SARS-Coronavirus Open Reading Frame-8b triggers intracellular stress pathways and activates NLRP3 inflammasomes

Cell Death Discovery

Volumn 5, Issue 1, 2019, Pages

  Shi, Chong Shan ^a   Nabar, Neel R ^a   Huang, Ning Na ^a   Kehrl, John H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85071104997     PISSN: None     EISSN: 20587716     Source Type: Journal    
DOI: 10.1038/s41420-019-0181-7     Document Type: Article

References (49)

1. Peiris, J. S., Guan, Y. & Yuen, K. Y. Severe acute respiratory syndrome. Nat. Med. 10, S88–S97 (2004).
2. Stadler, K. et al. SARS—beginning to understand a new virus. Nat. Rev. Microbiol. 1, 209–218 (2003).
3. Balboni, A., Battilani, M. & Prosperi, S. The SARS-like coronaviruses: the role of bats and evolutionary relationships with SARS coronavirus. New Microbiol. 35, 1–16 (2012).
4. Zaki, A. M., van Boheemen, S., Bestebroer, T. M., Osterhaus, A. D. & Fouchier, R. A. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367, 1814–1820 (2012).
5. Franks, T. J. et al. Lung pathology of severe acute respiratory syndrome (SARS): a study of 8 autopsy cases from Singapore. Hum. Pathol. 34, 743–748 (2003).
6. Nicholls, J., Dong, X. P., Jiang, G. & Peiris, M. SARS: clinical virology and pathogenesis. Respirology 8(Suppl), S6–S8 (2003).
7. Huang, K. J. et al. An interferon‐γ‐related cytokine storm in SARS patients. J. Med. Virol. 75, 185–194 (2004).
8. He, L. et al. Expression of elevated levels of pro‐inflammatory cytokines in SARS‐CoV‐infected ACE2 + cells in SARS patients: relation to the acute lung injury and pathogenesis of SARS. J. Pathol. 210, 288–297 (2006).
9. Channappanavar, R. et al. Dysregulated type I interferon and inflammatory monocyte-macrophage responses cause lethal pneumonia in SARS-CoV-infected mice. Cell Host Microbe 19, 181–193 (2016).
10. McBride, R. & Fielding, B. C. The role of severe acute respiratory syndrome (SARS)-coronavirus accessory proteins in virus pathogenesis. Viruses 4, 2902–2923 (2012).
11. Yue, Y. et al. SARS-Coronavirus Open Reading Frame-3a drives multimodal necrotic cell death. Cell Death Dis. 9, 904 (2018).
12. Shi, C. S. et al. SARS-Coronavirus Open Reading Frame-9b suppresses innate immunity by targeting mitochondria and the MAVS/TRAF3/TRAF6 signalosome. J. Immunol. 193, 3080–3089 (2014).
13. Wong, H. H. et al. Accessory proteins 8b and 8ab of severe acute respiratory syndrome coronavirus suppress the interferon signaling pathway by mediating ubiquitin-dependent rapid degradation of interferon regulatory factor 3. Virology 515, 165–175 (2018).
14. Oostra, M., de Haan, C. A. & Rottier, P. J. The 29-nucleotide deletion present in human but not in animal severe acute respiratory syndrome coronaviruses disrupts the functional expression of open reading frame 8. J. Virol. 81, 13876–13888 (2007).
15. Le, T. M. et al. Expression, post-translational modification and biochemical characterization of proteins encoded by subgenomic mRNA8 of the severe acute respiratory syndrome coronavirus. FEBS J. 274, 4211–4222 (2007).
16. Keng, C. T. et al. SARS coronavirus 8b reduces viral replication by down-regulating E via an ubiquitin-independent proteasome pathway. Microbes Infect. 13, 179–188 (2011).
17. Keng, C. T. et al. The human severe acute respiratory syndrome coronavirus (SARS-CoV) 8b protein is distinct from its counterpart in animal SARS-CoV and down-regulates the expression of the envelope protein in infected cells. Virology 354, 132–142 (2006).
18. Coll, R. C., O’Neill, L. & Schroder, K. Questions and controversies in innate immune research: what is the physiological role of NLRP3? Cell Death Discov. 2, 16019 (2016).
19. Ng, P. C. et al. Inflammatory cytokine profile in children with severe acute respiratory syndrome. Pediatrics 113, e7–e14 (2004).
20. Walsh, I., Seno, F., Tosatto, S. C. E. & Trovato, A. PASTA 2.0: an improved server for protein aggregation prediction. Nucleic Acids Res. 42, W301–W307 (2014).
