Interferon-induced transmembrane protein 3 is a type II transmembrane protein

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32184-32193

  Bailey, Charles C ^a   Kondur, Hema R ^a   Huang, I Chueh ^b   Farzan, Michael ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPLASMIC RETICULUM; INTRACELLULAR LOOP; MEMBRANE PROTEINS; POTENTIAL TARGETS; TRANS-MEMBRANE PROTEINS; TRANSMEMBRANE HELICES; TRANSMEMBRANE TOPOLOGY; TRANSMEMBRANES;

ANTIBIOTICS; ANTIBODIES; ENZYME ACTIVITY; EPITOPES; GLYCOPROTEINS; TOPOLOGY; VIRUSES;

CELL MEMBRANES;

INTERFERON INDUCED TRANSMEMBRANE PROTEIN 3; MEMBRANE PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; LYSOSOME; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF;

FLOW CYTOMETRY; IFITM3; INTERFERON; MEMBRANE PROTEINS; MICROSCOPIC IMAGING; VIRUS ENTRY;

AMINO ACID MOTIFS; ANIMALS; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; LYSOSOMES; MEMBRANE PROTEINS; MICE; PROTEIN STRUCTURE, TERTIARY;

EID: 84887417852     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.514356     Document Type: Article

References (32)

1. Zhang, Z., Liu, J., Li, M., Yang, H., and Zhang, C. (2012) Evolutionary dynamics of the interferon-induced transmembrane gene family in vertebrates. PLoS One 7, e49265
2. Diamond, M. S., and Farzan, M. (2013) The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 13, 46-57
3. Schoggins, J. W., Wilson, S. J., Panis, M., Murphy, M. Y., Jones, C. T., Bieniasz, P., and Rice, C. M. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472, 481-485
4. Huang, I.-C., Bailey, C. C., Weyer, J. L., Radoshitzky, S. R., Becker, M. M., Chiang, J. J., Brass, A. L., Ahmed, A. A., Chi, X., Dong, L., Longobardi, L. E., Boltz, D., Kuhn, J. H., Elledge, S. J., Bavari, S., Denison, M. R., Choe, H., and Farzan, M. (2011) Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 7, e1001258
5. Jiang, D., Weidner, J. M., Qing, M., Pan, X.-B., Guo, H., Xu, C., Zhang, X., Birk, A., Chang, J., Shi, P.-Y., Block, T. M., and Guo, J.-T. (2010) Identification of five interferon-induced cellular proteins that inhibit West Nile virus and dengue virus infections. J. Virol. 84, 8332-8341
6. Weidner, J. M., Jiang, D., Pan, X.-B., Chang, J., Block, T. M., and Guo, J.-T. (2010) Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J. Virol. 84, 12646-12657
7. Brass, A. L., Huang, I.-C., Benita, Y., John, S. P., Krishnan, M. N., Feeley, E. M., Ryan, B. J., Weyer, J. L., van der Weyden, L., Fikrig, E., Adams, D. J., Xavier, R. J., Farzan, M., and Elledge, S. J. (2009) The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139, 1243-1254
8. Anafu, A. A., Bowen, C. H., Chin, C. R., Brass, A. L., and Holm, G. H. (2013) Interferon-inducible transmembrane protein 3 (IFITM3) restricts reovirus cell entry. J. Biol. Chem. 288, 17261-17271
9. Mudhasani, R., Tran, J. P., Retterer, C., Radoshitzky, S. R., Kota, K. P., Altamura, L. A., Smith, J. M., Packard, B. Z., Kuhn, J. H., Costantino, J., Garrison, A. R., Schmaljohn, C. S., Huang, I.-C., Farzan, M., and Bavari, S. (2013) IFITM-2 and IFITM-3 but not IFITM-1 restrict rift valley fever virus. J. Virol. 87, 8451-8464
10. Lu, J., Pan, Q., Rong, L., He, W., Liu, S.-L., and Liang, C. (2011) The IFITM proteins inhibit HIV-1 infection. J. Virol. 85, 2126-2137
11. Jia, R., Pan, Q., Ding, S., Rong, L., Liu, S.-L., Geng, Y., Qiao, W., and Liang, C. (2012) The N-terminal region of IFITM3 modulates its antiviral activity by regulating IFITM3 cellular localization. J. Virol. 86, 13697-13707
12. Li, K., Markosyan, R. M., Zheng, Y.-M., Golfetto, O., Bungart, B., Li, M., Ding, S., He, Y., Liang, C., Lee, J. C., Gratton, E., Cohen, F. S., and Liu, S.-L. (2013) IFITM proteins restrict viral membrane hemifusion. PLoS Pathog. 9, e1003124
13. Everitt, A. R., Clare, S., Pertel, T., John, S. P., Wash, R. S., Smith, S. E., Chin, C. R., Feeley, E. M., Sims, J. S., Adams, D. J., Wise, H. M., Kane, L., Goulding, D., Digard, P., Anttila, V., Baillie, J. K., Walsh, T. S., Hume, D. A., Palotie, A., Xue, Y., Colonna, V., Tyler-Smith, C., Dunning, J., Gordon, S. B., GenISIS Investigators, MOSAIC Investigators, Smyth, R. L., Openshaw, P. J., Dougan, G., Brass, A. L., and Kellam, P. (2012) IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484, 519-523
