Autophagosomal protein dynamics and influenza virus infection

Frontiers in Immunology

Volumn 3, Issue MAR, 2012, Pages

  Dumit, Verónica I ^a   Dengjel, Jörn ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Autophagosome; Autophagy; Influenza; Organelle; Protein interaction; Ubiquitin

Indexed keywords

EID: 84868383605     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00043     Document Type: Review

References (88)

1. Abeliovich,H.,Dunn,W. A.,Kim,J.,and Klionsky, D. J. (2000). Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J. Cell Biol. 151, 1025-1034.
2. Ait-Goughoulte, M., Kanda, T., Meyer, K., Ryerse, J. S., Ray, R. B., and Ray, R. (2008). Hepatitis C virus genotype 1a growth and induc-tion of autophagy. J. Virol. 82, 2241-2249.
3. Axe, E. L., Walker, S. A., Manifava, M., Chandra, P., Roderick, H. L., Haber-Mann,A., Griffiths, G., and Ktistakis, N. T. (2008). Autophagosome for-mation from membrane compart-ments enriched in phosphatidyli-nositol 3-phosphate and dynami-cally connected to the endoplas-mic reticulum. J. Cell Biol. 182, 685-701.
4. Bjorkoy, G., Lamark, T., Brech, A., Out-Zen, 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.
5. Blanchet, F. P., Moris, A., Nikolic, D. S., Lehmann, M., Cardinaud, S., Stalder, R., Garcia, E., Dinkins, C., Leuba, F., Wu, L., Schwartz, O., Deretic, V., and Piguet, V. (2010). Human immunodeficiency virus-1 inhibi-tion of immunoamphisomes in den-dritic cells impairs early innate and adaptive immune responses. Immu-nity 32, 654-669.
6. Burman, C., and Ktistakis, N. T. (2010). Regulation of autophagy by phos-phatidylinositol 3-phosphate. FEBS Lett. 584, 1302-1312.
7. Chan, E. Y. (2009). mTORC1 phospho-rylates the ULK1-mAtg13-FIP200 autophagy regulatory complex. Sci. Signal. 2, pe51.
8. Chen, Y., and Klionsky, D. J. (2011). The regulation of autophagy -unan-swered questions. J. Cell Sci. 124, 161-170.
9. Comber, J. D., Robinson, T. M., Sicil-Iano, N. A., Snook, A. E., and Eisenlohr, L. C. (2011). Func-tional macroautophagy induction by influenza A virus without a contri-bution to major histocompatibility complex class II-restricted presenta-tion. J. Virol. 85, 6453-6463.
10. Crotzer, V. L., and Blum, J. S. (2010). Autophagy and adaptive immunity. Immunology 131, 9-17.
11. Dai, J., Wang, G., Li, W., Zhang, L., Yang, J., Zhao, X., Chen, X., Xu, Y., and Li, K. (2012). High-throughput screening for anti-influenza a virus drugs and study of the mechanism of procyani-din on influenza a virus induced autophagy. J. Biomol. Screen. doi:10.1177/1087057111435236
12. Dales, S., Eggers, H. J., Tamm, I., and Palade, G. E. (1965). Electron micro-scopic study of the formation of poliovirus. Virology 26, 379-389.
13. Dengjel, J., Hoyer-Hansen, M., Nielsen, M. O., Eisenberg, T., Harder, L. M., Schandorff, S., Farkas, T., Kirkegaard, T., Becker, A. C., Schroeder, S., Vanselow, K., Lund-Berg, E., Nielsen, M. M., Kristensen, A. R., Akimov, V., Bunkenborg, J., Madeo, F., Jäättelä, M., and Ander-sen, J. S. (2012). Identification of autophagosome-associated proteins and regulators by quantitative proteomic analysis and genetic screens. Mol. Cell. Proteomics. doi:10.1074/mcp.M111.014035
14. Dengjel, J., Schoor, O., Fischer, R., Reich, M., Kraus, M., Müller, M., Kreym-Borg, K., Altenberend, F., Branden-Burg, J., Kalbacher, H., Brock, R., Driessen, C., Rammensee, H. G., and Stevanovic, S. (2005). Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 7922-7927.
15. Deretic, V., and Levine, B. (2009). Autophagy, immunity, and micro-bial adaptations. Cell Host Microbe 5, 527-549.
16. Deshaies, R. J., and Joazeiro, C. A. (2009). RING domain E3 ubiqui-tin ligases. Annu. Rev. Biochem. 78, 399-434.
17. Dice, J. F. (2007). Chaperone-mediated autophagy. Autophagy 3, 295-299.
18. Dörfel, D., Appel, S., Grünebach, F., Weck, M. M., Müller, M. R., Heine, A., and Brossart, P. (2005). Pro-cessing and presentation of HLA class I and II epitopes by dendritic cells after transfection with in vitro-transcribed MUC1 RNA. Blood 105, 3199-3205.
