Cell-autonomous stress responses in innate immunity

Journal of Leukocyte Biology

Volumn 101, Issue 1, 2017, Pages 77-86

  Moretti, Julien ^a   Blander, J Magarian ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; DNA damage response; ER stress UPR; Mitochondrial stress; mTOR; Stress granules

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PATTERN RECOGNITION RECEPTOR; TARGET OF RAPAMYCIN KINASE;

ADAPTIVE IMMUNITY; AUTOPHAGY; CELL AUTONOMOUS STRESS RESPONSES; CELLULAR STRESS RESPONSE; CYTOKINE PRODUCTION; DNA DAMAGE RESPONSE; ENDOPLASMIC RETICULUM STRESS; IMMUNOREGULATION; INFECTION; INNATE IMMUNITY; METABOLIC STRESS; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; DNA DAMAGE; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGICAL STRESS;

ANIMALS; AUTOPHAGY; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; HUMANS; IMMUNITY, INNATE; STRESS, PHYSIOLOGICAL; TOR SERINE-THREONINE KINASES;

EID: 85008486135     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.2MR0416-201R     Document Type: Review

References (104)

1. Janeway, C. A., Jr. (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54, 1-13.
2. Janeway, C. A., Jr. (1992) The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol. Today 13, 11-16.
3. Thompson, M. R., Kaminski, J. J., Kurt-Jones, E. A., Fitzgerald, K. A. (2011) Pattern recognition receptors and the innate immune response to viral infection. Viruses 3, 920-940.
4. Moretti, J., Blander, J. M. (2014) Insights into phagocytosis-coupled activation of pattern recognition receptors and inflammasomes. Curr. Opin. Immunol. 26, 100-110.
5. MacMicking, J. D. (2012) Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat. Rev. Immunol. 12, 367-382.
6. Randow, F., MacMicking, J. D., James, L. C. (2013) Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340, 701-706.
7. He, C., Klionsky, D. J. (2009) Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93.
8. Mizushima, N. (2007) Autophagy: process and function. Genes Dev. 21, 2861-2873.
9. Glick, D., Barth, S., Macleod, K. F. (2010) Autophagy: cellular and molecular mechanisms. J. Pathol. 221, 3-12.
10. Kirkin, V., McEwan, D. G., Novak, I., Dikic, I. (2009) A role for ubiquitin in selective autophagy. Mol. Cell 34, 259-269.
11. Kraft, C., Peter, M., Hofmann, K. (2010) Selective autophagy: ubiquitinmediated recognition and beyond. Nat. Cell Biol. 12, 836-841.
12. Bernales, S., Schuck, S., Walter, P. (2007) ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 3, 285-287.
13. Youle, R. J., Narendra, D. P. (2011) Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14.
14. Boya, P., Reggiori, F., Codogno, P. (2013) Emerging regulation and functions of autophagy. Nat. Cell Biol. 15, 713-720.
15. Li, W. W., Li, J., Bao, J. K. (2012) Microautophagy: lesser-known selfeating. Cell. Mol. Life Sci. 69, 1125-1136.
16. Kaushik, S., Bandyopadhyay, U., Sridhar, S., Kiffin, R., Martinez-Vicente, M., Kon, M., Orenstein, S. J., Wong, E., Cuervo, A. M. (2011) Chaperone-mediated autophagy at a glance. J. Cell Sci. 124, 495-499.
17. Levine, B., Mizushima, N., Virgin, H. W. (2011) Autophagy in immunity and inflammation. Nature 469, 323-335.
18. Huang, J., Brumell, J. H. (2014) Bacteria-autophagy interplay: a battle for survival. Nat. Rev. Microbiol. 12, 101-114.
19. Jo, E. K., Yuk, J. M., Shin, D. M., Sasakawa, C. (2013) Roles of autophagy in elimination of intracellular bacterial pathogens. Front. Immunol. 4, 97.
20. Huett, A., Heath, R. J., Begun, J., Sassi, S. O., Baxt, L. A., Vyas, J. M., Goldberg, M. B., Xavier, R. J. (2012) The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium. Cell Host Microbe 12, 778-790.
21. Thurston, T. L., Ryzhakov, G., Bloor, S., von Muhlinen, N., Randow, F. (2009) The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10, 1215-1221.
