IRF-3, IRF-5, and IRF-7 Coordinately Regulate the Type I IFN Response in Myeloid Dendritic Cells Downstream of MAVS Signaling

PLoS Pathogens

Volumn 9, Issue 1, 2013, Pages

  Lazear, Helen M ^a   Lancaster, Alissa ^b   Wilkins, Courtney ^c   Suthar, Mehul S ^c,e   Huang, Albert ^c   Vick, Sarah C ^a   Clepper, Lisa ^b   Thackray, Larissa ^a   Brassil, Margaret M ^c   Virgin, Herbert W ^a   Nikolich Zugich, Janko ^d   Moses, Ashlee V ^b   Gale, Michael ^c   Früh, Klaus ^b   Diamond, Michael S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

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

^d UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 5; INTERFERON REGULATORY FACTOR 7; RETINOIC ACID INDUCIBLE PROTEIN I;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSFECTION; GENOTYPE; IMMUNE RESPONSE; MACROPHAGE; MICROARRAY ANALYSIS; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS INFECTION; VIRUS LOAD; WEST NILE FLAVIVIRUS; WESTERN BLOTTING;

EID: 84875065899     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003118     Document Type: Article

References (84)

1. Welsh RM, Bahl K, Marshall HD, Urban SL, (2012) Type 1 interferons and antiviral CD8 T-cell responses. PLoS Pathog 8: e1002352.
2. Paun A, Pitha PM, (2007) The innate antiviral response: new insights into a continuing story. Adv Virus Res 69: 1-66.
3. Wang BX, Fish EN, (2012) The yin and yang of viruses and interferons. Trends Immunol 33: 190-197.
4. Le Bon A, Tough DF, (2002) Links between innate and adaptive immunity via type I interferon. Curr Opin Immunol 14: 432-436.
5. Jensen S, Thomsen AR, (2012) Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. J Virol 86: 2900-2910.
6. Ramos HJ, Gale M Jr, (2011) RIG-I Like Receptors and Their Signaling Crosstalk in the Regulation of Antiviral Immunity. Curr Opin Virol 1: 167-176.
7. Wilkins C, Gale M Jr, (2010) Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22: 41-47.
8. Diamond MS, Gale M Jr, (2012) Cell-intrinsic innate immune control of West Nile virus infection. Trends Immunol 33: 522-530.
9. Honda K, Takaoka A, Taniguchi T, (2006) Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360.
10. Paun A, Pitha PM, (2007) The IRF family, revisited. Biochimie 89: 744-753.
11. Platanias LC, (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5: 375-386.
12. Sadler AJ, Williams BR, (2008) Interferon-inducible antiviral effectors. Nat Rev Immunol 8: 559-568.
13. 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.
14. 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.
15. Nakaya T, Sato M, Hata N, Asagiri M, Suemori H, et al. (2001) Gene induction pathways mediated by distinct IRFs during viral infection. Biochem Biophys Res Commun 283: 1150-1156.
16. Prakash A, Smith E, Lee CK, Levy DE, (2005) Tissue-specific positive feedback requirements for production of type I interferon following virus infection. J Biol Chem 280: 18651-18657.
17. 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.
18. Izaguirre A, Barnes BJ, Amrute S, Yeow WS, Megjugorac N, et al. (2003) Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol 74: 1125-1138.
19. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, et al. (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777.
20. Schmid S, Mordstein M, Kochs G, Garcia-Sastre A, Tenoever BR, (2010) Transcription factor redundancy ensures induction of the antiviral state. J Biol Chem 285: 42013-42022.
21. 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.
22. 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.
23. Keller BC, Fredericksen BL, Samuel MA, Mock RE, Mason PW, et al. (2006) Resistance to alpha/beta interferon is a determinant of West Nile virus replication fitness and virulence. J Virol 80: 9424-9434.
24. Lazear HM, Pinto AK, Vogt MR, Gale M Jr, Diamond MS, (2011) Beta interferon controls West Nile virus infection and pathogenesis in mice. J Virol 85: 7186-7194.
25. 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.
26. 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.
27. 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.
28. Szretter KJ, Daffis S, Patel J, Suthar MS, Klein RS, et al. (2010) The innate immune adaptor molecule MyD88 restricts West Nile virus replication and spread in neurons of the central nervous system. J Virol 84: 12125-12138.
29. 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.