21. Ogen-Shtern, N., Ben David, T. & Lederkremer, G. Z. Protein aggregation and ER stress. Brain Res. 1648, 658–666 (2016).
22. Nishitoh, H. CHOP is a multifunctional transcription factor in the ER stress response. J. Biochem. 151, 217–219 (2012).
23. Eskelinen, E.-L. & Saftig, P. Autophagy: a lysosomal degradation pathway with a central role in health and disease. Biochim. Biophys. Acta 1793, 664–673 (2009).
24. Nabar, N. R., Shi, C.-S. & Kehrl, J. H. Signaling by the toll-like receptors induces autophagy through modification of beclin-1: molecular mechanism. In Immunology, Vol. 1: immunotoxicology, immunopathology, and immunotherapy (ed Hayat M. A.) 75–84 (Academic Press, 2017).
25. Santaguida, S., Vasile, E., White, E. & Amon, A. Aneuploidy-induced cellular stresses limit autophagic degradation. Genes Dev. 29, 2010–2021 (2015).
26. Nabar, N. R. & Kehrl, J. H. The transcription factor EB links cellular stress to the immune response. Yale J. Biol. Med. 90, 301–315 (2017).
27. Aits, S. et al. Sensitive detection of lysosomal membrane permeabilization by lysosomal galectin puncta assay. Autophagy 11, 1408–1424 (2015).
28. Martina, J. A., Diab, H. I., Brady, O. A. & Puertollano, R. TFEB and TFE3 are novel components of the integrated stress response. EMBO J. 35, 479–495 (2016).
29. Sardiello, M. et al. A gene network regulating lysosomal biogenesis and function. Science 325, 473–477 (2009).
30. Medina, D. L. et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat. Cell Biol. 17, 288–299 (2015).
31. Settembre, C. et al. TFEB links autophagy to lysosomal biogenesis. Science 332, 1429–1433 (2011).
32. Klionsky, D. J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12, 1–222 (2016).
33. He, Y., Hara, H. & Nunez, G. Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem. Sci. 41, 1012–1021 (2016).
34. Vural, A. et al. Galphai2 signaling regulates inflammasome priming and cytokine production by biasing macrophage phenotype determination. J. Immunol. 202, 1510–1520 (2019). 10.4049/jimmunol.1801145.
35. Chen, J. & Chen, Z. J. PtdIns4P on dispersed trans-Golgi network mediates NLRP3 inflammasome activation. Nature 564, 71–76 (2018).
36. Chinese SARS Molecular Epidemiology Consortium Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China.Science 303, 1666–1669 (2004).
37. Currais, A., Fischer, W., Maher, P. & Schubert, D. Intraneuronal protein aggregation as a trigger for inflammation and neurodegeneration in the aging brain. FASEB J. 31, 5–10 (2017).
38. Liu, X.-D. et al. Transient aggregation of ubiquitinated proteins is a cytosolic unfolded protein response to inflammation and endoplasmic reticulum stress. J. Biol. Chem. 287, 19687–19698 (2012).
39. Moshe, A. & Gorovits, R. Virus-induced aggregates in infected cells. Viruses 4, 2218–2232 (2012).
40. Sung, S.-C., Chao, C.-Y., Jeng, K.-S., Yang, J.-Y. & Lai, M. M. C. The 8ab protein of SARS-CoV is a luminal ER membrane-associated protein and induces the activation of ATF6. Virology 387, 402–413 (2009).
41. Zhang, K. & Kaufman, R. J. From endoplasmic-reticulum stress to the inflammatory response. Nature 454, 455–462 (2008).
42. Pastore, N. et al. TFEB and TFE3 cooperate in the regulation of the innate immune response in activated macrophages. Autophagy 12, 1240–1258 (2016).
43. Kanneganti, T. D. Central roles of NLRs and inflammasomes in viral infection. Nat. Rev. Immunol. 10, 688–698 (2010).
44. Harris, J. et al. Autophagy and inflammasomes. Mol. Immunol. 86, 10–15 (2017).
45. Ichinohe, T., Pang, I. K. & Iwasaki, A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 11, 404–410 (2010).
46. Ito, M., Yanagi, Y. & Ichinohe, T. Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLoS Pathog. 8, e1002857 (2012).
47. McAuley, J. L. et al. Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog. 9, e1003392 (2013).
48. Marra, M. A. et al. The genome sequence of the SARS-associated coronavirus. Science 300, 1399 (2003).
49. Shi, C. S. et al. Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 13, 255–263 (2012).