Interferon-inducible transmembrane protein 3 (IFITM3) restricts reovirus cell entry

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17261-17271

  Anafu, Amanda A ^a   Bowen, Christopher H ^a   Chin, Christopher R ^b   Brass, Abraham L ^b   Holm, Geoffrey H ^a  

^a Center for Language and Brain   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE-STRANDED RNA; ENDOCYTIC PATHWAYS; ENDOSOMAL COMPARTMENTS; ENDOSOMAL PROTEOLYSIS; GASTROINTESTINAL TRACT; PROTEOLYTIC PROCESSING; TRANS-MEMBRANE PROTEINS; TYPE I INTERFERONS;

ANTIBIOTICS; CELL CULTURE; ENZYME ACTIVITY; GENES; GLYCOPROTEINS; MAMMALS; PROTEINS; PROTEOLYSIS; RNA; VIRUSES;

CELLS;

CAPSID PROTEIN; INTERFERON INDUCIBLE TRANSMEMBRANE PROTEIN 3; RAB7 PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; INFECTION SENSITIVITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REOVIRUS INFECTION; VIRION; VIRUS ENTRY; VIRUS PARTICLE; VIRUS REPLICATION;

ENDOSOMES; INNATE IMMUNITY; INTERFERON; INTERFERON-STIMULATED GENE; REOVIRUS; VIRUS ENTRY;

CAPSID; ENDOCYTOSIS; ENDOSOMES; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-ALPHA; KINETICS; MAMMALIAN ORTHOREOVIRUS 3; MEMBRANE PROTEINS; ORTHOREOVIRUS, MAMMALIAN; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; VIRION; VIRUS ASSEMBLY; VIRUS INTERNALIZATION; VIRUS REPLICATION;

INFLUENZA A VIRUS; MAMMALIA; MIRIDAE; ORTHOREOVIRUS; RNA VIRUSES;

EID: 84879048489     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.438515     Document Type: Article

References (68)

