Monitoring activation of the antiviral pattern recognition receptors RIG-I and PKR by limited protease digestion and native PAGE

Journal of Visualized Experiments

Volumn , Issue 89, 2014, Pages

  Weber, Michaela ^a   Weber, Friedemann ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; PROTEIN KINASE R; VIRUS RNA;

CELL LINE; GENETICS; HUMAN; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; RIFT VALLEY FEVER VIRUS; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; DEAD-BOX RNA HELICASES; EIF-2 KINASE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; RIFT VALLEY FEVER VIRUS; RNA, VIRAL;

EID: 84921689082     PISSN: 1940087X     EISSN: None     Source Type: Journal    
DOI: 10.3791/51415     Document Type: Article

References (46)

1. Gurtler, C., & Bowie, A. G. Innate immune detection of microbial nucleic acids. Trends in Microbiology. 21, 413-420, doi:10.1016/j.tim.2013.04.004 (2013).
2. Jensen, S., & Thomsen, A. R. Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. Journal of Virology. 86, 2900-2910, doi:10.1128/jvi.05738-11 (2012).
3. Kato, H., Takahasi, K., & Fujita, T. RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunological Reviews. 243, 91-98, doi:10.1111/j.1600-065X.2011.01052.x (2011).
4. Yoneyama, M. et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nature Immunology. 5, 730-737, doi:10.1038/ni1087 (2004).
5. Andrejeva, J. et al. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proceedings of the National Academy of Sciences of the United States of America. 101, 17264-17269, doi:10.1073/pnas.0407639101 (2004).
6. Saito, T. et al. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci U S A. 104, 582-587 (2007).
7. Ferrage, F. et al. Structure and dynamics of the second CARD of human RIG-I provide mechanistic insights into regulation of RIG-I activation. Structure (London, England: 1993). 20, 2048-2061, doi:10.1016/j.str.2012.09.003 (2012).
8. Kolakofsky, D., Kowalinski, E., & Cusack, S. A structure-based model of RIG-I activation. RNA (New York, N.Y.). 18, 2118-2127, doi:10.1261/rna.035949.112 (2012).
9. Luo, D., Kohlway, A., Vela, A., & Pyle, A. M. Visualizing the determinants of viral RNA recognition by innate immune sensor RIG-I. Structure (London, England: 1993). 20, 1983-1988, doi:10.1016/j.str.2012.08.029 (2012).
10. Kowalinski, E. et al. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell. 147, 423-435, doi:10.1016/j.cell.2011.09.039 (2011).
11. Luo, D. et al. Structural insights into RNA recognition by RIG-I. Cell. 147, 409-422, doi:10.1016/j.cell.2011.09.023 (2011).
12. Habjan, M. et al. Processing of genome 5 termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PloS One. 3, e2032, doi:10.1371/journal.pone.0002032 (2008).
13. Rehwinkel, J., & Reis, E. S. C. Targeting the viral Achilles'heel: recognition of 5'-triphosphate RNA in innate anti-viral defence. Current Opinion in Microbiology. 16, 485-492, doi:10.1016/j.mib.2013.04.009 (2013).
14. Pichlmair, A. et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science (New York, N.Y.) 314, 997-1001, doi:10.1126/science.1132998 (2006).
15. Hornung, V. et al. 5'-Triphosphate RNA is the ligand for RIG-I. Science (New York, N.Y.) 314, 994-997, doi:10.1126/science.1132505 (2006).
16. Saito, T., & Gale, M., Jr. Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. The Journal of Experimental Medicine. 205, 1523-1527, doi:10.1084/jem.20081210 (2008).
17. Takahasi, K. et al. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol Cell. 29, 428-440 (2008).
18. Binder, M. et al. Molecular mechanism of signal perception and integration by the innate immune sensor retinoic acid-inducible gene-I (RIG-I). J Biol Chem. 286, 27278-27287, doi:10.1074/jbc.M111.256974 (2011).
19. Jiang, X. et al. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity. 36, 959-973, doi:10.1016/j.immuni.2012.03.022 (2012).
20. Civril, F. et al. The RIG-I ATPase domain structure reveals insights into ATP-dependent antiviral signalling. EMBO reports. 12, 1127-1134, doi:10.1038/embor.2011.190 (2011).
21. Hiscott, J. Triggering the innate antiviral response through IRF-3 activation. The Journal of Biological Chemistry. 282, 15325-15329, doi:10.1074/jbc.R700002200 (2007).
22. Hertzog, P. J., & Williams, B. R. Fine tuning type I interferon responses. Cytokin., & Growth Factor Reviews. 24, 217-225, doi:10.1016/j.cytogfr.2013.04.002 (2013).
