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ORIGINAL ARTICLE

Autophagy as a Stress Response Pathway in the Immune System

&
Pages 382-402 | Accepted 12 Dec 2014, Published online: 20 Feb 2015

REFERENCES

  • Munz C. Enhancing immunity through autophagy. Ann Rev Immunol 2009;27:423–449. Epub 2008/12/25.
  • Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011;469(7330):323–335. Epub 2011/01/21.
  • Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy. Nature Cell Biol. 2013;15(7):713–720. Epub 2013/07/03.
  • Harris H, Rubinsztein DC. Control of autophagy as a therapy for neurodegenerative disease. Nature Rev Neurol. 2012;8(2):108–117. Epub 2011/12/22.
  • Dice JF. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem Sci 1990;15(8):305–309. Epub 1990/08/01.
  • Kaushik S, Cuervo AM. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 2012;22(8):407–417. Epub 2012/07/04.
  • Hurley JH, Schulman BA. Atomistic autophagy: the structures of cellular self-digestion. Cell 2014;157(2):300–311. Epub 2014/04/15.
  • He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009;43:67-93. Epub 2009/08/06.
  • Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Ann Rev Cell Dev Bio 2011;27:107–132. Epub 2011/08/02.
  • Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol : CB 2012;22(1):R29–34. Epub 2012/01/14.
  • Hosokawa N, Hara T, Kaizuka T, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009;20(7):1981–1991. Epub 2009/02/13.
  • Jung CH, Jun CB, Ro SH, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009;20(7):1992–2003. Epub 2009/02/20.
  • Kamada Y, Yoshino K, Kondo C, et al. Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Bbiol 2010;30(4):1049–1058.
  • Ma Y, Galluzzi L, Zitvogel L, Kroemer G. Autophagy and cellular immune responses. Immunity 2013;39(2):211–227. Epub 2013/08/27.
  • Wong AS, Cheung ZH, Ip NY. Molecular machinery of macroautophagy and its deregulation in diseases. Biochim Biophys Acta 2011;1812(11):1490–1497.
  • Axe EL, Walker SA, Manifava M, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008;182(4):685–701.
  • Polson HE, de Lartigue J, Rigden DJ, et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 2010;6(4):506–522.
  • Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008;19(12):5360–5372.
  • Takahashi Y, Coppola D, Matsushita N, et al. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007;9(10):1142–1151.
  • Takahashi Y, Meyerkord CL, Wang HG. Bif-1/endophilin B1: a candidate for crescent driving force in autophagy. Cell Death Differ 2009;16(7):947–955.
  • Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010;22(2):124–131.
  • Mizushima N, Noda T, Yoshimori T, et al. A protein conjugation system essential for autophagy. Nature 1998;395(6700):395–398.
  • Mizushima N, Sugita H, Yoshimori T, Ohsumi Y. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J Biol Chem 1998;273(51):33889-92.
  • Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 2008;19(5):2092–20100.
  • Hanada T, Noda NN, Satomi Y, et al. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 2007;282(52):37298–37302.
  • Kuballa P, Nolte WM, Castoreno AB, Xavier RJ. Autophagy and the immune system. Annu Rev Immunol 2012;30:611–646. Epub 2012/03/28.
  • Weidberg H, Shvets E, Shpilka T,et al. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 2010;29(11):1792–1802.
  • Noda NN, Ohsumi Y, Inagaki F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett 2010;584(7):1379–1385.
  • Codogno P, Mehrpour M, Proikas-Cezanne T. Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat Rev Mol Cell Biol 2012;13(1):7–12.
  • Luzio JP, Pryor PR, Bright NA. Lysosomes: fusion and function. Nat Rev Mol Cell Biol 2007;8(8):622–632.
  • Furuta N, Fujita N, Noda T,et al. Combinational soluble N-ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lysosomes. Mol Biol Cell 2010;21(6):1001–1010. Epub 2010/01/22.
  • Shanware NP, Bray K, Abraham RT. The PI3K, metabolic, and autophagy networks: interactive partners in cellular health and disease. Ann Rev Pharm Tox 2013;53:89–106. Epub 2013/01/09.
  • Hamasaki M, Furuta N, Matsuda A, et al. Autophagosomes form at ER-mitochondria contact sites. Nature 2013;495(7441):389–393. Epub 2013/03/05.
