Macroautophagy in T lymphocyte development and function

Frontiers in Immunology

Volumn 3, Issue FEB, 2012, Pages

  He, Ming Xiao ^a   McLeod, Ian X ^a   Jia, Wei ^a   He, You Wen ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Autophagy; Organelle homeostasis; T lymphocyte; Thymocyte selection

Indexed keywords

EID: 84872348186     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00022     Document Type: Review

References (59)

1. Arsov, I., Adebayo, A., Kucerova Levisohn, M., Haye, J., MacNeil, M., Papavasiliou, F. N., Yue, Z., and Ortiz, B. D. (2011). A role for autophagic protein beclin 1 early in lymphocyte development. J. Immunol. 186, 2201-2209.
2. Arsov, I., Li, X., Matthews, G., Coradin, J., Hartmann, B., Simon, A. K., Sealfon, S. C., and Yue, Z. (2008). BAC-mediated transgenic expression of fluorescent autophagic protein beclin 1 reveals a role for beclin 1inlymphocytedevelopment.Cell Death Differ. 15, 1385-1395.
3. Bell, B. D., Leverrier, S., Weist, B. M., Newton, R. H.,Arechiga, A. F., Luhrs, K. A., Morrissette, N. S., and Walsh, C. M. (2008). FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells. Proc. Natl. Acad. Sci. U.S.A. 105, 16677-16682.
4. Braun, R. D., Lanzen, J. L., Snyder, S. A., and Dewhirst, M. W. (2001). Comparison of tumor and normal tissue oxygen tension measurements using oxylite or microelectrodes in rodents. Am. J. Physiol. Heart Circ. Physiol. 280, H2533-H2544.
5. Cantrell, D. A., Collins, M. K., and Crumpton, M. J. (1988). Autocrine regulation of T-lymphocyte proliferation: differential induction of IL-2 and IL-2 receptor. Immunology 65, 343-349.
6. Ch'en, I. L., Tsau, J. S., Molkentin, J. D., Komatsu, M., and Hedrick, S. M. (2011). Mechanisms of necroptosis in T cells. J. Exp. Med. 208, 633-641.
7. Copetti, T., Bertoli, C., Dalla, E., Demarchi, F., and Schneider, C. (2009). p65/RelA modulates BECN1 transcription and autophagy. Mol. Cell. Biol. 29, 2594-2608.
8. Denizot, M., Varbanov, M., Espert, L., Robert-Hebmann, V., Sagnier, S., Garcia, E., Curriu, M., Mamoun, R., Blanco, J., and Biard-Piechaczyk, M. (2008). HIV-1 gp41 fusogenic function triggers autophagy in uninfected cells. Autophagy 4, 998-1008.
9. Dou, Z., Chattopadhyay, M., Pan, J. A., Guerriero, J. L., Jiang, Y. P., Ballou, L. M., Yue, Z., Lin, R. Z., and Zong, W. X. (2010). The class IA phosphatidylinositol 3-kinase p110-beta subunit is a positive regulator of autophagy. J. Cell Biol. 191, 827-843.
10. El-behi, M., Rostami, A., and Ciric, B. (2010). Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J. Neuroimmune Pharmacol. 5, 189-197.
11. Espert, L., Denizot, M., Grimaldi, M., Robert-Hebmann, V., Gay, B., Varbanov, M., Codogno, P., and Biard Piechaczyk, M. (2006). Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J. Clin. Invest. 116, 2161-2172.
12. Espert, L., Varbanov, M., RobertHebmann, V., Sagnier, S., Robbins, I., Sanchez, F., Lafont, V., and Biard-Piechaczyk, M. (2009). Differential role of autophagy in CD4 T cells and macrophages during X4 and R5 HIV-1 infection. PLoS ONE 4, e5787. doi:10.1371/journal.pone.0005787
13. Feng, C. G., Zheng, L., Jankovic, D., Bafica, A., Cannons, J. L., Watford, W. T., Chaussabel, D., Hieny, S., Caspar, P., Schwartzberg, P. L., Lenardo, M. J., and Sher, A. (2008). The immunity-related GTPase Irgm1 promotes the expansion of activated CD4+ T cell populations by preventing interferon-gammainduced cell death. Nat. Immunol. 9, 1279-1287.
14. Fox, C. J., Hammerman, P. S., and Thompson, C. B. (2005). Fuel feeds function:energymetabolismandthe T-cell response. Nat. Rev. Immunol. 5, 844-852.
15. Galluzzi, L., and Kroemer, G. (2008). Necroptosis: a specialized pathway of programmed necrosis. Cell 135, 1161-1163.
16. Gerland, L. M., Genestier, L., Peyrol, S., Michallet, M. C., Hayette, S., Urbanowicz, I., Ffrench, P., Magaud, J. P., and Ffrench, M. (2004). Autolysosomes accumulate during in vitro CD8+ T-lymphocyte aging and may participate in induced death sensitization of senescent cells. Exp. Gerontol. 39, 789-800.
