Antiviral autophagy restricts rift valley fever virus infection and is conserved from flies to mammals

Immunity

Volumn 40, Issue 1, 2014, Pages 51-65

  Moy, Ryan H ^a   Gold, Beth ^a   Molleston, Jerome M ^a   Schad, Veronica ^a   Yanger, Kilangsungla ^b   Salzano, Mary Virginia ^a   Yagi, Yoshimasa ^c   Fitzgerald, Katherine A ^d   Stanger, Ben Z ^b   Soldan, Samantha S ^a   Cherry, Sara ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NAGOYA UNIVERSITY   (Japan)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; PATTERN RECOGNITION RECEPTOR; PROTEIN KINASE B; PROTEIN P62; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUBULIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; 6 BROMO 4 ALLYLAMINO QUINAZOLINE; 6-BROMO-4-ALLYLAMINO-QUINAZOLINE; ALLYL COMPOUND; ANTIVIRUS AGENT; QUINAZOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DIPTERA; DROSOPHILA; HOST RESISTANCE; MAMMAL; MAMMAL CELL; MORTALITY; NONHUMAN; PRIORITY JOURNAL; RIFT VALLEY FEVER; RIFT VALLEY FEVER BUNYAVIRUS; VIRUS INHIBITION; VIRUS REPLICATION; ANIMAL; CELL CULTURE; DRUG EFFECT; HUMAN; IMMUNOLOGY; INFECTION CONTROL; LIVER CELL; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; MOUSE; NERVE CELL; RAT; VIROLOGY;

ALLYL COMPOUNDS; ANIMALS; ANTIVIRAL AGENTS; AUTOPHAGY; CELLS, CULTURED; DROSOPHILA; EVOLUTION, MOLECULAR; HEPATOCYTES; HUMANS; INFECTION CONTROL; MAMMALS; MICE; MYELOID DIFFERENTIATION FACTOR 88; NEURONS; QUINAZOLINES; RATS; RIFT VALLEY FEVER; RIFT VALLEY FEVER VIRUS; TOLL-LIKE RECEPTOR 7; VIRUS REPLICATION;

EID: 84892476191     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.10.020     Document Type: Article

References (64)

