STAT3 negatively regulates type I IFN-mediated antiviral response

Journal of Immunology

Volumn 187, Issue 5, 2011, Pages 2578-2585

  Wang, Wei Bei ^a   Levy, David E ^b   Lee, Chien Kuo ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CYTOKINE; INTERFERON; PROTEIN MDA5; STAT3 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIVIRAL RESPONSE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; VIRUS INFECTION;

ANIMALS; BLOTTING, WESTERN; GENE EXPRESSION REGULATION; INTERFERON TYPE I; LENTIVIRUS; LENTIVIRUS INFECTIONS; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 80052687211     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1004128     Document Type: Article

References (38)

1. Pitha, P. M., and M. S. Kunzi. 2007. Type I interferon: the ever unfolding story. Curr. Top. Microbiol. Immunol. 316: 41-70.
2. Schindler, C., D. E. Levy, and T. Decker. 2007. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282: 20059-20063. (Pubitemid 47099977)
3. Qureshi, S. A., M. Salditt-Georgieff, and J. E. Darnell Jr. 1995. Tyrosine-phosphorylated Stat1 and Stat2 plus a 48-kDa protein all contact DNA in forming interferon-stimulated-gene factor 3. Proc. Natl. Acad. Sci. USA 92: 3829-3833.
4. Baker, S. J., S. G. Rane, and E. P. Reddy. 2007. Hematopoietic cytokine receptor signaling. Oncogene 26: 6724-6737. (Pubitemid 47585098)
5. Durbin, J. E., R. Hackenmiller, M. C. Simon, and D. E. Levy. 1996. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84: 443-450. (Pubitemid 26058569)
6. Levy, D. E., and C. K. Lee. 2002. What does Stat3 do? J. Clin. Invest. 109: 1143-1148. (Pubitemid 34496591)
7. Meraz, M. A., J. M. White, K. C. Sheehan, E. A. Bach, S. J. Rodig, A. S. Dighe, D. H. Kaplan, J. K. Riley, A. C. Greenlund, D. Campbell, et al. 1996. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84: 431-442. (Pubitemid 26058568)
8. Aggarwal, B. B., A. B. Kunnumakkara, K. B. Harikumar, S. R. Gupta, S. T. Tharakan, C. Koca, S. Dey, and B. Sung. 2009. Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship? Ann. N. Y. Acad. Sci. 1171: 59-76.
9. Takeda, K., K. Noguchi, W. Shi, T. Tanaka, M. Matsumoto, N. Yoshida, T. Kishimoto, and S. Akira. 1997. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. USA 94: 3801-3804. (Pubitemid 27180453)
10. Bromberg, J. F., M. H. Wrzeszczynska, G. Devgan, Y. Zhao, R. G. Pestell, C. Albanese, and J. E. Darnell Jr. 1999. Stat3 as an oncogene. Cell 98: 295-303. (Pubitemid 29380565)
11. Yu, H., M. Kortylewski, and D. Pardoll. 2007. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol. 7: 41-51. (Pubitemid 46020826)
12. Yu, H., D. Pardoll, and R. Jove. 2009. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 9: 798-809.
13. Park, C., S. Li, E. Cha, and C. Schindler. 2000. Immune response in Stat2 knockout mice. Immunity 13: 795-804. (Pubitemid 32041802)
14. Dupuis, S., E. Jouanguy, S. Al-Hajjar, C. Fieschi, I. Z. Al-Mohsen, S. Al-Jumaah, K. Yang, A. Chapgier, C. Eidenschenk, P. Eid, et al. 2003. Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat. Genet. 33: 388-391. (Pubitemid 36278855)
15. Ho, H. H., and L. B. Ivashkiv. 2006. Role of STAT3 in type I interferon responses: negative regulation of STAT1-dependent inflammatory gene activation. J. Biol. Chem. 281: 14111-14118. (Pubitemid 43848338)
16. Waris, G., J. Turkson, T. Hassanein, and A. Siddiqui. 2005. Hepatitis C virus (HCV) constitutively activates STAT-3 via oxidative stress: role of STAT-3 in HCV replication. J. Virol. 79: 1569-1580. (Pubitemid 40459104)
17. Yang, C. H., A. Murti, and L. M. Pfeffer. 1998. STAT3 complements defects in an interferon-resistant cell line: evidence for an essential role for STAT3 in interferon signaling and biological activities. Proc. Natl. Acad. Sci. USA 95: 5568-5572. (Pubitemid 28224135)
18. Zhu, H., X. Shang, N. Terada, and C. Liu. 2004. STAT3 induces anti-hepatitis C viral activity in liver cells. Biochem. Biophys. Res. Commun. 324: 518-528. (Pubitemid 39345548)
