Virus Recognition by Toll-7 Activates Antiviral Autophagy in Drosophila

Immunity

Volumn 36, Issue 4, 2012, Pages 658-667

  Nakamoto, Margaret ^a   Moy, Ryan H ^a   Xu, Jie ^a   Bambina, Shelly ^a   Yasunaga, Ari ^a   Shelly, Spencer S ^a   Gold, Beth ^a   Cherry, Sara ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR 7;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVATION; IN VITRO STUDY; MORTALITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS; VESICULAR STOMATITIS VIRUS; VIRUS REPLICATION;

ANIMALS; AUTOPHAGY; CELL LINE; CELL MEMBRANE; CRICETINAE; DROSOPHILA MELANOGASTER; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7; VESICULAR STOMATITIS INDIANA VIRUS; VESICULAR STOMATITIS NEW JERSEY VIRUS; VIRUS REPLICATION;

EID: 84859991798     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.03.003     Document Type: Article

References (63)

1. Aggarwal K., Rus F., Vriesema-Magnuson C., Ertürk-Hasdemir D., Paquette N., Silverman N. Rudra interrupts receptor signaling complexes to negatively regulate the IMD pathway. PLoS Pathog. 2008, 4:e1000120.
2. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
3. Arsham A.M., Neufeld T.P. A genetic screen in Drosophila reveals novel cytoprotective functions of the autophagy-lysosome pathway. PLoS ONE 2009, 4:e6068.
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. Barton G.M. Viral recognition by Toll-like receptors. Semin. Immunol. 2007, 19:33-40.
6. Bieback K., Lien E., Klagge I.M., Avota E., Schneider-Schaulies J., Duprex W.P., Wagner H., Kirschning C.J., Ter Meulen V., Schneider-Schaulies S. Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J. Virol. 2002, 76:8729-8736.
7. Bilak H., Tauszig-Delamasure S., Imler J.L. Toll and Toll-like receptors in Drosophila. Biochem. Soc. Trans. 2003, 31:648-651.
8. Bilen J., Bonini N.M. Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet. 2007, 3:1950-1964.
9. Cerenius L., Kawabata S., Lee B.L., Nonaka M., Söderhäll K. Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem. Sci. 2010, 35:575-583.
10. Chang S., Dolganiuc A., Szabo G. Toll-like receptors 1 and 6 are involved in TLR2-mediated macrophage activation by hepatitis C virus core and NS3 proteins. J. Leukoc. Biol. 2007, 82:479-487.
11. Chen G.C., Lee J.Y., Tang H.W., Debnath J., Thomas S.M., Settleman J. Genetic interactions between Drosophila melanogaster Atg1 and paxillin reveal a role for paxillin in autophagosome formation. Autophagy 2008, 4:37-45.
12. Cherry S., Doukas T., Armknecht S., Whelan S., Wang H., Sarnow P., Perrimon N. Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes Dev. 2005, 19:445-452.
13. Comer J.A., Tesh R.B., Modi G.B., Corn J.L., Nettles V.F. Vesicular stomatitis virus, New Jersey serotype: replication in and transmission by Lutzomyia shannoni (Diptera: Psychodidae). Am. J. Trop. Med. Hyg. 1990, 42:483-490.
14. Compton T., Kurt-Jones E.A., Boehme K.W., Belko J., Latz E., Golenbock D.T., Finberg R.W. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 2003, 77:4588-4596.
15. Contamine D., Petitjean A.M., Ashburner M. Genetic resistance to viral infection: the molecular cloning of a Drosophila gene that restricts infection by the rhabdovirus sigma. Genetics 1989, 123:525-533.
16. Delgado M.A., Elmaoued R.A., Davis A.S., Kyei G., Deretic V. Toll-like receptors control autophagy. EMBO J. 2008, 27:1110-1121.
17. Delgado M., Singh S., De Haro S., Master S., Ponpuak M., Dinkins C., Ornatowski W., Vergne I., Deretic V. Autophagy and pattern recognition receptors in innate immunity. Immunol. Rev. 2009, 227:189-202.
18. Deretic V., Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009, 5:527-549.
19. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
20. Dostert C., Jouanguy E., Irving P., Troxler L., Galiana-Arnoux D., Hetru C., Hoffmann J.A., Imler J.L. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat. Immunol. 2005, 6:946-953.
21. Dru P., Bras F., Dezélée S., Gay P., Petitjean A.M., Pierre-Deneubourg A., Teninges D., Contamine D. Unusual variability of the Drosophila melanogaster ref(2)P protein which controls the multiplication of sigma rhabdovirus. Genetics 1993, 133:943-954.
22. Ferrandon D., Imler J.L., Hoffmann J.A. Sensing infection in Drosophila: Toll and beyond. Semin. Immunol. 2004, 16:43-53.
23. Fleuriet A. Maintenance of a hereditary virus, the sigma virus, in populations of its host, D. melanogaster. Evolutionary Biology 1988, Plenum Press, New York. M.K. Hecht, B. Wallace (Eds.).
24. García-Sastre A., Biron C.A. Type 1 interferons and the virus-host relationship: a lesson in détente. Science 2006, 312:879-882.
25. 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.
26. Imler J.L., Zheng L. Biology of Toll receptors: lessons from insects and mammals. J. Leukoc. Biol. 2004, 75:18-26.
27. Ip Y.T., Reach M., Engstrom Y., Kadalayil L., Cai H., González-Crespo S., Tatei K., Levine M. Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell 1993, 75:753-763.
28. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20:197-216.
29. Jin M.S., Lee J.O. Structures of the toll-like receptor family and its ligand complexes. Immunity 2008, 29:182-191.
30. Juhasz G., Neufeld T.P. Experimental control and characterization of autophagy in DrosInophila. Methods Mol. Biol. 2008, 445:125-133.
31. Kawai T., Akira S. TLR signaling. Cell Death Differ. 2006, 13:816-825.
32. Klionsky D.J., Abeliovich H., Agostinis P., Agrawal D.K., Aliev G., Askew D.S., Baba M., Baehrecke E.H., Bahr B.A., Ballabio A., et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
33. 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.
34. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25:697-743.
35. 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.
36. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
37. Ligoxygakis P., Bulet P., Reichhart J.M. Critical evaluation of the role of the Toll-like receptor 18-Wheeler in the host defense of Drosophila. EMBO Rep. 2002, 3:666-673.
38. Longdon B., Obbard D.J., Jiggins F.M. Sigma viruses from three species of Drosophila form a major new clade in the rhabdovirus phylogeny. Proc. Biol. Sci. 2010, 277:35-44.
39. Luo C., Shen B., Manley J.L., Zheng L. Tehao functions in the Toll pathway in Drosophila melanogaster: possible roles in development and innate immunity. Insect Mol. Biol. 2001, 10:457-464.
40. McPhee C.K., Baehrecke E.H. Autophagy in Drosophila melanogaster. Biochim. Biophys. Acta 2009, 1793:1452-1460.
41. McPhee C.K., Logan M.A., Freeman M.R., Baehrecke E.H. Activation of autophagy during cell death requires the engulfment receptor Draper. Nature 2010, 465:1093-1096.
42. Mead D.G., Howerth E.W., Murphy M.D., Gray E.W., Noblet R., Stallknecht D.E. Black fly involvement in the epidemic transmission of vesicular stomatitis New Jersey virus (Rhabdoviridae: Vesiculovirus). Vector Borne Zoonotic Dis. 2004, 4:351-359.
43. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
44. Narbonne-Reveau K., Charroux B., Royet J. Lack of an antibacterial response defect in Drosophila Toll-9 mutant. PLoS ONE 2011, 6:e17470.
45. Ooi J.Y., Yagi Y., Hu X., Ip Y.T. The Drosophila Toll-9 activates a constitutive antimicrobial defense. EMBO Rep. 2002, 3:82-87.
46. 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.
47. Ramsburg E., Publicover J., Buonocore L., Poholek A., Robek M., Palin A., Rose J.K. A vesicular stomatitis virus recombinant expressing granulocyte-macrophage colony-stimulating factor induces enhanced T-cell responses and is highly attenuated for replication in animals. J. Virol. 2005, 79:15043-15053.
48. Rusten T.E., Lindmo K., Juhász G., Sass M., Seglen P.O., Brech A., Stenmark H. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell 2004, 7:179-192.
49. Sabin L.R., Hanna S.L., Cherry S. Innate antiviral immunity in Drosophila. Curr. Opin. Immunol. 2010, 22:4-9.
50. Sanjuan M.A., Dillon C.P., Tait S.W., Moshiach S., Dorsey F., Connell S., Komatsu M., Tanaka K., Cleveland J.L., Withoff S., Green D.R. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 2007, 450:1253-1257.
51. 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.
52. Shin D.M., Yuk J.M., Lee H.M., Lee S.H., Son J.W., Harding C.V., Kim J.M., Modlin R.L., Jo E.K. Mycobacterial lipoprotein activates autophagy via TLR2/1/CD14 and a functional vitamin D receptor signalling. Cell. Microbiol. 2010, 12:1648-1665.
53. Sirén J., Pirhonen J., Julkunen I., Matikainen S. IFN-alpha regulates TLR-dependent gene expression of IFN-alpha, IFN-beta, IL-28, and IL-29. J. Immunol. 2005, 174:1932-1937.
54. Takeda K., Kaisho T., Akira S. Toll-like receptors. Annu. Rev. Immunol. 2003, 21:335-376.
55. Tauszig S., Jouanguy E., Hoffmann J.A., Imler J.L. Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc. Natl. Acad. Sci. USA 2000, 97:10520-10525.
56. Tauszig-Delamasure S., Bilak H., Capovilla M., Hoffmann J.A., Imler J.L. Drosophila MyD88 is required for the response to fungal and Gram-positive bacterial infections. Nat. Immunol. 2002, 3:91-97.
57. Uematsu S., Akira S. Toll-like receptors and innate immunity. J. Mol. Med. 2006, 84:712-725.
58. Waterhouse R.M., Kriventseva E.V., Meister S., Xi Z., Alvarez K.S., Bartholomay L.C., Barillas-Mury C., Bian G., Blandin S., Christensen B.M., et al. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316:1738-1743.
59. Williams M.J., Rodriguez A., Kimbrell D.A., Eldon E.D. The 18-wheeler mutation reveals complex antibacterial gene regulation in Drosophila host defense. EMBO J. 1997, 16:6120-6130.
60. Xu Y., Eissa N.T. Autophagy in innate and adaptive immunity. Proc. Am. Thorac. Soc. 2010, 7:22-28.
61. 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.
62. Yagi Y., Nishida Y., Ip Y.T. Functional analysis of Toll-related genes in Drosophila. Dev. Growth Differ. 2010, 52:771-783.
63. 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.