Up-regulation of IL-6 and TNF-α induced by SARS-coronavirus spike protein in murine macrophages via NF-κB pathway

Virus Research

Volumn 128, Issue 1-2, 2007, Pages 1-8

  Wang, Wei ^a   Ye, Linbai ^a   Ye, Li ^a   Li, Baozong ^a   Gao, Bo ^a   Zeng, Yingchun ^a   Kong, Lingbao ^a   Fang, Xiaonan ^a   Zheng, Hong ^a   Wu, Zhenghui ^a   She, Yinglong ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

IL 6; Macrophages; NF B; SARS coronavirus; Spike protein; TNF

Indexed keywords

CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VIRUS PROTEIN; VITRONECTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CORONAVIRUS; IMMUNE RESPONSE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEVERE ACUTE RESPIRATORY SYNDROME; UPREGULATION;

ANIMALS; CELL LINE; GENE EXPRESSION REGULATION; INTERLEUKIN-6; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; NF-KAPPA B; SARS VIRUS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; VIRAL ENVELOPE PROTEINS;

MURINAE; SARS CORONAVIRUS;

EID: 34547756320     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2007.02.007     Document Type: Article

References (45)

1. Banerjee S., Narayanan K., Mizutani T., and Makino S. Murine coronavirus replication-induced p38 mitogen-activated protein kinase activation promotes interleukin-6 production and virus replication in cultured cells. J. Virol. 76 12 (2002) 5937-5948
2. Bieback K., Lien E., Klagge I.M., Avota E., Schneider-Schaulies J., Duprex W.P., Wagner H., Kirschning C.J., Ter Meulen V., and Schneider-Schaulies S. Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J. Virol. 76 17 (2002) 8729-8736
3. Boehme K.W., and Compton T. Innate sensing of viruses by toll-like receptors. J. Virol. 78 15 (2004) 7867-7873
4. Chang Y.J., Liu C.Y., Chiang B.L., Chao Y.C., and Chen C.C. Induction of IL-8 release in lung cells via activator protein-1 by recombinant baculovirus displaying severe acute respiratory syndrome-coronavirus spike proteins: identification of two functional regions. J. Immunol. 173 12 (2004) 7602-7614
5. Chen Z., Zhang L., Qin C., Ba L., Yi C.E., Zhang F., Wei Q., He T., Yu W., Yu J., Gao H., Tu X., Gettie A., Farzan M., Yuen K.Y., and Ho D.D. Recombinant modified vaccinia virus Ankara expressing the spike glycoprotein of severe acute respiratory syndrome coronavirus induces protective neutralizing antibodies primarily targeting the receptor binding region. J. Virol. 79 5 (2005) 2678-2688
6. Compton T., Kurt-Jones E.A., Boehme K.W., Belko J., Latz E., Golenbock D.T., and Finberg R.W. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 77 8 (2003) 4588-4596
7. Cooper A., Tal G., Lider O., and Shaul Y. Cytokine induction by the hepatitis B virus capsid in macrophages is facilitated by membrane heparan sulfate and involves TLR2. J. Immunol. 175 5 (2005) 3165-3176
8. Dolganiuc A., Oak S., Kodys K., Golenbock D.T., Finberg R.W., Kurt-Jones E., and Szabo G. Hepatitis C core and nonstructural 3 proteins trigger toll-like receptor 2-mediated pathways and inflammatory activation. Gastroenterology 127 5 (2004) 1513-1524
9. Eliopoulos A.G., Gallagher N.J., Blake S.M., Dawson C.W., and Young L.S. Activation of the p38 mitogen-activated protein kinase pathway by Epstein-Barr virus-encoded latent membrane protein 1 coregulates interleukin-6 and interleukin-8 production. J. Biol. Chem. 274 23 (1999) 16085-16096
10. Gealy C., Denson M., Humphreys C., McSharry B., Wilkinson G., and Caswell R. Posttranscriptional suppression of interleukin-6 production by human cytomegalovirus. J. Virol. 79 1 (2005) 472-485
11. Ghosh S., May M.J., and Kopp E.B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16 (1998) 225-260
