Biphasic RLR-IFN-b response controls the balance between antiviral immunity and cell damage

Journal of Immunology

Volumn 190, Issue 3, 2013, Pages 1192-1200

  Hwang, Sun Young ^a   Hur, Kye Yeon ^a,b   Kim, Jeong Rae ^a   Cho, Kwang Hyun ^a   Kim, Seung Hwan ^a   Yoo, Joo Yeon ^a,b  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; DOUBLE STRANDED RNA; GREEN FLUORESCENT PROTEIN; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I LIKE RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CELL DAMAGE; CELL HETEROGENEITY; CELL POPULATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE AMPLIFICATION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MATHEMATICAL MODEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; SENDAI VIRUS; SIGNAL TRANSDUCTION; VIRUS IMMUNITY;

APOPTOSIS; AUTOCRINE COMMUNICATION; BREFELDIN A; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION; GENES, REPORTER; HEP G2 CELLS; HUMANS; INTERFERON INDUCERS; INTERFERON-BETA; MODELS, IMMUNOLOGICAL; POLY I-C; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; STOCHASTIC PROCESSES; TRANSCRIPTION, GENETIC; TRANSFECTION; VIRUS DISEASES;

EID: 84872689753     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202326     Document Type: Article

References (46)

1. Sen, G. C. 2001. Viruses and interferons. Annu. Rev. Microbiol. 55: 255-281. (Pubitemid 32978106)
2. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67: 227-264. (Pubitemid 28411130)
3. Goodbourn, S., L. Didcock, and R. E. Randall. 2000. Interferons: Cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81: 2341-2364.
4. Chawla-Sarkar, M., D. J. Lindner, Y. F. Liu, B. R. Williams, G. C. Sen, R. H. Silverman, and E. C. Borden. 2003. Apoptosis and interferons: Role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8: 237-249. (Pubitemid 36749609)
5. Apostolou, E., and D. Thanos. 2008. Virus Infection Induces NF-kB-dependent interchromosomal associations mediating monoallelic IFN-b gene expression. Cell 134: 85-96. (Pubitemid 351905745)
6. Enoch, T., K. Zinn, and T. Maniatis. 1986. Activation of the human b-interferon gene requires an interferon-inducible factor. Mol. Cell. Biol. 6: 801-810. (Pubitemid 16135945)
7. Hu, J., S. C. Sealfon, F. Hayot, C. Jayaprakash, M. Kumar, A. C. Pendleton, A. Ganee, A. Fernandez-Sesma, T. M. Moran, and J. G. Wetmur. 2007. Chromosome-specific and noisy IFNB1 transcription in individual virus-infected human primary dendritic cells. Nucleic Acids Res. 35: 5232-5241. (Pubitemid 47394206)
8. Senger, K., M. Merika, T. Agalioti, J. Yie, C. R. Escalante, G. Chen, A. K. Aggarwal, and D. Thanos. 2000. Gene repression by coactivator repulsion. Mol. Cell 6: 931-937.
9. Zawatzky, R., E. De Maeyer, and J. De Maeyer-Guignard. 1985. Identification of individual interferon-producing cells by in situ hybridization. Proc. Natl. Acad. Sci. USA 82: 1136-1140. (Pubitemid 15100509)
10. Zhao, M., J. Zhang, H. Phatnani, S. Scheu, and T. Maniatis. 2012. Stochastic expression of the interferon-b gene. PLoS Biol. 10: E1001249.
11. Becskei, A., B. Séraphin, and L. Serrano. 2001. Positive feedback in eukaryotic gene networks: Cell differentiation by graded to binary response conversion. EMBO J. 20: 2528-2535. (Pubitemid 32452871)
12. Xiong, W., and J. E. Ferrell, Jr. 2003. A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426: 460-465. (Pubitemid 37490134)
13. Wykoff, D. D., A. H. Rizvi, J. M. Raser, B. Margolin, and E. K. O'Shea. 2007. Positive feedback regulates switching of phosphate transporters in S. cerevisiae. Mol. Cell 27: 1005-1013. (Pubitemid 47488184)
14. Dubnau, D., and R. Losick. 2006. Bistability in bacteria. Mol. Microbiol. 61: 564-572. (Pubitemid 44324084)
15. Balaban, N. Q., J. Merrin, R. Chait, L. Kowalik, and S. Leibler. 2004. Bacterial persistence as a phenotypic switch. Science 305: 1622-1625. (Pubitemid 39296357)
16. Brandman, O., J. E. Ferrell, Jr., R. Li, and T. Meyer. 2005. Interlinked fast and slow positive feedback loops drive reliable cell decisions. Science 310: 496-498. (Pubitemid 41507964)
17. Acar, M., A. Becskei, and A. van Oudenaarden. 2005. Enhancement of cellular memory by reducing stochastic transitions. Nature 435: 228-232. (Pubitemid 40685951)
18. Ferrell, J. E., Jr. 2002. Self-perpetuating states in signal transduction: Positive feedback, double-negative feedback and bistability. Curr. Opin. Cell Biol. 14: 140-148. (Pubitemid 34219501)
19. Qiao, L., H. Phipps-Yonas, B. Hartmann, T. M. Moran, S. C. Sealfon, and F. Hayot. 2010. Immune response modeling of interferon b-pretreated influenza virus-infected human dendritic cells. Biophys. J. 98: 505-514.
20. Kawai, T., and S. Akira. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 1143: 1-20.
