Interferon-induced Ifit proteins: Their role in viral pathogenesis

Journal of Virology

Volumn 89, Issue 5, 2015, Pages 2462-2468

  Fensterl, Volker ^a   Sen, Ganes C ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 3; INTERFERON; INTERFERON REGULATORY FACTOR; MESSENGER RNA; RETINOIC ACID INDUCIBLE PROTEIN I; ANTIVIRUS AGENT; PROTEIN;

ENCEPHALOMYOCARDITIS VIRUS; GENE; GENETIC TRANSCRIPTION; HEPATITIS C VIRUS; HUMAN; IFIT GENE; IFIT1 GENE; IFIT2 GENE; IMMUNE EVASION; INTERFERON STIMULATED GENE; INTERNAL RIBOSOME ENTRY SITE; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; PARAINFLUENZA VIRUS 5; PROTEIN BINDING; PROTEIN STRUCTURE; SENDAI VIRUS INFECTION; SHORT SURVEY; TETRATRICOPEPTIDE REPEAT; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VESICULAR STOMATITIS; VIRUS PATHOGENESIS; VIRUS REPLICATION; WEST NILE FLAVIVIRUS; ANIMAL; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MOUSE; PROTEIN SYNTHESIS; VIRUS;

MURINAE; MUS;

ANIMALS; ANTIVIRAL AGENTS; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INTERFERONS; MICE; PROTEIN BIOSYNTHESIS; PROTEINS; VIRUSES;

EID: 84922983597     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02744-14     Document Type: Short Survey

References (66)

1. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921. http://dx.doi.org/10.1126/science.8009221.
2. Broz P, Monack DM. 2013. Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol 13:551-565. http://dx.doi.org/10.1038/nri3479.
3. Fensterl V, Sen GC. 2009. Interferons and viral infections. BioFactors 35:14-20. http://dx.doi.org/10.1002/biof.6.
4. 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 USA 95:15623-15628. http://dx.doi.org/10.1073/pnas.95.26.15623.
5. Schoggins JW, Rice CM. 2011. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 1:519-525. http://dx.doi.org/10.1016/j.coviro.2011.10.008.
6. Schoggins JW. 2014. Interferon-stimulated genes: roles in viral pathogenesis. Curr Opin Virol 6C:40-46. http://dx.doi.org/10.1016/j.coviro.2014.03.006.
7. Bandyopadhyay SK, Leonard GT, Jr, Bandyopadhyay T, Stark GR, Sen GC. 1995. Transcriptional induction by double-stranded RNA is mediated by interferon-stimulated response elements without activation of interferon-stimulated gene factor 3. J Biol Chem 270:19624-19629. http://dx.doi.org/10.1074/jbc.270.33.19624.
8. Barnes BJ, Richards J, Mancl M, Hanash S, Beretta L, Pitha PM. 2004. Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J Biol Chem 279:45194-45207. http://dx.doi.org/10.1074/jbc.M400726200.
9. Elco CP, Guenther JM, Williams BR, Sen GC. 2005. Analysis of genes induced by Sendai virus infection of mutant cell lines reveals essential roles of interferon regulatory factor 3, NF-kappaB, and interferon but not Toll-like receptor 3. J Virol 79:3920-3929. http://dx.doi.org/10.1128/JVI.79.7.3920-3929.2005.
10. Grandvaux N, Servant MJ, ten Oever B, Sen GC, Balachandran S, Barber GN, Lin R, Hiscott J. 2002. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J Virol 76:5532-5539. http://dx.doi.org/10.1128/JVI.76.11.5532-5539.2002.
11. Ikushima H, Negishi H, Taniguchi T. 2013. The IRF family transcription factors at the interface of innate and adaptive immune responses. Cold Spring Harb Symp Quant Biol 78:105-116. http://dx.doi.org/10.1101/sqb.2013.78.020321.
12. Diamond MS. 2014. IFIT1: a dual sensor and effector molecule that detects non-2'-O methylated viral RNA and inhibits its translation. Cytokine Growth Factor Rev 25:543-550. http://dx.doi.org/10.1016/j.cytogfr.2014.05.002.
13. Diamond MS, Farzan M. 2013. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol 13:46-57. http://dx.doi.org/10.1038/nri3344.
14. Vladimer GI, Gorna MW, Superti-Furga G. 2014. IFITs: emerging roles as key anti-viral proteins. Front Immunol 5:94. http://dx.doi.org/10.3389/fimmu.2014.00094.
15. Chebath J, Merlin G, Metz R, Benech P, Revel M. 1983. Interferon-induced 56,000 Mr protein and itsmRNAin human cells: molecular cloning and partial sequence of the cDNA. Nucleic Acids Res 11:1213-1226. http://dx.doi.org/10.1093/nar/11.5.1213.
16. Kusari J, Sen GC. 1987. Transcriptional analyses of interferon-inducible mRNAs. Mol Cell Biol 7:528-531.
17. Fensterl V, Sen GC. 2011. The ISG56/IFIT1 gene family. J Interferon Cytokine Res 31:71-78. http://dx.doi.org/10.1089/jir.2010.0101.
18. Habjan M, Hubel P, Lacerda L, Benda C, Holze C, Eberl CH, Mann A, Kindler E, Gil-Cruz C, Ziebuhr J, Thiel V, Pichlmair A. 2013. Sequestration by IFIT1 impairs translation of 2'O-unmethylated cappedRNA.PLoS Pathog 9:e1003663. http://dx.doi.org/10.1371/journal.ppat.1003663.
19. Kohli A, Zhang X, Yang J, Russell RS, Donnelly RP, Sheikh F, Sherman A, Young H, Imamichi T, Lempicki RA, Masur H, Kottilil S. 2012. Distinct and overlapping genomic profiles and antiviral effects of interferon-lambda and-alpha on HCV-infected and noninfected hepatoma cells. J Viral Hepat 19:843-853. http://dx.doi.org/10.1111/j.1365-2893.2012.01610.x.
20. Rauch I, Muller M, Decker T. 2013. The regulation of inflammation by interferons and their STATs. JAKSTAT 2:e23820. http://dx.doi.org/10.4161/jkst.23820.
21. Jakobsen MR, Bak RO, Andersen A, Berg RK, Jensen SB, Tengchuan J, Laustsen A, Hansen K, Ostergaard L, Fitzgerald KA, Xiao TS, Mikkelsen JG, Mogensen TH, Paludan SR. 2013. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc Natl Acad Sci USA 110:E4571-E4580. http://dx.doi.org/10.1073/pnas.1311669110.
22. Lam E, Stein S, Falck-Pedersen E. 2014. Adenovirus detection by the cGAS/STING/TBK1 DNA sensing cascade. J Virol 88:974-981. http://dx.doi.org/10.1128/JVI.02702-13.
23. Xiao S, Li D, Zhu HQ, Song MG, Pan XR, Jia PM, Peng LL, Dou AX, Chen GQ, Chen SJ, Chen Z, Tong JH. 2006. RIG-G as a key mediator of the antiproliferative activity of interferon-related pathways through enhancing p21 and p27 proteins. Proc Natl Acad SciUSA103:16448-16453. http://dx.doi.org/10.1073/pnas.0607830103.
