Mice lacking the ISG15 E1 enzyme UbE1L demonstrate increased susceptibility to both mouse-adapted and non-mouse-adapted influenza B virus infection

Journal of Virology

Volumn 83, Issue 2, 2009, Pages 1147-1151

  Lai, Caroline ^a   Struckhoff, Jessica J ^a   Schneider, Jana ^b   Martinez Sobrido, Luis ^c   Wolff, Thorsten ^b   García Sastre, Adolfo ^c,d   Zhang, Dong Er ^e,f   Lenschow, Deborah J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ROBERT KOCH INSTITUTE   (Germany)

^c Global Health and Emerging Pathogens Institute   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E1; INTERFERON STIMULATED GENE 15; UBE1L ENZYME; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CONJUGATION; CONTROLLED STUDY; INFECTION CONTROL; INFECTION SENSITIVITY; INFLUENZA; INFLUENZA VIRUS B; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN TARGETING; RADIOSENSITIVITY; STROMA CELL;

ANIMALS; CYTOKINES; GENETIC PREDISPOSITION TO DISEASE; INFLUENZA B VIRUS; LUNG; MICE; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITINS;

INFLUENZA B VIRUS; MUS; ORTHOMYXOVIRIDAE;

EID: 58149502576     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00105-08     Document Type: Article

References (35)

