The essential, nonredundant roles of RIG-I and MDA5 in detecting and controlling west nile virus infection

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11416-11425

  Errett, John S ^a   Suthar, Mehul S ^b   McMillan, Aimee ^a   Diamond, Michael S ^c   Gale Jr, Michael ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; PATTERN RECOGNITION RECEPTOR; PROTEIN MDA5; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG; VIRUS RNA; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; FLAVIVIRUS INFECTION; GENE; GENE INDUCTION; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; INNATE IMMUNITY; MALE; MDA5 GENE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RIG I GENE; VIRUS INFECTION; WEST NILE FLAVIVIRUS;

ANIMALS; CELLS, CULTURED; DEAD-BOX RNA HELICASES; DISEASE MODELS, ANIMAL; MICE; MICE, KNOCKOUT; RECEPTORS, PATTERN RECOGNITION; SURVIVAL ANALYSIS; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84886878320     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01488-13     Document Type: Article

References (57)

1. Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ. 2002. West Nile virus. Lancet Infect. Dis. 2:519-529.
2. Centers for Disease Control and Prevention. 2011. West Nile virus disease and other arboviral diseases-United States, 2010.MMWRMorb. Mortal. Wkly. Rep. 60:1009-1013.
3. Centers for Disease Control and Prevention. 2013. West Nile virus: final cumulative maps and data for 1999-2012. Centers for Disease Controland Prevention, Atlanta, GA. http://www.cdc.gov/westnile/statsMaps/cumMapsData.html.
4. Papa A, Xanthopoulou K, Gewehr S, Mourelatos S. 2011. Detection of West Nile virus lineage 2 in mosquitoes during a human outbreak in Greece. Clin. Microbiol. Infect. 17:1176-1180.
5. Savini G, Capelli G, Monaco F, Polci A, Russo F, Di Gennaro A, Marini V, Teodori L, Montarsi F, Pinoni C, Pisciella M, Terregino C, Marangon S, Capua I, Lelli R. 2012. Evidence of West Nile virus lineage 2 circulation in Northern Italy. Vet. Microbiol. 158:267-273.
6. Hayes EB, Komar N, Nasci RS, Montgomery SP, O'Leary DR, Campbell GL. 2005. Epidemiology and transmission dynamics of West Nile virus disease. Emerg. Infect. Dis. 11:1167-1173.
7. Samuel MA, Diamond MS. 2006. Pathogenesis of West Nile Virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J. Virol. 80:9349-9360.
8. Petersen LR, Hayes EB. 2004. Westward ho? The spread of West Nile virus. N. Engl. J. Med. 351:2257-2259.
9. Lim PY, Behr MJ, Chadwick CM, Shi PY, Bernard KA. 2011. Keratinocytes are cell targets of West Nile virus in vivo. J. Virol. 85:5197-5201.
10. Suthar MS, Diamond MS, Gale M, Jr. 2013. West Nile virus infection and immunity. Nat. Rev. Microbiol. 11:115-128.
11. Daffis S, Samuel MA, Suthar MS, Gale M, Jr, Diamond MS. 2008. Toll-like receptor 3 has a protective role against West Nile virus infection. J. Virol. 82:10349-10358.
12. Fredericksen BL, Keller BC, Fornek J, Katze MG, Gale M, Jr. 2008. Establishment and maintenance of the innate antiviral response to West Nile virus involves both RIG-I and MDA5 signaling through IPS-1. J. Virol. 82:609-616.
13. Fredericksen BL, Smith M, Katze MG, Shi PY, Gale M, Jr. 2004. The host response to West Nile virus infection limits viral spread through the activation of the interferon regulatory factor 3 pathway. J. Virol. 78:7737-7747.
14. Suthar MS, Ma DY, Thomas S, Lund JM, Zhang N, Daffis S, Rudensky AY, Bevan MJ, Clark EA, Kaja MK, Diamond MS, Gale M, Jr. 2010. IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog. 6:e1000757. doi:10.1371/journal.ppat.1000757.
15. Samuel MA, Whitby K, Keller BC, Marri A, Barchet W, Williams BR, Silverman RH, Gale M, Jr, Diamond MS. 2006. PKR and RNase L contribute to protection against lethal West Nile virus infection by controlling early viral spread in the periphery and replication in neurons. J. Virol. 80:7009-7019.
16. Daffis S, Samuel MA, Keller BC, Gale M, Jr, Diamond MS. 2007. Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. PLoS Pathog. 3:e106. doi:10.1371/journal.ppat.0030106.
