Alpha interferon induces long-lasting refractoriness of JAK-STAT signaling in the mouse liver through induction of USP18/UBP43

Molecular and Cellular Biology

Volumn 29, Issue 17, 2009, Pages 4841-4851

  Sarasin Filipowicz, Magdalena ^a   Wang, Xueya ^a   Yan, Ming ^b   Duong, Francois H T ^a   Poli, Valeria ^c   Hilton, Douglas J ^d   Zhang, Dong Er ^b   Heim, Markus H ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF TURIN   (Italy)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INTERLEUKIN 10; JANUS KINASE; PEGINTERFERON ALPHA; PEPTIDASE; STAT PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; UBIQUITIN SPECIFIC PEPTIDASE 18; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG EFFICACY; LIVER CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SENSITIVITY ANALYSIS; UPREGULATION;

ANIMALS; ENDOPEPTIDASES; HUMANS; INTERFERON TYPE I, RECOMBINANT; INTERLEUKIN-10; JANUS KINASES; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

HEPATITIS C VIRUS; MUS;

EID: 68849096074     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00224-09     Document Type: Article

References (56)

1. Alexander, W. S., R. Starr, J. E. Fenner, C. L. Scott, E. Handman, N. S. Sprigg, J. E. Corbin, A. L. Cornish, R. Darwiche, C. M. Owczarek, T. W. Kay, N. A. Nicola, P. J. Hertzog, D. Metcalf, and D. J. Hilton. 1999. SOCS1 is a critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98:597-608.
2. Alonzi, T., D. Maritano, B. Gorgoni, G. Rizzuto, C. Libert, and V. Poli. 2001. Essential role of STAT3 in the control of the acute-phase response as revealed by inducible gene inactivation in the liver. Mol. Cell. Biol. 21:1621-1632.
3. Auernhammer, C. J., C. Bousquet, and S. Melmed. 1999. Autoregulation of pituitary corticotroph SOCS-3 expression: characterization of the murine SOCS-3 promoter. Proc. Natl. Acad. Sci. USA 96:6964-6969.
4. Barouki, F. M., F. R. Witter, D. E. Griffin, P. I. Nadler, A. Woods, D. L. Wood, and P. S. Lietman. 1987. Time course of interferon levels, antiviral state, 2′,5′-oligoadenylate synthetase and side effects in healthy men. J. Interferon Res. 7:29-39.
5. Chen, L., I. Borozan, J. Feld, J. Sun, L. L. Tannis, C. Coltescu, J. Heathcote, A. M. Edwards, and I. D. McGilvray. 2005. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 128:1437-1444.
6. Croker, B. A., D. L. Krebs, J. G. Zhang, S. Wormald, T. A. Willson, E. G. Stanley, L. Robb, C. J. Greenhalgh, I. Forster, B. E. Clausen, N. A. Nicola, D. Metcalf, D. J. Hilton, A. W. Roberts, and W. S. Alexander. 2003. SOCS3 negatively regulates IL-6 signaling in vivo. Nat. Immunol. 4:540-545.
7. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742.
8. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
9. Darnell, J. E., Jr., I. M. Kerr, and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1421.
10. Der, S. D., A. Zhou, B. R. Williams, and R. H. Silverman. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 95:15623-15628.
11. Ejrnaes, M., C. M. Filippi, M. M. Martinic, E. M. Ling, L. M. Togher, S. Crotty, and M. G. von Herrath. 2006. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203:2461-2472.
12. Fried, M. W., M. L. Shiffman, K. R. Reddy, C. Smith, G. Marinos, F. L. Goncales, Jr., D. Haussinger, M. Diago, G. Carosi, D. Dhumeaux, A. Craxi, A. Lin, J. Hoffman, and J. Yu. 2002. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N. Engl. J. Med. 347:975-982.
13. Friedman, R. M. 2008. Clinical uses of interferons. Br. J. Clin. Pharmacol. 65:158-162.
14. Heim, M. H. 2000. Intracellular signalling and antiviral effects of interferons. Dig. Liver Dis. 32:257-263.
15. Heim, M. H. 1999. The Jak-STAT pathway: cytokine signalling from the receptor to the nucleus. J. Recept. Signal Transduct. Res. 19:75-120.
16. Heim, M. H., G. Gamboni, C. Beglinger, and K. Gyr. 1997. Specific activation of AP-1 but not Stat3 in regenerating liver in mice. Eur. J. Clin. Investig. 27:948-955.