1. Mogensen, T. H. (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Micro. Rev. 22, 240-273
2. Jensen, S., and Thomsen, A. R. (2012) Sensing of RNA viruses. A review of innate immune receptors involved in recognizing RNA virus invasion. J. Virol. 86, 2900-2910
3. Borden, E. C., and Williams, B. R. (2011) Interferon-stimulated genes and their protein products. what and how? J. Interferon Cytokine Res. 31, 1-4
4. Farrell, P. J., Balkow, K., Hunt, T., Jackson, R. J., and Trachsel, H. (1977) Phosphorylation of initiation factor eIF-2 and the control of reticulocyte protein synthesis. Cell 11, 187-200 (Pubitemid 8126067)
5. Ratner, L., Wiegand, R. C., Farrell, P. J., Sen, G. C., Cabrer, B., and Lengyel, P. (1978) Interferon, double-stranded RNA, and RNA degradation. Fractionation of the endonuclease INT system into two macromolecular components. Role of a small molecule in nuclease activation. Biochem. Biophys. Res. Commun. 81, 947-954 (Pubitemid 8327106)
6. Taylor, R. T., Lubick, K. J., Robertson, S. J., Broughton, J. P., Bloom, M. E., Bresnahan, W. A., and Best, S. M. (2011) TRIM79α, an interferon-stimulated gene product, restricts tick-borne encephalitis virus replication by degrading the viral RNA polymerase. Cell Host Microbe 10, 185-196
7. Evans, S. S., Collea, R. P., Leasure, J. A., and Lee, D. B. (1993) IFN-α induces homotypic adhesion and Leu-13 expression in human B lymphoid cells. J. Immunol. 150, 736-747 (Pubitemid 23133653)
8. Imai, T., and Yoshie, O. (1993) C33 antigen and M38 antigen recognized by monoclonal antibodies inhibitory to syncytium formation by human T cell leukemia virus type 1 are both members of the transmembrane 4 superfamily and associate with each other and with CD4 or CD8 in T cells. J. Immunol. 151, 6470-6481 (Pubitemid 23340393)
9. Lange, U. C., Saitou, M., Western, P. S., Barton, S. C., and Surani, M. A. (2003) The fragilis interferon-inducible gene family of transmembrane proteins is associated with germ cell specification in mice. BMC Dev. Biol. 3, 1
10. Smith, R. A., Young, J., Weis, J. J., and Weis, J. H. (2006) Expression of the mouse fragilis gene products in immune cells and association with receptor signaling complexes. Genes Immun. 7, 113-121 (Pubitemid 43336053)
11. 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
12. 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
13. 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
14. 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
15. Bailey, C. C., Huang, I.-C., Kam, C., and Farzan, M. (2012) Ifitm3 limits the severity of acute influenza in mice. PLoS Pathogens 8, e1002909
16. 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
17. Schiff, L. A., Nibert, M. L., and Tyler, K. L. in Field's Virology (Knipe, D. M., and Howley, P. M., eds.) 5th Ed., pp. 1853-1915, Lippincott Williams and Wilkins ET, Philadelphia
18. Barton, E. S., Forrest, J. C., Connolly, J. L., Chappell, J. D., Liu, Y., Schnell, F. J., Nusrat, A., Parkos, C. A., and Dermody, T. S. (2001) Junction adhesion molecule is a receptor for reovirus. Cell 104, 441-451 (Pubitemid 32206464)
19. Maginnis, M. S., Forrest, J. C., Kopecky-Bromberg, S. A., Dickeson, S. K., Santoro, S. A., Zutter, M. M., Nemerow, G. R., Bergelson, J. M., and Dermody, T. S. (2006) β1 integrin mediates internalization of mammalian reovirus. J. Virol. 80, 2760-2770 (Pubitemid 43346371)
20. Ebert, D. H., Deussing, J., Peters, C., and Dermody, T. S. (2002) Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. J. Biol. Chem. 277, 24609-24617 (Pubitemid 34951989)
21. Sturzenbecker, L. J., Nibert, M., Furlong, D., and Fields, B. N. (1987) Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J. Virol. 61, 2351-2361 (Pubitemid 17097545)
22. Chandran, K., Farsetta, D. L., and Nibert, M. L. (2002) Strategy for nonenveloped virus entry. A hydrophobic conformer of the reovirus membrane penetration protein m1 mediates membrane disruption. J. Virol. 76, 9920-9933 (Pubitemid 35006531)
23. Chandran, K., Parker, J. S., Ehrlich, M., Kirchhausen, T., and Nibert, M. L. (2003) The delta region of outer-capsid protein m1 undergoes conformational change and release from reovirus particles during cell entry. J. Virol. 77, 13361-13375 (Pubitemid 37494330)
24. Nibert, M. L., Odegard, A. L., Agosto, M. A., Chandran, K., and Schiff, L. A. (2005) Putative autocleavage of reovirus m1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J. Mol. Biol. 345, 461-474 (Pubitemid 39575917)
25. Odegard, A. L., Chandran, K., Zhang, X., Parker, J. S., Baker, T. S., and Nibert, M. L. (2004) Putative autocleavage of outer capsid protein m1, allowing release of myristoylated peptide μ1N during particle uncoating, is critical for cell entry by reovirus. J. Virol. 78, 8732-8745 (Pubitemid 39025138)
26. Nibert, M. L., and Fields, B. N. (1992) A carboxyl-terminal fragment of protein m1/m1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J. Virol. 66, 6408-6418
27. Mainou, B. A., and Dermody, T. S. (2012) Transport to late endosomes is required for efficient reovirus infection. J. Virol. 86, 8346-8358
28. Kobayashi, T., Ooms, L. S., Ikizler, M., Chappell, J. D., and Dermody, T. S. (2010) An improved reverse genetics system for mammalian orthoreoviruses. Virology 398, 194-200
29. Kobayashi, T., Antar, A. A., Boehme, K. W., Danthi, P., Eby, E. A., Guglielmi, K. M., Holm, G. H., Johnson, E. M., Maginnis, M. S., Naik, S., Skelton, W. B., Wetzel, J. D., Wilson, G. J., Chappell, J. D., and Dermody, T. S. (2007) A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1, 147-157 (Pubitemid 46554915)
30. Furlong, D. B., Nibert, M. L., and Fields, B. N. (1988) Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J. Virol. 62, 246-256 (Pubitemid 18050814)
31. Smith, R. E., Zweerink, H. J., and Joklik, W. K. (1969) Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39, 791-810
32. Virgin, H. W., 4th, Bassel-Duby, R., Fields, B. N., and Tyler, K. L. (1988) Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J. Virol. 62, 4594-4604 (Pubitemid 19006122)
