Interferon-Induced Transmembrane Protein-Mediated Inhibition of Host Cell Entry of Ebolaviruses

Journal of Infectious Diseases

Volumn 212, Issue , 2015, Pages S210-S218

  Wrensch, Florian ^a   Karsten, Christina B ^a,b   Gnirß, Kerstin ^a   Hoffmann, Markus ^a   Lu, Kai ^c   Takada, Ayato ^d   Winkler, Michael ^a   Simmons, Graham ^c   Pöhlmann, Stefan ^a  

^a GERMAN PRIMATE CENTER   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^d HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Ebola; entry; glycoprotein; IFITM; interferon

Indexed keywords

AMPHOTERICIN B; INTERFERON; INTERFERON INDUCED TRANSMEMBRANE PROTEIN; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 1; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 2; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 3; MEMBRANE PROTEIN; RETROVIRUS VECTOR; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; DIFFERENTIATION ANTIGEN; GLYCOPROTEIN; LEU-13 ANTIGEN; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; EBOLAVIRUS; HUMAN; HUMAN CELL; INFLUENZA A VIRUS; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS ENTRY; VIRUS LIKE AGENT; CELL LINE; EBOLA HEMORRHAGIC FEVER; HEK293 CELL LINE; METABOLISM; MONOCYTE; PATHOGENICITY; VIROLOGY;

ANTIGENS, DIFFERENTIATION; CELL LINE; EBOLAVIRUS; GLYCOPROTEINS; HEK293 CELLS; HEMORRHAGIC FEVER, EBOLA; HUMANS; INFLUENZA A VIRUS; INTERFERON TYPE I; MACROPHAGES; MEMBRANE PROTEINS; MONOCYTES; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84943339110     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv255     Document Type: Article

References (44)

