Antiviral role of IFITM proteins in African swine fever virus infection

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Muñoz Moreno, Raquel ^a,b   Cuesta Geijo, Miguel Ángel ^a,c   Martínez Romero, Carles ^b   Barrado Gil, Lucía ^a   Galindo, Inmaculada ^a   García Sastre, Adolfo ^b   Alonso, Covadonga ^a  

^a INIA   (Spain)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c GUY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON INDUCED TRANSMEMBRANE 1 PROTEIN; INTERFERON INDUCED TRANSMEMBRANE 2 PROTEIN; INTERFERON INDUCED TRANSMEMBRANE 3 PROTEIN; INTERFERON INDUCED TRANSMEMBRANE PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; CHOLESTEROL; DIFFERENTIATION ANTIGEN; DOUBLE STRANDED RNA; LEU-13 ANTIGEN;

AFRICAN SWINE FEVER VIRUS; ARTICLE; CELLULAR DISTRIBUTION; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; NONHUMAN; PROTEIN EXPRESSION; VERO CELL LINE; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS UNCOATING; ANIMAL; CELL MEMBRANE; CHLOROCEBUS AETHIOPS; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; HUMAN; METABOLISM; PATHOGENICITY; RNA VIRUS;

AFRICAN SWINE FEVER VIRUS; ANIMALS; ANTIGENS, DIFFERENTIATION; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CHOLESTEROL; ENDOCYTOSIS; ENDOSOMES; HEK293 CELLS; HUMANS; INTERFERONS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; RNA VIRUSES; RNA, DOUBLE-STRANDED; VERO CELLS; VIRUS INTERNALIZATION;

EID: 84978116694     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0154366     Document Type: Article

References (39)

