Macroautophagy during innate immune activation

Frontiers in Microbiology

Volumn 2, Issue APR, 2011, Pages

  Münz, Christian ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Atg; Inflammasome; NOD; RIG I; TLR

Indexed keywords

EID: 84655161743     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00072     Document Type: Article

References (95)

1. Alonso, S., Pethe, K., Russell, D. G., and Purdy, G. E. (2007). Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc. Natl. Acad. Sci. U.S.A. 104, 6031-6036.
2. Birmingham, C. L., Canadien, V., Kaniuk, N. A., Steinberg, B. E., Higgins, D. E., and Brumell, J. H. (2008). Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 451, 350-354.
3. Bjorkoy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H., and Johansen, T. (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.
4. Cadwell, K., Liu, J. Y., Brown, S. L., Miyoshi, H., Loh, J., Lennerz, J. K., Kishi, C., Kc, W., Carrero, J. A., Hunt, S., Stone, C. D., Brunt, E. M., Xavier, R. J., Sleckman, B. P., Li, E., Mizushima, N., Stappenbeck, T. S., and Virgin, H. W. IV. (2008). A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456, 259-263.
5. Cadwell, K., Patel, K. K., Maloney, N. S., Liu, T. C., Ng, A. C., Storer, C. E., Head, R. D., Xavier, R., Stappenbeck, T. S., and Virgin, H. W. (2010). Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141, 1135-1145.
6. Celli, J., de Chastellier, C., Franchini, D. M., Pizarro-Cerda, J., Moreno, E., and Gorvel, J. P. (2003). Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J. Exp. Med. 198, 545-556.
7. Chaturvedi, A., Dorward, D., and Pierce, S. K. (2008). The B cell receptor governs the subcellular location of Toll-like receptor 9 leading to hyperre-sponses to DNA-containing antigens. Immunity 28, 799-809.
8. Cooney, R., Baker, J., Brain, O., Danis, B., Pichulik, T., Allan, P., Ferguson, D. J., Campbell, B. J., Jewell, D., and Simmons, A. (2010). NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat. Med. 16, 90-97.
9. Dales, S., Eggers, H. J., Tamm, I., and Palade, G. E. (1965). Electron microscopic study of the formation of poliovirus. Virology 26, 379-389.
10. Delgado, M. A., Elmaoued, R. A., Davis, A. S., Kyei, G., and Deretic, V. (2008). Toll-like receptors control autophagy. EMBO J. 27, 1110-1121.
11. Djavaheri-Mergny, M., Amelotti, M., Mathieu, J., Besancon, F., Bauvy, C., Souquere, S., Pierron, G., and Codogno, P. (2006). NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J. Biol. Chem. 281, 30373-30382.
12. Dreux, M., and Chisari, F. V. (2010). Viruses and the autophagy machinery. Cell Cycle 9, 1295-1307.
13. Dreux, M., Gastaminza, P., Wieland, S. F., and Chisari, F. V. (2009). The autophagy machinery is required to initiate hepatitis C virus replication. Proc. Natl. Acad. Sci. U.S.A. 106, 14046-14051.
14. English, L., Chemali, M., Duron, J., Rondeau, C., Laplante, A., Gingras, D., Alexander, D., Leib, D., Norbury, C., Lippe, R., and Desjardins, M. (2009). Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat. Immunol. 10, 480-487.
15. Espert, L., Denizot, M., Grimaldi, M., Robert-Hebmann, V., Gay, B., Varbanov, M., Codogno, P., and Biard-Piechaczyk, M. (2006). Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J. Clin. Invest. 116, 2161-2172.
16. Fader, C. M., Sanchez, D., Furlan, M., and Colombo, M. I. (2008). Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells. Traffic 9, 230-250.
17. Gannage, M., Dormann, D., Albrecht, R., Dengjel, J., Torossi, T., Ramer, P. C., Lee, M., Strowig, T., Arrey, F., Conenello, G., Pypaert, M., Andersen, J., Garcia-Sastre, A., and Münz, C. (2009). Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 6, 367-380.
18. Gannage, M., and Münz, C. (2010). MHC presentation via autophagy and how viruses escape from it. Semin. Immunopathol. 32, 373-381.