  • Fujimoto M, Hayashi T. New insights into the role of mitochondria-associated endoplasmic reticulum membrane. Int Rev Cell Mol Biol 2011;292:73–117. Epub 2011/11/15.
  • Marchi S, Patergnani S, Pinton P. The endoplasmic reticulum-mitochondria connection: one touch, multiple functions. Biochim Biophys Acta 2014;1837(4):461–469. Epub 2013/11/12.
  • Bravo R, Vicencio JM, Parra V, et al. Increased ER-mitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. J Cell Sci 2011;124(Pt 13):2143–2152. Epub 2011/06/02.
  • Deniaud A, Sharaf el dein O, Maillier E, et al. Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene 2008;27(3):285–299. Epub 2007/08/19.
  • Mizushima N, Yamamoto A, Matsui M,et al. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004;15(3):1101–1111. Epub 2003/12/31.
  • Komatsu M, Waguri S, Ueno T, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005;169(3):425–434. Epub 2005/05/04.
  • Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature 2004;432(7020):1032–1036. Epub 2004/11/05.
  • Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 2010;40(2):310–322. Epub 2010/10/23.
  • Powell JD, Pollizzi KN, Heikamp EB, Horton MR. Regulation of immune responses by mTOR. Ann Rev Immunol 2012;30:39–68. Epub 2011/12/06.
  • Sancak Y, Bar-Peled L, Zoncu R, et al. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010;141(2):290–303. Epub 2010/04/13.
  • Inoki K, Li Y, Zhu T, et al. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 2002;4(9):648–657. Epub 2002/08/13.
  • Oshiro N, Takahashi R, Yoshino K, et al. The proline-rich Akt substrate of 40 kDa (PRAS40) is a physiological substrate of mammalian target of rapamycin complex 1. J Biol Chem 2007;282(28):20329–20339. Epub 2007/05/23.
  • Ma L, Chen Z, Erdjument-Bromage H, et al. Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 2005;121(2):179–193. Epub 2005/04/27.
  • Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012;13(4):251–262. Epub 2012/03/23.
  • Gwinn DM, Shackelford DB, Egan DF, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 2008;30(2):214–226. Epub 2008/04/29.
  • Sridharan S, Jain K, Basu A. Regulation of autophagy by kinases. Cancers 2011;3(2):2630–2654. Epub 2011/01/01.
  • Egan DF, Shackelford DB, Mihaylova MM, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Sci 2011;331(6016):456–461. Epub 2011/01/06.
  • Chiacchiera F, Simone C. Inhibition of p38alpha unveils an AMPK-FoxO3A axis linking autophagy to cancer-specific metabolism. Autophagy 2009;5(7):1030–1033. Epub 2009/07/10.
  • Ruderman NB, Xu XJ, Nelson L, et al. AMPK and SIRT1: a long-standing partnership? Am J Physiol Endocr Metab 2010;298(4):E751–60. Epub 2010/01/28.
  • Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010;40(2):280-93. Epub 2010/10/23.
  • Verfaillie T, Salazar M, Velasco G, Agostinis P. Linking ER Stress to Autophagy: Potential Implications for Cancer Therapy. Int J Cell Biol 2010;2010:930509. Epub 2010/02/11.
  • Milani M, Rzymski T, Mellor HR, et al. The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with Bortezomib. Canc Res 2009;69(10):4415–4423. Epub 2009/05/07.
  • B’Chir W, Maurin AC, Carraro V, et al. The eIF2alpha/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res 2013;41(16):7683–7699. Epub 2013/06/28.
  • Pua HH, Dzhagalov I, Chuck M, et al. A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J Exp Med 2007;204(1):25–31. Epub 2006/12/28.
  • Hubbard VM, Valdor R, Patel B, et al. Macroautophagy regulates energy metabolism during effector T cell activation. J Immunol 2010;185(12):7349–7357. Epub 2010/11/10.
  • Jia W, He YW. Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J Immunol 2011;186(9):5313–5322. Epub 2011/03/23.
  • He MX, McLeod IX, Jia W, He YW. Macroautophagy in T lymphocyte development and function. Front Immunol 2012;3:22. Epub 2012/05/09.
  • Scherz-Shouval R, Shvets E, Fass E, et al. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007;26(7):1749–1760. Epub 2007/03/10.