19. 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.
20. Engelke, R., Becker, A. C., and Dengjel, J. (2012). The degrada-tive inventory of the cell: pro-teomic insights. Antioxid Redox Sig-nal. doi:10.1089/ars.2011.4393
21. English,L.,Chemali,M.,Duron,J.,Ron-Deau, C., Laplante, A., Gingras, D., Alexander, D., Leib, D., Norbury, C., Lippé, R., and Desjardins, M. (2009). Autophagy enhances the presenta-tion of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat. Immunol. 10, 480-487.
22. Fujita, N., Itoh, T., Omori, H., Fukuda, M., Noda, T., and Yoshimori, T. (2008a). The Atg16L complex spec-ifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 19, 2092-2100.
23. Fujita, N., Hayashi-Nishino, M., Fuku-Moto, H., Omori, H., Yamamoto, A., Noda, T., and Yoshimori, T. (2008b). An Atg4B mutant hampers the lipi-dation of LC3 paralogues and causes defects in autophagosome closure. Mol. Biol. Cell 19, 4651-4659.
24. Gannagé, M., Dormann, D., Albrecht, R., Dengjel, J., Torossi, T., Rämer, P. C., Lee, M., Strowig, T., Arrey, F., Conenello, G., Pypaert, M., Ander-Sen, J., García-Sastre, A., and Münz, C. (2009). Matrix protein 2 of influenza A virus blocks autophago-some fusion with lysosomes. Cell Host Microbe 6, 367-380.
25. Gannagé, M., Rämer, P. C., and Münz, C. (2010). Targeting Beclin 1 for viral subversion of macroautophagy. Autophagy 6, 166-167.
26. Glatter, T., Schittenhelm, R. B., Rinner, O., Roguska, K., Wepf, A., Jünger, M. A., Köhler, K., Jevtov, I., Choi, H., Schmidt, A., Nesvizhskii, A. I., Stocker, H., Hafen, E., Aebersold, R., and Gstaiger, M. (2011). Mod-ularity and hormone sensitivity of the Drosophila melanogaster insulin receptor/target of rapamycin inter-action proteome. Mol. Syst. Biol. 7, 547-547.
27. Gordon, P. B., and Seglen, P. O. (1988). Prelysosomal convergence of autophagic and endocytic path-ways. Biochem. Biophys. Res. Com-mun. 151, 40-47.
28. Grabbe, C., Husnjak, K., and Dikic, I. (2011). The spatial and temporal organization of ubiquitin networks. Nat. Rev. Mol. Cell Biol. 12, 295-307.
29. 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 autophago-some biogenesis during starvation. Cell 141, 656-667.
30. Hanada, T., Noda, N. N., Satomi, Y., Ichimura, Y., Fujioka, Y., Takao, T., Inagaki, F., and Ohsumi, Y. (2007). The Atg12-Atg5 conjugate has a novel E3-like activity for protein lip-idation in autophagy. J. Biol. Chem. 282, 37298-37302.
31. 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 forma-tion. Nat. Cell Biol. 11, 1433-1437.
32. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2010). Elec-tron tomography reveals the endo-plasmic reticulum as a membrane source for autophagosome forma-tion. Autophagy 6, 301-303.
33. Hicke, L., Schubert, H. L., and Hill, C. P. (2005). Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6, 610-621
34. Hochstrasser, M. (2009). Origin and function of ubiquitin-like proteins. Nature 458, 422-429.
35. Huang, J., Lam, G. Y., and Brumell, J. H. (2011). Autophagy sig-naling through reactive oxygen species. Antioxid Redox Signal. 14, 2215-2231.
36. Humphrey, W., Dalke, A., and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38.
37. Inoue, Y., and Klionsky, D. J. (2010). Regulation of macroautophagy in Saccharomyces cerevisiae. Semin. Cell Dev. Biol. 21, 664-670.
38. Jackson, W. T., Giddings, T. H., Taylor, M. P., Mulinyawe, S., Rabinovitch, M., Kopito, R. R., and Kirkegaard, K. (2005). Subversion of cellu-lar autophagosomal machinery by RNA viruses. PLoS Biol. 3, 861-871. doi:10.1371/journal.pbio.0030156
39. Kim, J., and Guan, K. L. (2011). Amino acid signaling in TOR acti-vation. Annu. Rev. Biochem. 80, 1001-1032.
40. 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., Øvervatn, 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.
41. Klionsky, D. J., Cuervo, A. M., and Seglen, P. O. (2007). Methods for monitoring autophagy from yeast to human. Autophagy 3, 181-206.
42. Krauss, M., and Haucke, V. (2007). Phosphoinositide-metabolizing enzymes at the interface between membrane traffic and cell signalling. EMBO Rep. 8, 241-246.