24. Terenzi F, White C, Pal S, Williams BR, Sen GC. 2007. Tissue-specific and inducer-specific differential induction of ISG56 and ISG54 in mice. J Virol 81:8656-8665. http://dx.doi.org/10.1128/JVI.00322-07.
25. Wacher C, Muller M, Hofer MJ, Getts DR, Zabaras R, Ousman SS, Terenzi F, Sen GC, King NJ, Campbell IL. 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. http://dx.doi.org/10.1128/JVI.01167-06.
26. 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. http://dx.doi.org/10.1038/nm.3108.
27. D'Andrea LD, Regan L. 2003. TPR proteins: the versatile helix. Trends Biochem Sci 28:655-662. http://dx.doi.org/10.1016/j.tibs.2003.10.007.
28. Abbas YM, Pichlmair A, Gorna MW, Superti-Furga G, Nagar B. 2013. Structural basis for viral 5'-PPP-RNA recognition by human IFIT proteins. Nature 494:60-64. http://dx.doi.org/10.1038/nature11783.
29. Yang Z, Liang H, Zhou Q, Li Y, Chen H, Ye W, Chen D, Fleming J, Shu H, Liu Y. 2012. Crystal structure of ISG54 reveals a novel RNA binding structure and potential functional mechanisms. Cell Res 22:1328-1338. http://dx.doi.org/10.1038/cr.2012.111.
30. Pichlmair A, Lassnig C, Eberle CA, Gorna MW, Baumann CL, Burkard TR, Burckstummer T, Stefanovic A, Krieger S, Bennett KL, Rulicke T, Weber F, Colinge J, Muller M, Superti-Furga G. 2011. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat Immunol 12: 624-630. http://dx.doi.org/10.1038/ni.2048.
31. Stawowczyk M, Van Scoy S, Kumar KP, Reich NC. 2011. The interferon stimulated gene 54 promotes apoptosis. J Biol Chem 286:7257-7266. http://dx.doi.org/10.1074/jbc.M110.207068.
32. Guo J, Hui DJ, Merrick WC, Sen GC. 2000. A new pathway of translational regulation mediated by eukaryotic initiation factor 3. EMBO J 19: 6891-6899. http://dx.doi.org/10.1093/emboj/19.24.6891.
33. 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. http://dx.doi.org/10.1128/JVI.74.4.1892-1899.2000.
34. 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. http://dx.doi.org/10.1074/jbc.M305038200.
35. 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. http://dx.doi.org/10.1074/jbc.M406700200.
36. 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. http://dx.doi.org/10.1074/jbc.M605771200.
37. Terenzi F, Pal S, Sen GC. 2005. Induction and mode of action of the viral stress-inducible murine proteins, P56 and P54. Virology 340:116-124. http://dx.doi.org/10.1016/j.virol.2005.06.011.
38. Fraser CS, Doudna JA. 2007. Structural and mechanistic insights into hepatitis C viral translation initiation. Nat Rev Microbiol 5:29-38. http://dx.doi.org/10.1038/nrmicro1558.
39. Wang C, Pflugheber J, Sumpter R, Jr, Sodora DL, Hui D, Sen GC, Gale M, Jr. 2003. Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J Virol 77:3898-3912. http://dx.doi.org/10.1128/JVI.77.7.3898-3912.2003.
40. Lopez-Rodriguez R, Trapero-Marugan M, Borque MJ, Roman M, Hernandez-Bartolome A, Rodriguez-Munoz Y, Martin-Vilchez S, Abad-Santos F, Munoz de Rueda P, Vidal-Castineira JR, Rodrigo L, Salmeron J, Moreno-Otero R, Sanz-Cameno P. 2011. Genetic variants of interferon-stimulated genes and IL-28B as host prognostic factors of response to combination treatment for chronic hepatitis C. Clin Pharmacol Ther 90: 712-721. http://dx.doi.org/10.1038/clpt.2011.189.
41. 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. http://dx.doi.org/10.1038/emboj.2008.241.
42. Li C, Zhang W, Li Y, Guo L, Shu H, Liu Y. 2012. ISG60 negatively regulates cell antiviral responses by disrupting the VISA-associated complexes. Wuhan Univ J Nat Sci 17:1-6. http://dx.doi.org/10.1007/s11859-012-0795-6.
43. Li Y, Li C, Xue P, Zhong B, Mao AP, Ran Y, Chen H, Wang YY, Yang F, Shu HB. 2009. ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. Proc Natl Acad Sci USA 106: 7945-7950. http://dx.doi.org/10.1073/pnas.0900818106.
44. Liu XY, Chen W, Wei B, Shan YF, Wang C. 2011. IFN-induced TPR protein IFIT3 potentiates antiviral signaling by bridgingMAVSandTBK1.JImmunol 187:2559-2568. http://dx.doi.org/10.4049/jimmunol.1100963.
45. Zhang B, Liu X, Chen W, Chen L. 2013. IFIT5 potentiates anti-viral response through enhancing innate immune signaling pathways. Acta Biochim Biophys Sin 45:867-874. http://dx.doi.org/10.1093/abbs/gmt088.
46. Zust R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, Ziebuhr J, Szretter KJ, Baker SC, Barchet W, Diamond MS, Siddell SG, Ludewig B, Thiel V. 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. http://dx.doi.org/10.1038/ni.1979.