  • Alexander A, Cai SL, Kim Jet al., ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Nat Acad Sci USA 2010;107(9):4153–4158. Epub 2010/02/18.
  • Azad MB, Chen Y, Gibson SB. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxidants Redox Signaling 2009;11(4):777–7790. Epub 2008/10/03.
  • Budanov AV, Karin M. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 2008;134(3):451–460. Epub 2008/08/12.
  • Crighton D, Wilkinson S, O’Prey J, et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006;126(1):121–134. Epub 2006/07/15.
  • Bensaad K, Cheung EC, Vousden KH. Modulation of intracellular ROS levels by TIGAR controls autophagy. EMBO J 2009;28(19):3015–3026. Epub 2009/08/29.
  • Bellot G, Garcia-Medina R, Gounon P, et al. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Bbiol 2009;29(10):2570–2581. Epub 2009/03/11.
  • Liu L, Cash TP, Jones RG, et al. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell 2006;21(4):521–531. Epub 2006/02/18.
  • DeYoung MP, Horak P, Sofer A, et al. Hypoxia regulates TSC1/2-mTOR signaling and tumor suppression through REDD1-mediated 14-3-3 shuttling. Genes Dev 2008;22(2):239–251. Epub 2008/01/17.
  • Bernardi R, Guernah I, Jin D, et al. PML inhibits HIF-1alpha translation and neoangiogenesis through repression of mTOR. Nature 2006;442(7104):779–7185. Epub 2006/08/18.
  • Rouschop KM, van den Beucken T, Dubois L, et al. The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J Clin Invest 2010;120(1):127–141. Epub 2009/12/30.
  • Wilkinson S, O’Prey J, Fricker M, Ryan KM. Hypoxia-selective macroautophagy and cell survival signaled by autocrine PDGFR activity. Genes Dev 2009;23(11):1283–1288. Epub 2009/06/03.
  • Vasseur S, Afzal S, Tardivel-Lacombe Jet al., DJ-1/PARK7 is an important mediator of hypoxia-induced cellular responses. Proc Nat Acad Sci USA 2009;106(4):1111–1116. Epub 2009/01/16.
  • Gewirtz DA. The four faces of autophagy: implications for cancer therapy. Canc Res 2014;74(3):647–651. Epub 2014/01/25.
  • Ko A, Kanehisa A, Martins I, et al. Autophagy inhibition radiosensitizes in vitro, yet reduces radioresponses in vivo due to deficient immunogenic signalling. Cell Death Differ 2014;21(1):92–99. Epub 2013/09/17.
  • Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011;334(6059):1081–1086. Epub 2011/11/26.
  • Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007;14(9):1576–1582. Epub 2007/07/07.
  • Ogata M, Hino S, Saito A, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Bbiol 2006;26(24):9220–9231. Epub 2006/10/13.
  • Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol 2012;197(7):857–867. Epub 2012/06/27.
  • Lee AH, Chu GC, Iwakoshi NN, Glimcher LH. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J 2005;24(24):4368–4380. Epub 2005/12/20.
  • Huh WJ, Esen E, Geahlen JH, et al. XBP1 controls maturation of gastric zymogenic cells by induction of MIST1 and expansion of the rough endoplasmic reticulum. Gastroenterology 2010;139(6):2038–2049. Epub 2010/09/08.
  • Reimold AM, Etkin A, Clauss I, et al. An essential role in liver development for transcription factor XBP-1. Genes Dev 2000;14(2):152–157. Epub 2000/02/01.
  • Kaser A, Lee AH, Franke A, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008;134(5):743–756. Epub 2008/09/09.
  • Margariti A, Li H, Chen T, et al. XBP1 mRNA splicing triggers an autophagic response in endothelial cells through BECLIN-1 transcriptional activation. J Biol Chem 2013;288(2):859–872. Epub 2012/11/28.
  • Iwakoshi NN, Lee AH, Vallabhajosyula P, et al. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 2003;4(4):321–329. Epub 2003/03/04.
  • Moore KA, Hollien J. The unfolded protein response in secretory cell function. Annu Rev Genet 2012;46:165–183. Epub 2012/09/01.
  • Pengo N, Scolari M, Oliva L, et al. Plasma cells require autophagy for sustainable immunoglobulin production. Nat Immunol 2013;14(3):298–305. Epub 2013/01/29.
  • Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Ann Rev Immunol 2013;31:443–473. Epub 2013/01/10.
  • Dengjel J, Schoor O, Fischer R, et al. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Nat Acad Sci USA 2005;102(22):7922–7927. Epub 2005/05/17.
  • Schmid D, Pypaert M, Munz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 2007;26(1):79–92. Epub 2006/12/22.
  • 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(6):1506–1514. Epub 1997/06/01.
  • Nimmerjahn F, Milosevic S, Behrends U, et al. Major histocompatibility complex class II-restricted presentation of a cytosolic antigen by autophagy. Eur J Immunol 2003;33(5):1250–1259. Epub 2003/05/06.
  • Kasai M, Tanida I, Ueno T, et al. Autophagic compartments gain access to the MHC class II compartments in thymic epithelium. J Immunol 2009;183(11):7278–7285. Epub 2009/11/17.
  • Nedjic J, Aichinger M, Emmerich J, et al. Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 2008;455(7211):396–400. Epub 2008/08/15.
  • 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(2):287–300. Epub 2013/02/06.
  • Dorfel D, Appel S, Grunebach F, 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(8):3199–3205. Epub 2004/12/25.
  • Paludan C, Schmid D, Landthaler M, et al. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 2005;307(5709):593–596. Epub 2004/12/14.
  • Jagannath C, Lindsey DR, Dhandayuthapani S, et al. Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 2009;15(3):267–276. Epub 2009/03/03.
  • Lee HK, Mattei LM, Steinberg BE, et al. In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 2010;32(2):227–239. Epub 2010/02/23.
  • Reed M, Morris SH, Jang S, et al. Autophagy-inducing protein beclin-1 in dendritic cells regulates CD4 T cell responses and disease severity during respiratory syncytial virus infection. J Immunol 2013;191(5):2526–2537. Epub 2013/07/31.
  • Ireland JM, Unanue ER. Autophagy in antigen-presenting cells results in presentation of citrullinated peptides to CD4 T cells. J Exp Med 2011;208(13):2625–2632. Epub 2011/12/14.
  • Raychaudhuri S, Thomson BP, Remmers EF, et al. Genetic variants at CD28, PRDM1 and CD2/CD58 are associated with rheumatoid arthritis risk. Nat Genet 2009;41(12):1313–1318. Epub 2009/11/10.
  • Bhattacharya A, Eissa NT. Autophagy and autoimmunity crosstalks. Front Immunol 2013;4:88. Epub 2013/04/19.
  • Pierdominici M, Vomero M, Barbati C, et al. Role of autophagy in immunity and autoimmunity, with a special focus on systemic lupus erythematosus. FASEB J: Off Publ Fed Am Soc Exp Biol 2012;26(4):1400–1412. Epub 2012/01/17.
  • Bhattacharya A, Parillon X, Zeng S, et al. Deficiency of autophagy in dendritic cells protects against experimental autoimmune encephalomyelitis. J Biol Chem 2014. Epub 2014/08/01.
  • Cooney R, Baker J, Brain O, et al. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat Med 2010;16(1):90–97. Epub 2009/12/08.
  • Li Y, Wang LX, Yang G, et al. Efficient cross-presentation depends on autophagy in tumor cells. Canc Res 2008;68(17):6889–6895. Epub 2008/09/02.
  • Twitty CG, Jensen SM, Hu HM, Fox BA. Tumor-derived autophagosome vaccine: induction of cross-protective immune responses against short-lived proteins through a p62-dependent mechanism. Clin Canc Res: Off J Am Assoc Canc Res 2011;17(20):6467–6481. Epub 2011/08/04.
  • Li Y, Wang LX, Pang P, et al. Tumor-derived autophagosome vaccine: mechanism of cross-presentation and therapeutic efficacy. Clin Canc Res: Off J Am Assoc Canc Res 2011;17(22):7047–7057. Epub 2011/11/10.
  • English L, Chemali M, Duron J, et al. Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat Immunol 2009;10(5):480–487. Epub 2009/03/24.
  • Tey SK, Khanna R. Autophagy mediates transporter associated with antigen processing-independent presentation of viral epitopes through MHC class I pathway. Blood 2012;120(5):994–1004. Epub 2012/06/23.
