Autophagy in T-cell development, activation and differentiation

Immunology and Cell Biology

Volumn 93, Issue 1, 2015, Pages 25-34

  Bronietzki, Alisha W ^a,b   Schuster, Marc ^a,b   Schmitz, Ingo ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; CD4 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; APOPTOSIS REGULATORY PROTEIN; UBIQUITIN CONJUGATING ENZYME;

ADAPTIVE IMMUNITY; AGING; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; AUTOPHAGY; ENDOPLASMIC RETICULUM; HEMATOPOIETIC STEM CELL; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; MITOCHONDRION; NATURAL KILLER T CELL; REGULATORY T LYMPHOCYTE; REVIEW; STROMA CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMOCYTE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; DENDRITIC CELL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHAGOSOME; THYMUS;

AGING; ANIMALS; ANTIGEN PRESENTATION; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL DIFFERENTIATION; DENDRITIC CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MITOCHONDRIA; PHAGOSOMES; T-LYMPHOCYTES; THYMUS GLAND; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84920518692     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2014.81     Document Type: Review

References (100)

1. Agarraberes FA, Dice JF. A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J Cell Sci 2001; 114 (Part 1)2491-2499.
2. Hutson NJ, Lloyd CE, Mortimore GE. Degradation of intra-and extrahepatic protein by livers of normal and diabetic mice: differential responses to starvation. Proc Natl Acad Sci USA 1982; 79: 1737-1741.
3. Ravikumar B, Duden R, Rubinsztein DC. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 2002; 11: 1107-1117.
4. Ding WX, Yin XM. Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol Chem 2012; 393: 547-564.
5. Sakai Y, Oku M, van der Klei IJ, Kiel JA. Pexophagy: autophagic degradation of peroxisomes. Biochim Biophys Acta 2006; 1763: 1767-1775.
6. Bernales S, Schuck S, Walter P. ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 2007; 3: 285-287.
7. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15: 1101-1111.
8. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441: 885-889.
9. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441: 880-884.
10. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, Huse K et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 2007; 39: 207-211.
11. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, Huett A et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 2007; 39: 596-604.
12. Liu H, He Z, von Rutte T, Yousefi S, Hunger RE, Simon HU. Down-regulation of autophagy-related protein 5 (ATG5) contributes to the pathogenesis of early-stage cutaneous melanoma. Sci Transl Med 2013; 5: 202ra123.
13. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y et al. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007; 9: 1142-1151.
14. Del Roso A, Vittorini S, Cavallini G, Donati A, Gori Z, Masini M et al. Ageing-related changes in the in vivo function of rat liver macroautophagy and proteolysis. Exp Gerontol 2003; 38: 519-527.
15. Toth ML, Sigmond T, Borsos E, Barna J, Erdelyi P, Takacs-Vellai K et al. Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy 2008; 4: 330-338.
16. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina D, Settembre C et al. Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat Cell Biol 2010; 12: 863-875.
17. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M et al. Autophagy regulates lipid metabolism. Nature 2009; 458: 1131-1135.
18. Raben N, Wong A, Ralston E, Myerowitz R. Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. Am J Med Genet C 2012; 160C: 13-21.
19. Nishino I, Fu J, Tanji K, Yamada T, Shimojo S, Koori T et al. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature 2000; 406: 906-910.
20. Marsh BJ, Soden C, Alarcon C, Wicksteed BL, Yaekura K, Costin AJ et al. Regulated autophagy controls hormone content in secretory-deficient pancreatic endocrine betacells. Mol Endocrinol 2007; 21: 2255-2269.
21. Knodler LA, Celli J. Eating the strangers within: host control of intracellular bacteria via xenophagy. Cell Microbiol 2011; 13: 1319-1327.
