Human and murine IFIT1 proteins do not restrict infection of negative-sense RNA viruses of the orthomyxoviridae, Bunyaviridae, and filoviridae families

Journal of Virology

Volumn 89, Issue 18, 2015, Pages 9465-9476

  Pinto, Amelia K ^a   Williams, Graham D ^a   Szretter, Kristy J ^a   White, James P ^a   Proença Módena, José Luiz ^a,d   Liu, Gai ^a   Olejnik, Judith ^b   Brien, James D ^a   Ebihara, Hideki ^c   Mühlberger, Elke ^b   Amarasinghe, Gaya ^a   Diamond, Michael S ^a   Boona, Adrianus C M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; INTERFERON INDUCED PROTEIN WITH TETRATRICOPEPTIDE REPEAT 1; NUCLEOPROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; CARRIER PROTEIN; IFIT1 PROTEIN, HUMAN; IFIT1 PROTEIN, MOUSE;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; BUNYAVIRIDAE; BUNYAVIRUS INFECTION; FILOVIRIDAE; FILOVIRUS INFECTION; GENE FREQUENCY; GROWTH INHIBITION; HUMAN; HUMAN CELL; IFIT GENE; INFLUENZA VIRUS; MACROPHAGE; MOUSE; NONHUMAN; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRUS INFECTION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA STRUCTURE; VIROGENESIS; VIRUS GENE; VIRUS REPLICATION; ANIMAL; CELL LINE; EBOLAVIRUS; GENETICS; INFLUENZA A VIRUS; KNOCKOUT MOUSE; LA CROSSE VIRUS; METABOLISM; RNA VIRUS INFECTION;

ANIMALS; CARRIER PROTEINS; CELL LINE; EBOLAVIRUS; HUMANS; INFLUENZA A VIRUS; LA CROSSE VIRUS; MICE; MICE, KNOCKOUT; RNA VIRUS INFECTIONS;

EID: 84940486243     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00996-15     Document Type: Article

References (46)