19. Gutierrez, M. G., Master, S. S., Singh, S. B., Taylor, G. A., Colombo, M. I., and Deretic, V. (2004). Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766.
20. Hailey, D. W., Rambold, A. S., Satpute-Krishnan, P., Mitra, K., Sougrat, R., Kim, P. K., and Lippincott-Schwartz, J. (2010). Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141, 656-667.
21. Hampe, J., Franke, A., Rosenstiel, P., Till, A., Teuber, M., Huse, K., Albrecht, M., Mayr, G., De La Vega, F. M., Briggs, J., Gunther, S., Prescott, N. J., Onnie, C. M., Hasler, R., Sipos, B., Folsch, U. R., Lengauer, T., Platzer, M., Mathew, C. G., Krawczak, M., and Schreiber, S. (2007). A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 39, 207-211.
22. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., and Mizushima, N. (2006). Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889.
23. Harris, J., De Haro, S. A., Master, S. S., Keane, J., Roberts, E. A., Delgado, M., and Deretic, V. (2007). T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity 27, 505-517.
24. Harris, J., Hope, J. C., and Lavelle, E. C. (2009). Autophagy and the immune response to TB. Transbound. Emerg. Dis. 56, 248-254.
25. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2009). A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437.
26. He, C., and Klionsky, D. J. (2009). Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93.
27. He, C., Song, H., Yorimitsu, T., Monastyrska, I., Yen, W. L., Legakis, J. E., and Klionsky, D. J. (2006). Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J. Cell Biol. 175, 925-935.
28. Huang, J., Canadien, V., Lam, G. Y., Steinberg, B. E., Dinauer, M. C., Magalhaes, M. A., Glogauer, M., Grinstein, S., and Brumell, J. H. (2009). Activation of antibacterial autophagy by NADPH oxidases. Proc. Natl. Acad. Sci. U.S.A. 106, 6226-6231.
29. Hugot, J. P., Chamaillard, M., Zouali, H., Lesage, S., Cezard, J. P., Belaiche, J., Almer, S., Tysk, C., O'Morain, C. A., Gassull, M., Binder, V., Finkel, Y., Cortot, A., Modigliani, R., Laurent-Puig, P., Gower-Rousseau, C., Macry, J., Colombel, J. F., Sahbatou, M., and Thomas, G. (2001). Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411, 599-603.
30. Jackson, W. T., Giddings, T. H. Jr., Taylor, M. P., Mulinyawe, S., Rabinovitch, M., Kopito, R. R., and Kirkegaard, K. (2005). Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3, e156. doi: 10.1371/journal.pbio.0030156
31. Jager, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P., and Eskelinen, E. L. (2004). Role for Rab7 in maturation of late autophagic vacuoles. J. Cell. Sci. 117(Pt 20), 4837-4848.
32. Jia, K., Thomas, C., Akbar, M., Sun, Q., Adams-Huet, B., Gilpin, C., and Levine, B. (2009). Autophagy genes protect against Salmonella typhimurium infection and mediate insulin signaling-regulated pathogen resistance. Proc. Natl. Acad. Sci. U.S.A. 106, 14564-14569.
33. Jounai, N., Takeshita, F., Kobiyama, K., Sawano, A., Miyawaki, A., Xin, K. Q., Ishii, K. J., Kawai, T., Akira, S., Suzuki, K., and Okuda, K. (2007). The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. U.S.A. 104, 14050-14055.
34. Keller, C. W., Fokken, C., Turville, S. G., Lünemann, A., Schmidt, J., Münz, C., and Lünemann, J. D. (2011). TNF-alpha induces macroautophagy and regulates MHC class II expression in human skeletal muscle cells. J. Biol. Chem. 286, 3970-3980.
35. Kirkin, V., Lamark, T., Sou, Y. S., Bjorkoy, G., Nunn, J. L., Bruun, J. A., Shvets, E., McEwan, D. G., Clausen, T. H., Wild, P., Bilusic, I., Theurillat, J. P., Overvatn, A., Ishii, T., Elazar, Z., Komatsu, M., Dikic, I., and Johansen, T. (2009). A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33, 505-516.
36. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., and Tanaka, K. (2006). Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880-884.