22. Mercer CA, Kaliappan A, Dennis PB. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 2009; 5: 649-662.
23. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2001; 2: 330-335.
24. Proikas-Cezanne T, Waddell S, Gaugel A, Frickey T, Lupas A, Nordheim A. WIPI-1alpha (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene 2004; 23: 9314-9325.
25. Yamamoto H, Kakuta S, Watanabe TM, Kitamura A, Sekito T, Kondo-Kakuta C et al. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 2012; 198: 219-233.
26. Romanov J, Walczak M, Ibiricu I, Schuchner S, Ogris E, Kraft C et al. Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J 2012; 31: 4304-4317.
27. Dooley HC, Razi M, Polson HE, Girardin SE, Wilson MI, Tooze SA. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell 2014; 55: 238-252.
28. Noda NN, Fujioka Y, Hanada T, Ohsumi Y, Inagaki F. Structure of the Atg12-Atg5 conjugate reveals a platform for stimulating Atg8-PE conjugation. EMBO Rep 2013; 14: 206-211.
29. Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 2010; 29: 1792-1802.
30. Yu ZQ, Ni T, Hong B, Wang HY, Jiang FJ, Zou S et al. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy 2012; 8: 883-892.
31. Sou YS, Waguri S, Iwata J, Ueno T, Fujimura T, Hara T et al. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol Biol Cell 2008; 19: 4762-4775.
32. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432: 1032-1036.
33. Stolz A, Ernst A, Dikic I. Cargo recognition and trafficking in selective autophagy. Nat Cell Biol 2014; 16: 495-501.
34. Jotereau FV, Le Douarin NM. Demonstration of a cyclic renewal of the lymphocyte precursor cells in the quail thymus during embryonic and perinatal life. J Immunol 1982; 129: 1869-1877.
35. Suda T, Takubo K, Semenza GL. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 2011; 9: 298-310.
36. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007; 110: 3056-3063.
37. Salemi S, Yousefi S, Constantinescu MA, Fey MF, Simon HU. Autophagy is required for self-renewal and differentiation of adult human stem cells. Cell Res 2012; 22: 432-435.
38. Gurumurthy S, Xie SZ, Alagesan B, Kim J, Yusuf RZ, Saez B et al. The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature 2010; 468: 659-663.
39. Ito K, Hirao A, Arai F, Takubo K, Matsuoka S, Miyamoto K et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006; 12: 446-451.
40. Mortensen M, Watson AS, Simon AK. Lack of autophagy in the hematopoietic system leads to loss of hematopoietic stem cell function and dysregulated myeloid proliferation. Autophagy 2011; 7: 1069-1070.
41. Liu F, Lee JY, Wei H, Tanabe O, Engel JD, Morrison SJ et al. FIP200 is required for the cell-autonomous maintenance of fetal hematopoietic stem cells. Blood 2010; 116: 4806-4814.
42. Mortensen M, Soilleux EJ, Djordjevic G, Tripp R, Lutteropp M, Sadighi-Akha E et al. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med 2011; 208: 455-467.
43. Mortensen M, Simon AK. Nonredundant role of Atg7 in mitochondrial clearance during erythroid development. Autophagy 2010; 6: 423-425.
44. Nedjic J, Aichinger M, Emmerich J, Mizushima N, Klein L. Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 2008; 455: 396-400.
45. Brazil MI, Weiss S, Stockinger B. Excessive degradation of intracellular protein in macrophages prevents presentation in the context of major histocompatibility complex class II molecules. Eur J Immunol 1997; 27: 1506-1514.
46. Aichinger M, Wu C, Nedjic J, Klein L. Macroautophagy substrates are loaded onto MHC class II of medullary thymic epithelial cells for central tolerance. J Exp Med 2013; 210: 287-300.
47. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M et al. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci USA 2005; 102: 7922-7927.
48. Dorfel D, Appel S, Grunebach F, Weck MM, Muller MR, Heine A et al. Processing and presentation of HLA class I and II epitopes by dendritic cells after transfection with in vitro-transcribed MUC1 RNA. Blood 2005; 105: 3199-3205.
49. Kasai M, Kominami E, Mizuochi T. The antigen presentation pathway in medullary thymic epithelial cells, but not that in cortical thymic epithelial cells, conforms to the endocytic pathway. Eur J Immunol 1998; 28: 1867-1876.