30. Town T, Bai F, Wang T, Kaplan AT, Qian F, et al. (2009) Toll-like receptor 7 mitigates lethal West Nile encephalitis via interleukin 23-dependent immune cell infiltration and homing. Immunity 30: 242-253.
31. Daffis S, Lazear HM, Liu WJ, Audsley M, Engle M, et al. (2011) The naturally attenuated Kunjin strain of West Nile virus shows enhanced sensitivity to the host type I interferon response. J Virol 85: 5664-5668.
32. Steinberg C, Eisenacher K, Gross O, Reindl W, Schmitz F, et al. (2009) The IFN regulatory factor 7-dependent type I IFN response is not essential for early resistance against murine cytomegalovirus infection. Eur J Immunol 39: 1007-1018.
33. Schilte C, Buckwalter MR, Laird ME, Diamond MS, Schwartz O, et al. (2012) Cutting edge: independent roles for IRF-3 and IRF-7 in hematopoietic and nonhematopoietic cells during host response to Chikungunya infection. J Immunol 188: 2967-2971.
34. Rudd PA, Wilson J, Gardner J, Larcher T, Babarit C, et al. (2012) Interferon response factors 3 and 7 protect against Chikungunya virus hemorrhagic fever and shock. J Virol 86: 9888-9898.
35. Paun A, Reinert JT, Jiang Z, Medin C, Balkhi MY, et al. (2008) Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response. J Biol Chem 283: 14295-14308.
36. Takaoka A, Yanai H, Kondo S, Duncan G, Negishi H, et al. (2005) Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434: 243-249.
37. Yanai H, Chen HM, Inuzuka T, Kondo S, Mak TW, et al. (2007) Role of IFN regulatory factor 5 transcription factor in antiviral immunity and tumor suppression. Proc Natl Acad Sci U S A 104: 3402-3407.
38. Barnes BJ, Richards J, Mancl M, Hanash S, Beretta L, et al. (2004) Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J Biol Chem 279: 45194-45207.
39. Schoenemeyer A, Barnes BJ, Mancl ME, Latz E, Goutagny N, et al. (2005) The interferon regulatory factor, IRF5, is a central mediator of toll-like receptor 7 signaling. J Biol Chem 280: 17005-17012.
40. Brien JD, Daffis S, Lazear HM, Cho H, Suthar MS, et al. (2011) Interferon regulatory factor-1 (IRF-1) shapes both innate and CD8(+) T cell immune responses against West Nile virus infection. PLoS Pathog 7: e1002230.
41. 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.
42. 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: 11557-11566.
43. Atasheva S, Akhrymuk M, Frolova EI, Frolov I, (2012) New PARP Gene with an Anti-Alphavirus Function. J Virol 86: 8147-8160.
44. Eskildsen S, Hartmann R, Kjeldgaard NO, Justesen J, (2002) Gene structure of the murine 2′-5′-oligoadenylate synthetase family. Cell Mol Life Sci 59: 1212-1222.
45. Eskildsen S, Justesen J, Schierup MH, Hartmann R, (2003) Characterization of the 2′-5′-oligoadenylate synthetase ubiquitin-like family. Nucleic Acids Res 31: 3166-3173.
46. Scherbik SV, Stockman BM, Brinton MA, (2007) Differential expression of interferon (IFN) regulatory factors and IFN-stimulated genes at early times after West Nile virus infection of mouse embryo fibroblasts. J Virol 81: 12005-12018.
47. Munoz-Erazo L, Natoli R, Provis JM, Madigan MC, King NJ, (2012) Microarray analysis of gene expression in West Nile virus-infected human retinal pigment epithelium. Mol Vis 18: 730-743.
48. 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.
49. Koh WL, Ng ML, (2005) Molecular mechanisms of West Nile virus pathogenesis in brain cell. Emerg Infect Dis 11: 629-632.
50. Sheehan KC, Lai KS, Dunn GP, Bruce AT, Diamond MS, et al. (2006) Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J Interferon Cytokine Res 26: 804-819.
51. Kanazawa N, Kurosaki M, Sakamoto N, Enomoto N, Itsui Y, et al. (2004) Regulation of hepatitis C virus replication by interferon regulatory factor 1. J Virol 78: 9713-9720.
52. Pine R, (1992) Constitutive expression of an ISGF2/IRF1 transgene leads to interferon-independent activation of interferon-inducible genes and resistance to virus infection. J Virol 66: 4470-4478.
53. Julander JG, Winger QA, Rickords LF, Shi PY, Tilgner M, et al. (2006) West Nile virus infection of the placenta. Virology 347: 175-182.
54. McGee CE, Shustov AV, Tsetsarkin K, Frolov IV, Mason PW, et al. (2010) Infection, dissemination, and transmission of a West Nile virus green fluorescent protein infectious clone by Culex pipiens quinquefasciatus mosquitoes. Vector Borne Zoonotic Dis 10: 267-274.
55. Pierson TC, Diamond MS, Ahmed AA, Valentine LE, Davis CW, et al. (2005) An infectious West Nile virus that expresses a GFP reporter gene. Virology 334: 28-40.
