The transcription factor EB links cellular stress to the immune response

Yale Journal of Biology and Medicine

Volumn 90, Issue 2, 2017, Pages 301-315

  Nabar, Neel R ^a,b   Kehrl, John H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Autophagy; Calcium; Cell stress; Cross presentation; Dendritic cell; Immune; Inflammation; Lysosome; Macrophage; MITF; Phagocytosis; T cell; TFE3; TFEB

Indexed keywords

INFLAMMASOME; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; PROTEIN KINASE C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; TFEB PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; AUTOPHAGY; CELL STRESS; CELLULAR STRESS RESPONSE; ENDOPLASMIC RETICULUM STRESS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INNATE IMMUNITY; LYSOSOME; NONHUMAN; ORGANELLE BIOGENESIS; OXIDATIVE STRESS; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; IMMUNITY; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

AUTOPHAGY; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; HUMANS; IMMUNITY; INFLAMMASOMES; LYSOSOMES; STRESS, PHYSIOLOGICAL;

EID: 85021382567     PISSN: 00440086     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (127)

1. Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325(5939):473-7.
2. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332(6036):1429-33.
3. Raben N, Puertollano R. TFEB and TFE3: Linking Lysosomes to Cellular Adaptation to Stress. Annu Rev Cell Dev Biol. 2016;32:255-78.
4. De Duve C, Pressman BC, Gianetto R, Wattiaux R, Appelmans F. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J. 1955;60(4):604-17.
5. Ballabio A. The awesome lysosome. EMBO Molecular Medicine. 2016;8(2):73-6.
6. Tjelle TE, Brech A, Juvet LK, Griffiths G, Berg T. Isolation and characterization of early endosomes, late endosomes and terminal lysosomes: their role in protein degradation. J Cell Sci. 1996;109 (Pt 12):2905-14.
7. Jaconi ME, Lew DP, Carpentier JL, Magnusson KE, Sjögren M, Stendahl O. Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils. The Journal of Cell Biology. 1990;110(5):1555.
8. Xu H, Ren D. Lysosomal Physiology. Annual Review of Physiology. 2015;77(1):57-80.
9. Medzhitov R, Janeway C. Innate Immunity. New England Journal of Medicine. 2000;343(5):338-44.
10. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy Is a Defense Mechanism Inhibiting BCG and Mycobacterium tuberculosis Survival in Infected Macrophages. Cell. 2004;119(6):753-66.
11. Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13(10):722-37.
12. Watts C. The endosome–lysosome pathway and information generation in the immune system(). Biochimica et Biophysica Acta. 2012;1824(1):14-21.
13. Carr CS, Sharp PA. A helix-loop-helix protein related to the immunoglobulin E box-binding proteins. Mol Cell Biol. 1990;10(8):4384-8.
14. Hodgkinson CA, Moore KJ, Nakayama A, Steingrimsson E, Copeland NG, Jenkins NA, et al. Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell. 1993;74(2):395-404.
15. Beckmann H, Su LK, Kadesch T. TFE3: a helix-loop-helix protein that activates transcription through the immunoglobulin enhancer muE3 motif. Genes Dev. 1990;4(2):167-79.
16. Zhao GQ, Zhao Q, Zhou X, Mattei MG, de Crombrugghe B. TFEC, a basic helix-loop-helix protein, forms heterodimers with TFE3 and inhibits TFE3-dependent transcription activation. Mol Cell Biol. 1993;13(8):4505-12.
17. Steingrimsson E, Copeland NG, Jenkins NA. Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet. 2004;38:365-411.
18. Sato S, Roberts K, Gambino G, Cook A, Kouzarides T, Goding CR. CBP/p300 as a co-factor for the Microphthalmia transcription factor. Oncogene. 1997;14(25):3083-92.
19. Hemesath TJ, Steingrimsson E, McGill G, Hansen MJ, Vaught J, Hodgkinson CA, et al. microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev. 1994;8(22):2770-80.
20. Aksan I, Goding CR. Targeting the microphthalmia basic helix-loop-helix-leucine zipper transcription factor to a subset of E-box elements in vitro and in vivo. Mol Cell Biol. 1998;18(12):6930-8.
21. Pogenberg V, Ogmundsdottir MH, Bergsteinsdottir K, Schepsky A, Phung B, Deineko V, et al. Restricted leucine zipper dimerization and specificity of DNA recognition of the melanocyte master regulator MITF. Genes Dev. 2012;26(23):2647-58.
