Involvement of autophagy in viral infections: Antiviral function and subversion by viruses

Journal of Molecular Medicine

Volumn 85, Issue 8, 2007, Pages 811-823

  Espert, Lucile ^a   Codogno, Patrice ^a,b   Biard Piechaczyk, Martine ^a  

^a UNIV MONTPELLIER   (France)

^b INSERM   (France)

Author keywords

Autophagy; Interferon; Virophagy; Virus

Indexed keywords

ALPHA INTERFERON; ALPHA1 INTERFERON; AUTOPHAGIN 12; AUTOPHAGIN 16; AUTOPHAGIN 5; BETA INTERFERON; CELL PROTEIN; DEATH ASSOCIATED PROTEIN KINASE; DOUBLE STRANDED RNA; FAS ASSOCIATED DEATH DOMAIN PROTEIN; INTERFERON; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCL 2; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; CORONAVIRUS; HUMAN; MAMMAL CELL; MOLECULAR BIOLOGY; NONHUMAN; REVIEW; ROTAVIRUS; SIGNAL TRANSDUCTION; ULTRAVIOLET IRRADIATION; VIRUS INFECTION;

ANIMALS; AUTOPHAGY; HUMANS; IMMUNITY, NATURAL; INTERFERONS; SIGNAL TRANSDUCTION; VIRUS DISEASES; VIRUSES;

EID: 34447543924     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-007-0173-6     Document Type: Review

References (114)

1. Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373-428
2. Yorimitsu T, Klionsky DJ (2005) Autophagy: molecular machinery for self-eating. Cell Death Differ 12(Suppl 2):1542-1552
3. Massey AC, Zhang C, Cuervo AM (2006) Chaperone-mediated autophagy in aging and disease. Curr Top Dev Biol 73:205-235
4. Klionsky DJ (2005) Autophagy. Curr Biol 15:R282-R283
5. Cuervo AM (2004) Autophagy: many paths to the same end. Mol Cell Biochem 263:55-72
6. Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169-174
7. Komatsu M, Waguri S, Ueno T et al (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169:425-434
8. Juhasz G, Neufeld TP (2006) Autophagy: a forty-year search for a missing membrane source. PLoS Biol 4:e36
9. Dunn WA Jr (1990) Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J Cell Biol 110:1923-1933
10. Ashford TP, Porter KR (1962) Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 12:198-202
11. Seglen PO, Berg TO, Blankson H, Fengsrud M, Holen I, Stromhaug PE (1996) Structural aspects of autophagy. Adv Exp Med Biol 389:103-111
12. Marino G, Lopez-Otin C (2004) Autophagy: molecular mechanisms, physiological functions and relevance in human pathology. Cell Mol Life Sci 61:1439-1454
13. Deretic V (2006) Autophagy as an immune defense mechanism. Curr Opin Immunol 18:375-382
14. Dengjel J, Schoor O, Fischer R et al (2005) Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci USA 102:7922-7927
15. Schmid D, Dengjel J, Schoor O, Stevanovic S, Munz C (2006) Autophagy in innate and adaptive immunity against intracellular pathogens. J Mol Med 84:194-202
16. Colombo MI (2005) Pathogens and autophagy: subverting to survive. Cell Death Differ 12(Suppl 2):1481-1483
17. Kurmasheva RT, Houghton PJ (2006) IGF-I mediated survival pathways in normal and malignant cells. Biochim Biophys Acta 1766:1-22
18. Yin VP, Thummel CS (2005) Mechanisms of steroid-triggered programmed cell death in Drosophila. Semin Cell Dev Biol 16:237-243
19. Kadowaki M, Razaul Karim M, Carpi A, Miotto G (2006) Nutrient control of macroautophagy in mammalian cells. Mol Aspects Med 27:426-443
20. Heymann D (2006) Autophagy: a protective mechanism in response to stress and inflammation. Curr Opin Investig Drugs 7:443-450
21. Wang CW, Klionsky DJ (2003) The molecular mechanism of autophagy. Mol Med 9:65-76
22. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T (2001) Beclin- phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2:330-335
23. Zeng X, Overmeyer JH, Maltese WA (2006) Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 119:259-270
24. Pattingre S, Tassa A, Qu X et al (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939
25. Liang C, Feng P, Ku B et al (2006) Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 8:688-699
26. Mizushima N, Noda T, Yoshimori T et al (1998) A protein conjugation system essential for autophagy. Nature 395:395-398
27. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117:2805-2812
28. Mizushima N (2004) Methods for monitoring autophagy. Int J Biochem Cell Biol 36:2491-2502
29. Klionsky DJ (2005) The correct way to monitor autophagy in higher eukaryotes. Autophagy 1:65
30. Marino G, Uria JA, Puente XS, Quesada V, Bordallo J, Lopez-Otin C (2003) Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem 278:3671-3678
31. Hemelaar J, Lelyveld VS, Kessler BM, Ploegh HL (2003) A single protease, Apg4B, is specific for the autophagy-related ubiquitin-like proteins GATE-16, MAP1-LC3, GABARAP, and Apg8L. J Biol Chem 278:51841-51850
32. Mizushima N, Ohsumi Y, Yoshimori T (2002) Autophagosome formation in mammalian cells. Cell Struct Funct 27:421-429
33. Tanida I, Ueno T, Kominami E (2004) LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 36:2503-2518
34. Noda T, Kim J, Huang WP et al (2000) Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 148:465-480
35. Webber JL, Young AR, Tooze SA (2007) Atg9 Trafficking in Mammalian Cells. Autophagy 3:54-56
36. Berg TO, Fengsrud M, Stromhaug PE, Berg T, Seglen PO (1998) Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 273:21883-21892
37. Gutierrez MG, Munafo DB, Beron W, Colombo MI (2004) Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117:2687-2697
38. Jager S, Bucci C, Tanida I et al (2004) Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 117:4837-4848
39. Klionsky DJ (2005) The molecular machinery of autophagy: unanswered questions. J Cell Sci 118:7-18
40. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23:33-42
41. Teter SA, Eggerton KP, Scott SV, Kim J, Fischer AM, Klionsky DJ (2001) Degradation of lipid vesicles in the yeast vacuole requires function of Cvt17, a putative lipase. J Biol Chem 276:2083-2087
