Autophagy plays a protective role as an anti-oxidant system in human T cells and represents a novel strategy for induction of T-cell apoptosis

European Journal of Immunology

Volumn 44, Issue 8, 2014, Pages 2508-2520

  Watanabe, Ryu ^a   Fujii, Hiroshi ^a   Shirai, Tsuyoshi ^a   Saito, Shinichiro ^a   Ishii, Tomonori ^a   Harigae, Hideo ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Autophagy; Human T cell; Mitophagy; Reactive oxygen species

Indexed keywords

PEROXIREDOXIN 1; RETROVIRUS VECTOR;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CD4+ T LYMPHOCYTE; CELL DEATH; CONFOCAL MICROSCOPY; FLOW CYTOMETRY; FLUORESCENCE; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; JURKAT CELL LINE; MEMORY T LYMPHOCYTE; MITOCHONDRIAL VOLUME; MITOPHAGY; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN LIGHT CHAIN 3; PROTEIN STRUCTURE; RESPIRATORY CHAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; WESTERN BLOTTING;

APOPTOSIS; AUTOPHAGY; HUMAN T CELL; MITOPHAGY; REACTIVE OXYGEN SPECIES;

ANTIOXIDANTS; APOPTOSIS; AUTOPHAGY; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; GENETIC VECTORS; HUMANS; LEUKOCYTES, MONONUCLEAR; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; RETROVIRIDAE;

EID: 84906084611     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344248     Document Type: Article

References (34)