43. Kristensen, A. R., Schandorff, S., Hoyer-Hansen, M., Nielsen, M. O., Jäät-telä, M., Dengjel, J., and Andersen, J. S. (2008). Ordered organelle degra-dation during starvation-induced autophagy. Mol. Cell. Proteomics 7, 2419-2428.
44. 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 path-way intersects with HIV-1 biosyn-thesis and regulates viral yields in macrophages. J. Cell Biol. 186, 255-268.
45. Lamark, T., Kirkin, V., Dikic, I., and Johansen, T. (2009). NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 8, 1986-1990.
46. Law, A. H., Lee, D. C., Yuen, K. Y., Peiris, M., and Lau, A. S. (2010). Cellular response to influenza virus infec-tion: a potential role for autophagy in CXCL10 and interferon-alpha induction. Cell. Mol. Immunol. 7, 263-270.
47. Leevers, S. J., Vanhaesebroeck, B., and Waterfield, M. D. (1999). Sig-nalling through phosphoinositide 3-kinases: the lipids take centre stage. Curr. Opin. Cell Biol. 11, 219-225.
48. Levine, B., Mizushima, N., and Virgin, H. W. (2011). Autophagy in immu-nity and inflammation. Nature 469, 323-335.
49. Liang, C., E, X., and Jung, J. U. (2008). Downregulation of autophagy by herpesvirus Bcl-2 homologs. Autophagy 4, 268-272.
50. Matsumoto, G., Wada, K., Okuno, M., Kurosawa, M., and Nukina, N. (2011). Serine 403 phosphoryla-tion of p62/SQSTM1 regulates selec-tive autophagic clearance of ubiq-uitinated proteins. Mol. Cell 44, 279-289.
51. McLean, J. E., Datan, E., Matassov, D., and Zakeri, Z. F. (2009). Lack of Bax prevents influenza A virus-induced apoptosis and causes diminished viral replication. J. Virol. 83, 8233-8246.
52. Mizushima, N. (2010). The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 22, 132-139.
53. Mizushima, N., Yoshimori, T., and Ohsumi, Y. (2011). The role of atg proteins in autophagosome forma-tion. Annu.Rev.CellDev.Biol.27, 107-132.
54. Münz, C. (2011a). Beclin-1 targeting for viral immune escape. Viruses 3, 1166-1178.
55. Münz, C. (2011b). Antigen process-ing by macroautophagy for MHC presentation. Front. Immunol. 2:1-7. doi:10.3389/fimmu.2011.00042
56. Nair, U., Jotwani, A., Geng, J., Gammoh, N., Richerson, D., Yen, W. L., Grif-Fith, J., Nag, S., Wang, K., Moss, T., Baba, M., McNew, J. A., Jiang, X., Reggiori, F., Melia, T. J., and Klion-Sky, D. J. (2011). SNARE proteins are required for macroautophagy. Cell 146, 290-302.
57. Nakatogawa, H., Ichimura, Y., and Ohsumi,Y. (2007).Atg8,a ubiquitin-like protein required for autophago-some formation, mediates mem-brane tethering and hemifusion. Cell 130, 165-178.
58. Nimmerjahn, F., Milosevic, S., Behrends, U., Jaffee, E. M., Par-Doll, D. M., Bornkamm, G. W., and Mautner, J. (2003). Major histocom-patibility complex class II-restricted presentation of a cytosolic antigen by autophagy. Eur. J. Immunol. 33, 1250-1259.
59. Noda, T., Fujita, N., and Yoshimori, T. (2009). The late stages of autophagy: how does the end begin? Cell Death Differ. 16, 984-990.
60. Noda, T., Matsunaga, K., Taguchi-Atarashi, N., and Yoshimori, T. (2010). Regulation of membrane biogenesis in autophagy via PI3P dynamics. Semin. Cell Dev. Biol. 21, 671-676.
61. Novak, I., Kirkin, V., McEwan, D. G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Löhr, F., Popovic, D., Occhipinti, A., Reichert, A. S., Terzic, J., Dötsch, V., Ney, P. A., and Dikic, I. (2010). Nix is a selec-tive autophagy receptor for mito-chondrial clearance. EMBO Rep. 11, 45-51.
62. Oberstein, A., Jeffrey, P. D., and Shi, Y. (2007). Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J. Biol. Chem. 282, 13123-13132.
63. Orvedahl, A., Alexander, D., Tallóczy, Z., Sun, Q., Wei, Y., Zhang, W., Burns, D., Leib, D. A., and Levine, B. (2007). HSV-1 ICP34.5 con-fers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1, 23-35.
64. Paludan, C., Schmid, D., Landthaler, M., Vockerodt, M., Kube, D., Tuschl, T., and Münz, C. (2005). Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Sci-ence 307, 593-596.
65. Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Øvervatn, A., Bjorkoy, G., and Johansen, T. (2007). p62/SQSTM1 binds directly to Atg8/LC3 to facil-itate degradation of ubiquitinated proteinaggregatesbyautophagy.J. Biol. Chem. 282, 24131-24145.
66. Polson, H. E., de Lartigue, J., Rigden, D. J., Reedijk, M., Urbé, S., Clague, M. J., and Tooze, S. A. (2010). Mam-malian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipida-tion. Autophagy 6, 506-522.
67. Ravikumar, B., Moreau, K., Jahreiss, L., Puri, C., and Rubinsztein, D. C. (2010). Plasma membrane con-tributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 12, 747-757.
68. Rossman, J. S., and Lamb, R. A. (2009). Autophagy, apoptosis, and the influenza virus M2 protein. Cell Host Microbe 6, 299-300.
69. Scherz-Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L., and Elazar, Z. (2007). Reactive oxygen species are essential for autophagy and specif-ically regulate the activity of Atg4. EMBO J. 26, 1749-1760.
70. Schmid, D., Pypaert, M., and Münz, C. (2007). Antigen-loading compart-ments for major histocompatibility complex class II molecules con-tinuously receive input from autophagosomes. Immunity 26, 79-92.
71. Seglen, P. O., Gordon, P. B., and Holen, I. (1990). Non-selective autophagy. Semin. Cell Biol. 1, 441-448.
72. Shatsky, M., Nussinov, R., and Wolfson, H. J. (2004). A method for simulta-neous alignment of multiple protein structures. Proteins 56, 143-156.
73. Shpilka, T., Weidberg, H., Pietrokovski, S., and Elazar, Z. (2011). Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol. 12, 226-226.
74. Sinha, S., Colbert, C. L., Becker, N., Wei, Y., and Levine, B. (2008). Molecular basis of the regulation of Beclin 1-dependent autophagy by the gamma-herpesvirus 68 Bcl-2 homolog M11. Autophagy 4, 989-997.
75. Sinha, S., and Levine, B. (2008). The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 27(Suppl. 1), 137-148.
76. 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.
77. Tsukada, M., and Ohsumi, Y. (1993). Isolation and characterization of autophagy-defective mutants of Sac-charomyces cerevisiae. FEBS Lett. 333, 169-174.
78. Vergne, I., Roberts, E., Elmaoued, R. A., Tosch, V., Delgado, M. A., Proikas-Cezanne, T., Laporte, J., and Deretic, V. (2009). Control of autophagy initiation by phosphoinositide 3-phosphatase Jumpy. EMBO J. 28, 2244-2258.
79. Vlahos, R., Stambas, J., and Selemidis, S. (2012). Suppressing production of reactive oxygen species (ROS) for influenza A virus therapy. Trends Pharmacol. Sci. 33, 3-8.
80. Wang, J., Qiu, J. X., Soto, C., and DeGrado, W. F. (2011). Structural and dynamic mechanisms for the function and inhibition of the M2 proton channel from influenza A virus. Curr. Opin. Struct. Biol. 21, 68-80.
81. Weidberg, H., Shvets, E., and Elazar, Z. (2011a). Biogenesis and cargo selec-tivity of autophagosomes. Annu. Rev. Biochem. 80, 125-156.
82. Weidberg, H., Shpilka, T., Shvets, E., Abada, A., Shimron, F., and Elazar, Z. (2011b). LC3 and GATE-16 N termini mediate membrane fusion processes required for autophago-some biogenesis. Dev. Cell 20, 444-454.
83. 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., and Dikic, I. (2011). Phospho-rylation of the autophagy recep-tor optineurin restricts Salmonella growth. Science 333, 228-233.
84. Ylä-Anttila, P., Vihinen, H., Jokitalo, E., and Eskelinen, E. L. (2009). 3D tomography reveals connections between the phagophore and endo-plasmic reticulum. Autophagy 5, 1180-1185.
85. Zhou, D., Li, P., Lin, Y., Lott, J. M., Hislop, A. D., Canaday, D. H., Brutkiewicz, R. R., and Blum, J. S. (2005). Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 22, 571-581.
86. Zhou, Z., Jiang, X., Liu, D., Fan, Z., Hu, X., Yan, J., Wang, M., and Gao, G. F. (2009). Autophagy is involved in influenza A virus replication. Autophagy 5, 321-328.
87. Zimmermann, A. C., Zarei, M., Eise-Lein,S.,and Dengjel,J. (2010). Quan-titative proteomics for the analysis of spatio-temporal protein dynam-ics during autophagy. Autophagy 6, 1009-1016.
88. Zoncu, R., Efeyan, A., and Sabatini, D. M. (2011). mTOR: from growth sig-nal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35.