2′-O methylation of the viral mRNA cap by West Nile virus evades Ifit1-dependent and -independent mechanisms of host restriction in vivo

PLoS Pathogens

Volumn 8, Issue 5, 2012, Pages

  Szretter, Kristy J ^a   Daniels, Brian P ^a   Cho, Hyelim ^a   Gainey, Maria D ^a   Yokoyama, Wayne M ^a   Gale, Michael ^b   Virgin, Herbert W ^a   Klein, Robyn S ^a   Sen, Ganes C ^c   Diamond, Michael S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2' O METHYLTRANSFERASE; IFIT1 PROTEIN; INTERFERON REGULATORY FACTOR; MESSENGER RNA; METHYLTRANSFERASE; UNCLASSIFIED DRUG; VIRUS RNA; CAPPED RNA; CARRIER PROTEIN; IFIT1 PROTEIN, MOUSE; INTERFERON; NS5 PROTEIN, FLAVIVIRUS; VIRUS PROTEIN;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; BLOOD BRAIN BARRIER; BRAIN REGION; CD8+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; IMMUNE EVASION; IMMUNOPATHOGENESIS; IN VIVO STUDY; LD 50; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PROTEIN FUNCTION; RNA METHYLATION; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS GENE; VIRUS MUTANT; VIRUS REPLICATION; VIRUS STRAIN; WEST NILE FLAVIVIRUS; WILD TYPE; ANIMAL; C57BL MOUSE; ENDOTHELIUM CELL; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MACROPHAGE; METABOLISM; METHYLATION; MOUSE MUTANT; PATHOGENICITY; VIROLOGY; WEST NILE FEVER;

MUS; WEST NILE VIRUS;

ANIMALS; BLOOD-BRAIN BARRIER; CARRIER PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM; ENDOTHELIAL CELLS; FEMALE; IMMUNITY, INNATE; INTERFERON TYPE I; MACROPHAGES; METHYLATION; METHYLTRANSFERASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RNA CAPS; RNA, VIRAL; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84863711523     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002698     Document Type: Article

References (62)

