P. Carbone, and D. I. Gabrilovich. 2001. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 166: 678-689.
56. 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.
57. + tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105: 241-250.
58. 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.