IFITM-2 and IFITM-3 but Not IFITM-1 Restrict rift valley fever virus

Journal of Virology

Volumn 87, Issue 15, 2013, Pages 8451-8464

  Mudhasani, Rajini ^a   Tran, Julie P ^a   Retterer, Cary ^a   Radoshitzky, Sheli R ^a   Kota, Krishna P ^a   Altamura, Louis A ^a   Smith, Jeffrey M ^a   Packard, Beverly Z ^b   Kuhn, Jens H ^c   Costantino, Julie ^a   Garrison, Aura R ^a   Schmaljohn, Connie S ^a   Huang, I Chueh ^d   Farzan, Michael ^e   Bavari, Sina ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^b OncoImmunin Inc ^*  (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON INDUCED TRANSMEMBRANE PROTEIN 1; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 2; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 3; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANDES VIRUS; ARTICLE; BUNYAVIRUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HANTAVIRUS; LA CROSSE VIRUS; MEMBRANE FUSION; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RIFT VALLEY FEVER; RIFT VALLEY FEVER BUNYAVIRUS; VIRUS ATTACHMENT; VIRUS INHIBITION; VIRUS REPLICATION;

EID: 84880599167     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03382-12     Document Type: Article

References (51)

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.
2. Smith PL, Lombardi G, Foster GR. 2005. Type I interferons and the innate immune response-more than just antiviral cytokines. Mol. Immunol. 42:869-877.
3. MacMicking JD. 2012. Interferon-inducible effector mechanisms in cellautonomous immunity. Nat. Rev. Immunol. 12:367-382.
4. Friedman RL, Manly SP, McMahon M, Kerr IM, Stark GR. 1984. Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell 38:745-755.
5. Hickford D, Frankenberg S, Shaw G, Renfree MB. 2012. Evolution of vertebrate interferon inducible transmembrane proteins. BMC Genomics 13:155. doi:10.1186/1471-2164-13-155.
6. Reid LE, Brasnett AH, Gilbert CS, Porter AC, Gewert DR, Stark GR, Kerr IM. 1989. A single DNA response element can confer inducibility by both alpha- and gamma-interferons. Proc. Natl. Acad. Sci. U. S. A. 86:840-844.
7. Hanagata N, Li X, Morita H, Takemura T, Li J, Minowa T. 2011. Characterization of the osteoblast-specific transmembrane protein IFITM5 and analysis of IFITM5-deficient mice. J. Bone Mineral Metab. 29:279-290.
8. 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.
9. Huang IC, Bailey CC, Weyer JL, Radoshitzky SR, Becker MM, Chiang JJ, Brass AL, Ahmed AA, Chi X, Dong L, Longobardi LE, Boltz D, Kuhn JH, Elledge SJ, Bavari S, Denison MR, Choe H, Farzan M. 2011. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 7:e1001258. doi:10.1371/journal.ppat.1001258.
10. Jiang D, Weidner JM, Qing M, Pan XB, Guo H, Xu C, Zhang X, Birk A, Chang J, Shi PY, Block TM, Guo JT. 2010. Identification of five interferon-induced cellular proteins that inhibit West Nile virus and dengue virus infections. J. Virol. 84:8332-8341.
11. Lu J, Pan Q, Rong L, He W, Liu SL, Liang C. 2011. The IFITM proteins inhibit HIV-1 infection. J. Virol. 85:2126-2137.
12. Weidner JM, Jiang D, Pan XB, Chang J, Block TM, Guo JT. 2010. Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J. Virol. 84:12646-12657
13. Bailey CC, Huang IC, Kam C, Farzan M. 2012. Ifitm3 limits the severity of acute influenza in mice. PLoS Pathog. 8:e1002909. doi:10.1371/journal.ppat.1002909.
14. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE, Chin CR, Feeley EM, Sims JS, Adams DJ, Wise HM, Kane L, Goulding D, Digard P, Anttila V, Baillie JK, Walsh TS, Hume DA, Palotie A, Xue Y, Colonna V, Tyler-Smith C, Dunning J, Gordon SB, GenISIS Investigators, MOSAIC Investigators, Smyth RL, Openshaw PJ, Dougan G, Brass AL, Kellam P. 2012. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484:519-523.
15. Feeley EM, Sims JS, John SP, Chin CR, Pertel T, Chen LM, Gaiha GD, Ryan BJ, Donis RO, Elledge SJ, Brass AL. 2011. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog. 7:e1002337. doi:10.1371/journal.ppat.1002337.
16. Yount JS, Karssemeijer RA, Hang HC. 2012. S-Palmitoylation and ubiquitination differentially regulate interferon-induced transmembrane protein 3 (IFITM3)-mediated resistance to influenza virus. J. Biol. Chem. 287:19631-19641.
17. Daubney R, Hudson JR, Garnham PC. 1931. Enzootic hepatitis or rift valley fever. An undescribed virus disease of sheep, cattle and man from East Africa. J. Pathol. Bacteriol. 34:545-579.
18. Boshra H, Lorenzo G, Busquets N, Brun A. 2011. Rift valley fever: recent insights into pathogenesis and prevention. J. Virol. 85:6098-6105.
19. Ikegami T, Makino S. 2011. The pathogenesis of Rift Valley fever. Viruses 3:493-519.
20. Pepin M, Bouloy M, Bird BH, Kemp A, Paweska J. 2010. Rift Valley fever virus (Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Vet. Res. 41:61.
21. Coetzer JA. 1977. The pathology of Rift Valley fever. I. Lesions occurring in natural cases in new-born lambs. Onderstepoort J. Vet. Res. 44:205-211.
22. Coetzer JA. 1982. The pathology of Rift Valley fever. II. Lesions occurring in field cases in adult cattle, calves and aborted foetuses. Onderstepoort J. Vet. Res. 49:11-17.
23. Bouloy M, Flick R. 2009. Reverse genetics technology for Rift Valley fever virus: current and future applications for the development of therapeutics and vaccines. Antiviral Res. 84:101-118.
24. Caplen H, Peters CJ, Bishop DH. 1985. Mutagen-directed attenuation of Rift Valley fever virus as a method for vaccine development. J. Gen. Virol. 66(Pt 10):2271-2277.
25. Muller R, Saluzzo JF, Lopez N, Dreier T, Turell M, Smith J, Bouloy M. 1995. Characterization of clone 13, a naturally attenuated avirulent isolate of Rift Valley fever virus, which is altered in the small segment. Am. J. Trop. Med. Hyg. 53:405-411.
26. Naslund J, Lagerqvist N, Habjan M, Lundkvist A, Evander M, Ahlm C, Weber F, Bucht G. 2009. Vaccination with virus-like particles protects mice from lethal infection of Rift Valley fever virus. Virology 385:409-415.
27. Collett MS, Purchio AF, Keegan K, Frazier S, Hays W, Anderson DK, Parker MD, Schmaljohn C, Schmidt J, Dalrymple JM. 1985. Complete nucleotide sequence of the M RNA segment of Rift Valley fever virus. Virology 144:228-245.
28. Rice RM, Erlick BJ, Rosato RR, Eddy GA, Mohanty SB. 1980. Biochemical characterization of Rift Valley fever virus. Virology 105:256-260.
29. de Boer SM, Kortekaas J, de Haan CA, Rottier PJ, Moormann RJ, Bosch BJ. 2012. Heparan sulfate facilitates Rift Valley fever virus entry into the cell. J. Virol. 86:13767-13771.
30. Liu L, Celma CC, Roy P. 2008. Rift Valley fever virus structural proteins: expression, characterization and assembly of recombinant proteins. Virol. J. 5:82.
31. Rusu M, Bonneau R, Holbrook MR, Watowich SJ, Birmanns S, Wriggers W, Freiberg AN. 2012. An assembly model of Rift Valley fever virus. Front. Microbiol. 3:254.
32. Filone CM, Heise M, Doms RW, Bertolotti-Ciarlet A. 2006. Development and characterization of a Rift Valley fever virus cell-cell fusion assay using alphavirus replicon vectors. Virology 356:155-164.