19. Lee, C. K., R. Raz, R. Gimeno, R. Gertner, B. Wistinghausen, K. Takeshita, R. A. DePinho, and D. E. Levy. 2002. STAT3 is a negative regulator of granulopoiesis but is not required for G-CSF-dependent differentiation. Immunity 17: 63-72. (Pubitemid 34874619)
20. Chou, W. C., D. E. Levy, and C. K. Lee. 2006. STAT3 positively regulates an early step in B-cell development. Blood 108: 3005-3011.
21. Lee, C. K., E. Smith, R. Gimeno, R. Gertner, and D. E. Levy. 2000. STAT1 affects lymphocyte survival and proliferation partially independent of its role downstream of IFN-gamma. J. Immunol. 164: 1286-1292. (Pubitemid 30067241)
22. Schlessinger, K., and D. E. Levy. 2005. Malignant transformation but not normal cell growth depends on signal transducer and activator of transcription 3. Cancer Res. 65: 5828-5834. (Pubitemid 40911187)
23. Gough, D. J., A. Corlett, K. Schlessinger, J. Wegrzyn, A. C. Larner, and D. E. Levy. 2009. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 324: 1713-1716.
24. Niu, G., K. H. Shain, M. Huang, R. Ravi, A. Bedi, W. S. Dalton, R. Jove, and H. Yu. 2001. Overexpression of a dominant-negative signal transducer and activator of transcription 3 variant in tumor cells leads to production of soluble factors that induce apoptosis and cell cycle arrest. Cancer Res. 61: 3276-3280. (Pubitemid 32695012)
25. Lee, J. L., M. J. Wang, and J. Y. Chen. 2009. Acetylation and activation of STAT3 mediated by nuclear translocation of CD44. J. Cell Biol. 185: 949-957.
26. Yoneyama, M., M. Kikuchi, K. Matsumoto, T. Imaizumi, M. Miyagishi, K. Taira, E. Foy, Y. M. Loo, M. Gale, Jr., S. Akira, et al. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175: 2851-2858. (Pubitemid 41170502)
27. Vangrysperre, W., and K. De Clercq. 1996. Rapid and sensitive polymerase chain reaction based detection and typing of foot-and-mouth disease virus in clinical samples and cell culture isolates, combined with a simultaneous differentiation with other genomically and/or symptomatically related viruses. Arch. Virol. 141: 331-344.
28. Chen, L. S., P. C. Wei, T. Liu, C. H. Kao, L. M. Pai, and C. K. Lee. 2009. STAT2 hypomorphic mutant mice display impaired dendritic cell development and antiviral response. J. Biomed. Sci. 16: 22.
29. Berghäll, H., J. Sirén, D. Sarkar, I. Julkunen, P. B. Fisher, R. Vainionpää, and S. Matikainen. 2006. The interferon-inducible RNA helicase, mda-5, is involved in measles virus-induced expression of antiviral cytokines. Microbes Infect. 8: 2138-2144. (Pubitemid 44311582)
30. Takeuchi, O., and S. Akira. 2008. MDA5/RIG-I and virus recognition. Curr. Opin. Immunol. 20: 17-22.
31. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
32. Kamezaki, K., K. Shimoda, A. Numata, T. Haro, H. Kakumitsu, M. Yoshie, M. Yamamoto, K. Takeda, T. Matsuda, S. Akira, et al. 2005. Roles of Stat3 and ERK in G-CSF signaling. Stem Cells 23: 252-263. (Pubitemid 40239520)
33. Croker, B. A., D. Metcalf, L. Robb, W. Wei, S. Mifsud, L. DiRago, L. A. Cluse, K. D. Sutherland, L. Hartley, E. Williams, et al. 2004. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity 20: 153-165. (Pubitemid 38258392)
34. Kimura, A., I. Kinjyo, Y. Matsumura, H. Mori, R. Mashima, M. Harada, K. R. Chien, H. Yasukawa, and A. Yoshimura. 2004. SOCS3 is a physiological negative regulator for granulopoiesis and granulocyte colony-stimulating factor receptor signaling. J. Biol. Chem. 279: 6905-6910. (Pubitemid 38248833)
35. Hu, X., S. D. Chakravarty, and L. B. Ivashkiv. 2008. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feed-forward and feedback inhibition mechanisms. Immunol. Rev. 226: 41-56.
36. Murray, P. J. 2006. Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6: 379-386.
37. Kortylewski, M., M. Kujawski, A. Herrmann, C. Yang, L. Wang, Y. Liu, R. Salcedo, and H. Yu. 2009. Toll-like receptor 9 activation of signal transducer and activator of transcription 3 constrains its agonist-based immunotherapy. Cancer Res. 69: 2497-2505.
38. Takeda, K., B. E. Clausen, T. Kaisho, T. Tsujimura, N. Terada, I. Fö rster, and S. Akira. 1999. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10: 39-49. (Pubitemid 29077382)