1. Perreira JM, Chin CR, Feeley EM, Brass AL. IFITMs restrict the replication of multiple pathogenic viruses. J Mol Biol. 2013; 425(24):4937-55. Epub 2013/10/01. doi: 10.1016/j.jmb.2013.09.024 PMID: 24076421.
2. Friedman RL, Manly SP, McMahon M, Kerr IM, Stark GR. Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell. 1984; 38(3):745-55. Epub 1984/10/01. PMID: 6548414.
3. Lewin AR, Reid LE, McMahon M, Stark GR, Kerr IM. Molecular analysis of a human interferon-inducible gene family. Eur J Biochem. 1991; 199(2):417-23. Epub 1991/07/15. PMID: 1906403.
4. Diamond MS, Farzan M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nature reviews Immunology. 2013; 13(1):46-57. doi: 10.1038/nri3344 PMID: 23237964; PubMed Central PMCID: PMC3773942.
5. Bradbury LE, Kansas GS, Levy S, Evans RL, Tedder TF. The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. Journal of immunology. 1992; 149(9):2841-50. Epub 1992/11/01. PMID: 1383329.
6. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell. 2009; 139 (7):1243-54. Epub 2010/01/13. doi: 10.1016/j.cell.2009.12.017 PMID: 20064371; PubMed Central PMCID: PMC2824905.
7. Wilkins C, Woodward J, Lau DT, Barnes A, Joyce M, McFarlane N, et al. IFITM1 is a tight junction protein that inhibits hepatitis C virus entry. Hepatology. 2013; 57(2):461-9. Epub 2012/09/22. doi: 10. 1002/hep.26066 PMID: 22996292; PubMed Central PMCID: PMC3566288.
8. Zhu R, Wang J, Lei XY, Gui JF, Zhang QY. Evidence for Paralichthys olivaceus IFITM1 antiviral effect by impeding viral entry into target cells. Fish & shellfish immunology. 2013; 35(3):918-26. doi: 10.1016/j.fsi.2013.07.002 PMID: 23850425.
9. Warren CJ, Griffin LM, Little AS, Huang IC, Farzan M, Pyeon D. The antiviral restriction factors IFITM1, 2 and 3 do not inhibit infection of human papillomavirus, cytomegalovirus and adenovirus. PLoS One. 2014; 9(5):e96579. Epub 2014/05/16. doi: 10.1371/journal.pone.0096579 PMID: 24827144; PubMed Central PMCID: PMC4020762.
10. Iyer LM, Aravind L, Koonin EV. Common origin of four diverse families of large eukaryotic DNA viruses. Journal of virology. 2001; 75(23):11720-34. doi: 10.1128/JVI.75.23.11720-11734.2001 PMID: 11689653; PubMed Central PMCID: PMC114758.
11. Cuesta-Geijo MA, Galindo I, Hernaez B, Quetglas JI, Dalmau-Mena I, Alonso C. Endosomal maturation, Rab7 GTPase and phosphoinositides in African swine fever virus entry. PLoS One. 2012; 7(11): e48853. Epub 2012/11/08. doi: 10.1371/journal.pone.0048853 PONE-D-12-12986 [pii]. PMID: 23133661; PubMed Central PMCID: PMC3486801.
12. Galindo I, Cuesta-Geijo MA, Hlavova K, Munoz-Moreno R, Barrado-Gil L, Dominguez J, et al. African swine fever virus infects macrophages, the natural host cells, via clathrin-and cholesterol-dependent endocytosis. Virus research. 2015; 200:45-55. doi: 10.1016/j.virusres.2015.01.022 PMID: 25662020.
13. Alonso C, Galindo I, Cuesta-Geijo MA, Cabezas M, Hernaez B, Munoz-Moreno R. African swine fever virus-cell interactions: from virus entry to cell survival. Virus research. 2013; 173(1):42-57. doi: 10. 1016/j.virusres.2012.12.006 PMID: 23262167.
14. Animal Disease Notification System: Outbreaks per Disease. European Comission, 2014.
15. Cases of ASF confirmed in Latvia. The Veterinary record. 2014; 175(3):59. doi: 10.1136/vr.g4627 PMID: 25034678.
16. Pejsak Z, Truszczynski M, Niemczuk K, Kozak E, Markowska-Daniel I. Epidemiology of African Swine Fever in Poland since the detection of the first case. Polish journal of veterinary sciences. 2014; 17 (4):665-72. PMID: 25638980.
17. Hernaez B, Alonso C. Dynamin-and clathrin-dependent endocytosis in African swine fever virus entry. Journal of virology. 2010; 84(4):2100-9. doi: 10.1128/JVI.01557-09 PMID: 19939916; PubMed Central PMCID: PMC2812401.
18. Enjuanes L, Carrascosa AL, Moreno MA, Vinuela E. Titration of African swine fever (ASF) virus. The Journal of general virology. 1976; 32(3):471-7. PMID: 823294.
19. Hernaez B, Escribano JM, Alonso C. Visualization of the African swine fever virus infection in living cells by incorporation into the virus particle of green fluorescent protein-p54 membrane protein chimera. Virology. 2006; 350(1):1-14. doi: 10.1016/j.virol.2006.01.021 PMID: 16490226.
20. Appelqvist H, Nilsson C, Garner B, Brown AJ, Kagedal K, Ollinger K. Attenuation of the lysosomal death pathway by lysosomal cholesterol accumulation. Am J Pathol. 2011; 178(2):629-39. doi: 10. 1016/j.ajpath.2010.10.030 PMID: 21281795; PubMed Central PMCID: PMC3069902.
21. King DP, Reid SM, Hutchings GH, Grierson SS, Wilkinson PJ, Dixon LK, et al. Development of a Taq-Man PCR assay with internal amplification control for the detection of African swine fever virus. Journal of virological methods. 2003; 107(1):53-61. PMID: 12445938.