17. Heim, M. H., I. M. Kerr, G. R. Stark, and J. E. Darnell, Jr. 1995. Contribution of STAT SH2 groups to specific interferon signaling by the Jak-STAT pathway. Science 267:1347-1349.
18. Heim, M. H., D. Moradpour, and H. E. Blum. 1999. Expression of hepatitis C virus proteins inhibits signal transduction through the Jak-STAT pathway. J. Virol. 73:8469-8475.
19. Horvath, C. M. 2000. STAT proteins and transcriptional responses to extracellular signals. Trends Biochem. Sci. 25:496-502.
20. Isaacs, A., and J. Lindenmann. 1957. Virus interference. I. The interferon. Proc. R. Soc. London B Biol. Sci. 147:258-267.
21. Ito, S., P. Ansari, M. Sakatsume, H. Dickensheets, N. Vazquez, R. P. Donnelly, A. C. Larner, and D. S. Finbloom. 1999. Interleukin-10 inhibits expression of both interferon alpha- and interferon gamma-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93:1456-1463.
22. Kim, J. H., J. K. Luo, and D. E. Zhang. 2008. The level of hepatitis B virus replication is not affected by protein ISG15 modification but is reduced by inhibition of UBP43 (USP18) expression. J. Immunol. 181:6467-6472.
23. 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.
24. Knobeloch, K. P., O. Utermohlen, A. Kisser, M. Prinz, and I. Horak. 2005. Reexamination of the role of ubiquitin-like modifier ISG15 in the phenotype of UBP43-deficient mice. Mol. Cell. Biol. 25:11030-11034.
25. Krebs, D. L., and D. J. Hilton. 2001. SOCS proteins: negative regulators of cytokine signaling. Stem Cells 19:378-387.
26. Larner, A. C., A. Chaudhuri, and J. E. Darnell, Jr. 1986. Transcriptional induction by interferon. New protein(s) determine the extent and length of the induction. J. Biol. Chem. 261:453-459.
27. Lauer, G. M., and B. D. Walker. 2001. Hepatitis C virus infection. N. Engl. J. Med. 345:41-52.
28. Leyssen, P., C. Drosten, M. Paning, N. Charlier, J. Paeshuyse, E. De Clercq, and J. Neyts. 2003. Interferons, interferon inducers, and interferon-ribavirin in treatment of flavivirus-induced encephalitis in mice. Antimicrob. Agents Chemother. 47:777-782.
29. Li, X. L., J. A. Blackford, C. S. Judge, M. Liu, W. Xiao, D. V. Kalvakolanu, and B. A. Hassel. 2000. RNase-L-dependent destabilization of interferoninduced mRNAs. A role for the 2-5A system in attenuation of the interferon response. J. Biol. Chem. 275:8880-8888.
30. Liu, B., J. Liao, X. Rao, S. A. Kushner, C. D. Chung, D. D. Chang, and K. Shuai. 1998. Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. USA 95:10626-10631.
31. Liu, L. Q., R. Ilaria, Jr., P. D. Kingsley, A. Iwama, R. A. van Etten, J. Palis, and D. E. Zhang. 1999. A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation. Mol. Cell. Biol. 19:3029-3038.
32. Luik, A., S. Knapp, M. Thursz, H. C. Thomas, and J. F. Schlaak. 2004. Autoregulatory role of interleukin-10 in hepatitis C patients treated with IFN-alpha. J. Interferon Cytokine Res. 24:585-593.
33. 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.
34. Malakhova, O., M. Malakhov, C. Hetherington, and D. E. Zhang. 2002. Lipopolysaccharide activates the expression of ISG15-specific protease UBP43 via interferon regulatory factor 3. J. Biol. Chem. 277:14703-14711.
35. Malakhova, O. A., K. I. Kim, J. K. Luo, W. Zou, K. G. Kumar, S. Y. Fuchs, K. Shuai, and D. E. Zhang. 2006. UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J. 25:2358-2367.
36. Malakhova, O. A., M. Yan, M. P. Malakhov, Y. Yuan, K. J. Ritchie, K. I. Kim, L. F. Peterson, K. Shuai, and D. E. Zhang. 2003. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev. 17:455-460.
37. Manns, M. P., J. G. McHutchison, S. C. Gordon, V. K. Rustgi, M. Shiffman, R. Reindollar, Z. D. Goodman, K. Koury, M. Ling, and J. K. Albrecht. 2001. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 358:958-965.