12. Griego S.D., Weston C.B., Adams J.L., Tal-Singer R., and Dillon S.B. Role of p38 mitogen-activated protein kinase in rhinovirus-induced cytokine production by bronchial epithelial cells. J. Immunol. 165 9 (2000) 5211-5220
13. Hamming I., Timens W., Bulthuis M.L., Lely A.T., Navis G.J., and van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 203 2 (2004) 631-637
14. He Y., Zhou Y., Liu S., Kou Z., Li W., Farzan M., and Jiang S. Receptor-binding domain of SARS-CoV spike protein induces highly potent neutralizing antibodies: implication for developing subunit vaccine. Biochem. Biophys. Res. Commun. 324 2 (2004) 773-781
15. Hsueh P.R., Chen P.J., Hsiao C.H., Yeh S.H., Cheng W.C., Wang J.L., Chiang B.L., Chang S.C., Chang F.Y., Wong W.W., Kao C.L., and Yang P.C. Patient data, early SARS epidemic, Taiwan. Emerg. Infect. Dis. 10 3 (2004) 489-493
16. Karin M., and Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18 (2000) 621-663
17. Kurt-Jones E.A., Chan M., Zhou S., Wang J., Reed G., Bronson R., Arnold M.M., Knipe D.M., and Finberg R.W. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc. Natl. Acad. Sci. U.S.A. 101 5 (2004) 1315-1320
18. Law H.K., Cheung C.Y., Ng H.Y., Sia S.F., Chan Y.O., Luk W., Nicholls J.M., Peiris J.S., and Lau Y.L. Chemokine up-regulation in SARS-coronavirus-infected, monocyte-derived human dendritic cells. Blood 106 7 (2005) 2366-2374
19. Lee C.H., Chen R.F., Liu J.W., Yeh W.T., Chang J.C., Liu P.M., Eng H.L., Lin M.C., and Yang K.D. Altered p38 mitogen-activated protein kinase expression in different leukocytes with increment of immunosuppressive mediators in patients with severe acute respiratory syndrome. J. Immunol. 172 12 (2004) 7841-7847
20. Lee D.C., Cheung C.Y., Law A.H., Mok C.K., Peiris M., and Lau A.S. p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J. Virol. 79 16 (2005) 10147-10154
21. Lee N., Hui D., Wu A., Chan P., Cameron P., Joynt G.M., Ahuja A., Yung M.Y., Leung C.B., To K.F., Lui S.F., Szeto C.C., Chung S., and Sung J.J. A major outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348 20 (2003) 1986-1994
22. Lee S.E., Choi S.E., Kim J.H., Kim K.S., and Kang Y. Activation of mouse macrophage by soluble endogenous murine leukemia virus (MuLV) envelope protein. Immunol. Lett. 79 3 (2001) 221-227
23. Li F., Li W., Farzan M., and Harrison S.C. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309 5742 (2005) 1864-1868
24. Li Q., and Verma I.M. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2 10 (2002) 725-734
25. Li W., Moore M.J., Vasilieva N., Sui J., Wong S.K., Berne M.A., Somasundaran M., Sullivan J.L., Luzuriaga K., Greenough T.C., Choe H., and Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426 6965 (2003) 450-454
26. Li Z., Guo X., Hao W., Wu Y., Ji Y., Zhao Y., Liu F., and Xie X. The relationship between serum interleukins and T-lymphocyte subsets in patients with severe acute respiratory syndrome. Chin. Med. J. (Engl.) 116 7 (2003) 981-984
27. Lindemans C.A., Coffer P.J., Schellens I.M., de Graaff P.M., Kimpen J.L., and Koenderman L. Respiratory syncytial virus inhibits granulocyte apoptosis through a phosphatidylinositol 3-kinase and NF-kappaB-dependent mechanism. J. Immunol. 176 9 (2006) 5529-5537
28. Mizutani T., Fukushi S., Saijo M., Kurane I., and Morikawa S. Phosphorylation of p38 MAPK and its downstream targets in SARS coronavirus-infected cells. Biochem. Biophys. Res. Commun. 319 4 (2004) 1228-1234
29. Nicholls J.M., Poon L.L., Lee K.C., Ng W.F., Lai S.T., Leung C.Y., Chu C.M., Hui P.K., Mak K.L., Lim W., Yan K.W., Chan K.H., Tsang N.C., Guan Y., Yuen K.Y., and Peiris J.S. Lung pathology of fatal severe acute respiratory syndrome. Lancet 361 9371 (2003) 1773-1778