1. Liu SY, Sanchez DJ, Cheng G, (2011) New developments in the induction and antiviral effectors of type I interferon. Curr Opin Immunol 23: 57-64.
2. Wilkins C, Gale M Jr, (2010) Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22: 41-7.
3. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, et al. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485.
4. Fensterl V, Sen GC, (2011) The ISG56/IFIT1 Gene Family. J Interferon Cytokine Res 31: 71-78.
5. Zhu H, Cong JP, Shenk T, (1997) Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc Natl Acad Sci U S A 94: 13985-13990.
6. 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.
7. Wacher C, Muller M, Hofer MJ, Getts DR, Zabaras R, et al. (2007) Coordinated regulation and widespread cellular expression of interferon-stimulated genes (ISG) ISG-49, ISG-54, and ISG-56 in the central nervous system after infection with distinct viruses. J Virol 81: 860-871.
8. Guo J, Peters KL, Sen GC, (2000) Induction of the human protein P56 by interferon, double-stranded RNA, or virus infection. Virology 267: 209-219.
9. Guo J, Sen GC, (2000) Characterization of the interaction between the interferon-induced protein P56 and the Int6 protein encoded by a locus of insertion of the mouse mammary tumor virus. J Virol 74: 1892-1899.
10. Hui DJ, Bhasker CR, Merrick WC, Sen GC, (2003) Viral stress-inducible protein p56 inhibits translation by blocking the interaction of eIF3 with the ternary complex eIF2.GTP.Met-tRNAi. J Biol Chem 278: 39477-39482.
11. Hui DJ, Terenzi F, Merrick WC, Sen GC, (2005) Mouse p56 blocks a distinct function of eukaryotic initiation factor 3 in translation initiation. J Biol Chem 280: 3433-3440.
12. Terenzi F, Hui DJ, Merrick WC, Sen GC, (2006) Distinct induction patterns and functions of two closely related interferon-inducible human genes, ISG54 and ISG56. J Biol Chem 281: 34064-34071.
13. Fensterl V, White CL, Yamashita M, Sen GC, (2008) Novel characteristics of the function and induction of murine p56 family proteins. J Virol 82: 11045-11053.
14. Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, et al. (2010) 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468: 452-456.
15. Zust R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, et al. (2011) Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat Immunol 12: 137-143.
16. Pichlmair A, Lassnig C, Eberle CA, Gorna MW, Baumann CL, et al. (2011) IFIT1 is an antiviral protein that recognizes 5′-triphosphate RNA. Nat Immunol 12: 624-630.
17. Terenzi F, Saikia P, Sen GC, (2008) Interferon-inducible protein, P56, inhibits HPV DNA replication by binding to the viral protein E1. Embo J 27: 3311-3321.
18. Sumpter R Jr, Loo YM, Foy E, Li K, Yoneyama M, et al. (2005) Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79: 2689-2699.
19. Zhang Y, Burke CW, Ryman KD, Klimstra WB, (2007) Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J Virol 81: 11246-11255.
20. Wang C, Pflugheber J, Sumpter R Jr, Sodora DL, Hui D, et al. (2003) Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J Virol 77: 3898-3912.
21. Petersen LR, Hayes EB, (2008) West Nile virus in the Americas. Med Clin North Am 92: 1307-1322 ix.
22. Samuel MA, Wang H, Siddharthan V, Morrey JD, Diamond MS, (2007) Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc Natl Acad Sci U S A 104: 17140-17145.
23. Verma S, Lo Y, Chapagain M, Lum S, Kumar M, et al. (2009) West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: Transmigration across the in vitro blood-brain barrier. Virology 385: 425-433.
24. Verma S, Kumar M, Gurjav U, Lum S, Nerurkar VR, (2010) Reversal of West Nile virus-induced blood-brain barrier disruption and tight junction proteins degradation by matrix metalloproteinases inhibitor. Virology 397: 130-138.
25. Wang P, Dai J, Bai F, Kong KF, Wong SJ, et al. (2008) Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J Virol 82: 8978-8985.
26. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, et al. (2004) Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10: 1366-1373.
27. Ben-Nathan D, Huitinga I, Lustig S, van Rooijen N, Kobiler D, (1996) West Nile virus neuroinvasion and encephalitis induced by macrophage depletion in mice. Arch Virol 141: 459-469.
28. Bai F, Kong KF, Dai J, Qian F, Zhang L, et al. (2010) A paradoxical role for neutrophils in the pathogenesis of West Nile virus. J Infect Dis 202: 1804-1812.
29. Zhou Y, Ray D, Zhao Y, Dong H, Ren S, et al. (2007) Structure and function of flavivirus NS5 methyltransferase. J Virol 81: 3891-3903.
30. Samuel MA, Whitby K, Keller BC, Marri A, Barchet W, et al. (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.
31. Szretter KJ, Brien JD, Thackray LB, Virgin HW, Cresswell P, et al. (2011) The interferon-inducible gene viperin restricts West Nile virus pathogenesis J Virol 85: 115557-66.