38. Marin-Serrano, E., C. Rodriguez-Ramos, F. Diaz, L. Martin-Herrera, and J. A. Giron-Gonzalez. 2006. Modulation of the anti-inflammatory interleukin 10 and of proapoptotic IL-18 in patients with chronic hepatitis C treated with interferon alpha and ribavirin. J. Viral Hepat. 13:230-234.
39. McHutchison, J. G., S. C. Gordon, E. R. Schiff, M. L. Shiffman, W. M. Lee, V. K. Rustgi, Z. D. Goodman, M. H. Ling, S. Cort, J. K. Albrecht, et al. 1998. Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N. Engl. J. Med. 339:1485- 1492.
40. Mowen, K. A., J. Tang, W. Zhu, B. T. Schurter, K. Shuai, H. R. Herschman, and M. David. 2001. Arginine methylation of STAT1 modulates IFNα/β-induced transcription. Cell 104:731-741.
41. Osiak, A., O. Utermohlen, S. Niendorf, I. Horak, and K. P. Knobeloch. 2005. ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol. Cell. Biol. 25:6338-6345.
42. Postic, C., M. Shiota, K. D. Niswender, T. L. Jetton, Y. Chen, J. M. Moates, K. D. Shelton, J. Lindner, A. D. Cherrington, and M. A. Magnuson. 1999. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knockouts using Cre recombinase. J. Biol. Chem. 274:305-315.
43. Randall, G., L. Chen, M. Panis, A. K. Fischer, B. D. Lindenbach, J. Sun, J. Heathcote, C. M. Rice, A. M. Edwards, and I. D. McGilvray. 2006. Silencing of USP18 potentiates the antiviral activity of interferon against hepatitis C virus infection. Gastroenterology 131:1584-1591.
44. Rigopoulou, E. I., W. G. Abbott, P. Haigh, and N. V. Naoumov. 2005. Blocking of interleukin-10 receptor: a novel approach to stimulate T-helper cell type 1 responses to hepatitis C virus. Clin. Immunol. 117:57-64.
45. Ritchie, K. J., C. S. Hahn, K. I. Kim, M. Yan, D. Rosario, L. Li, J. C. de la Torre, and D. E. Zhang. 2004. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 10:1374-1378.
46. Ritchie, K. J., M. P. Malakhov, C. J. Hetherington, L. Zhou, M. T. Little, O. A. Malakhova, J. C. Sipe, S. H. Orkin, and D. E. Zhang. 2002. Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev. 16:2207-2212.
47. Sarasin-Filipowicz, M., E. J. Oakeley, F. H. Duong, V. Christen, L. Terracciano, W. Filipowicz, and M. H. Heim. 2008. Interferon signaling and treatment outcome in chronic hepatitis C. Proc. Natl. Acad. Sci. USA 105:7034-7039.
48. Shen, X., F. Hong, V. A. Nguyen, and B. Gao. 2000. IL-10 attenuates IFN-α-activated STAT1 in the liver: involvement of SOCS2 and SOCS3. FEBS Lett. 480:132-136.
49. Shuai, K. 2000. Modulation of STAT signaling by STAT-interacting proteins. Oncogene 19:2638-2644.
50. Shuai, K., G. R. Stark, I. M. Kerr, and J. E. Darnell, Jr. 1993. A single phosphotyrosine residue of Stat91 required for gene activation by interferongamma. Science 261:1744-1746.
51. Song, M. M., and K. Shuai. 1998. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J. Biol. Chem. 273:35056- 35062.
52. Starr, R., D. Metcalf, A. G. Elefanty, M. Brysha, T. A. Willson, N. A. Nicola, D. J. Hilton, and W. S. Alexander. 1998. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc. Natl. Acad. Sci. USA 95:14395-14399.
53. ten Hoeve, J., M. de Jesus Ibarra-Sanchez, Y. Fu, W. Zhu, M. Tremblay, M. David, and K. Shuai. 2002. Identification of a nuclear Stat1 protein tyrosine phosphatase. Mol. Cell. Biol. 22:5662-5668.
54. Wills, R. J. 1990. Clinical pharmacokinetics of interferons. Clin. Pharmacokinet. 19:390-399.
55. Yasukawa, H., M. Ohishi, H. Mori, M. Murakami, T. Chinen, D. Aki, T. Hanada, K. Takeda, S. Akira, M. Hoshijima, T. Hirano, K. R. Chien, and A. Yoshimura. 2003. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol. 4:551-556.
56. Zou, W., J. H. Kim, A. Handidu, X. Li, K. I. Kim, M. Yan, J. Li, and D. E. Zhang. 2007. Microarray analysis reveals that type I interferon strongly increases the expression of immune-response related genes in Ubp43 (Usp18) deficient macrophages. Biochem. Biophys. Res. Commun. 356:193-199.