1. 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.
2. Zhou X, Michal JJ, Zhang L, Ding B, Lunney JK, Liu B, Jiang Z. 2013. Interferon induced IFIT family genes in host antiviral defense. Int J Biol Sci 9:200-208. http://dx.doi.org/10.7150/ijbs.5613.
3. Liu Y, Zhang YB, Liu TK, Gui JF. 2013. Lineage-specific expansion of IFIT gene family: an insight into coevolution with IFN gene family. PLoS One 8:e66859. http://dx.doi.org/10.1371/journal.pone.0066859.
4. 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.
5. 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.
6. 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.
7. 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.
8. Saikia P, Fensterl V, Sen GC. 2010. The inhibitory action of P56 on select functions of E1 mediates interferon's effect on human papillomavirus DNA replication. J Virol 84:13036-13039. http://dx.doi.org/10.1128/JVI .01194-10.
9. 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.
10. 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.
11. 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.
12. Li SH, Dong H, Li XF, Xie X, Zhao H, Deng YQ, Wang XY, Ye Q, Zhu SY, Wang HJ, Zhang B, Leng QB, Zuest R, Qin ED, Qin CF, Shi PY. 2013. Rational design of a flavivirus vaccine by abolishing viral RNA 2=-O methylation. J Virol 87:5812-5819. http://dx.doi.org/10.1128/JVI.02806-12.
13. 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.
14. Zust R, Dong H, Li XF, Chang DC, Zhang B, Balakrishnan T, Toh YX, Jiang T, Li SH, Deng YQ, Ellis BR, Ellis EM, Poidinger M, Zolezzi F, Qin CF, Shi PY, Fink K. 2013. Rational design of a live attenuated dengue vaccine: 2=-O-methyltransferase mutants are highly attenuated and immunogenic in mice and macaques. PLoS Pathog 9:e1003521. http://dx.doi .org/10.1371/journal.ppat.1003521.
15. 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 capped RNA. PLoS Pathog 9:e1003663. http://dx.doi.org/10.1371 /journal.ppat.1003663.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. Hyde JL, Diamond MS. 2015. Innate immune restriction and antagonism of viral RNA lacking 2=-O methylation. Virology 479-480:66-74. http: //dx.doi.org/10.1016/j.virol.2015.01.019.
22. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823-826. http://dx.doi.org/10.1126/science.1232033.
23. 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. http://dx.doi.org/10.1128/JVI.00489-06.
24. Beutner C, Roy K, Linnartz B, Napoli I, Neumann H. 2010. Generation of microglial cells from mouse embryonic stem cells. Nat Protoc 5:1481- 1494. http://dx.doi.org/10.1038/nprot.2010.90.
25. You Y, Richer EJ, Huang T, Brody SL. 2002. Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am J Physiol Lung Cell Mol Physiol 283:L1315-L1321. http://dx.doi.org /10.1152/ajplung.00169.2002.
26. Boon AC, deBeauchamp J, Krauss S, Rubrum A, Webb AD, Webster RG, McElhaney J, Webby RJ. 2010. Cross-reactive neutralizing antibodies directed against pandemic H1N1 2009 virus are protective in a highly sensitive DBA/2 mouse influenza model. J Virol 84:7662-7667. http://dx .doi.org/10.1128/JVI.02444-09.
27. Zhou Y, Ray D, Zhao Y, Dong H, Ren S, Li Z, Guo Y, Bernard KA, Shi PY, Li H. 2007. Structure and function of flavivirus NS5 methyltransferase. J Virol 81:3891-3903. http://dx.doi.org/10.1128/JVI.02704-06.
28. Bray M, Davis K, Geisbert T, Schmaljohn C, Huggins J. 1998. A mouse model for evaluation of prophylaxis and therapy of Ebola hemorrhagic fever. J Infect Dis 178:651-661. http://dx.doi.org/10.1086/515386.
29. Proenca-Modena JL, Sesti-Costa R, Pinto AK, Richner JM, Lazear HM, Lucas T, Hyde JL, Diamond MS. 2015. Oropouche virus infection and pathogenesis are restricted by MAVS, IRF-3, IRF-7, and type I interferon signaling pathways in nonmyeloid cells. J Virol 89:4720-4737. http://dx .doi.org/10.1128/JVI.00077-15.
30. Oliphant T, Engle M, Nybakken GE, Doane C, Johnson S, Huang L, Gorlatov S, Mehlhop E, Marri A, Chung KM, Ebel GD, Kramer LD, Fremont DH, Diamond MS. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat Med 11:522-530. http://dx.doi.org/10.1038/nm1240.
31. You Y, Brody SL. 2013. Culture and differentiation of mouse tracheal epithelial cells. Methods Mol Biol 945:123-143. http://dx.doi.org/10.1007 /978-1-62703-125-7_9.
32. Fensterl V, Sen GC. 2015. Interferon-induced Ifit proteins: their role in viral pathogenesis. J Virol 89:2462-2468. http://dx.doi.org/10.1128/JVI .02744-14.
33. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, Ryan BJ, Weyer JL, van der Weyden L, Fikrig E, Adams DJ, Xavier RJ, Farzan M, Elledge SJ. 2009. The IFITM proteins mediate cellular resistance to influenzaAH1N1 virus, West Nile virus, and dengue virus. Cell 139:1243- 1254. http://dx.doi.org/10.1016/j.cell.2009.12.017.
34. Patterson JL, Holloway B, Kolakofsky D. 1984. La Crosse virions contain a primer-stimulated RNA polymerase and a methylated cap-dependent endonuclease. J Virol 52:215-222.
35. Patterson JL, Kolakofsky D. 1984. Characterization of La Crosse virus small-genome transcripts. J Virol 49:680-685.
36. Weik M, Modrof J, Klenk HD, Becker S, Muhlberger E. 2002. Ebola virus VP30-mediated transcription is regulated by RNA secondary structure formation. J Virol 76:8532-8539. http://dx.doi.org/10.1128/JVI.76 .17.8532-8539.2002.
37. Ogino T, Banerjee AK. 2007. Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol Cell 25:85-97. http://dx.doi.org/10.1016/j.molcel.2006.11.013.
38. Murti KG, Webster RG, Jones IM. 1988. Localization of RNA polymerases on influenza viral ribonucleoproteins by immunogold labeling. Virology 164:562-566. http://dx.doi.org/10.1016/0042-6822(88)90574-0.
39. Schreier E, Ladhoff AM, Stompor S, Michel S. 1988. Interaction between anti-influenza viral polymerase antibodies and RNP particles using the in vitro transcription process and an immunogold labelling technique. Acta Virol 32:403-408.
40. Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P. 1987. Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci U S A 84:8140- 8144. http://dx.doi.org/10.1073/pnas.84.22.8140.
41. Pflug A, Guilligay D, Reich S, Cusack S. 2014. Structure of influenza A polymerase bound to the viral RNA promoter. Nature 516:355-360. http: //dx.doi.org/10.1038/nature14008.
42. Habjan M, Andersson I, Klingstrom J, Schumann M, Martin A, Zimmermann P, Wagner V, Pichlmair A, Schneider U, Muhlberger E, Mirazimi A, Weber F. 2008. Processing of genome 5= termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS One 3:e2032. http://dx.doi.org/10.1371 /journal.pone.0002032.
43. 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.
44. 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.
45. 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.
46. 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.