33. Connolly, J. L., and Dermody, T. S. (2002) Virion disassembly is required for apoptosis induced by reovirus. J. Virol. 76, 1632-1641 (Pubitemid 34094610)
34. Fecek, R. J., Busch, R., Lin, H., Pal, K., Cunningham, C. A., and Cuff, C. F. (2006) Production of Alexa Fluor 488-labeled reovirus and characterization of target cell binding, competence, and immunogenicity of labeled virions. J. Immunol. Methods 314, 30-37 (Pubitemid 44189425)
35. Gauntt, C. J. (1973) Induction of interferon in L cells by reoviruses. Infect. Immun. 7, 711-717
36. Holm, G. H., Zurney, J., Tumilasci, V., Leveille, S., Danthi, P., Hiscott, J., Sherry, B., and Dermody, T. S. (2007) Retinoic acid-inducible gene-I and interferon-β promoter stimulator-1 augment proapoptotic responses after mammalian reovirus infection via interferon regulatory factor-3. J. Biol. Chem. 282, 21953-21961 (Pubitemid 47195783)
37. Maginnis, M. S., Mainou, B. A., Derdowski, A., Johnson, E. M., Zent, R., and Dermody, T. S. (2008) NPXY motifs in the β1 integrin cytoplasmic tail are required for functional reovirus entry. J. Virol. 82, 3181-3191 (Pubitemid 351429899)
38. Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R., and Neefjes, J. (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11, 1680-1685 (Pubitemid 33037779)
39. Barbero, P., Bittova, L., and Pfeffer, S. R. (2002) Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J. Cell Biol. 156, 511-518 (Pubitemid 34839898)
40. Dermody, T. S., Nibert, M. L., Wetzel, J. D., Tong, X., and Fields, B. N. (1993) Cells and viruses with mutations affecting viral entry are selected during persistent infections of L cells with mammalian reoviruses. J. Virol. 67, 2055-2063 (Pubitemid 23088379)
41. Tsai, B. (2007) Penetration of nonenveloped viruses into the cytoplasm. Annu. Rev. Cell Dev. Biol. 23, 23-43
42. Harrison, S. C. (2008) Viral membrane fusion. Nat. Struct. Mol. Biol. 15, 690-698
43. Friedman, R. L., Manly, S. P., McMahon, M., Kerr, I. M., and Stark, G. R. (1984) Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell 38, 745-755 (Pubitemid 15176105)
44. Lewin, A. R., Reid, L. E., McMahon, M., Stark, G. R., and Kerr, I. M. (1991) Molecular analysis of a human interferon-inducible gene family. Eur. J. Biochem. 199, 417-423
45. Seth, P. (1994) Mechanism of adenovirus-mediated endosome lysis. role of the intact adenovirus capsid structure. Biochem. Biophys. Res. Commun. 205, 1318-1324
46. 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
47. 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
48. 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
49. Wee, Y. S., Roundy, K. M., Weis, J. J., and Weis, J. H. (2012) 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, 834-845
50. 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
51. 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
52. Schulz, W. L., Haj, A. K., and Schiff, L. A. (2012) Reovirus uses multiple endocytic pathways for cell entry. J. Virol. 86, 12665-12675
53. Mundt, E. (2007) Human MxA protein confers resistance to double-stranded RNA viruses of two virus families. J. Gen. Virol. 88, 1319-1323
54. Stewart, M. J., Blum, M. A., and Sherry, B. (2003) PKR's protective role in viral myocarditis. Virology 314, 92-100 (Pubitemid 37158011)
55. Nilsen, T. W., Maroney, P. A., and Baglioni, C. (1982) Inhibition of protein synthesis in reovirus-infected HeLa cells with elevated levels of interferon-induced protein kinase activity. J. Biol. Chem. 257, 14593-14596 (Pubitemid 13159550)
56. Jacobs, B. L., and Ferguson, R. E. (1991) The Lang strain of reovirus serotype 1 and the Dearing strain of reovirus serotype 3 differ in their sensitivities to b interferon. J. Virol. 65, 5102-5104
57. Sherry, B., Torres, J., and Blum, M. A. (1998) Reovirus induction of and sensitivity to β interferon in cardiac myocyte cultures correlate with induction of myocarditis and are determined by viral core proteins. J. Virol. 72, 1314-1323 (Pubitemid 28116917)
58. Middleton, J. K., Agosto, M. A., Severson, T. F., Yin, J., and Nibert, M. L. (2007) Thermostabilizing mutations in reovirus outer-capsid protein m1 selected by heat inactivation of infectious subvirion particles. Virology 361, 412-425 (Pubitemid 46574850)
59. Sarkar, P., and Danthi, P. (2010) Determinants of strain-specific differences in efficiency of reovirus entry. J. Virol. 84, 12723-12732
60. Madren, J. A., Sarkar, P., and Danthi, P. (2012) Cell entry-associated conformational changes in reovirus particles are controlled by host protease activity. J. Virol. 86, 3466-3473
61. Parker, J. S., Murphy, W. J., Wang, D., O'Brien, S. J., and Parrish, C. R. (2001) Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J. Virol. 75, 3896-3902 (Pubitemid 32246398)
62. Parker, J. S., and Parrish, C. R. (2000) Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J. Virol. 74, 1919-1930 (Pubitemid 30434051)
63. Chardonnet, Y., and Dales, S. (1970) Early events in the interaction of adenoviruses with HeLa cells. II. Comparative observations on the penetration of types 1, 5, 7, and 12. Virology 40, 478-485
64. FitzGerald, D. J., Trowbridge, I. S., Pastan, I., and Willingham, M. C. (1983) Enhancement of toxicity of antitransferrin receptor antibody-Pseudomonas exotoxin conjugates by adenovirus. Proc. Natl. Acad. Sci. U.S.A. 80, 4134-4138 (Pubitemid 13072782)
65. Wolf, M., Vo, P. T., and Greenberg, H. B. (2011) Rhesus rotavirus entry into a polarized epithelium is endocytosis-dependent and involves sequential VP4 conformational changes. J. Virol. 85, 2492-2503
66. Wolf, M., Deal, E. M., and Greenberg, H. B. (2012) Rhesus rotavirus trafficking during entry into MA104 cells is restricted to the early endosome compartment. J. Virol. 86, 4009-4013
67. Blumenthal, R., Seth, P., Willingham, M. C., and Pastan, I. (1986) pH-dependent lysis of liposomes by adenovirus. Biochemistry 25, 2231-2237
68. Greber, U. F., Willetts, M., Webster, P., and Helenius, A. (1993) Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75, 477-486 (Pubitemid 23335073)