The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry

Cell Host and Microbe

Volumn 13, Issue 4, 2013, Pages 452-464

  Amini Bavil Olyaee, Samad ^a   Choi, Youn Jung ^a,b   Lee, Jun Han ^a   Shi, Mude ^a   Huang, I Chueh ^c   Farzan, Michael ^d   Jung, Jae U ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; INTERFERON INDUCIBLE TRANSMEMBRANE PROTEIN 3; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VESICLE MEMBRANE PROTEIN ASSOCIATED PROTEIN A;

ARTICLE; CELL MEMBRANE; CYTOSOL; ENDOSOME; GENE EXPRESSION; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; VIRION; VIRUS ENTRY; VIRUS INFECTION;

EID: 84876349734     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.03.006     Document Type: Article

References (59)

1. Y. Amako, A. Sarkeshik, H. Hotta, J. Yates 3rd, and A. Siddiqui Role of oxysterol binding protein in hepatitis C virus infection J. Virol. 83 2009 9237 9246
2. C.C. Bailey, I.C. Huang, C. Kam, and M. Farzan Ifitm3 limits the severity of acute influenza in mice PLoS Pathog. 8 2012 e1002909
3. A.L. Brass, I.C. Huang, Y. Benita, S.P. John, M.N. Krishnan, E.M. Feeley, B.J. Ryan, J.L. Weyer, L. van der Weyden, and E. Fikrig The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus Cell 139 2009 1243 1254
4. J.E. Carette, M. Raaben, A.C. Wong, A.S. Herbert, G. Obernosterer, N. Mulherkar, A.I. Kuehne, P.J. Kranzusch, A.M. Griffin, and G. Ruthel Ebola virus entry requires the cholesterol transporter Niemann-Pick C1 Nature 477 2011 340 343
5. T.H. Chang, J. Segovia, A. Sabbah, V. Mgbemena, and S. Bose Cholesterol-rich lipid rafts are required for release of infectious human respiratory syncytial virus particles Virology 422 2012 205 213
6. L.V. Chernomordik, E. Leikina, V. Frolov, P. Bronk, and J. Zimmerberg An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids J. Cell Biol. 136 1997 81 93
7. J. Chevallier, Z. Chamoun, G. Jiang, G. Prestwich, N. Sakai, S. Matile, R.G. Parton, and J. Gruenberg Lysobisphosphatidic acid controls endosomal cholesterol levels J. Biol. Chem. 283 2008 27871 27880
8. M. Côté, J. Misasi, T. Ren, A. Bruchez, K. Lee, C.M. Filone, L. Hensley, Q. Li, D. Ory, K. Chandran, and J. Cunningham Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection Nature 477 2011 344 348
9. P. Danthi, and M. Chow Cholesterol removal by methyl-beta-cyclodextrin inhibits poliovirus entry J. Virol. 78 2004 33 41
10. M.S. Diamond, and M. Farzan The broad-spectrum antiviral functions of IFIT and IFITM proteins Nat. Rev. Immunol. 13 2013 46 57
11. K. Ettayebi, and M.E. Hardy Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein J. Virol. 77 2003 11790 11797
12. A.R. Everitt, S. Clare, T. Pertel, S.P. John, R.S. Wash, S.E. Smith, C.R. Chin, E.M. Feeley, J.S. Sims, D.J. Adams GenISIS Investigators MOSAIC Investigators IFITM3 restricts the morbidity and mortality associated with influenza Nature 484 2012 519 523
13. E.M. Feeley, J.S. Sims, S.P. John, C.R. Chin, T. Pertel, L.M. Chen, G.D. Gaiha, B.J. Ryan, R.O. Donis, S.J. Elledge, and A.L. Brass IFITM3 inhibits influenza A virus infection by preventing cytosolic entry PLoS Pathog. 7 2011 e1002337
14. I.G. Ganley, and S.R. Pfeffer Cholesterol accumulation sequesters Rab9 and disrupts late endosome function in NPC1-deficient cells J. Biol. Chem. 281 2006 17890 17899
15. L. Gao, H. Aizaki, J.W. He, and M.M. Lai Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft J. Virol. 78 2004 3480 3488
16. T. Gianni, and G. Campadelli-Fiume αVβ3-integrin relocalizes nectin1 and routes herpes simplex virus to lipid rafts J. Virol. 86 2012 2850 2855