22. Martina JA, Diab HI, Li H, Puertollano R. Novel roles for the MiTF/TFE family of transcription factors in organelle biogenesis, nutrient sensing, and energy homeostasis. Cellular and Molecular Life Sciences. 2014;71(13):2483-97.
23. Rehli M, Lichanska A, Cassady AI, Ostrowski MC, Hume DA. TFEC is a macrophage-restricted member of the microphthalmia-TFE subfamily of basic helix-loop-helix leucine zipper transcription factors. J Immunol. 1999;162(3):1559-65.
24. Widlund HR, Fisher DE. Microphthalamia-associated transcription factor: a critical regulator of pigment cell development and survival. Oncogene. 2003;22(20):3035-41.
25. Steingrímsson E, Tessarollo L, Pathak B, Hou L, Arnheiter H, Copeland NG, et al. Mitf and Tfe3, two members of the Mitf-Tfe family of bHLH-Zip transcription factors, have important but functionally redundant roles in osteoclast development. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(7):4477-82.
26. Roundy K, Kollhoff A, Eichwald EJ, Weis JJ, Weis JH. Microphthalmic mice display a B cell deficiency similar to that seen for mast and NK cells. J Immunol. 1999;163(12):6671-8.
27. Stechschulte DJ, Sharma R, Dileepan KN, Simpson KM, Aggarwal N, Clancy J, Jr., et al. Effect of the mi allele on mast cells, basophils, natural killer cells, and osteoclasts in C57Bl/6J mice. J Cell Physiol. 1987;132(3):565-70.
28. Golan T, Messer Arielle R, Amitai-Lange A, Melamed Ze, Ohana R, Bell Rachel E, et al. Interactions of Melanoma Cells with Distal Keratinocytes Trigger Metastasis via Notch Signaling Inhibition of MITF. Molecular Cell. 2015;59(4):664-76.
29. Kitamura Y, Morii E, Jippo T, Ito A. Effect of MITF on mast cell differentiation. Mol Immunol. 2002;38(16-18):1173-6.
30. Yagil Z, Hadad Erlich T, Ofir-Birin Y, Tshori S, Kay G, Yekhtin Z, et al. Transcription factor E3, a major regulator of mast cell-mediated allergic response. J Allergy Clin Immunol. 2012;129(5):1357-66.e5.
31. Huan C, Kelly ML, Steele R, Shapira I, Gottesman SRS, Roman CAJ. Transcription factors TFE3 and TFEB are critical for CD40 ligand expression and thymus-dependent humoral immunity. Nature immunology. 2006;7(10):1082-91.
32. Betschinger J, Nichols J, Dietmann S, Corrin Philip D, Paddison Patrick J, Smith A. Exit from Pluripotency Is Gated by Intracellular Redistribution of the bHLH Transcription Factor Tfe3. Cell. 2013;153(2):335-47.
33. Steingrimsson E, Tessarollo L, Reid SW, Jenkins NA, Copeland NG. The bHLH-Zip transcription factor Tfeb is essential for placental vascularization. Development. 1998;125(23):4607-16.
34. Ferron M, Settembre C, Shimazu J, Lacombe J, Kato S, Rawlings DJ, et al. A RANKL-PKCbeta-TFEB signaling cascade is necessary for lysosomal biogenesis in osteoclasts. Genes Dev. 2013;27(8):955-69.
35. Samie M, Cresswell P. The transcription factor TFEB acts as a molecular switch that regulates exogenous antigen-presentation pathways. Nat Immunol. 2015;16(7):729-36.
36. Young NP, Kamireddy A, Van Nostrand JL, Eichner LJ, Shokhirev MN, Dayn Y, et al. AMPK governs lineage specification through Tfeb-dependent regulation of lysosomes. Genes & Development. 2016;30(5):535-52.
37. Rehli M, Sulzbacher S, Pape S, Ravasi T, Wells CA, Heinz S, et al. Transcription factor Tfec contributes to the IL-4-inducible expression of a small group of genes in mouse macrophages including the granulocyte colony-stimulating factor receptor. J Immunol. 2005;174(11):7111-22.
38. Napolitano G, Ballabio A. TFEB at a glance. Journal of Cell Science. 2016.
39. Rehli M, Den Elzen N, Cassady AI, Ostrowski MC, Hume DA. Cloning and characterization of the murine genes for bHLH-ZIP transcription factors TFEC and TFEB reveal a common gene organization for all MiT subfamily members. Genomics. 1999;56(1):111-20.
