Dengue virus NS2B protein targets cGAS for degradation and prevents mitochondrial DNA sensing during infection

Nature Microbiology

Volumn 2, Issue , 2017, Pages

  Aguirre, Sebastian ^a   Luthra, Priya ^a   Sanchez Aparicio, Maria T ^a   Maestre, Ana M ^a   Patel, Jenish ^a   Lamothe, Francise ^a   Fredericks, Anthony C ^a   Tripathi, Shashank ^a   Zhu, Tongtong ^a   Pintado Silva, Jessica ^a   Webb, Laurence G ^a   Bernal Rubio, Dabeiba ^a   Solovyov, Alexander ^a   Greenbaum, Benjamin ^a   Simon, Viviana ^a   Basler, Christopher F ^a   Mulder, Lubbertus C F ^a   García Sastre, Adolfo ^a   Fernandez Sesma, Ana ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; MB21D1 PROTEIN, HUMAN; MEMBRANE PROTEIN; MITOCHONDRIAL DNA; NUCLEOTIDYLTRANSFERASE; VIRAL PROTEIN;

CHEMISTRY; DEFICIENCY; DENDRITIC CELL; DENGUE; DENGUE VIRUS; ENZYMOLOGY; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIROLOGY;

DENDRITIC CELLS; DENGUE; DENGUE VIRUS; DNA, MITOCHONDRIAL; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; MEMBRANE PROTEINS; NUCLEOTIDYLTRANSFERASES; SIGNAL TRANSDUCTION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 85016277255     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2017.37     Document Type: Article

References (43)