17. J. Gruenberg Viruses and endosome membrane dynamics Curr. Opin. Cell Biol. 21 2009 582 588
18. I. Hamamoto, Y. Nishimura, T. Okamoto, H. Aizaki, M. Liu, Y. Mori, T. Abe, T. Suzuki, M.M. Lai, and T. Miyamura Human VAP-B is involved in hepatitis C virus replication through interaction with NS5A and NS5B J. Virol. 79 2005 13473 13482
19. J.C. Holthuis, and T.P. Levine Lipid traffic: floppy drives and a superhighway Nat. Rev. Mol. Cell Biol. 6 2005 209 220
20. I.C. Huang, C.C. Bailey, J.L. Weyer, S.R. Radoshitzky, M.M. Becker, J.J. Chiang, A.L. Brass, A.A. Ahmed, X. Chi, and L. Dong Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus PLoS Pathog. 7 2011 e1001258
21. E. Ikonen Cellular cholesterol trafficking and compartmentalization Nat. Rev. Mol. Cell Biol. 9 2008 125 138
22. Y.A. Ioannou Multidrug permeases and subcellular cholesterol transport Nat. Rev. Mol. Cell Biol. 2 2001 657 668
23. R. Jia, Q. Pan, S. Ding, L. Rong, S.L. Liu, Y. Geng, W. Qiao, and C. Liang The N-terminal region of IFITM3 modulates its antiviral activity by regulating IFITM3 cellular localization J. Virol. 86 2012 13697 13707
24. T. Kobayashi, M.H. Beuchat, M. Lindsay, S. Frias, R.D. Palmiter, H. Sakuraba, R.G. Parton, and J. Gruenberg Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport Nat. Cell Biol. 1 1999 113 118
25. S. Kunz Receptor binding and cell entry of Old World arenaviruses reveal novel aspects of virus-host interaction Virology 387 2009 245 249
26. M. Lakadamyali, M.J. Rust, and X. Zhuang Endocytosis of influenza viruses Microbes Infect. 6 2004 929 936
27. I. Le Blanc, P.P. Luyet, V. Pons, C. Ferguson, N. Emans, A. Petiot, N. Mayran, N. Demaurex, J. Fauré, and R. Sadoul Endosome-to-cytosol transport of viral nucleocapsids Nat. Cell Biol. 7 2005 653 664
28. C. Lebrand, M. Corti, H. Goodson, P. Cosson, V. Cavalli, N. Mayran, J. Fauré, and J. Gruenberg Late endosome motility depends on lipids via the small GTPase Rab7 EMBO J. 21 2002 1289 1300
29. S. Lev, D. Ben Halevy, D. Peretti, and N. Dahan The VAP protein family: from cellular functions to motor neuron disease Trends Cell Biol. 18 2008 282 290
30. T. Levine Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions Trends Cell Biol. 14 2004 483 490
31. J. Lu, Q. Pan, L. Rong, W. He, S.L. Liu, and C. Liang The IFITM proteins inhibit HIV-1 infection J. Virol. 85 2011 2126 2137
32. S. Mañes, G. del Real, and C. Martínez-A Pathogens: raft hijackers Nat. Rev. Immunol. 3 2003 557 568
33. B. Manicassamy, S. Manicassamy, A. Belicha-Villanueva, G. Pisanelli, B. Pulendran, and A. García-Sastre Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus Proc. Natl. Acad. Sci. USA 107 2010 11531 11536
34. F.R. Maxfield, and I. Tabas Role of cholesterol and lipid organization in disease Nature 438 2005 612 621
35. K. Narita, A. Choudhury, K. Dobrenis, D.K. Sharma, E.L. Holicky, D.L. Marks, S.U. Walkley, and R.E. Pagano Protein transduction of Rab9 in Niemann-Pick C cells reduces cholesterol storage FASEB J. 19 2005 1558 1560
36. S.N. Pattanakitsakul, J. Poungsawai, R. Kanlaya, S. Sinchaikul, S.T. Chen, and V. Thongboonkerd Association of Alix with late endosomal lysobisphosphatidic acid is important for dengue virus infection in human endothelial cells J. Proteome Res. 9 2010 4640 4648
37. K.B. Peake, and J.E. Vance Defective cholesterol trafficking in Niemann-Pick C-deficient cells FEBS Lett. 584 2010 2731 2739
38. M.K. Poh, G. Shui, X. Xie, P.Y. Shi, M.R. Wenk, and F. Gu U18666A, an intra-cellular cholesterol transport inhibitor, inhibits dengue virus entry and replication Antiviral Res. 93 2012 191 198