22. Petersen J, Drake MJ, Bruce EA, Riblett AM, Didigu CA, Wilen CB, et al. The major cellular sterol regulatory pathway is required for Andes virus infection. PLoS pathogens. 2014; 10(2):e1003911. doi: 10. 1371/journal.ppat.1003911 PMID: 24516383; PubMed Central PMCID: PMC3916400.
23. Amini-Bavil-Olyaee S, Choi YJ, Lee JH, Shi M, Huang IC, Farzan M, et al. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell host & microbe. 2013; 13(4):452-64. doi: 10.1016/j.chom.2013.03.006 PMID: 23601107; PubMed Central PMCID: PMC3646482.
24. Desai TM, Marin M, Chin CR, Savidis G, Brass AL, Melikyan GB. IFITM3 restricts influenza A virus entry by blocking the formation of fusion pores following virus-endosome hemifusion. PLoS pathogens. 2014; 10(4):e1004048. doi: 10.1371/journal.ppat.1004048 PMID: 24699674; PubMed Central PMCID: PMC3974867.
25. Li D, Shi JJ, Mao CJ, Liu S, Wang JD, Chen J, et al. Alteration of dynein function affects alpha-synuclein degradation via the autophagosome-lysosome pathway. International journal of molecular sciences. 2013; 14(12):24242-54. doi: 10.3390/ijms141224242 PMID: 24351814; PubMed Central PMCID: PMC3876108.
26. Altan-Bonnet N, Balla T. Phosphatidylinositol 4-kinases: hostages harnessed to build panviral replication platforms. Trends Biochem Sci. 2012; 37(7):293-302. Epub 2012/05/29. S0968-0004(12)00047-3 [pii] doi: 10.1016/j.tibs.2012.03.004 PMID: 22633842; PubMed Central PMCID: PMC3389303.
27. Salas ML, Andres G. African swine fever virus morphogenesis. Virus research. 2013; 173(1):29-41. doi: 10.1016/j.virusres.2012.09.016 PMID: 23059353.
28. Esparza I, Gonzalez JC, Vinuela E. Effect of interferon-alpha, interferon-gamma and tumour necrosis factor on African swine fever virus replication in porcine monocytes and macrophages. The Journal of general virology. 1988; 69 (Pt 12):2973-80. doi: 10.1099/0022-1317-69-12-2973 PMID: 3143809.
29. Paez E, Garcia F, Gil Fernandez C. Interferon cures cells lytically and persistently infected with African swine fever virus in vitro. Archives of virology. 1990; 112(1-2):115-27. PMID: 1695091.
30. Correia S, Ventura S, Parkhouse RM. Identification and utility of innate immune system evasion mechanisms of ASFV. Virus research. 2013; 173(1):87-100. Epub 2012/11/21. doi: 10.1016/j.virusres.2012. 10.013 PMID: 23165138.
31. de Oliveira VL, Almeida SC, Soares HR, Crespo A, Marshall-Clarke S, Parkhouse RM. A novel TLR3 inhibitor encoded by African swine fever virus (ASFV). Archives of virology. 2011; 156(4):597-609. doi: 10.1007/s00705-010-0894-7 PMID: 21203785; PubMed Central PMCID: PMC3066390.
32. Netherton CL, Simpson J, Haller O, Wileman TE, Takamatsu HH, Monaghan P, et al. Inhibition of a large double-stranded DNA virus by MxA protein. Journal of virology. 2009; 83(5):2310-20. doi: 10. 1128/JVI.00781-08 PMID: 19109387; PubMed Central PMCID: PMC2643742.
33. Feeley EM, Sims JS, John SP, Chin CR, Pertel T, Chen LM, et al. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS pathogens. 2011; 7(10):e1002337. doi: 10.1371/journal. ppat.1002337 PMID: 22046135; PubMed Central PMCID: PMC3203188.
34. Huang IC, Bailey CC, Weyer JL, Radoshitzky SR, Becker MM, Chiang JJ, et al. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS pathogens. 2011; 7(1):e1001258. Epub 2011/01/22. doi: 10.1371/journal.ppat.1001258 PMID: 21253575; PubMed Central PMCID: PMC3017121.
35. Sanchez EG, Quintas A, Perez-Nunez D, Nogal M, Barroso S, Carrascosa AL, et al. African swine fever virus uses macropinocytosis to enter host cells. PLoS pathogens. 2012; 8(6):e1002754. doi: 10. 1371/journal.ppat.1002754 PMID: 22719252; PubMed Central PMCID: PMC3375293.
36. John SP, Chin CR, Perreira JM, Feeley EM, Aker AM, Savidis G, et al. The CD225 domain of IFITM3 is required for both IFITM protein association and inhibition of influenza A virus and dengue virus replication. Journal of virology. 2013; 87(14):7837-52. doi: 10.1128/JVI.00481-13 PMID: 23658454; PubMed Central PMCID: PMC3700195.
37. Cuesta-Geijo MA, Chiappi M, Galindo I, Barrado-Gil L, Munoz-Moreno R, Carrascosa JL, et al. Cholesterol Flux Is Required for Endosomal Progression of African Swine Fever Virions during the Initial Establishment of Infection. Journal of virology. 2015; 90(3):1534-43. doi: 10.1128/JVI.02694-15 PMID: 26608317; PubMed Central PMCID: PMC4719630.
38. Raychaudhuri S, Prinz WA. The diverse functions of oxysterol-binding proteins. Annu Rev Cell Dev Biol. 2010; 26:157-77. Epub 2009/07/07. doi: 10.1146/annurev.cellbio.042308.113334 PMID: 19575662; PubMed Central PMCID: PMC3478074.
39. Compton AA, Bruel T, Porrot F, Mallet A, Sachse M, Euvrard M, et al. IFITM Proteins Incorporated into HIV-1 Virions Impair Viral Fusion and Spread. Cell host & microbe. 2014; 16(6):736-47. doi: 10.1016/j. chom.2014.11.001 PMID: 25464829.