37. Kuballa, P., Huett, A., Rioux, J. D., Daly, M. J., and Xavier, R. J. (2008). Impaired autophagy of an intracellular pathogen induced by a Crohn's disease associated ATG16L1 variant. PLoS ONE 3, e3391. doi: 10.1371/journal. pone.0003391
38. Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., and Mizushima, N. (2004). The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036.
39. Kyei, G. B., Dinkins, C., Davis, A. S., Roberts, E., Singh, S. B., Dong, C., Wu, L., Kominami, E., Ueno, T., Yamamoto, A., Federico, M., Panganiban, A., Vergne, I., and Deretic, V. (2009). Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J. Cell Biol. 186, 255-268.
40. Lapaquette, P., Glasser, A. L., Huett, A., Xavier, R. J., and Darfeuille-Michaud, A. (2010). Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly. Cell Microbiol. 12, 99-113.
41. Lee, D. Y., Lee, J., and Sugden, B. (2009). The unfolded protein response and autophagy: herpesviruses rule! J. Virol. 83, 1168-1172.
42. Lee, D. Y., and Sugden, B. (2008). The latent membrane protein 1 oncogene modifies B-cell physiology by regulating autophagy. Oncogene 27, 2833-2842.
43. Lee, H. K., Lund, J. M., Ramanathan, B., Mizushima, N., and Iwasaki, A. (2007). Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315, 1398-1401.
44. Lee, H. K., Mattei, L. M., Steinberg, B. E., Alberts, P., Lee, Y. H., Chervonsky, A., Mizushima, N., Grinstein, S., and Iwasaki, A. (2010). In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 32, 227-239.
45. Lee, Y. R., Lei, H. Y., Liu, M. T., Wang, J. R., Chen, S. H., Jiang-Shieh, Y. F., Lin, Y. S., Yeh, T. M., Liu, C. C., and Liu, H. S. (2008). Autophagic machinery activated by dengue virus enhances virus replication. Virology 374, 240-248.
46. Levine, B., and Deretic, V. (2007). Unveiling the roles of autophagy in innate and adaptive immunity. Nat. Rev. Immunol. 7, 767-777.
47. Liang, C., Lee, J. S., Inn, K. S., Gack, M. U., Li, Q., Roberts, E. A., Vergne, I., Deretic, V., Feng, P., Akazawa, C., and Jung, J. U. (2008). Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10, 776-787.
48. Liang, X. H., Kleeman, L. K., Jiang, H. H., Gordon, G., Goldman, J. E., Berry, G., Herman, B., and Levine, B. (1998). Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72, 8586-8596.
49. Lin, L. T., Dawson, P. W., and Richardson, C. D. (2010). Viral interactions with macroautophagy: a double-edged sword. Virology 402, 1-10.
50. Lynch-Day, M. A., Bhandari, D., Menon, S., Huang, J., Cai, H., Bartholomew, C. R., Brumell, J. H., Ferro-Novick, S., and Klionsky, D. J. (2010). Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy. Proc. Natl. Acad. Sci. U.S.A. 107, 7811-7816.
51. Massey, A. C., Zhang, C., and Cuervo, A. M. (2006). Chaperone-mediated autophagy in aging and disease. Curr. Top. Dev. Biol. 73, 205-235.
52. Mathew, R., Karp, C. M., Beaudoin, B., Vuong, N., Chen, G., Chen, H. Y., Bray, K., Reddy, A., Bhanot, G., Gelinas, C., Dipaola, R. S., Karantza-Wadsworth, V., and White, E. (2009). Autophagy suppresses tumorigenesis through elimination of p62. Cell 137, 1062-1075.
53. Matsunaga, K., Saitoh, T., Tabata, K., Omori, H., Satoh, T., Kurotori, N., Maejima, I., Shirahama-Noda, K., Ichimura, T., Isobe, T., Akira, S., Noda, T., and Yoshimori, T. (2009). Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat. Cell Biol. 11, 385-396.
54. McCarroll, S. A., Huett, A., Kuballa, P., Chilewski, S. D., Landry, A., Goyette, P., Zody, M. C., Hall, J. L., Brant, S. R., Cho, J. H., Duerr, R. H., Silverberg, M. S., Taylor, K. D., Rioux, J. D., Altshuler, D., Daly, M. J., and Xavier, R. J. (2008). Deletion polymorphism upstream of IRGM associated with altered IRGM expression and Crohn's disease. Nat. Genet. 40, 1107-1112.