30. Pathak S.K., Basu S., Bhattacharyya A., Pathak S., Banerjee A., Basu J., and Kundu M. TLR4-dependent NF-kappaB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-isomerase (HP0175)-mediated induction of IL-6 release from macrophages. J. Immunol. 177 11 (2006) 7950-7958
31. Peiris J.S., Lai S.T., Poon L.L., Guan Y., Yam L.Y., Lim W., Nicholls J., Yee W.K., Yan W.W., Cheung M.T., Cheng V.C., Chan K.H., Tsang D.N., Yung R.W., Ng T.K., and Yuen K.Y. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361 9366 (2003) 1319-1325
32. Pons J., Sauleda J., Regueiro V., Santos C., Lopez M., Ferrer J., Agusti A.G., and Bengoechea J.A. Expression of Toll-like receptor 2 is up-regulated in monocytes from patients with chronic obstructive pulmonary disease. Respir. Res. 7 (2006) 64
33. Sheng W.H., Chiang B.L., Chang S.C., Ho H.N., Wang J.T., Chen Y.C., Hsiao C.H., Hseuh P.R., Chie W.C., and Yang P.C. Clinical manifestations and inflammatory cytokine responses in patients with severe acute respiratory syndrome. J. Formos. Med. Assoc. 104 10 (2005) 715-723
34. Smith C., Andreakos E., Crawley J.B., Brennan F.M., Feldmann M., and Foxwell B.M. NF-kappaB-inducing kinase is dispensable for activation of NF-kappaB in inflammatory settings but essential for lymphotoxin beta receptor activation of NF-kappaB in primary human fibroblasts. J. Immunol. 167 10 (2001) 5895-5903
35. To K.F., and Lo A.W. Exploring the pathogenesis of severe acute respiratory syndrome (SARS): the tissue distribution of the coronavirus (SARS-CoV) and its putative receptor, angiotensin-converting enzyme 2 (ACE2). J. Pathol. 203 3 (2004) 740-743
36. Tseng C.T., Perrone L.A., Zhu H., Makino S., and Peters C.J. Severe acute respiratory syndrome and the innate immune responses: modulation of effector cell function without productive infection. J. Immunol. 174 12 (2005) 7977-7985
37. Verma I.M., Stevenson J.K., Schwarz E.M., Van Antwerp D., and Miyamoto S. Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation. Genes Dev. 9 22 (1995) 2723-2735
38. Wang J.P., Kurt-Jones E.A., Shin O.S., Manchak M.D., Levin M.J., and Finberg R.W. Varicella-zoster virus activates inflammatory cytokines in human monocytes and macrophages via Toll-like receptor 2. J. Virol. 79 20 (2005) 12658-12666
39. Wong C.K., Lam C.W., Wu A.K., Ip W.K., Lee N.L., Chan I.H., Lit L.C., Hui D.S., Chan M.H., Chung S.S., and Sung J.J. Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin. Exp. Immunol. 136 1 (2004) 95-103
40. Wong S.K., Li W., Moore M.J., Choe H., and Farzan M. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279 5 (2004) 3197-3201
41. Xie J., Han Y., Li T.S., Qiu Z.F., Ma X.J., Fan H.W., Lu W., Liu Z.Y., Wang Z., Wang H.L., and Deng G.H. Dynamic changes of plasma cytokine levels in patients with severe acute respiratory syndrome. Zhonghua Nei Ke Za Zhi 42 9 (2003) 643-645
42. Yilla M., Harcourt B.H., Hickman C.J., McGrew M., Tamin A., Goldsmith C.S., Bellini W.J., and Anderson L.J. SARS-coronavirus replication in human peripheral monocytes/macrophages. Virus Res. 107 1 (2005) 93-101
43. Yu S.Y., Hu Y.W., Liu X.Y., Xiong W., Zhou Z.T., and Yuan Z.H. Gene expression profiles in peripheral blood mononuclear cells of SARS patients. World J. Gastroenterol. 11 32 (2005) 5037-5043
44. Zhang Y., Li J., Zhan Y., Wu L., Yu X., Zhang W., Ye L., Xu S., Sun R., Wang Y., and Lou J. Analysis of serum cytokines in patients with severe acute respiratory syndrome. Infect. Immun. 72 8 (2004) 4410-4415
45. Zhu Z., Tang W., Ray A., Wu Y., Einarsson O., Landry M.L., Gwaltney Jr. J., and Elias J.A. Rhinovirus stimulation of interleukin-6 in vivo and in vitro. Evidence for nuclear factor kappa B-dependent transcriptional activation. J. Clin. Invest. 97 2 (1996) 421-430