1. Dastur, A., S. Beaudenon, M. Kelley, R. M. Krug, and J. M. Huibregtse. 2006. Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J. Biol. Chem. 281:4334-4338.
2. Dauber, B., G. Heins, and T. Wolff. 2004. The influenza B virus nonstructural NS1 protein is essential for efficient viral growth and antagonizes beta interferon induction. J. Virol. 78:1865-1872.
3. Dauber, B., J. Schneider, and T. Wolff. 2006. Double-stranded RNA binding of influenza B virus nonstructural NS1 protein inhibits protein kinase R but is not essential to antagonize production of alpha/beta interferon. J. Virol. 80:11667-11677.
4. D'Cunha, J., E. Knight, Jr., A. L. Haas, R. L. Truitt, and E. C. Borden. 1996. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc. Natl. Acad. Sci. USA 93:211-215.
5. D'Cunha, J., S. Ramanujam, R. J. Wagner, P. L. Witt, E. Knight, Jr., and E. C. Borden. 1996. In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine. J. Immunol. 157:4100-4108.
6. Donelan, N. R., B. Dauber, X. Wang, C. F. Basler, T. Wolff, and A. Garcia-Sastre. 2004. The N- and C-terminal domains of the NS1 protein of influenza B virus can independently inhibit IRF-3 and beta interferon promoter activation. J. Virol. 78:11574-11582.
7. Frias-Staheli, N., N. V. Giannakopoulos, M. Kikkert, S. L. Taylor, A. Bridgen, J. J. Paragas, J. A. Richt, R. R. Rowland, C. S. Schmaljohn, D. J. Lenschow, E. J. Snijder, A. Garcia-Sastre, and H. W. Virgin. 2007. Ovarian tumor (OTU)-domain containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2:404-416.
8. Giannakopoulos, N. V., J. K. Luo, V. Papov, W. G. Zou, D. J. Lenschow, B. S. Jacobs, E. C. Borden, J. Li, H. W. Virgin, and D. E. Zhang. 2005. Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem. Biophys. Res. Commun. 336:496-506.
9. Guerra, S., A. Caceres, K. P. Knobeloch, I. Horak, and M. Esteban. 2008. Vaccinia virus E3 protein prevents the antiviral action of ISG15. PLoS Pathogen 4:e100096.
10. Hamerman, J. A., F. Hayashi, L. A. Schroeder, S. P. Gygi, A. L. Haas, L. Hampson, P. Coughlin, R. Aebersold, and A. Aderem. 2002. Serpin 2a is induced in activated macrophages and conjugates to a ubiquitin homolog. J. Immunol. 168:2415-2423.
11. Kim, K. I., N. V. Giannakopoulos, H. W. Virgin, and D. E. Zhang. 2004. Interferon-inducible ubiquitin E2, Ubc8, is a conjugating enzyme for protein ISGylation. Mol. Cell. Biol. 24:9592-9600.
12. Kim, K. I., M. Yan, O. Malakhova, J. K. Luo, M. F. Shen, W. Zou, J. C. de la Torre, and D. E. Zhang. 2006. Ube1L and protein ISGylation are not essential for alpha/beta interferon signaling. Mol. Cell. Biol. 26:472-479.
13. Lenschow, D. J., N. V. Giannakopoulos, L. J. Gunn, C. Johnston, A. K. O'Guin, R. E. Schmidt, B. Levine, and H. W. Virgin. 2005. Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. J. Virol. 79:13974-13983.
14. Lenschow, D. J., C. Lai, N. Frias-Staheli, N. V. Giannakopoulos, A. Lutz, T. Wolff, A. Osiak, B. Levine, R. E. Schmidt, A. Garcia-Sastre, D. A. Leib, A. Pekosz, K. P. Knobeloch, I. Horak, and H. W. Virgin. 2007. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. USA 104:1371-1376.
15. Loeb, K. R., and A. L. Haas. 1992. The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 267:7806-7813.
16. Malakhov, M. P., K. I. Kim, O. A. Malakhova, B. S. Jacobs, E. C. Borden, and D. E. Zhang. 2003. High-throughput Immunoblotting. Ubiquitin-like protein ISG15 modifies key regulators of signal transduction. J. Biol. Chem. 278:16608-16613.
17. Malakhov, M. P., O. A. Malakhova, K. I. Kim, K. J. Ritchie, and D. E. Zhang. 2002. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277:9976-9981.
18. Malakhova, O. A., and D. E. Zhang. 2008. ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J. Biol. Chem. 283:8783-8787.
19. Narasimhan, J., M. Wang, Z. Fu, J. M. Klein, A. L. Haas, and J. J. Kim. 2005. Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J. Biol. Chem. 280:27356-27365.
20. Okumura, A., G. Lu, I. Pitha-Rowe, and P. M. Pitha. 2006. Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15. Proc. Natl. Acad. Sci. USA 103:1440-1445.
21. Okumura, A., P. M. Pitha, and R. N. Harty. 2008. ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc. Natl. Acad. Sci. USA 105:3974-3979.
22. Okumura, F., W. Zou, and D. E. Zhang. 2007. ISG15 modification of the eIF4E cognate 4EHP enhances cap structure-binding activity of 4EHP. Genes Dev. 21:255-260.
23. Owhashi, M., Y. Taoka, K. Ishii, S. Nakazawa, H. Uemura, and H. Hambara. 2003. Identification of a ubiquitin family protein as a novel neutrophil chemotactic factor. Biochem. Biophys. Res. Commun. 309:533-539.
24. Padovan, E., L. Terracciano, U. Certa, B. Jacobs, A. Reschner, M. Bolli, G. C. Spagnoli, E. C. Borden, and M. Heberer. 2002. Interferon stimulated gene 15 constitutively produced by melanoma cells induces e-cadherin expression on human dendritic cells. Cancer Res. 62:3453-3458.
25. Recht, M., E. C. Borden, and E. Knight, Jr. 1991. A human 15-kDa IFN-induced protein induces the secretion of IFN-gamma. J. Immunol. 147:2617-2623.
26. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
27. Shornick, L. P., A. G. Wells, Y. Zhang, A. C. Patel, G. Huang, K. Takami, M. Sosa, N. A. Shukla, E. Agapov, and M. J. Holtzman. 2008. Airway epithelial versus immune cell Stat 1 function for innate defense against respiratory viral infection. J. Immunol. 180:3319-3328.
28. Stetson, D. B., and R. Medzhitov. 2006. Type I interferons in host defense. Immunity 25:373-381.
29. Wang, F., Y. Ma, J. W. Barrett, X. Gao, J. Loh, E. Barton, H. W. Virgin, and G. McFadden. 2004. Disruption of Erk-dependent type I interferon induction breaks the myxoma virus species barrier. Nat. Immunol. 5:1266-1274.
30. Wong, J. J., Y. F. Pung, N. S. Sze, and K. C. Chin. 2006. HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proc. Natl. Acad. Sci. USA 103:10735- 10740.
31. Yuan, W., and R. M. Krug. 2001. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20:362-371.
32. Zhang, Y., C. W. Burke, K. D. Ryman, and W. B. Klimstra. 2007. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J. Virol. 81:11246-11255.
33. Zhao, C., S. L. Beaudenon, M. L. Kelley, M. B. Waddell, W. Yuan, B. A. Schulman, J. M. Huibregtse, and R. M. Krug. 2004. The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-alpha/beta-induced ubiquitin-like protein. Proc. Natl. Acad. Sci. USA 101:7578-7582.
34. Zhao, C., C. Denison, J. M. Huibregtse, S. Gygi, and R. M. Krug. 2005. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc. Natl. Acad. Sci. USA 102:10200-10205.
35. Zou, W., and D. E. Zhang. 2006. The interferon-inducible ubiquitin-protein isopeptide ligase (E3) EFP also functions as an ISG15 E3 ligase. J. Biol. Chem. 281:3989-3994.