17. Gomes, L. C., Di Benedetto, G., and Scorrano, L. (2011). During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 13, 589-598.
18. He, C., and Klionsky, D. J. (2009). Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93.
19. Heino, M., Peterson, P., Kudoh, J., Nagamine, K., Lagerstedt, A., Ovod, V., Ranki, A., Rantala, I., Nieminen, M., Tuukkanen, J., Scott, H. S., Antonarakis, S. E., Shimizu, N., and Krohn, K. (1999). Autoimmune regulator is expressed in the cells regulating immune tolerance in thymus medulla. Biochem. Biophys. Res. Commun. 257, 821-825.
20. Hildeman, D. A., Mitchell, T., Kappler, J., and Marrack, P. (2003). T cell apoptosis and reactive oxygen species. J. Clin. Invest. 111, 575-581.
21. Hubbard, V. M., Valdor, R., Patel, B., Singh, R., Cuervo, A. M., and Macian, F. (2010). Macroautophagy regulates energy metabolism during effector T cell activation. J. Immunol. 185, 7349-7357.
22. Jia, W., and He, Y. W. (2011). Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J. Immunol. 186, 5313-5322.
23. Jia, W., Pua, H. H., Li, Q. J., and He, Y. W. (2011). Autophagy regulates endoplasmic reticulum homeostasis and calcium mobilization in T lymphocytes. J. Immunol. 186, 1564-1574.
24. Kim, H. J., Lee, S., and Jung, J. U. (2010). When autophagy meets viruses: a double-edged sword with functions in defense and offense. Semin. Immunopathol. 32, 323-341.
25. Klionsky, D. J., and Emr, S. D. (2000). Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721.
26. Kovacs, J. R., Li, C., Yang, Q., Li, G., Garcia, I. G., Ju, S., Roodman, D. G., Windle, J. J., Zhang, X., and Lu, B. (2012). Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery. Cell Death Differ. 19, 144-152.
27. Kraft, C., Reggiori, F., and Peter, M. (2009). Selective types of autophagy in yeast. Biochim. Biophys.Acta 1793, 1404-1412.
28. Laurent-Crawford, A. G., Krust, B., Riviere, Y., Desgranges, C., Muller, S., Kieny, M. P., Dauguet, C., and Hovanessian, A. G. (1993). Membrane expression of HIV envelope glycoproteins triggers apoptosis in CD4 cells. AIDS Res. Hum. Retroviruses 9, 761-773.
29. Levine, B., Mizushima, N., and Virgin, H. W. (2011). Autophagy in immunity and inflammation. Nature 469, 323-335.
30. Li, C., Capan, E., Zhao, Y., Zhao, J., Stolz, D., Watkins, S. C., Jin, S., and Lu, B. (2006). Autophagy is induced in CD4+ T cells and important for the growth factor-withdrawal cell death. J. Immunol. 177, 5163-5168.
31. Liang, X. H., Kleeman, L. K., Jiang, H. H., Gordon, G., Goldman, J. E., Berry, G., Herman, B., and Levine, B. (1998). Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72, 8586-8596.
32. Longatti, A., and Tooze, S. A. (2009). Vesicular trafficking and autophagosome formation. Cell Death Differ. 16, 956-965.
33. Mattoo, H., Faulkner, M., Kandpal, U., Das, R., Lewis, V., George, A., Rath, S., Durdik, J. M., and Bal, V. (2009). Naive CD4 T cells from aged mice show enhanced death upon primary activation. Int. Immunol. 21, 1277-1289.
34. McLeod, I. X., Zhou, X., Li, Q. J., Wang, F., and He, Y. W. (2011). The class III kinase Vps34 promotes T lymphocyte survival through regulating IL-7Ralpha surface expression. J. Immunol. 187, 5051-5061.
35. Mortimore, G. E., and Poso, A. R. (1987). Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu. Rev. Nutr. 7, 539-564.
36. Nedjic, J., Aichinger, M., Emmerich, J., Mizushima, N., and Klein, L. (2008a). Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 455, 396-400.
37. Nedjic, J., Aichinger, M., and Klein, L. (2008b). Autophagy and T cell education in the thymus: eat yourself to know yourself. Cell Cycle 7, 3625-3628.
38. Ohsumi, Y., and Mizushima, N. (2004). Two ubiquitin-like conjugation systems essential for autophagy. Semin. Cell Dev. Biol. 15, 231-236.
