SARS coronavirus spike protein-induced innate immune response occurs via activation of the NF-κB pathway in human monocyte macrophages in vitro

Virus Research

Volumn 142, Issue 1-2, 2009, Pages 19-27

  Dosch, Susan F ^a   Mahajan, Supriya D ^a   Collins, Arlene R ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Human monocyte macrophages; Innate immunity; NF B activation; SARS; Spike protein

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; CCL15 CHEMOKINE; CCL16 CHEMOKINE; CHEMOKINE; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P35; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LEPTIN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCLONAL ANTIBODY; RECOMBINANT PROTEIN; TOLL LIKE RECEPTOR 2; TOSYLPHENYLALANYL CHLOROMETHYL KETONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR P65 NF KAPPA B; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG; VIRUS E PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS SPIKE PROTEIN;

ANTIVIRAL ACTIVITY; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE FUNCTION; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MICROARRAY ANALYSIS; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARS CORONAVIRUS; SENSITIVITY AND SPECIFICITY;

CELL LINE; CELLS, CULTURED; GENE EXPRESSION; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; MACROPHAGES; MEMBRANE GLYCOPROTEINS; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; TRANSCRIPTION FACTOR RELA; VIRAL ENVELOPE PROTEINS;

SARS CORONAVIRUS;

EID: 67349224644     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2009.01.005     Document Type: Article

References (50)