42. Yang Z, Huang J, Geng J, Nair U, Klionsky DJ (2006) Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. Mol Biol Cell 17:5094-5104
43. Yang YP, Liang ZQ, Gu ZL, Qin ZH (2005) Molecular mechanism and regulation of autophagy. Acta Pharmacol Sin 26:1421-1434
44. Codogno P, Meijer AJ (2005) Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 12(Suppl 2):1509-1518
45. Kamada Y, Sekito T, Ohsumi Y (2004) Autophagy in yeast: a TOR-mediated response to nutrient starvation. Curr Top Microbiol Immunol 279:73-84
46. Young AR, Chan EY, Hu XW et al (2006) Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 119:3888-3900
47. Yamamoto A, Cremona ML, Rothman JE (2006) Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway. J Cell Biol 172:719-731
48. Sarkar S, Rubinsztein DC (2006) Inositol and IP3 levels regulate autophagy: biology and therapeutic speculations. Autophagy 2:132-134
49. Talloczy Z, Jiang W, Virgin HWt et al (2002) Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci USA 99:190-195
50. Kouroku Y, Fujita E, Tanida I et al (2007) ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14:230-239
51. Ogata M, Hino S, Saito A et al (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220-9231
52. He B (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 13:393-403
53. Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 181:195-213
54. Kuma A, Hatano M, Matsui M et al (2004) The role of autophagy during the early neonatal starvation period. Nature 432:1032-1036
55. Lum JJ, Bauer DE, Kong M et al (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237-248
56. Boya P, Gonzalez-Polo RA, Casares N et al (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25:1025-1040
57. Bursch W, Ellinger A, Kienzl H et al (1996) Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 17:1595-1607
58. Kondo Y, Kanzawa T, Sawaya R, Kondo S (2005) The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 5:726-734
59. Debnath J, Baehrecke EH, Kroemer G (2005) Does autophagy contribute to cell death? Autophagy 1:66-74
60. Gonzalez-Polo RA, Boya P, Pauleau AL et al (2005) The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J Cell Sci 118:3091-3102
61. Djavaheri-Mergny M, Amelotti M, Mathieu J et al (2006) NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem 281:30373-30382
62. Espert L, Denizot M, Grimaldi M et al (2006) Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 116:2161-2172
63. Aita VM, Liang XH, Murty VV et al (1999) Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59:59-65
64. Crighton D, Wilkinson S, O'Prey J et al (2006) DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126:121-134
65. Hait WN, Jin S, Yang JM (2006) A matter of life or death (or both): understanding autophagy in cancer. Clin Cancer Res 12:1961-1965
66. Eskelinen EL (2005) Doctor Jekyll and Mister Hyde: autophagy can promote both cell survival and cell death. Cell Death Differ 12(Suppl 2):1468-1472
67. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115:2679-2688
68. Kirkegaard K, Taylor MP, Jackson WT (2004) Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2:301-314
69. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119:753-766
70. Nakagawa I, Amano A, Mizushima N et al (2004) Autophagy defends cells against invading group A Streptococcus. Science 306:1037-1040
71. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C (2005) Escape of intracellular Shigella from autophagy. Science 307:727-731
72. Schnaith A, Kashkar H, Leggio S, Addicks K, Kronke M, Krut O (2007) Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem 282:2695-2706
73. Paludan C, Schmid D, Landthaler M et al (2005) Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307:593-596
74. Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305-315
75. Morel JB, Dangl JL (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4:671-683
76. Liu Y, Schiff M, Czymmek K, Talloczy Z, Levine B, Dinesh-Kumar SP (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121:567-577
77. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD (1998) How cells respond to interferons. Annu Rev Biochem 67:227-264
78. Decman V, Freeman ML, Kinchington PR, Hendricks RL (2005) Immune control of HSV-1 latency. Viral Immunol 18:466-473
79. He B, Gross M, Roizman B (1997) The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 94:843-848
80. Leib DA (2002) Counteraction of interferon-induced antiviral responses by herpes simplex viruses. Curr Top Microbiol Immunol 269:171-185
81. Leib DA, Machalek MA, Williams BR, Silverman RH, Virgin HW (2000) Specific phenotypic restoration of an attenuated virus by knockout of a host resistance gene. Proc Natl Acad Sci USA 97:6097-6101