22. Wild, P., Farhan, H., McEwan, D. G., Wagner, S., Rogov, V. V., Brady, N. R., Richter, B., Korac, J., Waidmann, O., Choudhary, C., Dötsch, V., Bumann, D., Dikic, I. (2011) Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233.
23. Zheng, Y. T., Shahnazari, S., Brech, A., Lamark, T., Johansen, T., Brumell, J. H. (2009) The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J. Immunol. 183, 5909-5916.
24. Thurston, T. L., Wandel, M. P., von Muhlinen, N., Foeglein, A., Randow, F. (2012) Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414-418.
25. Orvedahl, A., MacPherson, S., Sumpter, R., Jr., Tallóczy, Z., Zou, Z., Levine, B. (2010) Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7, 115-127.
26. Delgado, M. A., Deretic, V. (2009) Toll-like receptors in control of immunological autophagy. Cell Death Differ. 16, 976-983.
27. Jabir, M. S., Ritchie, N. D., Li, D., Bayes, H. K., Tourlomousis, P., Puleston, D., Lupton, A., Hopkins, L., Simon, A. K., Bryant, C., Evans, T. J. (2014) Caspase-1 cleavage of the TLR adaptor TRIF inhibits autophagy and b-interferon production during Pseudomonas aeruginosa infection. Cell Host Microbe 15, 214-227.
28. Sanjuan, M. A., Dillon, C. P., Tait, S. W., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., Green, D. R. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257.
29. Shi, C. S., Kehrl, J. H. (2008) MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J. Biol. Chem. 283, 33175-33182.
30. Cooney, R., Baker, J., Brain, O., Danis, B., Pichulik, T., Allan, P., Ferguson, D. J., Campbell, B. J., Jewell, D., Simmons, A. (2010) NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat. Med. 16, 90-97.
31. Jounai, N., Takeshita, F., Kobiyama, K., Sawano, A., Miyawaki, A., Xin, K. Q., Ishii, K. J., Kawai, T., Akira, S., Suzuki, K., Okuda, K. (2007) The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. USA 104, 14050-14055.
32. Wu, B., Hur, S. (2015) How RIG-I like receptors activate MAVS. Curr. Opin. Virol. 12, 91-98.
33. Shin, D. M., Jeon, B. Y., Lee, H. M., Jin, H. S., Yuk, J. M., Song, C. H., Lee, S. H., Lee, Z. W., Cho, S. N., Kim, J. M., Friedman, R. L., Jo, E. K. (2010) Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog. 6, e1001230.
34. Tattoli, I., Sorbara, M. T., Vuckovic, D., Ling, A., Soares, F., Carneiro, L. A., Yang, C., Emili, A., Philpott, D. J., Girardin, S. E. (2012) Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe 11, 563-575.
35. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N., Sasakawa, C. (2005) Escape of intracellular Shigella from autophagy. Science 307, 727-731.
36. Dortet, L., Mostowy, S., Cossart, P. (2012) Listeria and autophagy escape: involvement of InlK, an internalin-like protein. Autophagy 8, 132-134.
37. Py, B. F., Lipinski, M. M., Yuan, J. (2007) Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy 3, 117-125.
38. Meunier, E., Dick, M. S., Dreier, R. F., Schürmann, N., Kenzelmann Broz, D., Warming, S., Roose-Girma, M., Bumann, D., Kayagaki, N., Takeda, K., Yamamoto, M., Broz, P. (2014) Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 509, 366-370.
39. Saitoh, T., Fujita, N., Jang, M. H., Uematsu, S., Yang, B. G., Satoh, T., Omori, H., Noda, T., Yamamoto, N., Komatsu, M., Tanaka, K., Kawai, T., Tsujimura, T., Takeuchi, O., Yoshimori, T., Akira, S. (2008) Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456, 264-268.
40. Harris, J., Hartman, M., Roche, C., Zeng, S. G., O’Shea, A., Sharp, F. A., Lambe, E. M., Creagh, E. M., Golenbock, D. T., Tschopp, J., Kornfeld, H., Fitzgerald, K. A., Lavelle, E. C. (2011) Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J. Biol. Chem. 286, 9587-9597.
41. Shi, C. S., Shenderov, K., Huang, N. N., Kabat, J., Abu-Asab, M., Fitzgerald, K. A., Sher, A., Kehrl, J. H. (2012) Activation of autophagy by inflammatory signals limits IL-1b production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 13, 255-263.
42. Lee, H. K., Lund, J. M., Ramanathan, B., Mizushima, N., Iwasaki, A. (2007) Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315, 1398-1401.