47. Kimura T, Katoh H, Kayama H, Saiga H, Okuyama M, Okamoto T, Umemoto E, Matsuura Y, Yamamoto M, Takeda K. 2013. Ifit1 inhibits Japanese encephalitis virus replication through binding to 5' capped 2'-O unmethylated RNA. J Virol 87:9997-10003. http://dx.doi.org/10.1128/JVI.00883-13.
48. Kumar P, Sweeney TR, Skabkin MA, Skabkina OV, Hellen CU, Pestova TV. 2014. Inhibition of translation by IFIT family members is determined by their ability to interact selectively with the 5'-terminal regions of cap0-, cap1-and 5'ppp-mRNAs. Nucleic Acids Res 42:3228-3245. http://dx.doi.org/10.1093/nar/gkt1321.
49. Gerlier D, Lyles DS. 2011. Interplay between innate immunity and negative-strand RNA viruses: towards a rational model. Microbiol Mol Biol Rev 75:468-490. http://dx.doi.org/10.1128/MMBR.00007-11.
50. Raychoudhuri A, Shrivastava S, Steele R, Kim H, Ray R, Ray RB. 2011. ISG56 and IFITM1 proteins inhibit hepatitis C virus replication. J Virol 85:12881-12889. http://dx.doi.org/10.1128/JVI.05633-11.
51. Cho H, Shrestha B, Sen GC, Diamond MS. 2013. A role for Ifit2 in restricting West Nile virus infection in the brain. J Virol 87:8363-8371. http://dx.doi.org/10.1128/JVI.01097-13.
52. Andrejeva J, Norsted H, Habjan M, Thiel V, Goodbourn S, Randall RE. 2013. ISG56/IFIT1 is primarily responsible for interferon-induced changes to patterns of parainfluenza virus type 5 transcription and protein synthesis. J Gen Virol 94:59-68. http://dx.doi.org/10.1099/vir.0.046797-0.
53. Fensterl V, Wetzel JL, Ramachandran S, Ogino T, Stohlman SA, Bergmann CC, Diamond MS, Virgin HW, Sen GC. 2012. Interferon-induced Ifit2/ISG54 protects mice from lethal VSV neuropathogenesis. PLoS Pathog 8:e1002712. http://dx.doi.org/10.1371/journal.ppat.1002712.
54. Fensterl V, Wetzel JL, Sen GC. 2014. Interferon-induced protein ifit2 protects mice from infection of the peripheral nervous system by vesicular stomatitis virus. J Virol 88:10303-10311. http://dx.doi.org/10.1128/JVI.01341-14.
55. Plakhov IV, Arlund EE, Aoki C, Reiss CS. 1995. The earliest events in vesicular stomatitis virus infection of the murine olfactory neuroepithelium and entry of the central nervous system. Virology 209:257-262. http://dx.doi.org/10.1006/viro.1995.1252.
56. van den Pol AN, Ding S, Robek MD. 2014. Long-distance interferon signaling within the brain blocks virus spread. J Virol 88:3695-3704. http://dx.doi.org/10.1128/JVI.03509-13.
57. Iannacone M, Moseman EA, Tonti E, Bosurgi L, Junt T, Henrickson SE, Whelan SP, Guidotti LG, von Andrian UH. 2010. Subcapsular sinus macrophages prevent CNS invasion on peripheral infection with a neurotropic virus. Nature 465:1079-1083. http://dx.doi.org/10.1038/nature09118.
58. Butchi NB, Hinton DR, Stohlman SA, Kapil P, Fensterl V, Sen GC, Bergmann CC. 2014. Ifit2 deficiency results in uncontrolled neurotropic coronavirus replication and enhanced encephalitis via impaired alpha/beta interferon induction in macrophages. J Virol 88:1051-1064. http://dx.doi.org/10.1128/JVI.02272-13.
59. Wetzel JL, Fensterl V, Sen GC. 2014. Sendai virus pathogenesis in mice is prevented by Ifit2 and exacerbated by interferon. J Virol 88:13593-13601. http://dx.doi.org/10.1128/JVI.02201-14.
60. 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. http://dx.doi.org/10.1038/nature09489.
61. Szretter KJ, Daniels BP, Cho H, Gainey MD, Yokoyama WM, Gale M, Jr, Virgin HW, Klein RS, Sen GC, Diamond MS. 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. http://dx.doi.org/10.1371/journal.ppat.1002698.
62. Menachery VD, Yount BL, Jr, Josset L, Gralinski LE, Scobey T, Agnihothram S, Katze MG, Baric RS. 2014. Attenuation and restoration of severe acute respiratory syndrome coronavirus mutant lacking 2'-Omethyltransferase activity. J Virol 88:4251-4264. http://dx.doi.org/10.1128/JVI.03571-13.
63. Hyde JL, Gardner CL, Kimura T, White JP, Liu G, Trobaugh DW, Huang C, Tonelli M, Paessler S, Takeda K, Klimstra WB, Amarasinghe GK, Diamond MS. 2014. A viral RNA structural element alters host recognition of nonself RNA. Science 343:783-787. http://dx.doi.org/10.1126/science.1248465.
64. 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. http://dx.doi.org/10.1128/JVI.01282-07.
65. Zhao C, Denison C, Huibregtse JM, Gygi S, Krug RM. 2005. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc Natl Acad SciUSA 102:10200-10205. http://dx.doi.org/10.1073/pnas.0504754102.
66. Mukherjee C, Patil DP, Kennedy BA, Bakthavachalu B, Bundschuh R, Schoenberg DR. 2012. Identification of cytoplasmic capping targets reveals a role for cap homeostasis in translation and mRNA stability. Cell Rep 2:674-684. http://dx.doi.org/10.1016/j.celrep.2012.07.011.