56. Diamond MS, (2009) Mechanisms of evasion of the type I interferon antiviral response by flaviviruses. J Interferon Cytokine Res 29: 521-530.
57. 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.
58. 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.
59. Szretter KJ, Daniels BP, Cho H, Gainey MD, Yokoyama WM, et al. (2012) 2′-O methylation of the viral mRNA cap by West Nile virus evades ifit1-dependent and-independent mechanisms of host restriction in vivo. PLoS Pathog 8: e1002698.
60. Medigeshi GR, Lancaster AM, Hirsch AJ, Briese T, Lipkin WI, et al. (2007) West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J Virol 81: 10849-10860.
61. Mungrue IN, Pagnon J, Kohannim O, Gargalovic PS, Lusis AJ, (2009) CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J Immunol 182: 466-476.
62. Smith SM, Moran AP, Duggan SP, Ahmed SE, Mohamed AS, et al. (2011) Tribbles 3: a novel regulator of TLR2-mediated signaling in response to Helicobacter pylori lipopolysaccharide. J Immunol 186: 2462-2471.
63. He B, (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 13: 393-403.
64. Ambrose RL, Mackenzie JM, (2011) West Nile virus differentially modulates the unfolded protein response to facilitate replication and immune evasion. J Virol 85: 2723-2732.
65. Clavarino G, Claudio N, Couderc T, Dalet A, Judith D, et al. (2012) Induction of GADD34 Is Necessary for dsRNA-Dependent Interferon-beta Production and Participates in the Control of Chikungunya Virus Infection. PLoS Pathog 8: e1002708.
66. Venter M, Myers TG, Wilson MA, Kindt TJ, Paweska JT, et al. (2005) Gene expression in mice infected with West Nile virus strains of different neurovirulence. Virology 342: 119-140.
67. Bourgeois MA, Denslow ND, Seino KS, Barber DS, Long MT, (2011) Gene expression analysis in the thalamus and cerebrum of horses experimentally infected with West Nile virus. PLoS One 6: e24371.
68. 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.
69. Faul EJ, Wanjalla CN, Suthar MS, Gale M, Wirblich C, et al. (2010) Rabies virus infection induces type I interferon production in an IPS-1 dependent manner while dendritic cell activation relies on IFNAR signaling. PLoS Pathog 6: e1001016.
70. Barnes BJ, Kellum MJ, Field AE, Pitha PM, (2002) Multiple regulatory domains of IRF-5 control activation, cellular localization, and induction of chemokines that mediate recruitment of T lymphocytes. Mol Cell Biol 22: 5721-5740.
71. Negishi H, Yanai H, Nakajima A, Koshiba R, Atarashi K, et al. (2012) Cross-interference of RLR and TLR signaling pathways modulates antibacterial T cell responses. Nat Immunol 13: 659-666.
72. Li S, Wang L, Berman M, Kong YY, Dorf ME, (2011) Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 35: 426-440.
73. Ebel GD, Dupuis AP 2nd, Ngo K, Nicholas D, Kauffman E, et al. (2001) Partial genetic characterization of West Nile virus strains, New York State, 2000. Emerg Infect Dis 7: 650-653.
74. 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. Journal of Virology 77: 2578-2586.
75. Xiao SY, Guzman H, Zhang H, Travassos da Rosa AP, Tesh RB, (2001) West Nile virus infection in the golden hamster (Mesocricetus auratus): a model for West Nile encephalitis. Emerg Infect Dis 7: 714-721.
76. Thackray LB, Wobus CE, Chachu KA, Liu B, Alegre ER, et al. (2007) Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J Virol 81: 10460-10473.
77. Chachu KA, Strong DW, LoBue AD, Wobus CE, Baric RS, et al. (2008) Antibody is critical for the clearance of murine norovirus infection. J Virol 82: 6610-6617.
78. Purtha WE, Swiecki M, Colonna M, Diamond MS, Bhattacharya D, (2012) Spontaneous mutation of the Dock2 gene in Irf5-/- mice complicates interpretation of type I interferon production and antibody responses. Proc Natl Acad Sci U S A 109: E898-904.
79. 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.
80. Oliphant T, Engle M, Nybakken GE, Doane C, Johnson S, et al. (2005) Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat Med 11: 522-530.
81. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit R, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor. New York: Springer. pp. 397-420.
82. Saito T, Hirai R, Loo YM, Owen D, Johnson CL, et al. (2007) Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci U S A 104: 582-587.
83. 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.
84. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.