55. Meixlsperger, S., and Münz, C. (2009). Morbus Crohn - a disease of failing macroautophagy in the immune system? Int. Immunol. 21, 1205-1211.
56. Mizushima, N., and Klionsky, D. J. (2007). Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 27, 19-40.
57. Mizushima, N., Levine, B., Cuervo, A. M., and Klionsky, D. J. (2008). Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075.
58. Münz, C. (2009). Enhancing immunity through autophagy. Annu. Rev. Immunol. 27, 423-429.
59. Nakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., Nara, A., Funao, J., Nakata, M., Tsuda, K., Hamada, S., and Yoshimori, T. (2004). Autophagy defends cells against invading group A Streptococcus. Science 306, 1037-1040.
60. Nakatogawa, H., Ichimura, Y., and Ohsumi, Y. (2007). Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130, 165-178.
61. Nedjic, J., Aichinger, M., Emmerich, J., Mizushima, N., and Klein, L. (2008). Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 455, 396-400.
62. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N., and Sasakawa, C. (2005). Escape of intracellular Shigella from autophagy. Science 307, 727-731.
63. Ogura, Y., Bonen, D. K., Inohara, N., Nicolae, D. L., Chen, F. F., Ramos, R., Britton, H., Moran, T., Karaliuskas, R., Duerr, R. H., Achkar, J. P., Brant, S. R., Bayless, T. M., Kirschner, B. S., Hanauer, S. B., Nunez, G., and Cho, J. H. (2001). A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411, 603-606.
64. Ohsumi, Y. (2001). Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2, 211-216.
65. Orvedahl, A., Alexander, D., Talloczy, Z., Sun, Q., Wei, Y., Zhang, W., Burns, D., Leib, D., and Levine, B. (2007). HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1, 23-35.
66. Orvedahl, A., MacPherson, S., Sumpter, R. Jr., Talloczy, Z., Zou, Z., and Levine, B. (2010). Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7, 115-127.
67. Parkes, M., Barrett, J. C., Prescott, N. J., Tremelling, M., Anderson, C. A., Fisher, S. A., Roberts, R. G., Nimmo, E. R., Cummings, F. R., Soars, D., Drummond, H., Lees, C. W., Khawaja, S. A., Bagnall, R., Burke, D. A., Todhunter, C. E., Ahmad, T., Onnie, C. M., McArdle, W., Strachan, D., Bethel, G., Bryan, C., Lewis, C. M., Deloukas, P., Forbes, A., Sanderson, J., Jewell, D. P., Satsangi, J., Mansfield, J. C., Cardon, L., and Mathew, C. G. (2007). Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat. Genet. 39, 830-832.
68. Ponpuak, M., Davis, A. S., Roberts, E. A., Delgado, M. A., Dinkins, C., Zhao, Z., Virgin, H. W. t., Kyei, G. B., Johansen, T., Vergne, I., and Deretic, V. (2010). Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 32, 329-341.
69. Pua, H. H., Dzhagalov, I., Chuck, M., Mizushima, N., and He, Y. W. (2007). A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J. Exp. Med. 204, 25-31.
70. Ravikumar, B., Moreau, K., Jahreiss, L., Puri, C., and Rubinsztein, D. C. (2010). Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 12, 747-757.
71. Rioux, J. D., Xavier, R. J., Taylor, K. D., Silverberg, M. S., Goyette, P., Huett, A., Green, T., Kuballa, P., Barmada, M. M., Datta, L. W., Shugart, Y. Y., Griffiths, A. M., Targan, S. R., Ippoliti, A. F., Bernard, E. J., Mei, L., Nicolae, D. L., Regueiro, M., Schumm, L. P., Steinhart, A. H., Rotter, J. I., Duerr, R. H., Cho, J. H., Daly, M. J., and Brant, S. R. (2007). Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 39, 596-604.
72. 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., and Akira, S. (2008). Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456, 264-268.
73. Sanjuan, M. A., Dillon, C. P., Tait, S. W., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., and Green, D. R. (2007). Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257.
