Impaired autophagy, defective t cell homeostasis, and a wasting syndrome in mice with a t cell-specific deletion of Vps34

Journal of Immunology

Volumn 190, Issue 10, 2013, Pages 5086-5101

  Parekh, Vrajesh V ^a   Wu, Lan ^a   Boyd, Kelli L ^a   Williams, Janice A ^b   Gaddy, Jennifer A ^a   Olivares Villagomez, Danyvid ^a   Cover, Timothy L ^a,c   Zong, Wei Xing ^d   Zhang, Jianhua ^e,f   Van Kaer, Luc ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d STONY BROOK UNIVERSITY   (United States)

^e University of Alabama at Birmingham   (United States)

^f BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSCRIPTION FACTOR FOXP3;

ANEMIA; ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CD4+ T LYMPHOCYTE; CELL ORGANELLE; CONTROLLED STUDY; ENTERITIS; GENE DELETION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; WASTING SYNDROME; WEIGHT REDUCTION;

ADOPTIVE TRANSFER; AGING; ANIMALS; APOPTOSIS; AUTOPHAGY; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; COLITIS; FORKHEAD TRANSCRIPTION FACTORS; INFLAMMATION; INTERLEUKIN-2; MICE; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; T-LYMPHOCYTES, REGULATORY; WASTING SYNDROME;

EID: 84877832630     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202071     Document Type: Article

References (54)