14. Zhang, Y.-H., Zhao, Y., Li, N., Peng, Y.-C., Giannoulatou, E., Jin, R.-H., Yan, H.-P., Wu, H., Liu, J.-H., Liu, N., Wang, D.-Y., Shu, Y.-L., Ho, L.-P., Kellam, P., McMichael, A., and Dong, T. (2013) Interferon-induced transmembrane protein-3 genetic variant rs12252-C is associated with severe influenza in Chinese individuals. Nat. Commun. 4, 1418
15. Hanagata, N., Li, X., Morita, H., Takemura, T., Li, J., and Minowa, T. (2011) Characterization of the osteoblast-specific transmembrane protein IFITM5 and analysis of IFITM5-deficient mice. J. Bone Miner. Metab. 29, 279-290
16. Cho, T.-J., Lee, K.-E., Lee, S.-K., Song, S. J., Kim, K. J., Jeon, D., Lee, G., Kim, H.-N., Lee, H. R., Eom, H.-H., Lee, Z. H., Kim, O.-H., Park, W.-Y., Park, S. S., Ikegawa, S., Yoo, W. J., Choi, I. H., and Kim, J.-W. (2012) A single recurrent mutation in the 5'-UTR of IFITM5 causes osteogenesis imperfecta type V. Am. J. Hum. Genet. 91, 343-348
17. Bailey, C. C., Huang, I.-C., Kam, C., and Farzan, M. (2012) Ifitm3 limits the severity of acute influenza in mice. PLoS Pathog. 8, e1002909
18. Wakim, L. M., Gupta, N., Mintern, J. D., and Villadangos, J. A. (2013) Enhanced survival of lung tissue-resident memory CD8+ T cells during infection with influenza virus due to selective expression of IFITM3. Nat. Immunol. 14, 238-245
19. Lange, U. C., Adams, D. J., Lee, C., Barton, S., Schneider, R., Bradley, A., and Surani, M. A. (2008) Normal germ line establishment in mice carrying a deletion of the Ifitm/Fragilis gene family cluster. Mol. Cell. Biol. 28, 4688-4696
20. Feeley, E. M., Sims, J. S., John, S. P., Chin, C. R., Pertel, T., Chen, L.-M., Gaiha, G. D., Ryan, B. J., Donis, R. O., Elledge, S. J., and Brass, A. L. (2011) IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog. 7, e1002337
21. Amini-Bavil-Olyaee, S., Choi, Y. J., Lee, J. H., Shi, M., Huang, I.-C., Farzan, M., and Jung, J. U. (2013) The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 13, 452-464
22. Yount, J. S., Moltedo, B., Yang, Y.-Y., Charron, G., Moran, T. M., López, C. B., and Hang, H. C. (2010) Palmitoylome profiling reveals S-palmitoylation- dependent antiviral activity of IFITM3. Nat. Chem. Biol. 6, 610-614
23. Singer, S. J. (1990) The structure and insertion of integral proteins in membranes. Annu. Rev. Cell Biol. 6, 247-296
24. Evans, S. S., Lee, D. B., Han, T., Tomasi, T. B., and Evans, R. L. (1990) Monoclonal antibody to the interferon-inducible protein Leu-13 triggers aggregation and inhibits proliferation of leukemic B cells. Blood 76, 2583-2593
25. Chen, Y. X., Welte, K., Gebhard, D. H., and Evans, R. L. (1984) Induction of T cell aggregation by antibody to a 16kd human leukocyte surface antigen. J. Immunol. 133, 2496-2501
26. Takahashi, S., Doss, C., Levy, S., and Levy, R. (1990) TAPA-1, the target of an antiproliferative antibody, is associated on the cell surface with the Leu-13 antigen. J. Immunol. 145, 2207-2213
27. Yount, J. S., Karssemeijer, R. A., and Hang, H. C. (2012) S-Palmitoylation and ubiquitination differentially regulate interferon-induced transmembrane protein 3 (IFITM3)-mediated resistance to influenza virus. J. Biol. Chem. 287, 19631-19641
28. Hach, J. C., McMichael, T., Chesarino, N. M., and Yount, J. S. (2013) Palmitoylation on conserved and nonconserved cysteines of murine IFITM1 regulates its stability and anti-influenza A virus activity. J. Virol. 87, 9923-9927
29. Huang, I.-C., Li, W., Sui, J., Marasco, W., Choe, H., and Farzan, M. (2008) Influenza A virus neuraminidase limits viral superinfection. J. Virol. 82, 4834-4843
30. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
31. Tang, B. L., Wong, S. H., Low, S. H., and Hong, W. (1992) Retention of a type II surface membrane protein in the endoplasmic reticulum by the Lys-Asp-Glu-Leu sequence. J. Biol. Chem. 267, 7072-7076
32. UniProt Consortium (2013) Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 41, D43-D47