74. Schmid, D., and Münz, C. (2007). Innate and adaptive immunity through autophagy. Immunity 26, 11-21.
75. Shahnazari, S., and Brumell, J. H. (2009). Eating twice for the sake of immunity: a phagocytic receptor that activates autophagy. Cell Host Microbe 6, 297-298.
76. Shelly, S., Lukinova, N., Bambina, S., Berman, A., and Cherry, S. (2009). Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 30, 588-598.
77. Shi, C. S., and Kehrl, J. H. (2008). MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J. Biol. Chem. 283, 33175-33182.
78. Shi, C. S., and Kehrl, J. H. (2010). TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci. Signal. 3, ra42.
79. Singh, S. B., Davis, A. S., Taylor, G. A., and Deretic, V. (2006). Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313, 1438-1441.
80. Sir, D., Chen, W. L., Choi, J., Wakita, T., Yen, T. S., and Ou, J. H. (2008). Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 48, 1054-1061.
81. Stappenbeck, T. S., Rioux, J. D., Mizoguchi, A., Saitoh, T., Huett, A., Darfeuille-Michaud, A., Wileman, T., Mizushima, N., Carding, S., Akira, S., Parkes, M., and Xavier, R. J. (2011). Crohn disease: a current perspective on genetics, autophagy and immunity. Autophagy 7, 355-374.
82. Suzuki, T., Franchi, L., Toma, C., Ashida, H., Ogawa, M., Yoshikawa, Y., Mimuro, H., Inohara, N., Sasakawa, C., and Nunez, G. (2007). Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 3, e111. doi: 10.1371/journal. ppat.0030111
83. Tal, M. C., Sasai, M., Lee, H. K., Yordy, B., Shadel, G. S., and Iwasaki, A. (2009). Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 2770-2775.
84. Talloczy, Z., Jiang, W., Virgin, H. W. IV, Leib, D. A., Scheuner, D., Kaufman, R. J., Eskelinen, E. L., and Levine, B. (2002). Regulation of starvation-and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 99, 190-195.
85. Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E. L., Hartmann, D., Lullmann-Rauch, R., Janssen, P. M., Blanz, J., von Figura, K., and Saftig, P. (2000). Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406, 902-906.
86. Taylor, G. S., Mautner, J., and Münz, C. (2011) Autophagy in herpesvirus immune control and immune escape. Herpesviridae 2,2.
87. Thurston, T. L., Ryzhakov, G., Bloor, S., von Muhlinen, N., and Randow, F. (2009). The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10, 1215-1221.
88. Travassos, L. H., Carneiro, L. A., Ramjeet, M., Hussey, S., Kim, Y. G., Magalhaes, J. G., Yuan, L., Soares, F., Chea, E., Le Bourhis, L., Boneca, I. G., Allaoui, A., Jones, N. L., Nunez, G., Girardin, S. E., and Philpott, D. J. (2010). Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 11, 55-62.
89. Xu, Y., Jagannath, C., Liu, X. D., Sharafkhaneh, A., Kolodziejska, K. E., and Eissa, N. T. (2007). Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 27, 135-144.
90. Yano, T., Mita, S., Ohmori, H., Oshima, Y., Fujimoto, Y., Ueda, R., Takada, H., Goldman, W. E., Fukase, K., Silverman, N., Yoshimori, T., and Kurata, S. (2008). Autophagic control of listeria through intracellular innate immune recognition in Drosophila. Nat. Immunol. 9, 908-916.
91. Yen, W. L., Shintani, T., Nair, U., Cao, Y., Richardson,B., C., Li, Z., Hughson, F. M., Baba, M., and Klionsky, D. J. (2010). The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J. Cell Biol. 188, 101-114.
92. Yla-Anttila, P., Vihinen, H., Jokitalo, E., and Eskelinen, E. L. (2009). 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5, 1180-1185
93. Yoshikawa, Y., Ogawa, M., Hain, T., Yoshida, M., Fukumatsu, M., Kim, M., Mimuro, H., Nakagawa, I., Yanagawa, T., Ishii, T., Kakizuka, A., Sztul, E., Chakraborty, T., and Sasakawa, C. (2009). Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 11, 1233-1240.
94. Zhang, C., and Cuervo, A. M. (2008). Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat. Med. 14, 959-965.
95. Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., Heintz, N., and Yue, Z. (2009). Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 11, 468-476.