43. Henault, J., Martinez, J., Riggs, J. M., Tian, J., Mehta, P., Clarke, L., Sasai, M., Latz, E., Brinkmann, M. M., Iwasaki, A., Coyle, A. J., Kolbeck, R., Green, D. R., Sanjuan, M. A. (2012) Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 37, 986-997.
44. Sasai, M., Linehan, M. M., Iwasaki, A. (2010) Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 329, 1530-1534.
45. Deretic, V., Saitoh, T., Akira, S. (2013) Autophagy in infection, inflammation and immunity. Nat. Rev. Immunol. 13, 722-737.
46. Laplante, M., Sabatini, D. M. (2012) mTOR signaling in growth control and disease. Cell 149, 274-293.
47. Laplante, M., Sabatini, D. M. (2009) mTOR signaling at a glance. J. Cell Sci. 122, 3589-3594.
48. Copp, J., Manning, G., Hunter, T. (2009) TORC-specific phosphorylation of mammalian target of rapamycin (mTOR): phospho-Ser2481 is a marker for intact mTOR signaling complex 2. Cancer Res. 69, 1821-1827.
49. Jung, C. H., Jun, C. B., Ro, S. H., Kim, Y. M., Otto, N. M., Cao, J., Kundu, M., Kim, D. H. (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 20, 1992-2003.
50. Jung, C. H., Ro, S. H., Cao, J., Otto, N. M., Kim, D. H. (2010) mTOR regulation of autophagy. FEBS Lett. 584, 1287-1295.
51. Weichhart, T., Costantino, G., Poglitsch, M., Rosner, M., Zeyda, M., Stuhlmeier, K. M., Kolbe, T., Stulnig, T. M., Hörl, W. H., Hengstschläger, M., Müller, M., Säemann, M. D. (2008) The TSCmTOR signaling pathway regulates the innate inflammatory response. Immunity 29, 565-577.
52. Ivanov, S. S., Roy, C. R. (2013) Pathogen signatures activate a ubiquitination pathway that modulates the function of the metabolic checkpoint kinase mTOR. Nat. Immunol. 14, 1219-1228.
53. Ohtani, M., Hoshii, T., Fujii, H., Koyasu, S., Hirao, A., Matsuda, S. (2012) Cutting edge: mTORC1 in intestinal CD11c+ CD11b+ dendritic cells regulates intestinal homeostasis by promoting IL-10 production. J. Immunol. 188, 4736-4740.
54. Pan, H., O’Brien, T. F., Zhang, P., Zhong, X. P. (2012) The role of tuberous sclerosis complex 1 in regulating innate immunity. J. Immunol. 188, 3658-3666.
55. Hetz, C. (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102.
56. Schröder, M. (2008) Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 65, 862-894.
57. Tabas, I., Ron, D. (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13, 184-190.
58. Szegezdi, E., Logue, S. E., Gorman, A. M., Samali, A. (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7, 880-885.
59. Kouroku, Y., Fujita, E., Tanida, I., Ueno, T., Isoai, A., Kumagai, H., Ogawa, S., Kaufman, R. J., Kominami, E., Momoi, T. (2007) ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamineinduced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 14, 230-239.
60. Appenzeller-Herzog, C., Hall, M. N. (2012) Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling. Trends Cell Biol. 22, 274-282.
61. Qi, M., Zhou, H., Fan, S., Li, Z., Yao, G., Tashiro, S., Onodera, S., Xia, M., Ikejima, T. (2013) mTOR inactivation by ROS-JNK-p53 pathway plays an essential role in psedolaric acid B induced autophagydependent senescence in murine fibrosarcoma L929 cells. Eur. J. Pharmacol. 715, 76-88.
62. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H. P., Ron, D. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666.
63. Hasnain, S. Z., Lourie, R., Das, I., Chen, A. C., McGuckin, M. A. (2012) The interplay between endoplasmic reticulum stress and inflammation. Immunol. Cell Biol. 90, 260-270.
64. Clavarino, G., Cláudio, N., Couderc, T., Dalet, A., Judith, D., Camosseto, V., Schmidt, E. K., Wenger, T., Lecuit, M., Gatti, E., Pierre, P. (2012) Induction of GADD34 is necessary for dsRNA-dependent interferon-b production and participates in the control of Chikungunya virus infection. PLoS Pathog. 8, e1002708.