33. Anderson GW, Jr, Peters CJ. 1988. Viral determinants of virulence for Rift Valley fever (RVF) in rats. Microb. Pathog. 5:241-250.
34. Guu TS, Zheng W, Tao YJ. 2012. Bunyavirus: structure and replication. Adv. Exp. Med. Biol. 726:245-266.
35. Morrill JC, Czarniecki CW, Peters CJ. 1991. Recombinant human interferon-gamma modulates Rift Valley fever virus infection in the rhesus monkey. J. Interferon Res. 11:297-304.
36. Saluzzo JF, Smith JF. 1990. Use of reassortant viruses to map attenuating and temperature-sensitive mutations of the Rift Valley fever virus MP-12 vaccine. Vaccine 8:369-375.
37. Habjan M, Pichlmair A, Elliott RM, Overby AK, Glatter T, Gstaiger M, Superti-Furga G, Unger H, Weber F. 2009. NSs protein of Rift Valley fever virus induces the specific degradation of the double-stranded RNAdependent protein kinase. J. Virol. 83:4365-4375.
38. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, Makino S. 2009. Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog. 5:e1000287. doi:10.1371/journal.ppat.1000287.
39. Morrill JC, Ikegami T, Yoshikawa-Iwata N, Lokugamage N, Won S,Terasaki K, Zamoto-Niikura A, Peters CJ, Makino S. 2010. Rapid accumulation of virulent Rift Valley fever virus in mice from an attenuated virus carrying a single nucleotide substitution in the mRNA. PLoS One 5:e9986. doi:10.1371/journal.pone.0009986.
40. Drosten C, Gottig S, Schilling S, Asper M, Panning M, Schmitz H, Gunther S. 2002. Rapid detection and quantification of RNA of Ebola and Marburg viruses, Lassa virus, Crimean-Congo hemorrhagic fever virus, Rift Valley fever virus, dengue virus, and yellow fever virus by real-time reverse transcription-PCR. J. Clin. Microbiol. 40:2323-2330.
41. 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.
42. Jia R, Pan Q, Ding S, Rong L, Liu SL, Geng Y, Qiao W, Liang C. 2012. The N-terminal region of IFITM3 modulates its antiviral activity by regulating IFITM3 cellular localization. J. Virol. 86:13697-13707.
43. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485.
44. Lozach PY, Mancini R, Bitto D, Meier R, Oestereich L, Overby AK, Pettersson RF, Helenius A. 2010. Entry of bunyaviruses into mammalian cells. Cell Host Microbe 7:488-499.
45. Gonzalez-Scarano F, Pobjecky N, Nathanson N. 1984. La Crosse bunyavirus can mediate pH-dependent fusion from without. Virology 132: 222-225.
46. Ogino M, Yoshimatsu K, Ebihara H, Araki K, Lee BH, Okumura M, Arikawa J. 2004. Cell fusion activities of Hantaan virus envelope glycoproteins. J. Virol. 78:10776-10782.
47. Ray N, Whidby J, Stewart S, Hooper JW, Bertolotti-Ciarlet A. 2010. Study of Andes virus entry and neutralization using a pseudovirion system. J. Virol. Methods 163:416-423.
48. Simon M, Johansson C, Mirazimi A. 2009. Crimean-Congo hemorrhagic fever virus entry and replication is clathrin-, pH- and cholesteroldependent. J. Gen. Virol. 90:210-215.
49. Morrill JC, Jennings GB, Cosgriff TM, Gibbs PH, Peters CJ. 1989. Prevention of Rift Valley fever in rhesus monkeys with interferon-alpha. Rev. Infect. Dis. 11(Suppl 4):S815-S825.
50. Filone CM, Hanna SL, Caino MC, Bambina S, Doms RW, Cherry S. 2010. Rift valley fever virus infection of human cells and insect hosts is promoted by protein kinase C epsilon. PLoS One 5:e15483. doi:10.1371 /journal.pone.0015483.
51. Garry CE, Garry RF. 2004. Proteomics computational analyses suggest that the carboxyl terminal glycoproteins of Bunyaviruses are class II viral fusion protein (beta-penetrenes). Theor. Biol. Med. Model. 1:10. doi:10 .1186/1742-4682-1-10