1. Kuhn JH, Becker S, Ebihara H, et al. Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Arch Virol 2010; 155:2083-103.
2. Feldmann H, Geisbert TW. Ebola haemorrhagic fever. Lancet 2011; 377:849-62.
3. Misasi J, Sullivan NJ. Camouflage and misdirection: The full-on assault of Ebola virus disease. Cell 2014; 159:477-86.
4. WHO Ebola Response Team; Agua-Agum J, Ariyarajah A, Aylward B, et al. West African Ebola epidemic after one year-slowing but not yet under control. N Engl J Med 2015; 372:584-7.
5. World Health Organization. Ebola response roadmap-situation report. http://apps.who.int/ebola/current-situation/ebola-situation-report-15-april-2015.
6. Miranda ME, Miranda NL. Reston ebolavirus in humans and animals in the Philippines: A review. J Infect Dis 2011; 204(suppl 3):S757-60.
7. Leroy EM, Kumulungui B, Pourrut X, et al. Fruit bats as reservoirs of Ebola virus. Nature 2005; 438:575-6.
8. Taniguchi S, Watanabe S, Masangkay JS, et al. Reston ebolavirus antibodies in bats, the Philippines. Emerg Infect Dis 2011; 17:1559-60.
9. Negredo A, Palacios G, Vazquez-Moron S, et al. Discovery of an ebolavirus-like filovirus in Europe. PLoS Pathog 2011; 7:e1002304.
10. Kühl A, Pöhlmann S. How Ebola virus counters the interferon system. Zoonoses Public Health 2012; 59(suppl 2):116-31.
11. Brass AL, Huang IC, Benita Y, et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009; 139:1243-54.
12. Huang IC, Bailey CC, Weyer JL, et al. Distinct patterns of IFITMmediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog 2011; 7:e1001258.
13. Perreira JM, Chin CR, Feeley EM, Brass AL. IFITMs restrict the replication of multiple pathogenic viruses. J Mol Biol 2013; 425:4937-55.
14. 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 Pathog 2014; 10:e1004048.
15. Li K, Markosyan RM, Zheng YM, et al. IFITM proteins restrict viral membrane hemifusion. PLoS Pathog 2013; 9:e1003124.
16. Amini-Bavil-Olyaee S, Choi YJ, Lee JH, et al. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 2013; 13:452-64.
17. Wrensch F,Winkler M, Pöhlmann S. IFITM proteins inhibit entry driven by the MERS-coronavirus spike protein: evidence for cholesterolindependent mechanisms. Viruses 2014; 6:3683-98.
18. Lin TY, Chin CR, Everitt AR, et al. Amphotericin B increases influenza A virus infection by preventing IFITM3-mediated restriction. Cell Rep 2013; 5:895-908.
19. Everitt AR, Clare S, Pertel T, et al. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 2012; 484:519-23.
20. Zhang YH, Zhao Y, Li N, et al. Interferon-induced transmembrane protein-3 genetic variant rs12252-C is associated with severe influenza in Chinese individuals. Nat Commun 2013; 4:1418.
21. Mills TC, Rautanen A, Elliott KS, et al. IFITM3 and susceptibility to respiratory viral infections in the community. J Infect Dis 2014; 209:1028-31.
22. Williams DE, Wu WL, Grotefend CR, et al. IFITM3 polymorphism rs12252-C restricts influenza A viruses. PLoS One 2014; 9:e110096.
23. Marzi A, Gramberg T, Simmons G, et al. DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J Virol 2004; 78: 12090-5.
24. Simmons G, Reeves JD, Grogan CC, et al. DC-SIGN and DC-SIGNR bind Ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 2003; 305:115-23.
25. Lu J, Pan Q, Rong L, HeW, Liu SL, Liang C. The IFITM proteins inhibit HIV-1 infection. J Virol 2011; 85:2126-37.
26. Kremers GJ, Goedhart J, van Munster EB, Gadella TW Jr. Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Forster radius. Biochemistry 2006; 45:6570-80.
27. Bertram S, Dijkman R, Habjan M, et al. TMPRSS2 activates the human coronavirus 229E for cathepsin-independent host cell entry and is expressed in viral target cells in the respiratory epithelium. J Virol 2013; 87:6150-60.
28. Remy I, Michnick SW. A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat Methods 2006; 3:977-9.
29. O'Doherty U, Swiggard WJ, Malim MH. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 2000; 74:10074-80.
30. Nakayama E, Tomabechi D, Matsuno K, et al. Antibody-dependent enhancement of Marburg virus infection. J Infect Dis 2011; 204(suppl 3): S978-85.
31. Zhang Z, Liu J, Li M, Yang H, Zhang C. Evolutionary dynamics of the interferon-induced transmembrane gene family in vertebrates. PLoS One 2012; 7:e49265.
32. Geisbert TW, Hensley LE, Larsen T, et al. Pathogenesis of Ebola hemorrhagic fever in cynomolgus macaques: evidence that dendritic cells are early and sustained targets of infection. Am J Pathol 2003; 163:2347-70.
33. Martinez O, Leung LW, Basler CF. The role of antigen-presenting cells in filoviral hemorrhagic fever: gaps in current knowledge. Antiviral Res 2012; 93:416-28.
34. John SP, Chin CR, Perreira JM, et al. The CD225 domain of IFITM3 is required for both IFITM protein association and inhibition of influenza A virus and dengue virus replication. J Virol 2013; 87:7837-52.
35. Hutchinson KL, Rollin PE. Cytokine and chemokine expression in humans infected with Sudan Ebola virus. J Infect Dis 2007; 196(suppl 2): S357-63.
36. Villinger F, Rollin PE, Brar SS, et al. Markedly elevated levels of interferon (IFN)-gamma, IFN-alpha, interleukin (IL)-2, IL-10, and tumor necrosis factor-alpha associated with fatal Ebola virus infection. J Infect Dis 1999; 179(suppl 1):S188-91.
37. Maruyama J, Miyamoto H, Kajihara M, et al. Characterization of the envelope glycoprotein of a novel filovirus, Lloviu virus. J Virol 2014; 88:99-109.
38. Ng M, Ndungo E, Jangra RK, et al. Cell entry by a novel European filovirus requires host endosomal cysteine proteases and Niemann-Pick C1. Virology 2014; 468-470:637-46.
39. Bailey CC, Huang IC, Kam C, Farzan M. Ifitm3 limits the severity of acute influenza in mice. PLoS Pathog 2012; 8:e1002909.
40. Qian J, Duff YL, Wang Y, et al. Primate lentiviruses are differentially inhibited by interferon-induced transmembrane proteins. Virology 2015; 474:10-8.
41. Zhao X, Guo F, Liu F, et al. Interferon induction of IFITM proteins promotes infection by human coronavirus OC43. Proc Natl Acad Sci U S A 2014; 111:6756-61.
42. Saphire EO. An update on the use of antibodies against the filoviruses. Immunotherapy 2013; 5:1221-33.
43. Kajihara M, Marzi A, Nakayama E, et al. Inhibition of Marburg virus budding by nonneutralizing antibodies to the envelope glycoprotein. J Virol 2012; 86:13467-74.
44. Compton AA, Bruel T, Porrot F, et al. IFITM proteins incorporated into HIV-1 virions impair viral fusion and spread. Cell Host Microbe 2014; 16:736-47.