65. Goodall, J. C., Wu, C., Zhang, Y., McNeill, L., Ellis, L., Saudek, V., Gaston, J. S. (2010) Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc. Natl. Acad. Sci. USA 107, 17698-17703.
66. Martinon, F., Chen, X., Lee, A. H., Glimcher, L. H. (2010) TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11, 411-418.
67. Keestra-Gounder, A. M., Byndloss, M. X., Seyffert, N., Young, B. M., Chávez-Arroyo, A., Tsai, A. Y., Cevallos, S. A., Winter, M. G., Pham, O. H., Tiffany, C. R., de Jong, M. F., Kerrinnes, T., Ravindran, R., Luciw, P. A., McSorley, S. J., Bäumler, A. J., Tsolis, R. M. (2016) NOD1 and NOD2 signalling links ER stress with inflammation. Nature 532, 394-397.
68. Adolph, T. E., Tomczak, M. F., Niederreiter, L., Ko, H. J., Böck, J., Martinez-Naves, E., Glickman, J. N., Tschurtschenthaler, M., Hartwig, J., Hosomi, S., Flak, M. B., Cusick, J. L., Kohno, K., Iwawaki, T., Billmann-Born, S., Raine, T., Bharti, R., Lucius, R., Kweon, M. N., Marciniak, S. J., Choi, A., Hagen, S. J., Schreiber, S., Rosenstiel, P., Kaser, A., Blumberg, R. S. (2013) Paneth cells as a site of origin for intestinal inflammation. Nature 503, 272-276.
69. Adolph, T. E., Niederreiter, L., Blumberg, R. S., Kaser, A. (2012) Endoplasmic reticulum stress and inflammation. Dig. Dis. 30, 341-346.
70. Woo, C. W., Kutzler, L., Kimball, S. R., Tabas, I. (2012) Toll-like receptor activation suppresses ER stress factor CHOP and translation inhibition through activation of eIF2B. Nat. Cell Biol. 14, 192-200.
71. He, B. (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ. 13, 393-403.
72. Celli, J., Tsolis, R. M. (2015) Bacteria, the endoplasmic reticulum and the unfolded protein response: friends or foes? Nat. Rev. Microbiol. 13, 71-82.
73. Pillich, H., Loose, M., Zimmer, K. P., Chakraborty, T. (2012) Activation of the unfolded protein response by Listeria monocytogenes. Cell. Microbiol. 14, 949-964.
74. Malhotra, J. D., Kaufman, R. J. (2011) ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb. Perspect. Biol. 3, a004424.
75. Lebreton, A., Stavru, F., Cossart, P. (2015) Organelle targeting during bacterial infection: insights from Listeria. Trends Cell Biol. 25, 330-338.
76. Stavru, F., Bouillaud, F., Sartori, A., Ricquier, D., Cossart, P. (2011) Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc. Natl. Acad. Sci. USA 108, 3612-3617.
77. Narendra, D., Tanaka, A., Suen, D. F., Youle, R. J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803.
78. Wild, P., Dikic, I. (2010) Mitochondria get a Parkin’ ticket. Nat. Cell Biol. 12, 104-106.
79. Bulua, A. C., Simon, A., Maddipati, R., Pelletier, M., Park, H., Kim, K. Y., Sack, M. N., Kastner, D. L., Siegel, R. M. (2011) Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J. Exp. Med. 208, 519-533.
80. Nakahira, K., Haspel, J. A., Rathinam, V. A., Lee, S. J., Dolinay, T., Lam, H. C., Englert, J. A., Rabinovitch, M., Cernadas, M., Kim, H. P., Fitzgerald, K. A., Ryter, S. W., Choi, A. M. (2011) Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12, 222-230.
81. Zhou, R., Yazdi, A. S., Menu, P., Tschopp, J. (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221-225.
82. Zhong, Z., Umemura, A., Sanchez-Lopez, E., Liang, S., Shalapour, S., Wong, J., He, F., Boassa, D., Perkins, G., Ali, S. R., McGeough, M. D., Ellisman, M. H., Seki, E., Gustafsson, A. B., Hoffman, H. M., Diaz-Meco, M. T., Moscat, J., Karin, M. (2016) NF-kB restricts inflammasome activation via elimination of damaged mitochondria. Cell 164, 896-910.
83. West, A. P., Khoury-Hanold, W., Staron, M., Tal, M. C., Pineda, C. M., Lang, S. M., Bestwick, M., Duguay, B. A., Raimundo, N., MacDuff, D. A., Kaech, S. M., Smiley, J. R., Means, R. E., Iwasaki, A., Shadel, G. S. (2015) Mitochondrial DNA stress primes the antiviral innate immune response. Nature 520, 553-557.
84. Ciccia, A., Elledge, S. J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204.
