Nucleocapsid protein of SARS-CoV activates interleukin-6 expression through cellular transcription factor NF-κB

Virology

Volumn 365, Issue 2, 2007, Pages 324-335

  Zhang, Xue ^a   Wu, Kailang ^a   Wang, Di ^a   Yue, Xin ^a   Song, Degui ^b   Zhu, Ying ^a   Wu, Jianguo ^a  

^a WUHAN UNIVERSITY   (China)

^b GUANGXI NORMAL UNIVERSITY   (China)

Author keywords

Gene regulation; IL 6; Inflammation; N protein; NF B; Pathogenesis; SARS CoV; Virus infection

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; NUCLEOCAPSID PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; GENE CONTROL; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SARS CORONAVIRUS;

ARTIFICIAL GENE FUSION; CELL LINE; CELL NUCLEUS; CYTOPLASM; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPITHELIAL CELLS; GENES, REPORTER; HUMANS; IMMUNOPRECIPITATION; INTERLEUKIN-6; LUCIFERASES; LUNG; MUTATION; NF-KAPPA B; NUCLEOCAPSID PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; SARS VIRUS; SEQUENCE DELETION;

SARS CORONAVIRUS;

EID: 34547697435     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.04.009     Document Type: Article

References (40)

1. Akira S., and Kishimoto T. IL-6 and NF-IL6 in acute-phase response and viral infection. Immunol. Rev. 127 (1992) 25-50
2. Akira S., and Kishimoto T. NF-IL6 and NF-κB in cytokine gene regulation. Adv. Immunol. 65 (1997) 1-46
3. Akira S., Taga T., and Kishimoto T. Interleukin-6 in biology and medicine. Adv. Immunol. 54 (1993) 1-78
4. Baccam M., Woo S.-Y., Vinson C., and Bishop G.A. CD40-Mediated transcriptional regulation of the IL-6 gene in B lymphocytes: involvement of NF-κB, AP-1, and C/EBP. J. Immunol. 170 (2003) 3099-3108
5. Carlotti F., Dower S.K., and Qwarnstrom E.E. Dynamic shuttling of nuclear factor kappa B between the nucleus and cytoplasm as a consequence of inhibitor dissociation. J. Biol. Chem. 275 (2000) 41028-41034
6. Chang M., Lu S., Ho Y.T., Wu C.C., Wei T.Y., Chen C.J., Hsu Y.T., Chu P.C., Chen C.H., Chu J.M., et al. Antibody detection of SARS-CoV spike and nucleocapsid protein. Biochem. Biophys. Res. Commun. 314 (2004) 931-936
7. Eickelberg O., Pansky A., Mussmanni R., Bihl M., Tamm M., Hildebrand P., Perruchoud A., and Roth M. Transforming growth factor-b1 induces Interleukin-6 expression via activating protein-1 consisting of JunD homodimers in primary human lung fibroblasts. J. Biol. Chem. 274 (1999) 12933-12938
8. Erschler W.B., and Keller E.T. Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu. Rev. Med. 51 (2000) 245-270
9. Galien R., Evans H.F., and Garcia T. Involvement of CCAAT/enhancer-binding protein and nuclear factor-κB binding sites in Interleukin-6 promoter inhibition by estrogens. Mol. Endocrinol. 10 (1996) 713-722
10. He R., Leeson A., Andonov A., Li Y., Bastien N., Cao J., Osiowy C., Dobie F., Cutts T., Ballantine M., and Li X. Activation of AP-1 signal transduction pathway by SARS coronavirus nucleocapsid protein. Biochem. Biophys. Res. Commun. 311 (2003) 870-876
11. He R., Dobie F., Ballantime M., et al. Analysis of multimerization of the SARS coronavirus nucleocapsid protein. Biochem. Biophys. Res. Commun. 317 (2004) 1030-1036
12. Hirano T. Kishimoto. Molecular biology and immunology of interleukin-6. Res. Immunol. 143 (1992) 723-783
13. Hogue B.G. Bovine coronavirus nucleocapsid protein processing and assembly. Adv. Exp. Med. Biol. 380 (1995) 259-263
14. Hsueh P.R., Chen P.J., Hsiao C.H., Yeh S.H., Cheng W.C., Wang J.L., et al. Patient data, early epidemic, Taiwan. Emerg. Infect. Dis. 10 (2004) 489-491
15. Keller E.T., Wanagat J., and Ershler W.B. Molecular and cellular biology of interleukin-6 and its receptor. Front Biosci. 1 (1996) 340-357
16. Kuo L., and Masters P.S. Genetic evidence for a structural interaction between the carboxy termini of the membrane and nucleocapsid proteins of mouse hepatitis virus. J. Virol. 76 (2002) 4987-4999
17. Liao Q., Ye L., Timani K.A., Zeng Y., She Y., Ye L., and Wu Z. Activation of NF-κB by the full-length nucleocapsid protein of the SARS coronavirus. Acta Biochim. Biophys. Sin. 37 (2005) 607-612
18. Lieberman T.A., and Baltimore D. Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol. Cell. Biol. 10 (1990) 2327-2334
19. Liu C., Kokuho T., Kubota T., Watanabe S., Inumaru S., Yokomizo Y., and Onodera T. DNA mediated immunization with encoding the nucleoprotein gene of porcine transmissible gastroenteritis virus. Virus Res. 80 (2001) 75-82