40. Hallsson JH, Haflidadóttir BS, Stivers C, Odenwald W, Arnheiter H, Pignoni F, et al. The Basic Helix-Loop-Helix Leucine Zipper Transcription Factor Mitf Is Conserved in Drosophila and Functions in Eye Development. Genetics. 2004;167(1):233.
41. Bouché V, Espinosa AP, Leone L, Sardiello M, Ballabio A, Botas J. Drosophila Mitf regulates the V-ATPase and the lysosomal-autophagic pathway. Autophagy. 2016;12(3):484-98.
42. Saftig P, Haas A. Turn up the lysosome. Nat Cell Biol. 2016;18(10):1025-7.
43. 2+In Late Endosome–Lysosome Heterotypic Fusion and in the Reformation of Lysosomes from Hybrid Organelles. The Journal of Cell Biology. 2000;149(5):1053.
44. Reddy A, Caler EV, Andrews NW. Plasma Membrane Repair Is Mediated by Ca2+-Regulated Exocytosis of Lysosomes. Cell. 2001;106(2):157-69.
45. Helip-Wooley A, Thoene JG. Sucrose-induced vacuolation results in increased expression of cholesterol biosynthesis and lysosomal genes. Exp Cell Res. 2004;292(1):89-100.
46. Palmieri M, Impey S, Kang H, di Ronza A, Pelz C, Sardiello M, et al. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet. 2011;20(19):3852-66.
47. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2008;451(7182):1069-75.
48. Kim S, Choi KJ, Cho S-J, Yun S-M, Jeon J-P, Koh YH, et al. Fisetin stimulates autophagic degradation of phosphorylated tau via the activation of TFEB and Nrf2 transcription factors. Scientific Reports. 2016;6:24933.
49. Decressac M, Mattsson B, Weikop P, Lundblad M, Jakobsson J, Bjorklund A. TFEB-mediated autophagy rescues midbrain dopamine neurons from alpha-synuclein toxicity. Proc Natl Acad Sci U S A. 2013;110(19):E1817-26.
50. Pastore N, Ballabio A, Brunetti-Pierri N. Autophagy master regulator TFEB induces clearance of toxic SERPINA1/α-1-antitrypsin polymers. Autophagy. 2013;9(7):1094-6.
51. Xiao Q, Yan P, Ma X, Liu H, Perez R, Zhu A, et al. Neuronal-Targeted TFEB Accelerates Lysosomal Degradation of APP, Reducing Aβ Generation and Amyloid Plaque Pathogenesis. The Journal of Neuroscience. 2015;35(35):12137.
52. Nezich CL, Wang C, Fogel AI, Youle RJ. MiT/TFE transcription factors are activated during mitophagy down-stream of Parkin and Atg 5. J Cell Biol. 2015;210(3):435-50.
53. Settembre C, De Cegli R, Mansueto G, Saha PK, Vetrini F, Visvikis O, et al. TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat Cell Biol. 2013;15(6):647-58.
54. Pena-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, Wolff NC, Tran TA, Zou L, et al. Regulation of TFEB and V-ATPases by mTORC1. Embo j. 2011;30(16):3242-58.
55. Medina Diego L, Fraldi A, Bouche V, Annunziata F, Mansueto G, Spampanato C, et al. Transcriptional Activation of Lysosomal Exocytosis Promotes Cellular Clearance. Developmental Cell. 2011;21(3):421-30.
56. Polito VA, Li H, Martini-Stoica H, Wang B, Yang L, Xu Y, et al. Selective clearance of aberrant tau proteins and rescue of neurotoxicity by transcription factor EB. EMBO Mol Med. 2014;6(9):1142-60.
57. Spampanato C, Feeney E, Li L, Cardone M, Lim JA, Annunziata F, et al. Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol Med. 2013;5(5):691-706.
58. Ugolino J, Ji YJ, Conchina K, Chu J, Nirujogi RS, Pandey A, et al. Loss of C9orf72 Enhances Autophagic Activity via Deregulated mTOR and TFEB Signaling. PLoS Genet. 2016;12(11):e1006443.
59. Tsunemi T, Ashe TD, Morrison BE, Soriano KR, Au J, Roque RA, et al. PGC-1alpha rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci Transl Med. 2012;4(142):142ra97.