32. Samuel MA, Diamond MS, (2005) Type I IFN protects against lethal West Nile Virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol 79: 13350-13361.
33. Lazear HM, Pinto AK, Vogt MR, Gale M Jr, Diamond MS, (2011) Interferon-{beta} controls West Nile virus infection and pathogenesis in mice. J Virol 85: 7186-7194.
34. Daffis S, Samuel MA, Suthar MS, Keller BC, Gale M Jr, et al. (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.
35. Suthar MS, Ma DY, Thomas S, Lund JM, Zhang N, et al. (2010) IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog 6: e1000757.
36. Purtha WE, Myers N, Mitaksov V, Sitati E, Connolly J, et al. (2007) Antigen-specific cytotoxic T lymphocytes protect against lethal West Nile virus encephalitis. Eur J Immunol 37: 1845-1854.
37. Berth SH, Leopold PL, Morfini GN, (2009) Virus-induced neuronal dysfunction and degeneration. Front Biosci 14: 5239-5259.
38. Samuel MA, Morrey JD, Diamond MS, (2007) Caspase-3 dependent cell death of neurons contributes to the pathogenesis of West Nile virus encephalitis. J Virol 81: 2614-2623.
39. Choi DW, (1992) Excitotoxic cell death. J Neurobiol 23: 1261-1276.
40. Wang Y, Lobigs M, Lee E, Mullbacher A, (2003) CD8+ T cells mediate recovery and immunopathology in West Nile virus encephalitis. J Virol 77: 13323-13334.
41. Grandvaux N, Servant MJ, tenOever B, Sen GC, Balachandran S, et al. (2002) Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J Virol 76: 5532-5539.
42. Der SD, Zhou A, Williams BR, Silverman RH, (1998) Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 15623-15628.
43. Fredericksen BL, Smith M, Katze MG, Shi PY, Gale M, (2004) The host response to West Nile virus infection limits spread through the activation of the interferon regulatory factor 3 pathway. J Virol 78: 7737-7747.
44. Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S, et al. (2008) A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4: 579-591.
45. Funk A, Truong K, Nagasaki T, Torres S, Floden N, et al. (2010) RNA structures required for production of subgenomic flavivirus RNA. J Virol 84: 11407-11417.
46. Jiang D, Weidner JM, Qing M, Pan XB, Guo H, et al. (2010) Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections. J Virol 84: 8332-8341.
47. Li Y, Li C, Xue P, Zhong B, Mao AP, et al. (2009) ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. Proc Natl Acad Sci U S A 106: 7945-7950.
48. Klein RS, Lin E, Zhang B, Luster AD, Tollett J, et al. (2005) Neuronal CXCL10 directs CD8+ T cell recruitment and control of West Nile virus encephalitis. J Virol 79: 11457-11466.
49. Zhang B, Chan YK, Lu B, Diamond MS, Klein RS, (2008) CXCR3 mediates region-specific antiviral T cell trafficking within the central nervous system during West Nile virus encephalitis. J Immunol 180: 2641-2649.
50. Stawowczyk M, Van Scoy S, Kumar KP, Reich NC, (2011) The interferon stimulated gene 54 promotes apoptosis. J Biol Chem 286: 7257-7266.
51. Shrestha B, Diamond MS, (2004) The role of CD8+ T cells in the control of West Nile virus infection. J Virol 78: 8312-8321.
52. Shrestha B, Samuel MA, Diamond MS, (2006) CD8+ T cells require perforin to clear West Nile virus from infected neurons. J Virol 80: 119-129.
53. Brien JD, Uhrlaub JL, Nikolich-Zugich J, (2007) Protective capacity and epitope specificity of CD8(+) T cells responding to lethal West Nile virus infection. Eur J Immunol 37: 1855-1863.
54. Vogt MR, Moesker B, Goudsmit J, Jongeneelen M, Austin SK, et al. (2009) Human Monoclonal Antibodies Induced by Natural Infection Against West Nile Virus Neutralize at a Post-Attachment Step. J Virol 83: 6494-6507.
55. 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.
56. Fuchs A, Pinto AK, Schwaeble WJ, Diamond MS, (2011) The lectin pathway of complement activation contributes to protection from West Nile virus infection. Virology 412: 101-109.
57. Szretter KJ, Daffis S, Patel J, Suthar MS, Klein RS, et al. (2010) The innate immune adaptor molecule MyD88 restricts West Nile replication and spread in neurons of the central nervous system. J Virol 84: 12125-12138.
58. 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.
59. Perriere N, Demeuse P, Garcia E, Regina A, Debray M, et al. (2005) Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 93: 279-289.
60. Cruz-Orengo L, Holman DW, Dorsey D, Zhou L, Zhang P, et al. (2011) CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J Exp Med 208: 327-339.
61. Szretter KJ, Samuel MA, Gilfillan S, Fuchs A, Colonna M, et al. (2009) The immune adaptor molecule SARM modulates tumor necrosis factor alpha production and microglia activation in the brainstem and restricts West Nile Virus pathogenesis. J Virol 83: 9329-9338.
62. Shrestha B, Gottlieb DI, Diamond MS, (2003) Infection and injury of neurons by West Nile Encephalitis virus. J Virol 77: 13203-13213.