1. Simonsen, A., and S. A. Tooze. 2009. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 186: 773-782.
2. Xue, L., G. C. Fletcher, and A. M. Tolkovsky. 1999. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol. Cell. Neurosci. 14: 180-198. (Pubitemid 29449222)
3. Bursch, W. 2001. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8: 569-581. (Pubitemid 32590778)
4. Fengsrud, M., E. S. Erichsen, T. O. Berg, C. Raiborg, and P. O. Seglen. 2000. Ultrastructural characterization of the delimiting membranes of isolated autophagosomes and amphisomes by freeze-fracture electron microscopy. Eur. J. Cell Biol. 79: 871-882. (Pubitemid 32000721)
5. Munz, C. 2009. Enhancing immunity through autophagy. Annu. Rev. Immunol. 27: 423-449.
6. Crotzer, V. L., and J. S. Blum. 2005. Autophagy and intracellular surveillance: modulating MHC class II antigen presentation with stress. Proc. Natl. Acad. Sci. USA 102: 7779-7780. (Pubitemid 40781014)
7. Klionsky, D. J. 2007. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8: 931-937. (Pubitemid 47622558)
8. Khalfan, W. A., and D. J. Klionsky. 2002. Molecular machinery required for autophagy and the cytoplasm to vacuole targeting (Cvt) pathway in S. cerevisiae. Curr. Opin. Cell Biol. 14: 468-475. (Pubitemid 35279107)
9. Ohsumi, Y. 2001. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2: 211-216. (Pubitemid 33675746)
10. Axe, E. L., S. A. Walker, M. Manifava, P. Chandra, H. L. Roderick, A. Habermann, G. Griffiths, and N. T. Ktistakis. 2008. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182: 685-701.
11. Levine, B., N. Mizushima, and H. W. Virgin. 2011. Autophagy in immunity and inflammation. Nature 469: 323-335.
12. Mizushima, N., Y. Ohsumi, and T. Yoshimori. 2002. Autophagosome formation in mammalian cells. Cell Struct. Funct. 27: 421-429. (Pubitemid 36267711)
13. Longatti, A., and S. A. Tooze. 2009. Vesicular trafficking and autophagosome formation. Cell Death Differ. 16: 956-965.
14. Polson, H. E., J. de Lartigue, D. J. Rigden, M. Reedijk, S. Urbé, M. J. Clague, and S. A. Tooze. 2010. Mammalian Atg18 (WIPI2) localizes to omegasomeanchored phagophores and positively regulates LC3 lipidation. Autophagy 6: 506-522.
15. Suzuki, K., Y. Kubota, T. Sekito, and Y. Ohsumi. 2007. Hierarchy of Atg proteins in pre-Autophagosomal structure organization. Genes Cells 12: 209-218. (Pubitemid 46152659)
16. Jaber, N., Z. Dou, J. S. Chen, J. Catanzaro, Y. P. Jiang, L. M. Ballou, E. Selinger, X. Ouyang, R. Z. Lin, J. Zhang, and W. X. Zong. 2012. Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc. Natl. Acad. Sci. USA 109: 2003-2008.
17. Zhou, X., L. Wang, H. Hasegawa, P. Amin, B. X. Han, S. Kaneko, Y. He, and F. Wang. 2010. Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc. Natl. Acad. Sci. USA 107: 9424-9429.
18. McLeod, I. X., X. Zhou, Q. J. Li, F. Wang, and Y. W. He. 2011. The class III kinase Vps34 promotes T lymphocyte survival through regulating IL-7Ra surface expression. J. Immunol. 187: 5051-5061.
19. Tanner, V. A., T. Ploug, and J. H. Tao-Cheng. 1996. Subcellular localization of SV2 and other secretory vesicle components in PC12 cells by an efficient method of preembedding EM immunocytochemistry for cell cultures. J. Histochem. Cytochem. 44: 1481-1488.
20. Ott, C., K. Ross, S. Straub, B. Thiede, M. Gotz, C. Goosmann, M. Krischke, M. J. Mueller, G. Krohne, T. Rudel, and V. Kozjak-Pavlovic. 2012. Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes. Mol. Cell. Biol. 32: 1173-1188.
21. Jia, W., and Y. W. He. 2011. Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J. Immunol. 186: 5313-5322.
22. Parekh, V. V., M. T. Wilson, D. Olivares-Villagómez, A. K. Singh, L. Wu, C. R. Wang, S. Joyce, and L. Van Kaer. 2005. Glycolipid antigen induces longterm natural killer T cell anergy in mice. J. Clin. Invest. 115: 2572-2583. (Pubitemid 41266220)
23. + regulatory T cells. J. Immunol. 170: 3939-3943. (Pubitemid 36428153)
24. Olivares-Villagómez, D., H. M. Algood, K. Singh, V. V. Parekh, K. E. Ryan, M. B. Piazuelo, K. T. Wilson, and L. Van Kaer. 2011. Intestinal epithelial cells modulate CD4 T cell responses via the thymus leukemia antigen. J. Immunol. 187: 4051-4060.
25. Edinger, A. L., C. M. Linardic, G. G. Chiang, C. B. Thompson, and R. T. Abraham. 2003. Differential effects of rapamycin on mammalian target of rapamycin signaling functions in mammalian cells. Cancer Res. 63: 8451-8460. (Pubitemid 37549501)
26. Dunning, K. R., K. Cashman, D. L. Russell, J. G. Thompson, R. J. Norman, and R. L. Robker. 2010. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83: 909-918.