50. Kasai M, Tanida I, Ueno T, Kominami E, Seki S, Ikeda T et al. Autophagic compartments gain access to the MHC class II compartments in thymic epithelium. J Immunol 2009; 183: 7278-7285.
51. Ireland JM, Unanue ER. Autophagy in antigen-presenting cells results in presentation of citrullinated peptides to CD4 T cells. J Exp Med 2011; 208: 2625-2632.
52. Schmid D, Pypaert M, Munz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 2007; 26: 79-92.
53. Sukseree S, Mildner M, Rossiter H, Pammer J, Zhang CF, Watanapokasin R et al. Autophagy in the thymic epithelium is dispensable for the development of selftolerance in a novel mouse model. PLoS One 2012; 7: e38933.
54. Arsov I, Adebayo A, Kucerova-Levisohn M, Haye J, MacNeil M, Papavasiliou FN et al. A role for autophagic protein beclin 1 early in lymphocyte development. J Immunol 2011; 186: 2201-2209.
55. Pua HH, Dzhagalov I, Chuck M, Mizushima N, He YW. A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J Exp Med 2007; 204: 25-31.
56. Parekh VV, Wu L, Boyd KL, Williams JA, Gaddy JA, Olivares-Villagomez D et al. Impaired autophagy, defective T cell homeostasis, and a wasting syndrome in mice with a T cell-specific deletion of Vps34. J Immunol 2013; 190: 5086-5101.
57. Willinger T, Flavell RA. Canonical autophagy dependent on the class III phosphoinositide-3 kinase Vps34 is required for naive T-cell homeostasis. Proc Natl Acad Sci USA 2012; 109: 8670-8675.
58. Jia W, He YW. Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J Immunol 2011; 186: 5313-5322.
59. Pua HH, Guo J, Komatsu M, He YW. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J Immunol 2009; 182: 4046-4055.
60. Stephenson LM, Miller BC, Ng A, Eisenberg J, Zhao Z, Cadwell K et al. Identification of Atg5-dependent transcriptional changes and increases in mitochondrial mass in Atg5-deficient T lymphocytes. Autophagy 2009; 5: 625-635.
61. Jia W, Pua HH, Li QJ, He YW. Autophagy regulates endoplasmic reticulum homeostasis and calcium mobilization in T lymphocytes. J Immunol 2011; 186: 1564-1574.
62. McLeod IX, Zhou X, Li QJ, Wang F, He YW. The class III kinase Vps34 promotes T lymphocyte survival through regulating IL-7Ralpha surface expression. J Immunol 2011; 187: 5051-5061.
63. Kovacs JR, Li C, Yang Q, Li G, Garcia IG, Ju S et al. Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery. Cell Death Differ 2012; 19: 144-152.
64. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18: 571-580.
65. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, Plas DR et al. The CD28 signaling pathway regulates glucose metabolism. Immunity 2002; 16: 769-777.
66. Carr EL, Kelman A, Wu GS, Gopaul R, Senkevitch E, Aghvanyan A et al. Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J Immunol 2010; 185: 1037-1044.
67. Powell JD, Lerner CG, Schwartz RH. Inhibition of cell cycle progression by rapamycin induces T cell clonal anergy even in the presence of costimulation. J Immunol 1999; 162: 2775-2784.
68. Edinger AL, Thompson CB. Akt maintains cell size and survival by increasing mTORdependent nutrient uptake. Mol Biol Cell 2002; 13: 2276-2288.
69. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011; 35: 871-882.
70. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T et al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 2009; 458: 762-765.
71. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006; 3: 177-185.
72. Macian F, Garcia-Cozar F, Im SH, Horton HF, Byrne MC, Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2002; 109: 719-731.
73. Negulescu PA, Shastri N, Cahalan MD. Intracellular calcium dependence of gene expression in single T lymphocytes. Proc Natl Acad Sci USA 1994; 91: 2873-2877.
74. Sena LA, Li S, Jairaman A, Prakriya M, Ezponda T, Hildeman DA et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 2013; 38: 225-236.
75. Tamas P, Hawley SA, Clarke RG, Mustard KJ, Green K, Hardie DG et al. Regulation of the energy sensor AMP-activated protein kinase by antigen receptor and Ca2+ in T lymphocytes. J Exp Med 2006; 203: 1665-1670.
76. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13: 132-141.