1. Mizushima, N. and Komatsu, M., Autophagy: renovation of cells and tissues. Cell 2011. 147: 728-741.
2. Mizushima, N., Yoshimori, T. and Levine, B., Methods in mammalian autophagy research. Cell 2010. 140: 313-326.
3. Klionsky, D. J., The autophagy connection. Dev. Cell 2010. 19: 11-12.
4. Kuballa, P., Nolte, W. M., Castoreno, A. B. and Xavier, R. J., Autophagy and the immune system. Annu. Rev. Immunol. 2012. 30: 611-646.
5. Laplante, M. and Sabatini, D. M., mTOR signaling in growth control and disease. Cell 2012. 149: 274-293.
6. Kim, J., Kundu, M., Viollet, B. and Guan, K.L., AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011. 13: 132-141.
7. Hara, T., Takamura, A., Kishi, C., Iemura, S., Natsume, T., Guan, J.L. and Mizushima, N., FIP200, a ULK1-interacting protein, is required for autophagosome formation in mammalian cells. J. Cell Biol. 2008. 181: 497-510.
8. Chan, E. Y., Longatti, A., McKnight, N. C. and Tooze, S.A., Kinase-inactivated ULK1 proteins inhibit autophagy via their conserved c-terminal domains using an Atg 13-independent mechanism. Mol. Cell Biol. 2009. 29: 157-171.
9. Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., Agholme, L. et al., Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012. 8: 445-544.
10. Shvets, E., Fass, E. and Elazar, Z., Utilizing flow cytometry to monitor autophagy in living mammalian cells. Autophagy 2008. 4: 621-628.
11. Janku, F., McConkey, D. J., Hong, D. S. and Kurzrock, R., Autophagy as a target for anticancer therapy. Nat. Rev. Clin. Oncol. 2011. 8: 528-539.
12. Zhou, X. J. and Zhang, H., Autophagy in immunity: implications in etiology of autoimmune/autoinflammatory diseases. Autophagy 2012. 8: 1286-1299.
13. Hubbard, V. M., Valdor, R., Patel, B., Singh, R., Cuervo, A. M. and Macian, F., Macroautophagy regulates energy metabolism during effector T cell activation. J. Immunol. 2010. 185: 7349-7357.
14. Pua, H. H., Dzhagalov, I., Chuck, M., Mizushima, N. and He, Y. W., A critical role for the autophagy gene Atg 5 in T cell survival and proliferation. J. Exp. Med. 2007. 204: 25-31.
15. Pua, H. H., Guo, J., Komatsu, M. and He, Y. W., Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J. Immunol. 2009. 182: 4046-4055.
16. Jia, W. and He, Y. W., Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J. Immunol. 2011. 186: 5313-5322.
17. Liu, L., Feng, M., Chen, G., Chen, M., Zheng, Q., Song, P., Ma, Q. et al., Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 2012. 14: 177-186.
18. Neumann, C. A., Cao, J. and Manevish, Y., Peroxiredoxin I and its role in cell signaling. Cell Cycle 2009. 8: 4072-4078.
19. Fritsch, R. D., Shen, X., Sims, G. P., Hathcock, K. S., Hodes, R. J. and Lipsky, P. E., Stepwise differentiation of CD4 memory T cells defined by expression of CCR7 and CD27. J. Immunol. 2005. 175: 6489-6497.
20. + T cell memory development. Immunity 2012. 36: 68-78.
21. Fujii, H., Shao, L., Colmegna, I., Goronzy, J. J. and Weyand, C. M., Telomerase insufficiency in rheumatoid arthritis. Proc. Natl. Acad. Sci. U.S.A. 2009. 106: 4360-4365.
22. Lee, J., Giordano, S. and Zhang, J., Autophagy, mitochondria and oxidative stress: cross-talk and redox signaling. Biochem. J. 2012. 441: 523-540.
23. Pelicano, H., Feng, L., Zhou, Y., Carew, J. S., Hileman, E. O., Plunkett, W., Keating, M. J. et al., Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J. Bio. Chem. 2003. 278: 37832-37839.
24. Liu, J., Xia, H., Kim, M., Xu, L., Li, Y., Zhang, L., Cai, Y. et al., Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell 2011. 147: 223-234.
25. Willinger, T. and Flavell, R. A., Canonical autophagy dependent on the class III phosphoinositide-3 kinase Vps34 is required for naïve T-cell homeostasis. Proc. Natl. Acad. Sci. U.S.A. 2012. 109: 8670-8675.
26. Kovacs, J. R., Yang, C. Q., Garcia, G. I., Roodman, S. D., Windle, J. J., Zhang, X. and Lu, B., Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery. Cell Death Differ. 2012. 19: 144-152.
27. Tait, S. W. and Green, D. R., Mitochondria and cell death: outer membrane permiabilization and beyond. Nat. Cell Biol. 2010. 11: 621-632.
28. Tripathi, P. and Hildeman, D., Sensitization of T cells to apoptosis-a role for ROS? Apoptosis 2004. 9: 515-523.
29. Rubinsztein, D. C., Marino, G. and Kroemer, G., Autophagy and aging. Cell 2011. 146: 682-695.
30. Phadwal, K., Abarrategui, J. A., Watson, A. S., Anbalagan, S., Hammond, E. M., Martins, R. W., McMichael, A. et al., A novel method for autophagy detection in primary cells. Autophagy 2012. 8: 1-14.
31. Kryston, T. B., Georgiev, A. B., Pissis, P. and Georgakilas, A. G., Role of oxidative stress and DNA damage in human carcinogenesis. Mutat. Res. 2011. 711: 193-201.
32. Townsend, K. N., Hughson, L. R., Schlie, K., Poon, V. I., Westerback, A. and Lum, J. J., Autophagy inhibition in cancer therapy: metabolic considerations for antitumor immunity. Immunol. Rev. 2012. 249: 176-194.
33. Bobe, P., Bonardelle, D., Benihoud, K., Opolon, P. and Chelbi-Alix, M. K., Arsenic trioxide: a promising novel therapeutic agent for lymphoproliferative and autoimmune syndromes in MRL/lpr mice. Blood 2006. 108: 3967-3975.
34. Abad, J. L., Serrano, F., SanRoman, A. L., Delgado, R., Bernad, A. and Gonzalez, M. A., Single-step, multiple retroviral transduction of human T cells. J. Gene Med. 2002. 4: 27-37.