17. Daffis S, Samuel MA, Suthar MS, Keller BC, Gale M, Jr, Diamond MS. 2008. Interferon regulatory factor IRF-7 induces the antiviral alpha interferon response and protects against lethal West Nile virus infection. J. Virol. 82:8465-8475.
18. Samuel MA, Diamond MS. 2005. Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J. Virol. 79:13350-13361.
19. Glass WG, Lim JK, Cholera R, Pletnev AG, Gao JL, Murphy PM. 2005. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J. Exp. Med. 202:1087-1098.
20. Diamond MS, Shrestha B, Marri A, Mahan D, Engle M. 2003. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J. Virol. 77:2578-2586.
21. Shrestha B, Diamond MS. 2004. Role of CD8 T cells in control of West Nile virus infection. J. Virol. 78:8312-8321.
22. Sitati EM, Diamond MS. 2006. CD4 T-cell responses are required for clearance of West Nile virus from the central nervous system. J. Virol. 80:12060-12069.
23. Cho H, Proll SC, Szretter KJ, Katze MG, Gale M, Jr, Diamond MS. 2013. Differential innate immune response programs in neuronal subtypes determine susceptibility to infection in the brain by positivestranded RNA viruses. Nat. Med. 19:458-464.
24. Suthar MS, Brassil MM, Blahnik G, McMillan A, Ramos HJ, Proll SC, Belisle SE, Katze MG, Gale M, Jr. 2013. A systems biology approach reveals that tissue tropism to West Nile virus is regulated by antiviral genes and innate immune cellular processes. PLoS Pathog. 9:e1003168. doi:10.1371/journal.ppat.1003168.
25. Loo YM, Gale M, Jr. 2011. Immune signaling by RIG-I-like receptors. Immunity 34:680-692.
26. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez-Sobrido L, Akira S, Gill MA, Garcia-Sastre A, Katze MG, Gale M, Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82:335-345.
27. Daffis S, Suthar MS, Szretter KJ, Gale M, Jr, Diamond MS. 2009. Induction of IFN-beta and the innate antiviral response in myeloid cells occurs through an IPS-1-dependent signal that does not require IRF-3 and IRF-7. PLoS Pathog. 5:e1000607. doi:10.1371/journal.ppat.1000607.
28. Fredericksen BL, Gale M, Jr. 2006. West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J. Virol. 80: 2913-2923.
29. Lazear HM, Lancaster A, Wilkins C, Suthar MS, Huang A, Vick SC, Clepper L, Thackray L, Brassil MM, Virgin HW, Nikolich-Zugich J, Moses AV, Gale M, Jr, Fruh K, Diamond MS. 2013. IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog. 9:e1003118. doi:10.1371/journal.ppat.1003118.
30. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172.
31. Paz S, Sun Q, Nakhaei P, Romieu-Mourez R, Goubau D, Julkunen I, Lin R, Hiscott J. 2006. Induction of IRF-3 and IRF-7 phosphorylation following activation of the RIG-I pathway. Cell. Mol. Biol. (Noisy-legrand) 52:17-28.
32. Shipley JG, Vandergaast R, Deng L, Mariuzza RA, Fredericksen BL. 2012. Identification of multiple RIG-I-specific pathogen associated molecular patterns within the West Nile virus genome and antigenome. Virology 432:232-238.
33. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G. 2006. 5'Triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
34. Marques JT, Devosse T, Wang D, Zamanian-Daryoush M, Serbinowski P, Hartmann R, Fujita T, Behlke MA, Williams BR. 2006. A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat. Biotechnol. 24:559-565.
35. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M, Jr. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454:523-527.
36. Schlee M, Roth A, Hornung V, Hagmann CA, Wimmenauer V, Barchet W, Coch C, Janke M, Mihailovic A, Wardle G, Juranek S, Kato H, Kawai T, Poeck H, Fitzgerald KA, Takeuchi O, Akira S, Tuschl T, Latz E, Ludwig J, Hartmann G. 2009. Recognition of 5= triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 31:25-34.
37. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C. 2006. RIG-I-mediated antiviral responses to singlestranded RNA bearing 5=-phosphates. Science 314:997-1001.
38. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, Hiiragi A, Dermody TS, Fujita T, Akira S. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acidinducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205:1601-1610.
39. Pichlmair A, Schulz O, Tan CP, Rehwinkel J, Kato H, Takeuchi O, Akira S, Way M, Schiavo G, Reis e Sousa C. 2009. Activation of MDA5 requires higher-order RNA structures generated during virus infection. J. Virol. 83:10761-10769.
40. Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S, van der Aa L, Liu WJ, Palmenberg AC, Shi PY, Hall RA, Khromykh AA. 2008. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4:579-591.
41. Gillespie LK, Hoenen A, Morgan G, Mackenzie JM. 2010. The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J. Virol. 84:10438-10447.
42. Hoenen A, Liu W, Kochs G, Khromykh AA, Mackenzie JM. 2007. West Nile virus-induced cytoplasmic membrane structures provide partial protection against the interferon-induced antiviral MxA protein. J. Gen. Virol. 88:3013-3017.
43. Lindenbach BDR, CM. 2001. Flaviviridae: the viruses and their replication, p 991-1041. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 4th ed, vol 1. Lippincott Williams and Wilkins, Philadelphia, PA.
44. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
45. Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D, Pirani A, Gernert K, Deng J, Marzolf B, Kennedy K, Wu H, Bennouna S, Oluoch H, Miller J, Vencio RZ, Mulligan M, Aderem A, Ahmed R, Pulendran B. 2009. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol. 10:116-125.
46. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988.
47. Suthar MS, Ramos HJ, Brassil MM, Netland J, Chappell CP, Blahnik G, McMillan A, Diamond MS, Clark EA, Bevan MJ, Gale M, Jr. 2012. The RIG-I-like receptor LGP2 controls CD8() T cell survival and fitness. Immunity 37:235-248.
48. Lazear HM, Pinto AK, Ramos HJ, Vick SC, Shrestha B, Suthar MS, Gale M, Jr, Diamond MS. 2013. Pattern recognition receptor MDA5 modulates CD8 T cell-dependent clearance of West Nile virus from the central nervous system. J. Virol. 87:11401-11415.
49. Dong H, Ren S, Zhang B, Zhou Y, Puig-Basagoiti F, Li H, Shi PY. 2008. West Nile virus methyltransferase catalyzes two methylations of the viral RNAcap through a substrate-repositioning mechanism. J. Virol. 82:4295-4307.
50. Perwitasari O, Cho H, Diamond MS, Gale M, Jr. 2011. Inhibitor of kappaB kinase epsilon (IKK(epsilon)), STAT1, and IFIT2 proteins define novel innate immune effector pathway against West Nile virus infection. J. Biol. Chem. 286:44412-44423.
51. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA, Diamond MS, Colonna M. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U. S. A. 103:8459-8464.
52. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, Nakaya T, Katsuki M, Noguchi S, Tanaka N, Taniguchi T. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13:539-548.
53. Keller BC, Fredericksen BL, Samuel MA, Mock RE, Mason PW, Diamond MS, Gale M, Jr. 2006. Resistance to alpha/beta interferon is a determinant of West Nile virus replication fitness and virulence. J. Virol. 80:9424-9434.
54. Laurent-Rolle M, Boer EF, Lubick KJ, Wolfinbarger JB, Carmody AB, Rockx B, Liu W, Ashour J, Shupert WL, Holbrook MR, Barrett AD, Mason PW, Bloom ME, Garcia-Sastre A, Khromykh AA, Best SM. 2010. The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J. Virol. 84:3503-3515.
55. Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, Errett J, Lin TY, Schneller S, Zust R, Dong H, Thiel V, Sen GC, Fensterl V, Klimstra WB, Pierson TC, Buller RM, Gale M, Jr., Shi PY, Diamond MS.2010. 2=-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468:452-456.
56. Malathi K, Dong B, Gale M, Jr, Silverman RH. 2007. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 448: 816-819.
57. Berke IC, Modis Y. 2012. MDA5 cooperatively forms dimers and ATPsensitive filaments upon binding double-stranded RNA. EMBO J. 31: 1714-1726.