77. Jia W, He MX, McLeod IX, He YW. Autophagy, a novel pathway to regulate calcium mobilization in T lymphocytes. Front Immunol 2013; 4: 179.
78. Fox CJ, Hammerman PS, Thompson CB. The Pim kinases control rapamycin-resistant T cell survival and activation. J Exp Med 2005; 201: 259-266.
79. Li C, Capan E, Zhao Y, Zhao J, Stolz D, Watkins SC et al. Autophagy is induced in CD4 + T cells and important for the growth factor-withdrawal cell death. J Immunol 2006; 177: 5163-5168.
80. Hubbard VM, Valdor R, Patel B, Singh R, Cuervo AM, Macian F. Macroautophagy regulates energy metabolism during effector T cell activation. J Immunol 2010; 185: 7349-7357.
81. Denton D, Xu T, Kumar S. Autophagy as a pro-death pathway. Immunol Cell Biol 2014 (doi:10.1038/icb.2014.85).
82. Criollo A, Chereau F, Malik SA, Niso-Santano M, Marino G, Galluzzi L et al. Autophagy is required for the activation of NFkappaB. Cell Cycle 2012; 11: 194-199.
83. Kingeter LM, Paul S, Maynard SK, Cartwright NG, Schaefer BC. Cutting edge: TCR ligation triggers digital activation of NF-kappaB. J Immunol 2010; 185: 4520-4524.
84. Paul S, Kashyap AK, Jia W, He YW, Schaefer BC. Selective autophagy of the adaptor protein Bcl10 modulates T cell receptor activation of NF-kappaB. Immunity 2012; 36: 947-958.
85. Romao S, Gasser N, Becker AC, Guhl B, Bajagic M, Vanoaica D et al. Autophagy proteins stabilize pathogen-containing phagosomes for prolonged MHC II antigen processing. J Cell Biol 2013; 203: 757-766.
86. Paludan C, Schmid D, Landthaler M, Vockerodt M, Kube D, Tuschl T et al. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 2005; 307: 593-596.
87. Russmann H, Panthel K, Kohn B, Jellbauer S, Winter SE, Garbom S et al. Alternative endogenous protein processing via an autophagy-dependent pathway compensates for Yersinia-mediated inhibition of endosomal major histocompatibility complex class II antigen presentation. Infect Immun 2010; 78: 5138-5150.
88. Jagannath C, Lindsey DR, Dhandayuthapani S, Xu Y, Hunter RL Jr, Eissa NT. Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 2009; 15: 267-276.
89. Nimmerjahn F, Milosevic S, Behrends U, Jaffee EM, Pardoll DM, Bornkamm GW et al. Major histocompatibility complex class II-restricted presentation of a cytosolic antigen by autophagy. Eur J Immunol 2003; 33: 1250-1259.
90. Li Y, Wang LX, Yang G, Hao F, Urba WJ, Hu HM. Efficient cross-presentation depends on autophagy in tumor cells. Cancer Res 2008; 68: 6889-6895.
91. Uhl M, Kepp O, Jusforgues-Saklani H, Vicencio JM, Kroemer G, Albert ML. Autophagy within the antigen donor cell facilitates efficient antigen cross-priming of virus-specific CD8+ T cells. Cell Death Differ 2009; 16: 991-1005.
92. Tey SK, Khanna R. Autophagy mediates transporter associated with antigen processing-independent presentation of viral epitopes through MHC class I pathway. Blood 2012; 120: 994-1004.
93. Michalek RD, Gerriets VA, Jacobs SR, Macintyre AN, MacIver NJ, Mason EF et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol 2011; 186: 3299-3303.
94. Delgoffe GM, Pollizzi KN, Waickman AT, Heikamp E, Meyers DJ, Horton MR et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol 2011; 12: 295-303.
95. Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 2011; 208: 1367-1376.
96. Pearce EL, Walsh MC, Cejas PJ, Harms GM, Shen H, Wang LS et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009; 460: 103-107.
97. O'Sullivan D, van der Windt GJ, Huang SC, Curtis JD, Chang CH, Buck MD et al. Memory CD8(+) T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity 2014; 41: 75-88.
98. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF et al. mTOR regulates memory CD8 T-cell differentiation. Nature 2009; 460: 108-112.
99. Ren T, Dong W, Takahashi Y, Xiang D, Yuan Y, Liu X et al. HTLV-2 Tax immortalizes human CD4+ memory T lymphocytes by oncogenic activation and dysregulation of autophagy. J Biol Chem 2012; 287: 34683-34693.
100. Ren T, Takahashi Y, Liu X, Loughran TP, Sun SC, Wang HG et al. HTLV-1 Tax deregulates autophagy by recruiting autophagic molecules into lipid raft microdomains. Oncogene (e-pub ahead of pirnt, 23 December 2013; doi:10.1038/onc.2013.552).