60. Chen Y, Liu H, Guan Y, Wang Q, Zhou F, Jie L, et al. The altered autophagy mediated by TFEB in animal and cell models of amyotrophic lateral sclerosis. Am J Transl Res. 2015;7(9):1574-87.
61. Martina JA, Diab HI, Lishu L, Jeong A L, Patange S, Raben N, et al. The Nutrient-Responsive Transcription Factor TFE3 Promotes Autophagy, Lysosomal Biogenesis, and Clearance of Cellular Debris. Science Signaling. 2014;7(309):ra9.
62. Ploper D, Taelman VF, Robert L, Perez BS, Titz B, Chen HW, et al. MITF drives endolysosomal biogenesis and potentiates Wnt signaling in melanoma cells. Proc Natl Acad Sci U S A. 2015;112(5):E420-9.
63. Martina JA, Chen Y, Gucek M, Puertollano R. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy. 2012;8(6):903-14.
64. Roczniak-Ferguson A, Petit CS, Froehlich F, Qian S, Ky J, Angarola B, et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal. 2012;5(228):ra42.
65. Medina DL, Di Paola S, Peluso I, Armani A, De Stefani D, Venditti R, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol. 2015;17(3):288-99.
66. Vega-Rubin-de-Celis S, Peña-Llopis S, Konda M, Brugarolas J. Multistep regulation of TFEB by MTORC1. Autophagy. 2017;13(3):464-72.
67. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Erdin S, et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. The EMBO Journal. 2012;31(5):1095-108.
68. Li Y, Xu M, Ding X, Yan C, Song Z, Chen L, et al. Protein kinase C controls lysosome biogenesis independently of mTORC1. Nat Cell Biol. 2016;18(10):1065-77.
69. Palmieri M, Pal R, Nelvagal HR, Lotfi P, Stinnett GR, Seymour ML, et al. mTORC1-independent TFEB activation via Akt inhibition promotes cellular clearance in neurodegenerative storage diseases. Nature Communications. 2017;8:14338.
70. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell. 2010;141(2):290-303.
71. Zhang X, Cheng X, Yu L, Yang J, Calvo R, Patnaik S, et al. MCOLN1 is a ROS sensor in lysosomes that regulates autophagy. Nature Communications. 2016;7:12109.
72. Sbano L, Bonora M, Marchi S, Baldassari F, Medina DL, Ballabio A, et al. TFEB-mediated increase in peripheral lysosomes regulates store-operated calcium entry. Scientific Reports. 2017;7:40797.
73. Höglinger D, Haberkant P, Aguilera-Romero A, Riezman H, Porter FD, Platt FM, et al. Intracellular sphingosine releases calcium from lysosomes. eLife. 2015;4:e10616.
74. Shin HJ, Kim H, Oh S, Lee JG, Kee M, Ko HJ, et al. AMPK-SKP2-CARM1 signalling cascade in transcriptional regulation of autophagy. Nature. 2016;534(7608):553-7.
75. Chauhan S, Goodwin JG, Chauhan S, Manyam G, Wang J, Kamat AM, et al. ZKSCAN3 is a master transcriptional repressor of autophagy. Mol Cell. 2013;50(1):16-28.
76. Martina JA, Diab HI, Brady OA, Puertollano R. TFEB and TFE3 are novel components of the integrated stress response. Embo j. 2016;35(5):479-95.
77. Lin J, Shi S-S, Zhang J-q, Zhang Y-j, Zhang L, Liu Y, et al. Giant Cellular Vacuoles Induced by Rare Earth Oxide Nanoparticles are Abnormally Enlarged Endo/Lysosomes and Promote mTOR-Dependent TFEB Nucleus Translocation. Small. 2016;12(41):5759-68.
78. Santaguida S, Vasile E, White E, Amon A. Aneuploidy-induced cellular stresses limit autophagic degradation. Genes Dev. 2015;29(19):2010-21.
79. Narendra D, Kane LA, Hauser DN, Fearnley IM, Youle RJ. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy. 2010;6(8):1090-106.
80. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci. 2011;36(1):30-8.
81. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13(2):89-102.
82. Marchand B, Arsenault D, Raymond-Fleury A, Boisvert FM, Boucher MJ. Glycogen synthase kinase-3 (GSK3) inhibition induces prosurvival autophagic signals in human pancreatic cancer cells. J Biol Chem. 2015;290(9):5592-605.