23. Pindel, A., & Sadler, A. The role of protein kinase R in the interferon response. Journal of Interfero., & Cytokine Research: the Official Journal of the International Society for Interferon and Cytokine Research. 31, 59-70, doi:10.1089/jir.2010.0099 (2011).
24. Donnelly, N., Gorman, A. M., Gupta, S., & Samali, A. The eIF2alpha kinases: their structures and functions. Cellular and Molecular Life Sciences: CMLS. 70, 3493-3511, doi:10.1007/s00018-012-1252-6 (2013).
25. Cole, J. L. Activation of PKR: an open and shut case? Trends in Biochemical Sciences. 32, 57-62, doi:10.1016/j.tibs.2006.12.003 (2007).
26. Dauber, B., & Wolff, T. Activation of the Antiviral Kinase PKR and Viral Countermeasures. Viruses. 1, 523-544, doi:10.3390/v1030523 (2009).
27. Dey, M. et al. Mechanistic link between PKR dimerization, autophosphorylation, and eIF2alpha substrate recognition. Cell. 122, 901-913, doi:10.1016/j.cell.2005.06.041 (2005).
28. Gack, M. U. et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature. 446, 916-920, doi:10.1038/nature05732 (2007).
29. Zeng, W. et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell. 141, 315-330, doi:10.1016/j.cell.2010.03.029 (2010).
30. Anderson, E., & Cole, J. L. Domain stabilities in protein kinase R (PKR): evidence for weak interdomain interactions. Biochemistry. 47, 4887-4897, doi:10.1021/bi702211j (2008).
31. Habjan, M. et al. NSs protein of rift valley fever virus induces the specific degradation of the double-stranded RNA-dependent protein kinase. Journal of Virology. 83, 4365-4375, doi:10.1128/jvi.02148-08 (2009).
32. Weber, M. et al. Incoming RNA virus nucleocapsids containing a 5'-triphosphorylated genome activate RIG-I and antiviral signaling. Cell Hos., & Microbe. 13, 336-346, doi:10.1016/j.chom.2013.01.012 (2013).
33. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 72, 248-254 (1976).
34. Wittig, I., & Schagger, H. Advantages and limitations of clear-native PAGE. Proteomics. 5, 4338-4346, doi:10.1002/pmic.200500081 (2005).
35. Muller, R. et al. Characterization of clone 13, a naturally attenuated avirulent isolate of Rift Valley fever virus, which is altered in the small segment. Am J Trop Med Hyg. 53, 405-411 (1995).
36. Bouloy, M. et al. Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs. Journal of Virology. 75, 1371-1377, doi:10.1128/jvi.75.3.1371-1377.2001 (2001).
37. Ikegami, T. et al. Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathogens. 5, e1000287, doi:10.1371/journal.ppat.1000287 (2009).
38. Iwamura, T. et al. Induction of IRF-3/-7 kinase and NF-kappaB in response to double-stranded RNA and virus infection: common and unique pathways. Genes to Cells: Devoted to Molecula., & Cellular Mechanisms. 6, 375-388 (2001).
39. Yoneyama, M., Suhara, W., & Fujita, T. Control of IRF-3 activation by phosphorylation. Journal of Interfero., & Cytokine Research: the Official Journal of the International Society for Interferon and Cytokine Research. 22, 73-76, doi:10.1089/107999002753452674 (2002).
40. Bamming, D., & Horvath, C. M. Regulation of signal transduction by enzymatically inactive antiviral RNA helicase proteins MDA5, RIG-I, and LGP2. The Journal of Biological Chemistry. 284, 9700-9712, doi:10.1074/jbc.M807365200 (2009).
41. Wu, B. et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell. 152, 276-289, doi:10.1016/j.cell.2012.11.048 (2013).
42. Berke, I. C., & Modis, Y. MDA5 cooperatively forms dimers and ATP-sensitive filaments upon binding double-stranded RNA. The EMBO Journal. 31, 1714-1726, doi:10.1038/emboj.2012.19 (2012).
43. Garcia-Sastre, A. Induction and evasion of type I interferon responses by influenza viruses. Virus Research. 162, 12-18, doi:10.1016/j.virusres.2011.10.017 (2011).
44. Taylor, K. E., & Mossman, K. L. Recent advances in understanding viral evasion of type I interferon. Immunology. 138, 190-197, doi:10.1111/imm.12038 (2013).
45. Goodbourn, S., & Randall, R. E. The regulation of type I interferon production by paramyxoviruses. Journal of Interfero., & Cytokine Research: the Official Journal of the International Society for Interferon and Cytokine Research. 29, 539-547, doi:10.1089/jir.2009.0071 (2009).
46. Versteeg, G. A., & Garcia-Sastre, A. Viral tricks to grid-lock the type I interferon system. Current Opinion in Microbiology. 13, 508-516, doi:10.1016/j.mib.2010.05.009 (2010).