82. Talloczy Z, Virgin HWt, Levine B (2006) PKR-Dependent Autophagic Degradation of Herpes Simplex Virus Type 1. Autophagy 2:24-29
83. Dales S, Eggers HJ, Tamm I, Palade GE (1965) Electron microscopic study of the formation of poliovirus. Virology 26:379-389
84. 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
85. Jackson WT, Giddings TH Jr, Taylor MP et al (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3:e156
86. Kirkegaard K, Jackson WT (2005) Topology of double-membraned vesicles and the opportunity for non-lytic release of cytoplasm. Autophagy 1:182-184
87. Belov GA, Altan-Bonnet N, Kovtunovych G, Jackson CL, Lippincott-Schwartz J, Ehrenfeld E (2007) Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J Virol 81:558-567
88. Fauci AS (1988) The human immunodeficiency virus: infectivity and mechanisms of pathogenesis. Science 239:617-622
89. Terai C, Kornbluth RS, Pauza CD, Richman DD, Carson DA (1991) Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HIV-1. J Clin Invest 87:1710-1715
90. Finkel TH, Tudor-Williams G, Banda NK et al (1995) Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1:129-134
91. Espert L, Denizot M, Grimaldi M et al (2007) Autophagy and CD4(+) T Lymphocyte Destruction by HIV-1. Autophagy 3:32-34
92. Finzi A, Brunet A, Xiao Y, Thibodeau J, Cohen EA (2006) Major histocompatibility complex class II molecules promote human immunodeficiency virus type 1 assembly and budding to late endosomal/multivesicular body compartments. J Virol 80:9789-9797
93. Jouvenet N, Neil SJ, Bess C et al (2006) Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol 4:e435
94. Levine B, Goldman JE, Jiang HH, Griffin DE, Hardwick JM (1996) Bc1-2 protects mice against fatal alphavirus encephalitis. Proc Natl Acad Sci USA 93:4810-4815
95. Liang XH, Kleeman LK, Jiang HH et al (1998) Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 72:8586-8596
96. Chisaka H, Morita E, Yaegashi N, Sugamura K (2003) Parvovirus B19 and the pathogenesis of anaemia. Rev Med Virol 13:347-359
97. Morita E, Tada K, Chisaka H et al (2001) Human parvovirus B19 induces cell cycle arrest at G(2) phase with accumulation of mitotic cyclins. J Virol 75:7555-7563
98. Nakashima A, Tanaka N, Tamai K et al (2006) Survival of parvovirus B19-infected cells by cellular autophagy. Virology 349:254-263
99. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR (2004) Coronavirus replication complex formation utilises components of cellular autophagy. J Biol Chem 279:10136-10141
100. Snijder EJ, van der Meer Y, Zevenhoven-Dobbe J et al (2006) Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80:5927-5940
101. Berkova Z, Crawford SE, Trugnan G, Yoshimori T, Morris AP, Estes MK (2006) Rotavirus NSP4 induces a novel vesicular compartment regulated by calcium and associated with viroplasms. J Virol 80:6061-6071
102. Fricke J, Voss C, Thumm M, Meyers G (2004) Processing of a pestivirus protein by a cellular protease specific for light chain 3 of microtubule-associated proteins. J Virol 78:5900-5912
103. Haller O, Kochs G, Weber F (2006) The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344:119-130
104. Pyo JO, Jang MH, Kwon YK et al (2005) Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death. J Biol Chem 280:20722-20729
105. Hovanessian AG, Brown RE, Kerr IM (1977) Synthesis of low molecular weight inhibitor of protein synthesis with enzyme from interferon-treated cells. Nature 268:537-540
106. Meurs E, Chong K, Galabru J et al (1990) Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62:379-390
107. Williams BR (1999) PKR; a sentinel kinase for cellular stress. Oncogene 18:6112-6120
108. Li S, Min JY, Krug RM, Sen GC (2006) Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349:13-21
109. Shohat G, Shani G, Eisenstein M, Kimchi A (2002) The DAP-kinase family of proteins: study of a novel group of calcium-regulated death-promoting kinases. Biochim Biophys Acta 1600:45-50
110. Inbal B, Shani G, Cohen O, Kissil JL, Kimchi A (2000) Death-associated protein kinase-related protein 1, a novel serine/threonine kinase involved in apoptosis. Mol Cell Biol 20:1044-1054
111. Inbal B, Bialik S, Sabanay I, Shani G, Kimchi A (2002) DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J Cell Biol 157:455-468
112. Mills KR, Reginato M, Debnath J, Queenan B, Brugge JS (2004) Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc Natl Acad Sci USA 101:3438-3443
113. Peter ME, Krammer PH (2003) The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 10:26-35
114. Thorburn J, Moore F, Rao A et al (2005) Selective inactivation of a Fas-associated death domain protein (FADD)-dependent apoptosis and autophagy pathway in immortal epithelial cells. Mol Biol Cell 16:1189-1199