20. Liu M., Yang Y.B., Gu C.F., Wu K.K., Wu J., and Zhu Y. Spike protein of SARS-CoV stimulates cyclooxygenase-2 expression via both calcium-dependent and calcium-independent protein kinase C pathways. FASEB J. (2007) (Electronic publication ahead of print)
21. Marra M.A., Jones S.J., Astell C.R., et al. The genome sequence of the SARS-associated coronavirus. Science 300 (2003) 1399-1404
22. Myers T.M., and Moyer S.A. An amino-terminal domain of the Sendai virus nucleocapsid protein is required for template function in viral RNA synthesis. J. Virol. 71 (1997) 918-924
23. Narayanan K., Maeda A., Maeda J., and Makino S. Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells. J. Virol. 74 (2000) 8127-8134
24. Narayanan K., Chen C.J., Maeda J., and Makino S. Nucleocapsid independent specific viral RNA packaging via viral envelope protein and viral RNA signal. J. Virol. 77 (2003) 2922-2927
25. Papanicolaou D.A., Wilder R.L., Manolagas S.C., and Chrousos G.P. The pathophysiologic role of interleukin-6 in human disease. Ann. Intern. Med. 128 (1998) 127-137
26. Parker M.M., and Masters P.S. Sequence comparison of the N genes of 5 strains of the coronavirus mouse hepatitis virus suggests a 3 domain-structure for the nucleocapsid protein. Virology 179 (1990) 463-468
27. Peiris J.S.M., Yuen K.Y., Osterhaus A.D.M.E., and Stöhr K. The severe acute respiratory syndrome. N. Engl. J. Med. 349 (2003) 2431-2441
28. Rota P.A., Oberste M.S., Monroe S.S., et al. Characterization of a novel coronavirus associated with Severe Acute Respiratory Syndrome. Science 300 (2003) 1394-1399
29. Sen R., and Baltimore D. Inducibility of kappa immunoglobulin enhancer binding protein NF-κB by a post-translational mechanism. Cell 47 (1986) 921-928
30. Snick J.V. Interleukin-6: an overview. Annu. Rev. Immunol. 8 (1990) 253-278
31. Sutjit M., Liu B., Jameel S., Chow V.T.K., and Lal S.K. The SARS coronavirus nucleocapsid protein induces actin reorganization and apoptosis in COS-1 cells in the absence of growth factors. Biochem. J. 383 (2004) 13-18
32. Timani K.A., Ye L., Zhu Y., Wu Z., and Gong Z. Cloning, sequencing, expression, and purification of SARS-associated coronavirus nucleocapsid protein for serodiagnosis of SARS. J. Clin. Virol. 30 (2004) 309-312
33. Timani K.A., Liao Q., Ye L., Zeng Y., Liu J., Zheng Y., Ye L., Yang X., Gao L., Ke J., and Zhu Y. Nuclear/nucleolar localization properties of C-terminal nucleocapsid protein of SARS coronavirus. Virus Res. 114 (2005) 23-34
34. Verma I.M., Stevenson J.K., Schwarz E.M., Antwerp D.V., and Miyamoto S. Rel/NF-κB/I-κB family: intimate tales of association and dissociation. Genes Dev. 9 (1995) 2723-2735
35. Wang J., Ye J., Ji J., Zhao X., Wen J., Li W., Hu J., Li D., Sun M., Zeng H., Hu Y., Tian H., Tan X., Xu N., Zeng C., Wang J., Bi S., and Yang H. The structure analysis and antigenicity study of the N protein of SARS-CoV. Geno. Prot. Bioinfo. 1 (2003) 145-156
36. Wu G.D., Zhu Y., and Wu K. Upregulation of p300 binding and p50 acetylation in tumor necrosis factor-alpha induced cyclooxygeanse-2 promoter activation. J. Biol. Chem. 278 (2003) 4770-4777
37. Wurm T., Chen H., Hodgson T., Britton P., Brooks G., and Hiscox J.A. Localization to the nucleolus is a common feature of coronavirus nucleoproteins and the protein may disrupt host cell division. J. Virol. 75 (2001) 9345-9356
38. Yan S.F., Tritto I., Pinsky D., Liao H., Huang J., Fuller G., Brett J., May L., and Stern D. Induction of interleukin 6 (IL-6) by hypoxia in vascular cells. Central role of the binding site for nuclear factor-IL-6. J. Biol. Chem. 270 (1995) 11463-11471
39. Yan X., Hao Q., Mu Y., Timani K.A., Ye L., Zhu Y., and Wu J. Nucleocapsid protein of SARS-CoV activates the expression of cyclooxygenase-2 by binding directly to regulatory elements for nuclear factor kappa B and CCAAT/enhancer binding protein. Int. J. Biochem. Cell Biol. 3 (2006) 1417-1428
40. Zhu Y., Liu M., Zhao W., Zhang J., Zhang X., Wang K., Gu C., Wu K., Li Y., Zheng C., Xiao G., Yan H., Zhang J., Guo D., Tien P., and Wu J. Isolation of virus from a SARS patient and genome-wide analysis of genetic mutations related to pathogenesis and epidemiology from 47 SARS-CoV isolates. Virus Genes 30 (2005) 93-102