85. Grenon, M., Gilbert, C., Lowndes, N. F. (2001) Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat. Cell Biol. 3, 844-847.
86. Nishi, R., Okuda, Y., Watanabe, E., Mori, T., Iwai, S., Masutani, C., Sugasawa, K., Hanaoka, F. (2005) Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol. Cell. Biol. 25, 5664-5674.
87. Krokan, H. E., Bjørås, M. (2013) Base excision repair. Cold Spring Harb. Perspect. Biol. 5, a012583.
88. Peña-Diaz, J., Jiricny, J. (2012) Mammalian mismatch repair: error-free or error-prone? Trends Biochem. Sci. 37, 206-214.
89. Chatzinikolaou, G., Karakasilioti, I., Garinis, G. A. (2014) DNA damage and innate immunity: links and trade-offs. Trends Immunol. 35, 429-435.
90. Zhang, X., Brann, T. W., Zhou, M., Yang, J., Oguariri, R. M., Lidie, K. B., Imamichi, H., Huang, D. W., Lempicki, R. A., Baseler, M. W., Veenstra, T. D., Young, H. A., Lane, H. C., Imamichi, T. (2011) Cutting edge: Ku70 is a novel cytosolic DNA sensor that induces type III rather than type I IFN. J. Immunol. 186, 4541-4545.
91. Ferguson, B. J., Mansur, D. S., Peters, N. E., Ren, H., Smith, G. L. (2012) DNA-PK is a DNA sensor for IRF-3-dependent innate immunity. eLife 1, e00047.
92. Kondo, T., Kobayashi, J., Saitoh, T., Maruyama, K., Ishii, K. J., Barber, G. N., Komatsu, K., Akira, S., Kawai, T. (2013) DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING trafficking. Proc. Natl. Acad. Sci. USA 110, 2969-2974.
93. Roth, S., Rottach, A., Lotz-Havla, A. S., Laux, V., Muschaweckh, A., Gersting, S. W., Muntau, A. C., Hopfner, K. P., Jin, L., Vanness, K., Petrini, J. H., Drexler, I., Leonhardt, H., Ruland, J. (2014) Rad50-CARD9 interactions link cytosolic DNA sensing to IL-1b production. Nat. Immunol. 15, 538-545.
94. Kang, C., Xu, Q., Martin, T. D., Li, M. Z., Demaria, M., Aron, L., Lu, T., Yankner, B. A., Campisi, J., Elledge, S. J. (2015) The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science 349, aaa5612.
95. Buchan, J. R., Parker, R. (2009) Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36, 932-941.
96. Onomoto, K., Yoneyama, M., Fung, G., Kato, H., Fujita, T. (2014) Antiviral innate immunity and stress granule responses. Trends Immunol. 35, 420-428.
97. Berlanga, J. J., Ventoso, I., Harding, H. P., Deng, J., Ron, D., Sonenberg, N., Carrasco, L., de Haro, C. (2006) Antiviral effect of the mammalian translation initiation factor 2alpha kinase GCN2 against RNA viruses. EMBO J. 25, 1730-1740.
98. Fung, G., Ng, C. S., Zhang, J., Shi, J., Wong, J., Piesik, P., Han, L., Chu, F., Jagdeo, J., Jan, E., Fujita, T., Luo, H. (2013) Production of a dominant-negative fragment due to G3BP1 cleavage contributes to the disruption of mitochondria-associated protective stress granules during CVB3 infection. PLoS One 8, e79546.
99. Ng, C. S., Jogi, M., Yoo, J. S., Onomoto, K., Koike, S., Iwasaki, T., Yoneyama, M., Kato, H., Fujita, T. (2013) Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J. Virol. 87, 9511-9522.
100. White, J. P., Cardenas, A. M., Marissen, W. E., Lloyd, R. E. (2007) Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2, 295-305.
101. Borghese, F., Michiels, T. (2011) The leader protein of cardioviruses inhibits stress granule assembly. J. Virol. 85, 9614-9622.
102. Okonski, K. M., Samuel, C. E. (2013) Stress granule formation induced by measles virus is protein kinase PKR dependent and impaired by RNA adenosine deaminase ADAR1. J. Virol. 87, 756-766.
103. Katoh, H., Okamoto, T., Fukuhara, T., Kambara, H., Morita, E., Mori, Y., Kamitani, W., Matsuura, Y. (2013) Japanese encephalitis virus core protein inhibits stress granule formation through an interaction with Caprin-1 and facilitates viral propagation. J. Virol. 87, 489-502.
104. Onomoto, K., Jogi, M., Yoo, J. S., Narita, R., Morimoto, S., Takemura, A., Sambhara, S., Kawaguchi, A., Osari, S., Nagata, K., Matsumiya, T., Namiki, H., Yoneyama, M., Fujita, T. (2012) Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS One 7, e43031.