21. Honda, K., A. Takaoka, and T. Taniguchi. 2006. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360. (Pubitemid 44354220)
22. Meylan, E., and J. Tschopp. 2006. Toll-like receptors and RNA helicases: Two parallel ways to trigger antiviral responses. Mol. Cell 22: 561-569. (Pubitemid 43817607)
23. Meylan, E., J. Tschopp, and M. Karin. 2006. Intracellular pattern recognition receptors in the host response. Nature 442: 39-44. (Pubitemid 44064203)
24. 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)
25. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5: 730-737. (Pubitemid 39023305)
26. Marié, I., J. E. Durbin, and D. E. Levy. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17: 6660-6669. (Pubitemid 28521799)
27. Prakash, A., E. Smith, C. K. Lee, and D. E. Levy. 2005. Tissue-specific positive feedback requirements for production of type I interferon following virus infection. J. Biol. Chem. 280: 18651-18657. (Pubitemid 41379565)
28. Arimoto, K., H. Takahashi, T. Hishiki, H. Konishi, T. Fujita, and K. Shimotohno. 2007. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. USA 104: 7500-7505. (Pubitemid 47185935)
29. Friedman, C. S., M. A. O'Donnell, D. Legarda-Addison, A. Ng, W. B. Cárdenas, J. S. Yount, T. M. Moran, C. F. Basler, A. Komuro, C. M. Horvath, et al. 2008. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 9: 930-936.
30. Kim, M. J., S. Y. Hwang, T. Imaizumi, and J. Y. Yoo. 2008. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J. Virol. 82: 1474-1483.
31. Rothenfusser, S., N. Goutagny, G. DiPerna, M. Gong, B. G. Monks, A. Schoenemeyer, M. Yamamoto, S. Akira, and K. A. Fitzgerald. 2005. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 175: 5260-5268. (Pubitemid 41456411)
32. Satoh, T., H. Kato, Y. Kumagai, M. Yoneyama, S. Sato, K. Matsushita, T. Tsujimura, T. Fujita, S. Akira, and O. Takeuchi. 2010. LGP2 is a positive regulator of RIG-I-and MDA5-mediated antiviral responses. Proc. Natl. Acad. Sci. USA 107: 1512-1517.
33. Hartigan, J. A., and P. M. Hartigan. 1985. The DIP test of unimodality. Ann. Statist. 13: 70-84.
34. Li, K., Z. Chen, N. Kato, M. Gale, Jr., and S. M. Lemon. 2005. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-b production in hepatocytes. J. Biol. Chem. 280: 16739-16747. (Pubitemid 41389131)
35. Preiss, S., A. Thompson, X. Chen, S. Rodgers, V. Markovska, P. Desmond, K. Visvanathan, K. Li, S. Locarnini, and P. Revill. 2008. Characterization of the innate immune signalling pathways in hepatocyte cell lines. J. Viral Hepat. 15: 888-900.
36. Versteeg, G. A., and A. García-Sastre. 2010. Viral tricks to grid-lock the type I interferon system. Curr. Opin. Microbiol. 13: 508-516.
37. Angeli, D., J. E. Ferrell, Jr., and E. D. Sontag. 2004. Detection of multistability, bifurcations, and hysteresis in a large class of biological positive-feedback systems. Proc. Natl. Acad. Sci. USA 101: 1822-1827. (Pubitemid 38228975)
38. Reimer, T., M. Schweizer, and T. W. Jungi. 2007. Type I IFN induction in response to Listeria monocytogenes in human macrophages: Evidence for a differential activation of IFN regulatory factor 3 (IRF3). J. Immunol. 179: 1166-1177.
39. Dai, J., N. J. Megjugorac, S. B. Amrute, and P. Fitzgerald-Bocarsly. 2004. Regulation of IFN regulatory factor-7 and IFN-a production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J. Immunol. 173: 1535-1548. (Pubitemid 38971583)
40. Phipps-Yonas, H., J. Seto, S. C. Sealfon, T. M. Moran, and A. Fernandez-Sesma. 2008. Interferon-b pretreatment of conventional and plasmacytoid human den-dritic cells enhances their activation by influenza virus. PLoS Pathog. 4: E1000193.
41. Sadler, A. J., and B. R. Williams. 2008. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8: 559-568. (Pubitemid 351913674)
42. Iwasaki, A., and R. Medzhitov. 2010. Regulation of adaptive immunity by the innate immune system. Science 327: 291-295.
43. Freeman, M. 2000. Feedback control of intercellular signalling in development. Nature 408: 313-319.
44. Hu, J., G. Nudelman, Y. Shimoni, M. Kumar, Y. Ding, C. Lo'pez, F. Hayot, J. G. Wetmur, and S. C. Sealfon. 2011. Role of cell-to-cell variability in activating a positive feedback antiviral response in human dendritic cells. PLoS ONE 6: E16614.
45. Rand, U., M. Rinas, J. Schwerk, G. Nohren, M. Linnes, A. Kroger, M. Flossdorf, K. Kaly-Kullai, H. Hauser, T. Hofer, and M. Koster. 2012. Multi-layered stochasticity and paracrine signal propagation shape the type-I interferon response. Mol. Syst. Biol. 8: 584.
46. Mariani, L., E. G. Schulz, M. H. Lexberg, C. Helmstetter, A. Radbruch, M. Lohning, and T. Hofer. 2010. Short-term memory in gene induction reveals the regulatory principle behind stochastic IL-4 expression. Mol. Syst. Biol. 6: 359.