83. Newton AC. Protein kinase C: structure, function, and regulation. J Biol Chem. 1995;270(48):28495-8.
84. Loegering DJ, Lennartz MR. Protein Kinase C and Toll-Like Receptor Signaling. Enzyme Research. 2011;2011:7.
85. Shi CS, Kehrl JH. TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci Signal. 2010;3(123):ra42.
86. Shi C-S, Shenderov K, Huang N-N, Kabat J, Abu-Asab M, Fitzgerald KA, et al. Activation of autophagy by inflammatory signals limits IL-1[beta] production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol. 2012;13(3):255-63.
87. Crotzer VL, Blum JS. Autophagy and its role in MHC-mediated antigen presentation. Journal of immunology (Baltimore, Md.: 1950). 2009;182(6):3335-41.
88. Jiang S, Dupont N, Castillo EF, Deretic V. Secretory vs. degradative autophagy: unconventional secretion of inflammatory mediators. Journal of innate immunity. 2013;5(5):471-9.
89. Menu P, Mayor A, Zhou R, Tardivel A, Ichijo H, Mori K, et al. ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis. 2012;3:e261.
90. Aballay A, Ausubel FM. Programmed cell death mediated by ced-3 and ced-4 protects Caenorhabditis elegans from Salmonella typhimurium-mediated killing. Proc Natl Acad Sci U S A. 2001;98(5):2735-9.
91. Bidere N, Su HC, Lenardo MJ. Genetic disorders of programmed cell death in the immune system. Annu Rev Immunol. 2006;24:321-52.
92. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature. 2011;469(7330):323-35.
93. Coelho C, Souza AC, Derengowski Lda S, de Leon-Rodriguez C, Wang B, Leon-Rivera R, et al. Macrophage mitochondrial and stress response to ingestion of Cryptococcus neoformans. J Immunol. 2015;194(5):2345-57.
94. Kirienko NV, Ausubel FM, Ruvkun G. Mitophagy confers resistance to siderophore-mediated killing by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2015;112(6):1821-6.
95. Bischof LJ, Kao C-Y, Los FCO, Gonzalez MR, Shen Z, Briggs SP, et al. Activation of the Unfolded Protein Response Is Required for Defenses against Bacterial Pore-Forming Toxin In Vivo. PLOS Pathogens. 2008;4(10):e1000176.
96. Cho JA, Lee AH, Platzer B, Cross BC, Gardner BM, De Luca H, et al. The unfolded protein response element IRE-1alpha senses bacterial proteins invading the ER to activate RIG-I and innate immune signaling. Cell Host Microbe. 2013;13(5):558-69.
97. Mulvey M, Arias C, Mohr I. Maintenance of endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor. J Virol. 2007;81(7):3377-90.
98. Visvikis O, Ihuegbu N, Labed Sid A, Luhachack Lyly G, Alves A-Maria F, Wollenberg Amanda C, et al. Innate Host Defense Requires TFEB-Mediated Transcription of Cytoprotective and Antimicrobial Genes. Immunity. 2014;40(6):896-909.
99. Tiller George R, Garsin Danielle A. Of Worms and Men: HLH-30 and TFEB Regulate Tolerance to Infection. Immunity. 2014;40(6):857-8.
100. Ermolaeva MA, Schumacher B. Insights from the worm: the C. elegans model for innate immunity. Semin Immunol. 2014;26(4):303-9.
101. Lawrence T. The Nuclear Factor NF-κB Pathway in Inflammation. Cold Spring Harbor Perspectives in Biology. 2009;1(6):a001651.
102. Vural A, Al-Khodor S, Cheung GY, Shi CS, Srinivasan L, McQuiston TJ, et al. Activator of G-Protein Signaling 3-Induced Lysosomal Biogenesis Limits Macrophage Intracellular Bacterial Infection. J Immunol. 2016;196(2):846-56.
103. Pastore N, Brady OA, Diab HI, Martina JA, Sun L, Huynh T, et al. TFEB and TFE3 cooperate in the regulation of the innate immune response in activated macrophages. Autophagy. 2016;12(8):1240-58.
104. Hasan M, Koch J, Rakheja D, Pattnaik AK, Brugarolas J, Dozmorov I, et al. Trex1 regulates lysosomal biogenesis and interferon-independent activation of antiviral genes. Nat Immunol. 2013;14(1):61-71.