1. Uchida, L. et al. The dengue virus conceals double-stranded RNA in the intracellular membrane to escape from an interferon response. Sci. Rep. 4, 7395 (2014).
2. Espada-Murao, L. A. & Morita, K. Delayed cytosolic exposure of Japanese encephalitis virus double-stranded RNA impedes interferon activation and enhances viral dissemination in porcine cells. J. Virol. 85, 6736-6749 (2011).
3. Goubau, D., Deddouche, S. & Reis e Sousa, C. Cytosolic sensing of viruses. Immunity 38, 855-869 (2013).
4. Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504-507 (2013).
5. Welsch, S. et al. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5, 365-375 (2009).
6. Munoz-Jordan, J. L., Sanchez-Burgos, G. G., Laurent-Rolle, M. & Garcia-Sastre, A. Inhibition of interferon signaling by dengue virus. Proc. Natl Acad. Sci. USA 100, 14333-14338 (2003).
7. Ashour, J., Laurent-Rolle, M., Shi, P. Y. & Garcia-Sastre, A. NS5 of dengue virus mediates STAT2 binding and degradation. J. Virol. 83, 5408-5418 (2009).
8. Morrison, J., Aguirre, S. & Fernandez-Sesma, A. Innate immunity evasion by dengue virus. Viruses 4, 397-413 (2012).
9. Sun, L., Wu, J., Du, F., Chen, X. & Chen, Z. J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339, 786-791 (2013).
10. Aguirre, S. et al. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog. 8, e1002934 (2012).
11. Yu, C. Y. et al. Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLoS Pathog. 8, e1002780 (2012).
12. Rodriguez-Madoz, J. R., Bernal-Rubio, D., Kaminski, D., Boyd, K. & Fernandez-Sesma, A. Dengue virus inhibits the production of type I interferon in primary human dendritic cells. J. Virol. 84, 4845-4850 (2010).
13. Rodriguez-Madoz, J. R. et al. Inhibition of the type I interferon response in human dendritic cells by dengue virus infection requires a catalytically active NS2B3 complex. J. Virol. 84, 9760-9774 (2010).
14. Munoz-Jordan, J. L. et al. Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J. Virol. 79, 8004-8013 (2005).
15. Fernandez-Sesma, A. et al. Influenza virus evades innate and adaptive immunity via the NS1 protein. J. Virol. 80, 6295-6304 (2006).
16. Dai, P. et al. Modified vaccinia virus Ankara triggers type I IFN production in murine conventional dendritic cells via a cGAS/STING-mediated cytosolic DNA-sensing pathway. PLoS Pathog. 10, e1003989 (2014).
17. Zhong, B. et al. The adaptor protein MITA links virus sensing receptors to IRF3 transcription factor activation. Immunity 29, 538-550 (2008).
18. Gao, D. et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341, 903-906 (2013).
19. Civril, F. et al. Structural mechanism of cytosolic DNA sensing by cGAS. Nature 498, 332-337 (2013).
20. Li, X. D. et al. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341, 1390-1394 (2013).
21. Li, J. et al. Functional profiling of recombinant NS3 proteases from all four serotypes of dengue virus using tetrapeptide and octapeptide substrate libraries. J. Biol. Chem. 280, 28766-28774 (2005).
22. Heaton, N. S. & Randall, G. Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe 8, 422-432 (2010).
23. Stroikin, Y., Dalen, H., Loof, S. & Terman, A. Inhibition of autophagy with 3-methyladenine results in impaired turnover of lysosomes and accumulation of lipofuscin-like material. Eur. J. Cell Biol. 83, 583-590 (2004).
24. Kranzusch, P. J., Lee, A. S., Berger, J. M. & Doudna, J. A. Structure of human cGAS reveals a conserved family of second-messenger enzymes in innate immunity. Cell Rep. 3, 1362-1368 (2013).
25. Chan, Y. K. & Gack, M. U. A phosphomimetic-based mechanism of dengue virus to antagonize innate immunity. Nat. Immunol. 17, 523-530 (2016).
26. Schoggins, J. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505, 691-695 (2013).
27. Catteau, A., Roue, G., Yuste, V. J., Susin, S. A. & Despres, P. Expression of dengue ApoptoM sequence results in disruption of mitochondrial potential and caspase activation. Biochimie 85, 789-793 (2003).
28. El-Bacha, T. et al. Mitochondrial and bioenergetic dysfunction in human hepatic cells infected with dengue 2 virus. Biochim. Biophys. Acta 1772, 1158-1166 (2007).
29. Nasirudeen, A. M., Wang, L. & Liu, D. X. Induction of p53-dependent and mitochondria-mediated cell death pathway by dengue virus infection of human and animal cells. Microbes Infect. 10, 1124-1132 (2008).
30. Lam, E., Stein, S. & Falck-Pedersen, E. Adenovirus detection by the cGAS/STING/TBK1 DNA sensing cascade. J. Virol. 88, 974-981 (2014).
31. Hartlova, A. et al. DNA damage primes the type I interferon system via the cytosolic DNA sensor STING to promote anti-microbial innate immunity. Immunity 42, 332-343 (2015).
32. West, A. P. et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature 520, 553-557 (2015).
33. Schoggins, J.W. et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472, 481-485 (2011).
34. Rowland, A. A. & Voeltz, G. K. Endoplasmic reticulum-mitochondria contacts: function of the junction. Nat. Rev. Mol. Cell Biol. 13, 607-625 (2012).
35. Yu, C. Y. et al. Dengue virus impairs mitochondrial fusion by cleaving mitofusins. PLoS Pathog. 11, e1005350 (2015).
36. Ablasser, A. et al. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503, 530-534 (2013).
37. Diamond, M. S. et al. Modulation of dengue virus infection in human cells by alpha, beta, and gamma interferons. J. Virol. 74, 4957-4966 (2000).
38. Diamond, M. S., Edgil, D., Roberts, T. G., Lu, B. & Harris, E. Infection of human cells by dengue virus is modulated by different cell types and viral strains. J. Virol. 74, 7814-7823 (2000).
39. Gebhard, L. G. et al. A proline-rich N-terminal region of the dengue virus NS3 is crucial for infectious particle production. J. Virol. 90, 5451-5461 (2016).
40. Sanchez-Aparicio, M. T., Ayllon, J., Leo-Macias, A., Wolff, T. & Garcia-Sastre, A. Subcellular localizations of RIG-I, TRIM25, and MAVS complexes. J. Virol. 91, e01155-16 (2017).
41. Harrow, J. et al. GENCODE: the reference human genome annotation for the ENCODE project. Genome Res. 22, 1760-1774 (2012).
42. Chaisson, M. J. & Tesler, G. Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinformatics 13, 238 (2012).
43. Jayaprakash, A. D. et al. Stable heteroplasmy at the single-cell level is facilitated by intercellular exchange of mtDNA. Nucleic Acids Res. 43, 2177-2187 (2015).