  • Tey SK, Khanna R. Host immune system strikes back: autophagy-mediated antigen presentation bypasses viral blockade of the classic MHC class I processing pathway. Autophagy 2012;8(12):1839–1841. Epub 2012/08/31.
  • Li H, Li Y, Jiao J, Hu HM. Alpha-alumina nanoparticles induce efficient autophagy-dependent cross-presentation and potent antitumour response. Nat Nanotechnol 2011;6(10):645–650. Epub 2011/09/20.
  • Shin JN, Fattah EA, Bhattacharya A, et al. Inflammasome activation by altered proteostasis. J Biol Chem 2013;288(50):35886–35895. Epub 2013/11/02.
  • Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011;469(7329):221–225. Epub 2010/12/03.
  • Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 2013;13(10):722–737. Epub 2013/09/26.
  • Bonilla DL, Bhattacharya A, Sha Y, et al. Autophagy regulates phagocytosis by modulating the expression of scavenger receptors. Immunity 2013;39(3):537–547. Epub 2013/09/17.
  • Wildenberg ME, Vos AC, Wolfkamp SC, et al. Autophagy attenuates the adaptive immune response by destabilizing the immunologic synapse. Gastroenterology 2012;142(7):1493–1503 e6. Epub 2012/03/01.
  • Jia W, Pua HH, Li QJ, He YW. Autophagy regulates endoplasmic reticulum homeostasis and calcium mobilization in T lymphocytes. J Immunol 2011;186(3):1564–1574. Epub 2010/12/31.
  • Pua HH, Guo J, Komatsu M, He YW. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J Immunol 2009;182(7):4046—4055. Epub 2009/03/21.
  • Miller BC, Zhao Z, Stephenson LM, et al. The autophagy gene ATG5 plays an essential role in B lymphocyte development. Autophagy 2008;4(3):309–314. Epub 2008/01/12.
  • Bell BD, Leverrier S, Weist BMet al., FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells. Proc Nat Acad Sci USA 2008;105(43):16677–16682. Epub 2008/10/24.
  • Espert L, Denizot M, Grimaldi M, et al. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 2006;116(8):2161–2172. Epub 2006/08/04.
  • Phadwal K, Alegre-Abarrategui J, Watson AS, et al. A novel method for autophagy detection in primary cells: impaired levels of macroautophagy in immunosenescent T cells. Autophagy 2012;8(4):677–689. Epub 2012/02/04.
  • Li C, Capan E, Zhao Y, et al. Autophagy is induced in CD4+ T cells and important for the growth factor-withdrawal cell death. J Immunol 2006;177(8):5163–5168. Epub 2006/10/04.
  • Kovacs JR, Li C, Yang Q, et al. Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery. Cell Death Differ 2012;19(1):144–152. Epub 2011/06/11.
  • Alirezaei M, Fox HS, Flynn CT, et al. Elevated ATG5 expression in autoimmune demyelination and multiple sclerosis. Autophagy 2009;5(2):152–158. Epub 2008/12/11.
  • Araki K, Turner AP, Shaffer VO, et al. mTOR regulates memory CD8 T-cell differentiation. Nature 2009;460(7251):108–112. Epub 2009/06/23.
  • Zhang Z, Wu X, Duan J, et al. Low dose rapamycin exacerbates autoimmune experimental uveitis. PloS one 2012;7(5):e36589. Epub 2012/05/11.
  • Watanabe K, Ichinose S, Hayashizaki K, Tsubata T. Induction of autophagy by B cell antigen receptor stimulation and its inhibition by costimulation. Biochem Biophys Res Commun 2008;374(2):274–281. Epub 2008/07/16.
  • Li W, Zhou M, Ren H, et al. Tumor-derived autophagosomes (DRibbles) induce B cell activation in a TLR2-MyD88 dependent manner. PloS one 2013;8(1):e53564. Epub 2013/01/18.
  • Chaturvedi A, Dorward D, Pierce SK. The B cell receptor governs the subcellular location of Toll-like receptor 9 leading to hyperresponses to DNA-containing antigens. Immunity 2008;28(6):799–809. Epub 2008/06/03.
  • Chen M, Hong MJ, Sun H, et al. Essential role for autophagy in the maintenance of immunological memory against influenza infection. Nat Med 2014;20(5):503–510. Epub 2014/04/22.

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