27. Pearce, E. L., M. C. Walsh, P. J. Cejas, G. M. Harms, H. Shen, L. S. Wang, R. G. Jones, and Y. Choi. 2009. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460: 103-107.
28. + T lymphocytes. Science 268: 863-865.
29. + T cells by CD1-expressing cortical thymocytes. J. Exp. Med. 182: 2091-2096.
30. Bjørkøy, G., T. Lamark, A. Brech, H. Outzen, M. Perander, A. Overvatn, H. Stenmark, and T. Johansen. 2005. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171: 603-614. (Pubitemid 41668720)
31. Klionsky, D. J., H. Abeliovich, P. Agostinis, D. K. Agrawal, G. Aliev, D. S. Askew, M. Baba, E. H. Baehrecke, B. A. Bahr, A. Ballabio, et al. 2008. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175. (Pubitemid 351231180)
32. Lee, P. P., D. R. Fitzpatrick, C. Beard, H. K. Jessup, S. Lehar, K. W. Makar, M. Pérez-Melgosa, M. T. Sweetser, M. S. Schlissel, S. Nguyen, et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15: 763-774. (Pubitemid 34008504)
33. Crispe, I. N., and M. J. Bevan. 1987. Expression and functional significance of the J11d marker on mouse thymocytes. J. Immunol. 138: 2013-2018. (Pubitemid 17046245)
34. Matsuda, J. L., T. Mallevaey, J. Scott-Browne, and L. Gapin. 2008. CD1drestricted iNKT cells, the "Swiss-Army knife" of the immune system. Curr. Opin. Immunol. 20: 358-368.
35. Bendelac, A., P. B. Savage, and L. Teyton. 2007. The biology of NKT cells. Annu. Rev. Immunol. 25: 297-336. (Pubitemid 46697911)
36. Taniguchi, M., M. Harada, S. Kojo, T. Nakayama, and H. Wakao. 2003. The regulatory role of Va14 NKT cells in innate and acquired immune response. Annu. Rev. Immunol. 21: 483-513. (Pubitemid 37174539)
37. Kronenberg, M. 2005. Toward an understanding of NKT cell biology: progress and paradoxes. Annu. Rev. Immunol. 23: 877-900. (Pubitemid 40563188)
38. Honey, K., K. Benlagha, C. Beers, K. Forbush, L. Teyton, M. J. Kleijmeer, A. Y. Rudensky, and A. Bendelac. 2002. Thymocyte expression of cathepsin L is essential for NKT cell development. Nat. Immunol. 3: 1069-1074. (Pubitemid 35363660)
39. Godfrey, D. I., S. Stankovic, and A. G. Baxter. 2010. Raising the NKT cell family. Nat. Immunol. 11: 197-206.
40. Godfrey, D. I., and S. P. Berzins. 2007. Control points in NKT-cell development. Nat. Rev. Immunol. 7: 505-518. (Pubitemid 46987785)
41. Benlagha, K., D. G. Wei, J. Veiga, L. Teyton, and A. Bendelac. 2005. Characterization of the early stages of thymic NKT cell development. J. Exp. Med. 202: 485-492. (Pubitemid 41186947)
42. Benlagha, K., T. Kyin, A. Beavis, L. Teyton, and A. Bendelac. 2002. A thymic precursor to the NK T cell lineage. Science 296: 553-555. (Pubitemid 34408679)
43. Yue, X., A. Izcue, and T. Borggrefe. 2011. Essential role of mediator subunit Med1 in invariant natural killer T-cell development. Proc. Natl. Acad. Sci. USA 108: 17105-17110.
44. Matsuda, J. L., L. Gapin, S. Sidobre, W. C. Kieper, J. T. Tan, R. Ceredig, C. D. Surh, and M. Kronenberg. 2002. Homeostasis of Va14i NKT cells. Nat. Immunol. 3: 966-974.
45. Pua, H. H., I. Dzhagalov, M. Chuck, N. Mizushima, and Y. W. He. 2007. A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J. Exp. Med. 204: 25-31. (Pubitemid 46148752)
46. + T cells and important for the growth factorwithdrawal cell death. J. Immunol. 177: 5163-5168. (Pubitemid 44527588)
47. Willinger, T., and R. A. Flavell. 2012. Canonical autophagy dependent on the class III phosphoinositide-3 kinase Vps34 is required for naive T-cell homeostasis. Proc. Natl. Acad. Sci. USA 109: 8670-8675.
48. Jia, W., H. H. Pua, Q. J. Li, and Y. W. He. 2011. Autophagy regulates endoplasmic reticulum homeostasis and calcium mobilization in T lymphocytes. J. Immunol. 186: 1564-1574.
49. Willinger, T., and R. A. Flavell. 2012. Canonical autophagy dependent on the class III phosphoinositide-3 kinase Vps34 is required for naive T-cell homeostasis. Proc. Natl. Acad. Sci. USA 109: 8670-8675.
50. Hubbard, V. M., R. Valdor, B. Patel, R. Singh, A. M. Cuervo, and F. Macian. 2010. Macroautophagy regulates energy metabolism during effector T cell activation. J. Immunol. 185: 7349-7357.
51. Millikin, P. D. 1984. On the possible origin of extra-epithelial enterochromaffin cells by budding from the crypts of Lieberkuhn. J. Pathol. 143: 51-56. (Pubitemid 14122496)
52. + T cells. Eur. J. Immunol. 25: 3053-3059.
53. + T cells: evidence for two distinct regulatory mechanisms. Eur. J. Immunol. 31: 1637-1645. (Pubitemid 32547325)
54. Ma, A., M. Datta, E. Margosian, J. Chen, and I. Horak. 1995. T cells, but not B cells, are required for bowel inflammation in interleukin 2-deficient mice. J. Exp. Med. 182: 1567-1572.