39. S. Raychaudhuri, and W.A. Prinz The diverse functions of oxysterol-binding proteins Annu. Rev. Cell Dev. Biol. 26 2010 157 177
40. J.M. Rojek, and S. Kunz Cell entry by human pathogenic arenaviruses Cell. Microbiol. 10 2008 828 835
41. S.L. Roth, and G.R. Whittaker Promotion of vesicular stomatitis virus fusion by the endosome-specific phospholipid bis(monoacylglycero)phosphate (BMP) FEBS Lett. 585 2011 865 869
42. A.J. Sadler, and B.R. Williams Interferon-inducible antiviral effectors Nat. Rev. Immunol. 8 2008 559 568
43. J.W. Schoggins, S.J. Wilson, M. Panis, M.Y. Murphy, C.T. Jones, P. Bieniasz, and C.M. Rice A diverse range of gene products are effectors of the type I interferon antiviral response Nature 472 2011 481 485
44. C. Schroeder Cholesterol-binding viral proteins in virus entry and morphogenesis Subcell. Biochem. 51 2010 77 108
45. F. Siegrist, M. Ebeling, and U. Certa The small interferon-induced transmembrane genes and proteins J. Interferon Cytokine Res. 31 2011 183 197
46. K. Sobo, I. Le Blanc, P.P. Luyet, M. Fivaz, C. Ferguson, R.G. Parton, J. Gruenberg, and F.G. van der Goot Late endosomal cholesterol accumulation leads to impaired intra-endosomal trafficking PLoS ONE 2 2007 e851
47. K. Subramanian, and W.E. Balch NPC1/NPC2 function as a tag team duo to mobilize cholesterol Proc. Natl. Acad. Sci. USA 105 2008 15223 15224
48. Y. Tang, I.C. Leao, E.M. Coleman, R.S. Broughton, and J.E. Hildreth Deficiency of niemann-pick type C-1 protein impairs release of human immunodeficiency virus type 1 and results in Gag accumulation in late endosomal/lysosomal compartments J. Virol. 83 2009 7982 7995
49. P. Uchil, and W. Mothes Viral entry: a detour through multivesicular bodies Nat. Cell Biol. 7 2005 641 642
50. M. Veit, and B. Thaa Association of influenza virus proteins with membrane rafts Adv. Virol. 2011 2011 370606
51. W. Wang, Y.J. Fu, Y.G. Zu, N. Wu, J. Reichling, and T. Efferth Lipid rafts play an important role in the vesicular stomatitis virus life cycle Arch. Virol. 154 2009 595 600
52. Y.S. Wee, K.M. Roundy, J.J. Weis, and J.H. Weis Interferon-inducible transmembrane proteins of the innate immune response act as membrane organizers by influencing clathrin and v-ATPase localization and function Innate Immun. 18 2012 834 845
53. J.M. Weidner, D. Jiang, X.B. Pan, J. Chang, T.M. Block, and J.T. Guo Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms J. Virol. 84 2010 12646 12657
54. J.P. Wyles, C.R. McMaster, and N.D. Ridgway Vesicle-associated membrane protein-associated protein-A (VAP-A) interacts with the oxysterol-binding protein to modify export from the endoplasmic reticulum J. Biol. Chem. 277 2002 29908 29918
55. N. Yan, and Z.J. Chen Intrinsic antiviral immunity Nat. Immunol. 13 2012 214 222
56. J.S. Yount, R.A. Karssemeijer, and H.C. Hang S-palmitoylation and ubiquitination differentially regulate interferon-induced transmembrane protein 3 (IFITM3)-mediated resistance to influenza virus J. Biol. Chem. 287 2012 19631 19641
57. J.S. Yount, B. Moltedo, Y.Y. Yang, G. Charron, T.M. Moran, C.B. López, and H.C. Hang Palmitoylome profiling reveals S-palmitoylation- dependent antiviral activity of IFITM3 Nat. Chem. Biol. 6 2010 610 614
58. M. Zhang, L. Chen, S. Wang, and T. Wang Rab7: roles in membrane trafficking and disease Biosci. Rep. 29 2009 193 209
59. Z. Zhang, J. Liu, M. Li, H. Yang, and C. Zhang Evolutionary dynamics of the interferon-induced transmembrane gene family in vertebrates PLoS ONE 7 2012 e49265