105. Grieves JL, Fye JM, Harvey S, Grayson JM, Hollis T, Perrino FW. Exonuclease TREX1 degrades double-stranded DNA to prevent spontaneous lupus-like inflammatory disease. Proceedings of the National Academy of Sciences. 2015;112(16):5117-22.
106. Honda K, Taniguchi T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol. 2006;6(9):644-58.
107. Campbell GR, Rawat P, Bruckman RS, Spector SA. Human Immunodeficiency Virus Type 1 Nef Inhibits Autophagy through Transcription Factor EB Sequestration. PLOS Pathogens. 2015;11(6):e1005018.
108. Najibi M, Labed Sid A, Visvikis O, Irazoqui Javier E. An Evolutionarily Conserved PLC-PKD-TFEB Pathway for Host Defense. Cell Reports. 2016;15(8):1728-42.
109. Rozengurt E. Protein kinase D signaling: multiple biological functions in health and disease. Physiology (Bethesda). 2011;26(1):23-33.
110. Cuschieri J, Billgren J, Maier RV. Phosphatidylcholine-specific phospholipase C (PC-PLC) is required for LPS-mediated macrophage activation through CD14. J Leukoc Biol. 2006;80(2):407-14.
111. Sajjan US, Yang JH, Hershenson MB, LiPuma JJ. Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells. Cell Microbiol. 2006;8(9):1456-66.
112. Flannagan RS, Jaumouille V, Grinstein S. The cell biology of phagocytosis. Annu Rev Pathol. 2012;7:61-98.
113. Gray Matthew A, Choy Christopher H, Dayam Roya M, Ospina-Escobar E, Somerville A, Xiao X, et al. Phagocytosis Enhances Lysosomal and Bactericidal Properties by Activating the Transcription Factor TFEB. Current Biology. 2016;26(15):1955-64.
114. Chen HD, Kao CY, Liu BY, Huang SW, Kuo CJ, Ruan JW, et al. HLH-30/TFEB-mediated autophagy functions in a cell-autonomous manner for epithelium intrinsic cellular defense against bacterial pore-forming toxin in C. elegans. Autophagy. 2016:0.
115. Yang X, Chang HY, Baltimore D. Autoproteolytic Activation of Pro-Caspases by Oligomerization. Molecular Cell. 1998;1(2):319-25.
116. Martinon F, Burns K, Tschopp J. The Inflammasome: A Molecular Platform Triggering Activation of Inflammatory Caspases and Processing of proIL-β. Molecular Cell. 2002;10(2):417-26
117. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440(7081):228-32.
118. Kanneganti T-D, Ozoren N, Body-Malapel M, Amer A, Park J-H, Franchi L, et al. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/ Nalp3. Nature. 2006;440(7081):233-6.
119. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature. 2009;458(7237):514-8.
120. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature. 2009;458(7237):509-13.
121. Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol. 2013;13(6):397-411.
122. Emanuel R, Sergin I, Bhattacharya S, Turner J, Epelman S, Settembre C, et al. Induction of Lysosomal Biogenesis in Atherosclerotic Macrophages Can Rescue Lipid-Induced Lysosomal Dysfunction and Downstream Sequelae. Arteriosclerosis, thrombosis, and vascular biology. 2014;34(9):1942-52.
123. Van Muiswinkel WB, Van Soest PL. The T cell-dependent period of the immune response to sheep erythrocytes. Immunology. 1976;31(1):111-8.
124. Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, Noelle RJ. Molecular mechanism and function of CD40/ CD40L engagement in the immune system. Immunological reviews. 2009;229(1):10.1111/j.600-065X.2009.00782.x.
125. Baixauli F, Acín-Pérez R, Villarroya-Beltrí C, Mazzeo C, Nuñez-Andrade N, Gabandé-Rodriguez E, et al. Mitochondrial Respiration Controls Lysosomal Function during Inflammatory T Cell Responses. Cell Metabolism. 2015;22(3):485-98.
126. Joffre OP, Segura E, Savina A, Amigorena S. Cross-presentation by dendritic cells. Nat Rev Immunol. 2012;12(8):557-69.
127. Accapezzato D, Visco V, Francavilla V, Molette C, Donato T, Paroli M, et al. Chloroquine enhances human CD8(+) T cell responses against soluble antigens in vivo. The Journal of Experimental Medicine. 2005;202(6):817-28.