Abstract
Autophagy is a cellular process that creates double-membraned vesicles, engulfs and degrades cytoplasmic material, and generates and recycles nutrients. A recognized participant in the innate immune response to microbial infection, a functional autophagic response can help to control the replication of many viruses. However, for several viruses, there is functional and mechanistic evidence that components of the autophagy pathway act as host factors in viral replicative cycles, viral dissemination, or both. Investigating the mechanisms by which viruses subvert or imitate autophagy, as well as the mechanisms by which they inhibit autophagy, will reveal cell biological tools and processes that will be useful for understanding the many functional ramifications of the double-membraned vesicle formation and cytosolic entrapment unique to the autophagy pathway.
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References
Ait-Goughoulte M, Kanda T, Meyer K, Ryerse JS, Ray RB, Ray R (2008) Hepatitis C virus genotype 1a growth and induction of autophagy. J Virol 82:2241–2249
Al-Molawi N, Beardmore VA, Carter MJ, Kass GE, Roberts LO (2003) Caspase-mediated cleavage of the feline calicivirus capsid protein. J Gen Virol 84:1237–1244
Alvarez M, Casadevall A (2006) Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr Biol 16:2161–2165
Best SM (2008) Viral subversion of apoptotic enzymes: escape from death row. Annu Rev Microbiol 62:171–192
Best SM, Shelton JF, Pompey JM, Wolfinbarger JB, Bloom ME (2003) Caspase cleavage of the nonstructural protein NS1 mediates replication of Aleutian mink disease parvovirus. J Virol 77:5305–5312
Bienz K, Egger D, Rasser Y, Bossart W (1983) Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures. Virology 131:39–48
Brabec-Zaruba M, Berka U, Blaas D, Fuchs R (2007) Induction of autophagy does not affect human rhinovirus type 2 production. J Virol 81:10815–10817
Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, Xavier RJ, Lieberman J, Elledge SJ (2008) Identification of host proteins requried for HIV infection through a functional genomic screen. Science 319:921–926
Clem RJ, Fechheimer M, Miller LK (1991) Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254:1388–1390
Dales S, Eggers HJ, Tamm I, Palade GE. (1965) Electron microscopic study of the formation of poliovirus. Virology 26:379–389
Dodd DA, Giddings TH, Jr., Kirkegaard K. (2001) Poliovirus 3A protein limits interleukin-6 (IL-6), IL-8, and beta interferon secretion during viral infection. J Virol 75:8158–8165
Fass E, Shvets E, Degani I, Hirschberg K, Elazar Z (2006) Microtubules support production of starvation-induced autophagosomes but not their targeting and fusion with lysosomes. J Biol Chem 281:36303–36316
Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G (2008) Viral control of mitochondrial apoptosis. PLoS Pathog 4:e1000018
Hollinger FB, Ticehurst J (1990) Hepatitis A virus. In: Fields BN et al. (eds) Fields virology, 2nd edn. Raven, New York, pp 631–667
Jackson WT, Giddings TH Jr, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3:e156
Jahreiss L, Menzies FM, Rubinsztein DC (2008) The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9:574–587
Kimura S, Noda T, Yoshimori T (2008) Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct 33:109–122
Kirkegaard K, Jackson WT (2005) Topology of double-membraned vesicles and the opportunity for non-lytic release of cytoplasm. Autophagy 1:182–184
Koechl R, Hu XW, Chan EYW, Tooze S (2006) Microtubules faciliate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 7:129–145
Kuznetsov SA, Gelfand VI (1987) 18 kDa microtubule-associated protein: identification as a new light chain (LC-3) of microtubule-associated protein 1 (MAP-1). FEBS Lett 212:145–148
Lee YR, Lei HY, Liu MT, Wang JR, Chen SH, Jiang-Shieh YF, Lin YS, Yeh TM, Liu CC, Liu HS (2008) Autophagic machinery activated by dengue virus enhances virus replication. Virology 374:240–248
Mendez E, Salas-Ocampo E, Arias CF (2004) Caspases mediate processing of the capsid precursor and cell release of human astroviruses. J Virol 78:8601–8608
Miller DJ, Schwartz MD, Dye BT, Ahlquist P (2003) Engineered retargeting of viral RNA replication complexes to an alternative intracellular membrane. J Virol 77:12193–12202
Mizushima N, Ohsumi Y, Yoshimori T (2002) Autophagosome formation in mammalian cells. Cell Struct Funct 27:421–429
Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451:1069–1075
Ren PH, Lauckner JE, Kachirskaia I, Heusor JE, Melki R, Kopita RR (2009) Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine. Nat Cell Biol 11(2):219–225 (epub 2009)
Roussarie JP, Ruffie C, Edgar JM, Griffiths I, Brahic M (2007) Axon myelin transfer of a non-enveloped virus. PLoS ONE 2:e1331
Schlegel A, Giddings TH, Jr., Ladinsky MS, Kirkegaard K. (1996) Cellular origin and ultrastructure of membranes induced during poliovirus infection. J Virol 70:6576–6588
Sir D, Chen WL, Choi J, Wakita T, Yen TS, Ou JH. (2008) Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 48:1054–1061
Stinchcombe J, Bossi G, Griffiths GM. (2004) Linking albinism and immunity: the secrets of secretory lysosomes. Science 305:55–59
Suhy DA, Giddings TH, Jr., Kirkegaard K (2000) Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 74:8953–8965
Taylor MP, Kirkegaard K (2007) Modification of cellular autophagy protein LC3 by poliovirus. J Virol 81:12543–12553
Taylor MP, Burgon TB, Kirkegaard K, Jackson WT (2009) Role of microtubules in extracellular release of poliovirus. J Viral 83(13):6599–6609 (epub 2009)
Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, Luo H (2008) Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 82:9143–9153
Zhao Z, Thackray L, Miller B, Lynn T, Becker M, Ward E, Mizushima N, Denison M, Virgin HT (2007) Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3:581–585
Acknowledgments
I would especially like to thank Thomas H. Giddings, Jr., whose electron micrographs allowed us to rediscover the double-membraned character of poliovirus-induced vesicles, and Andrew Staehelin, who first taught me about the autophagy pathway. I am grateful to the members of the laboratory who have worked on this topic over several years: Andreas Schlegel, David Suhy, William T. Jackson and Matthew Taylor. I thank Michel Brahic for stimulating discussions of non-lytic viral release and Arturo Casadevall for communicating results prior to publication. This work has been funded by the National Institutes of Health.
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Kirkegaard, K. (2009). Subversion of the Cellular Autophagy Pathway by Viruses. In: Levine, B., Yoshimori, T., Deretic, V. (eds) Autophagy in Infection and Immunity. Current Topics in Microbiology and Immunology, vol 335. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00302-8_16
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DOI: https://doi.org/10.1007/978-3-642-00302-8_16
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