1. Akhouayri I., Turc C., Royet J., Charroux B. Toll-8/Tollo negatively regulates antimicrobial response in the Drosophila respiratory epithelium. PLoS Pathog. 2011, 7:e1002319.
2. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
3. Anand P.K., Tait S.W., Lamkanfi M., Amer A.O., Nunez G., Pagès G., Pouysségur J., McGargill M.A., Green D.R., Kanneganti T.D. TLR2 and RIP2 pathways mediate autophagy of Listeria monocytogenes via extracellular signal-regulated kinase (ERK) activation. J.Biol. Chem. 2011, 286:42981-42991.
4. Barbalat R., Lau L., Locksley R.M., Barton G.M. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 2009, 10:1200-1207.
5. Beatman E., Oyer R., Shives K.D., Hedman K., Brault A.C., Tyler K.L., Beckham J.D. West Nile virus growth is independent of autophagy activation. Virology 2012, 433:262-272.
6. Bouloy M., Janzen C., Vialat P., Khun H., Pavlovic J., Huerre M., Haller O. Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs. J.Virol. 2001, 75:1371-1377.
7. Campbell G.R., Spector S.A. Toll-like receptor 8 ligands activate a vitamin D mediated autophagic response that inhibits human immunodeficiency virus type 1. PLoS Pathog. 2012, 8:e1003017.
8. Cha G.H., Cho K.S., Lee J.H., Kim M., Kim E., Park J., Lee S.B., Chung J. Discrete functions of TRAF1 and TRAF2 in Drosophila melanogaster mediated by c-Jun N-terminal kinase and NF-kappaB-dependent signaling pathways. Mol. Cell. Biol. 2003, 23:7982-7991.
9. Connor J.H., Lyles D.S. Vesicular stomatitis virus infection alters the eIF4F translation initiation complex and causes dephosphorylation of the eIF4E binding protein 4E-BP1. J.Virol. 2002, 76:10177-10187.
10. Deddouche S., Matt N., Budd A., Mueller S., Kemp C., Galiana-Arnoux D., Dostert C., Antoniewski C., Hoffmann J.A., Imler J.L. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nat. Immunol. 2008, 9:1425-1432.
11. Delgado M.A., Elmaoued R.A., Davis A.S., Kyei G., Deretic V. Toll-like receptors control autophagy. EMBO J. 2008, 27:1110-1121.
12. Deretic V., Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009, 5:527-549.
13. Dixit E., Boulant S., Zhang Y., Lee A.S., Odendall C., Shum B., Hacohen N., Chen Z.J., Whelan S.P., Fransen M., et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 2010, 141:668-681.
14. Ermler M.E., Yerukhim E., Schriewer J., Schattgen S., Traylor Z., Wespiser A.R., Caffrey D.R., Chen Z.J., King C.H., Gale M., et al. RNA helicase signaling is critical for type i interferon production and protection against Rift Valley fever virus during mucosal challenge. J.Virol. 2013, 87:4846-4860.
15. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., Coyle A.J., Liao S.M., Maniatis T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4:491-496.
16. Georgel P., Jiang Z., Kunz S., Janssen E., Mols J., Hoebe K., Bahram S., Oldstone M.B., Beutler B. Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway. Virology 2007, 362:304-313.
17. Habjan M., Andersson I., Klingström J., Schümann M., Martin A., Zimmermann P., Wagner V., Pichlmair A., Schneider U., Mühlberger E., et al. Processing of genome 5' termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE 2008, 3:e2032.
18. Hwang S., Maloney N.S., Bruinsma M.W., Goel G., Duan E., Zhang L., Shrestha B., Diamond M.S., Dani A., Sosnovtsev S.V., et al. Nondegradative role of Atg5-Atg12/ Atg16L1 autophagy protein complex in antiviral activity of interferon gamma. Cell Host Microbe 2012, 11:397-409.
19. Ikegami T., Makino S. The pathogenesis of Rift Valley fever. Viruses 2011, 3:493-519.
20. Joubert P.E., Werneke S.W., de la Calle C., Guivel-Benhassine F., Giodini A., Peduto L., Levine B., Schwartz O., Lenschow D.J., Albert M.L. Chikungunya virus-induced autophagy delays caspase-dependent cell death. J.Exp. Med. 2012, 209:1029-1047.
21. Kato H., Sato S., Yoneyama M., Yamamoto M., Uematsu S., Matsui K., Tsujimura T., Takeda K., Fujita T., Takeuchi O., Akira S. Cell type-specific involvement of RIG-I in antiviral response. Immunity 2005, 23:19-28.
22. Krejbich-Trotot P., Gay B., Li-Pat-Yuen G., Hoarau J.J., Jaffar-Bandjee M.C., Briant L., Gasque P., Denizot M. Chikungunya triggers an autophagic process which promotes viral replication. Virol. J. 2011, 8:432.
23. Kuma A., Hatano M., Matsui M., Yamamoto A., Nakaya H., Yoshimori T., Ohsumi Y., Tokuhisa T., Mizushima N. The role of autophagy during the early neonatal starvation period. Nature 2004, 432:1032-1036.
24. Kurt-Jones E.A., Sandor F., Ortiz Y., Bowen G.N., Counter S.L., Wang T.C., Finberg R.W. Use of murine embryonic fibroblasts to define Toll-like receptor activation and specificity. J.Endotoxin Res. 2004, 10:419-424.
25. Lee H.K., Lund J.M., Ramanathan B., Mizushima N., Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 2007, 315:1398-1401.
26. Leib D.A., Alexander D.E., Cox D., Yin J., Ferguson T.A. Interaction of ICP34.5 with Beclin 1 modulates herpes simplex virus type 1 pathogenesis through control of CD4+ T-cell responses. J.Virol. 2009, 83:12164-12171.
27. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
28. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
29. Loo Y.M., Gale M. Immune signaling by RIG-I-like receptors. Immunity 2011, 34:680-692.
30. Lum J.J., DeBerardinis R.J., Thompson C.B. Autophagy in metazoans: cell survival in the land of plenty. Nat. Rev. Mol. Cell Biol. 2005, 6:439-448.
31. Mizushima N., Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011, 147:728-741.
32. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
33. Mohankumar V., Dhanushkodi N.R., Raju R. Sindbis virus replication, is insensitive to rapamycin and torin1, and suppresses Akt/mTOR pathway late during infection in HEK cells. Biochem. Biophys. Res. Commun. 2011, 406:262-267.
34. Moser T.S., Schieffer D., Cherry S. AMP-activated kinase restricts Rift Valley fever virus infection by inhibiting fatty acid synthesis. PLoS Pathog. 2012, 8:e1002661.
35. Nakamoto M., Moy R.H., Xu J., Bambina S., Yasunaga A., Shelly S.S., Gold B., Cherry S. Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity 2012, 36:658-667.
36. Noh W.C., Mondesire W.H., Peng J., Jian W., Zhang H., Dong J., Mills G.B., Hung M.C., Meric-Bernstam F. Determinants of rapamycin sensitivity in breast cancer cells. Clin. Cancer Res. 2004, 10:1013-1023.
37. O'Neill L.A., Bowie A.G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 2007, 7:353-364.
38. Orvedahl A., Alexander D., Tallóczy Z., Sun Q., Wei Y., Zhang W., Burns D., Leib D.A., Levine B. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 2007, 1:23-35.
39. Orvedahl A., MacPherson S., Sumpter R., Tallóczy Z., Zou Z., Levine B. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 2010, 7:115-127.
40. Ross T.M., Bhardwaj N., Bissel S.J., Hartman A.L., Smith D.R. Animal models of Rift Valley fever virus infection. Virus Res. 2012, 163:417-423.
41. Rubinsztein D.C., Codogno P., Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat. Rev. Drug Discov. 2012, 11:709-730.
42. Sarkar S., Perlstein E.O., Imarisio S., Pineau S., Cordenier A., Maglathlin R.L., Webster J.A., Lewis T.A., O'Kane C.J., Schreiber S.L., Rubinsztein D.C. Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat. Chem. Biol. 2007, 3:331-338.
43. Scott R.C., Schuldiner O., Neufeld T.P. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 2004, 7:167-178.
44. Shatz M., Menendez D., Resnick M.A. The human TLR innate immune gene family is differentially influenced by DNA stress and p53 status in cancer cells. Cancer Res. 2012, 72:3948-3957.
45. Shelly S., Lukinova N., Bambina S., Berman A., Cherry S. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 2009, 30:588-598.
46. Shen B., Liu H., Skolnik E.Y., Manley J.L. Physical and functional interactions between Drosophila TRAF2 and Pelle kinase contribute to Dorsal activation. Proc. Natl. Acad. Sci. USA 2001, 98:8596-8601.
47. Shi C.S., Kehrl J.H. MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J.Biol. Chem. 2008, 283:33175-33182.
48. Shi C.S., Kehrl J.H. TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci. Signal. 2010, 3:ra42.
49. Shoji-Kawata S., Sumpter R., Leveno M., Campbell G.R., Zou Z., Kinch L., Wilkins A.D., Sun Q., Pallauf K., MacDuff D., et al. Identification of a candidate therapeutic autophagy-inducing peptide. Nature 2013, 494:201-206.
50. Sun L., Deng L., Ea C.K., Xia Z.P., Chen Z.J. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell 2004, 14:289-301.
51. Szretter K.J., Daffis S., Patel J., Suthar M.S., Klein R.S., Gale M., Diamond M.S. The innate immune adaptor molecule MyD88 restricts West Nile virus replication and spread in neurons of the central nervous system. J.Virol. 2010, 84:12125-12138.
52. Tal M.C., Sasai M., Lee H.K., Yordy B., Shadel G.S., Iwasaki A. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc. Natl. Acad. Sci. USA 2009, 106:2770-2775.
53. Tallóczy Z., Jiang W., Virgin H.W., Leib D.A., Scheuner D., Kaufman R.J., Eskelinen E.L., Levine B. Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. USA 2002, 99:190-195.
54. Uematsu S., Akira S. Toll-like receptors and innate immunity. J.Mol. Med. 2006, 84:712-725.
55. Vandergaast R., Fredericksen B.L. West Nile virus (WNV) replication is independent of autophagy in mammalian cells. PLoS ONE 2012, 7:e45800.
56. Walter C.T., Barr J.N. Recent advances in the molecular and cellular biology of bunyaviruses. J.Gen. Virol. 2011, 92:2467-2484.
57. Watson R.O., Manzanillo P.S., Cox J.S. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 2012, 150:803-815.
58. Weber M., Gawanbacht A., Habjan M., Rang A., Borner C., Schmidt A.M., Veitinger S., Jacob R., Devignot S., Kochs G., et al. Incoming RNA virus nucleocapsids containing a 5'-triphosphorylated genome activate RIG-I and antiviral signaling. Cell Host Microbe 2013, 13:336-346.
59. Xu Y., Jagannath C., Liu X.D., Sharafkhaneh A., Kolodziejska K.E., Eissa N.T. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 2007, 27:135-144.
60. Xu J., Grant G., Sabin L.R., Gordesky-Gold B., Yasunaga A., Tudor M., Cherry S. Transcriptional pausing controls a rapid antiviral innate immune response in Drosophila. Cell Host Microbe 2012, 12:531-543.
61. Yagi Y., Nishida Y., Ip Y.T. Functional analysis of Toll-related genes in Drosophila. Dev. Growth Differ. 2010, 52:771-783.
62. Yano T., Mita S., Ohmori H., Oshima Y., Fujimoto Y., Ueda R., Takada H., Goldman W.E., Fukase K., Silverman N., et al. Autophagic control of listeria through intracellular innate immune recognition in drosophila. Nat. Immunol. 2008, 9:908-916.
63. Yordy B., Iwasaki A. Cell type-dependent requirement of autophagy in HSV-1 antiviral defense. Autophagy 2012, 9:236-238.
64. Zhao Z., Fux B., Goodwin M., Dunay I.R., Strong D., Miller B.C., Cadwell K., Delgado M.A., Ponpuak M., Green K.G., et al. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 2008, 4:458-469.