39. Osborn, S. L., Diehl, G., Han, S. J., Xue, L., Kurd, N., Hsieh, K., Cado, D., Robey, E. A., and Winoto, A. (2010). Fas-associated death domain (FADD) is a negative regulator of T-cell receptor-mediated necroptosis. Proc. Natl. Acad. Sci. U.S.A. 107, 13034-13039.
40. Pua, H. H., Dzhagalov, I., Chuck, M., Mizushima, N., and He, Y.W. (2007). A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J. Exp. Med. 204, 25-31.
41. Pua, H. H., Guo, J., Komatsu, M., and He,Y.W. (2009).Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J. Immunol. 182, 4046-4055.
42. Pyo, J. O., Jang, M. H., Kwon, Y. K., Lee, H. J., Jun, J. I., Woo, H. N., Cho, D. H., Choi, B., Lee, H., Kim, J. H., Mizushima, N., Oshumi, Y., and Jung,Y. K. (2005). Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death. J. Biol. Chem. 280, 20722-20729.
43. Schatz,D. G.,and Ji,Y. (2011). Recombination centres and the orchestration of V(D)J recombination. Nat. Rev. Immunol. 11, 251-263.
44. Sitkovsky, M., and Lukashev, D. (2005). Regulation of immune cells by localtissue oxygen tension: HIF1 alpha and adenosine receptors. Nat. Rev. Immunol. 5, 712-721.
45. Son, Y. M., Kwak, C. W., Lee, Y. J., Yang, D. C., Park, B. C., Lee, W. K., Han, S. H., and Yun, C. H. (2010). Ginsenoside Re enhances survival of human CD4+ T cells through regulation of autophagy. Int. Immunopharmacol. 10, 626-631.
46. Stephenson, L. M., Miller, B. C., Ng, A., Eisenberg, J., Zhao, Z., Cadwell, K., Graham, D. B., Mizushima, N. N., Xavier, R., Virgin, H. W., and Swat, W. (2009). Identification of Atg5-dependent transcriptional changes and increases in mitochondrial mass in Atg5-deficient T lymphocytes. Autophagy 5, 625-635.
47. Takahama, Y., Nitta, T., Mat Ripen, A., Nitta, S., Murata, S., and Tanaka, K. (2010). Role of thymic cortexspecific self-peptides in positive selection of T cells. Semin. Immunol. 22, 287-293.
48. Takahashi, Y., Coppola, D., Matsushita, N., Cualing, H. D., Sun, M., Sato, Y., Liang, C., Jung, J. U., Cheng, J. Q., Mule, J. J., Pledger, W. J., and Wang, H. G. (2007). Bif-1 interacts with beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat. Cell Biol. 9, 1142-1151.
49. Takahashi, Y., Meyerkord, C. L., and Wang, H. G. (2009). Bif1/endophilin B1: a candidate for crescent driving force in autophagy. Cell Death Differ. 16, 947-955.
50. Thorburn, A. (2008). Apoptosis and autophagy: regulatory connections between two supposedly different processes. Apoptosis 13, 1-9.
51. Uddin, M. N., Nishio, N., Ito, S., Suzuki, H., and Isobe, K. (2012). Autophagic activity in thymus and liver during aging. Age (Dordr) 34, 75-85.
52. Wei, Y., Sinha, S., and Levine, B. (2008). Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4, 949-951.
53. Wu, Y. T., Tan, H. L., Huang, Q., Sun, X. J., Zhu, X., and Shen, H. M. (2011). zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFalpha mediated by the PKC-MAPKs-AP1 pathway. Cell Death Differ. 18, 26-37.
54. Yousefi, S., Perozzo, R., Schmid, I., Ziemiecki, A., Schaffner, T., Scapozza, L., Brunner, T., and Simon, H. U. (2006). Calpainmediated cleavage of Atg5 switches autophagy to apoptosis. Nat. Cell Biol. 8, 1124-1132.
55. Yu, L., Alva, A., Su, H., Dutt, P., Freundt, E., Welsh, S., Baehrecke, E. H., and Lenardo, M. J. (2004). Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500-1502.
56. Yue, Z., Jin, S., Yang, C., Levine, A. J., and Heintz, N. (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 100, 15077-15082.
57. Zhang, J., Cado, D., Chen, A., Kabra, N. H., and Winoto, A. (1998). Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature 392, 296-300.
58. Zhang, N., Hartig, H., Dzhagalov, I., Draper, D., and He, Y. W. (2005). The role of apoptosis in the development and function of T lymphocytes. Cell Res. 15, 749-769.
59. Zhou, D., and Spector, S. A. (2008). Human immunodeficiency virus type-1 infection inhibits autophagy. AIDS 22, 695-699.