1. Barton G.M., and Medzhitov R. Toll-like receptor signaling pathways. Science 6 (2003) 712-721
2. Beniac D.R., Andonov A., Grudeski E., and Booth T.F. Architecture of the SARS coronavirus prefusion spike. Nat. Struct. Mol. Biol. 13 (2006) 751-752
3. Bosch B.J., Bartelink W., and Rottier P.J. Cathepsin L functionally cleaves the severe acute respiratory syndrome coronavirus class I fusion protein upstream of rather than adjacent to the fusion peptide. J. Virol. 82 (2008) 8887-8890
4. Cameron M.J., Ran L., Xu L., Danesh A., Bermejo-Martin J.F., Cameron C.M., Muller M.P., Gold W.L., Richardson S.E., Poutanen S.M., Willey B.M., DeVries M.E., Fang Y., Seneviratne C., Bosinger S.E., Persad D., Wilkinson P., Greller L.D., Somogyi R., Humar A., Keshavjee S., Louie M., Loeb M.B., Brunton J., McGeer A.J., Kelvin D.J., and The Canadian SARS Research Network. Interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in patients with severe acute respiratory syndrome. J. Virol. 81 (2007) 8692-8706
5. Chang Y.J., Liu C.Y.-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 (2004) 7602-7614
6. Chen J., and Subbarao K. The immunobiology of SARS. Ann. Rev. Immunol. 25 (2007) 443-447
7. Cheung C.Y., Poon L.L., Ng I.H., Luk W., Sia S.F., Wu M.H., Chan K.H., Yuen K.Y., Gordon S., Guan Y., and Peiris J.S. Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis. J. Virol. 79 (2005) 7819-7826
8. Collins A.R. In vitro detection of apoptosis in monocytes/macrophages infected with human coronavirus 229E. Clin. Diag. Lab. Immunol. 9 (2002) 1392-1395
9. Collins A.R., and Grubb A. Cystatin D, a natural salivary cysteine protease inhibitor, inhibits coronavirus replication at its physiologic concentration. Oral Microbiol. Immunol. 13 (1998) 59-61
10. Corver J., Broer R., van Kasteren P., and Spaan W. GxxxG motif of severe acute respiratory syndrome coronavirus spike glycoprotein transmembrane domain is not involved in trimerization and is not important for entry. J. Virol. 81 (2007) 8352-8355
11. Davis J.N., Kucuk O., Djuric Z., and Sarkar F.H. Soy isoflavone supplementation in healthy men prevents NF-κB activation by TNF-α in blood lymphocytes. Free Radic. Biol. Med. 30 (2001) 1293-1302
12. Du L., Kao R.Y., Zhou Y., He Y., Zhao G., Wong C., Jiang S., Yuen K.Y., Jin D.Y., and Zheng B.J. Cleavage of spike protein of SARS coronavirus by protease factor Xa is associated with viral infectivity. Biochem. Biophys. Res. Commun. 359 (2007) 174-179
13. Elass E., Aubry L., Masson M., Denys A., Guérardel Y., Maes E., Legrand D., Mazurier J., and Kremer L. Mycobacterial lipomannan induces matrix metalloproteinase-9 expression in human macrophagic cells through a Toll-like receptor 1 (TLR1)/TLR2- and CD14-dependent mechanism. Infect. Immun. 73 (2005) 7064-7068
14. Fan J., Ye R.D., and Malik A.B. Transcriptional mechanisms of acute lung injury. Am. J. Physiol. Lung. Cell. Mol. Physiol. 281 (2001) 1037-1050
15. Finberg R.W., Wang J.P., and Kurt-Jones E.A. Toll like receptors and viruses. Rev. Med. Virol. 17 (2007) 35-43
16. Frieman M., Heise M., and Baric R. SARS coronavirus and innate immunity. Virus Res. 133 (2008) 101-112
17. He Y., Zhou Y., Siddiqui P., and Jiang S. Inactivated SARS-CoV vaccine elicits high titers of spike protein-specific antibodies that block receptor binding and virus entry. Bioch. Biophys. Res. Commun. 325 (2004) 445-452
18. He L., Ding Y., Zhang Q., Che X., He Y., Shen H., Wang H., Li Z., Zhao L., Geng J., Deng Y., Yang L., Li J., Cai J., Qiu L., Wen K., Xu X., and Jiang S. 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 (2006) 288-297
19. He, L., Ding,Y.Q., Wang, W., Zhang, Q.L., Zhang, J.H., Geng, J., Cai, J.J., 2003. Expression of immune cells and their roles in the involved tissues of SARS patients. [Article in Chinese] Di Yi Jun Yi Da Xue Xue Bao. 8, 774-6, 780.
20. Henkel T., Machleidt T., Alkalay I., Krönke M., Ben-Neriah Y., and Baeuerle P.A. Rapid proteolysis of IκB-α is necessary for activation of transcription factor NF-κB. Nature 365 (1993) 182-185
21. Hillian A.D., Londono D., Dunn J.M., Goddard K.A., Pace R.G., Knowles M.R., Drumm M.L., and CF Gene Modifier Study Group. Modulation of cystic fibrosis lung disease by variants in interleukin-8. Genes Immun. 9 (2008) 501-508
22. 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. Emerg. Infect. Dis. 10 (2004) 489-493
23. Huang I.C., Bosch B.J., Li F., Li W., Lee K.H., Ghiran S., Vasilieva N., Dermody T.S., Harrison S.C., Dormitzer P.R., Farzan M., Rottier P.J., and Choe H. SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J. Biol Chem. 281 (2006) 3198-3203
24. Inoue Y., Tanaka N., Tanaka Y., Inoue S., Morita K., Zhuang M., Hattori T., and Sugamura K. Clathrin-dependent entry of severe acute respiratory syndrome coronavirus into target cells expressing ACE2 with the cytoplasmic tail deleted. J. Virol. 81 (2007) 8722-8729
25. Jovasevic V., Liang L., and Roizman B. Proteolytic cleavage of VP1-2 is required for release of herpes simplex virus 1 DNA into the nucleus. J. Virol. 82 (2008) 3311-3319
26. Kawase M., Shirato K., Matsuyama S., and Taguchi F. Protease-mediated entry via the endosome of human coronavirus 229E. J. Virol. 83 (2009) 712-721
27. Li F., Berardi M., Li W., Farzan M., Dormitzer P.R., and Harrison S.C. Conformational states of the severe acute respiratory syndrome coronavirus spike protein ectodomainn. J. Virol. 80 (2006) 6794-6800
28. Li L., Wo J., Shao J., Zhu H., Wu N., Li M., Yao H., Hu M., and Dennin R.H. SARS-coronavirus replicates in mononuclear cells of peripheral blood (PBMCs) from SARS patients. J. Clin. Virol. 28 (2003) 239-244
29. 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 (2003) 450-454
30. Li Q., and Verma I.M. NF-kappaB regulation in the immune system. Nat. Rev. Immunology 2 (2002) 725-743
31. Luo Z., Matthews A.M., and Weiss S.R. Amino acid substitutions within the leucine zipper domain of the murine coronavirus spike protein cause defects in oligomerization and the ability to induce cell-to-cell fusion. J. Virol. 73 (1999) 8152-8159
32. Maeda J., Repass J.F., Maeda A., and Makino S. Membrane topology of coronavirus E protein. Virology 281 (2001) 163-169
33. Mahajan S.D., Schwartz S.A., Aalinkeel R., Chawda R.P., Sykes D.E., and Nair M.P. Morphine modulates chemokine gene regulation in normal human astrocytes. Clin. Immunol. 115 (2005) 323-332
34. Mizzen L., Daya M., and Anderson R. The role of protease-dependent cell membrane fusion in persistent and lytic infections of murine hepatitis virus. Adv. Exp. Biol. Med. 218 (1986) 175-186
35. Pulford D.J., and Britton P. Intracellular processing of the porcine coronavirus transmissible gastroenteritic virus spike protein expressed by recombinant vaccinia virus. Virology 182 (1991) 765-773
36. Reghunathan R., Jayapal M., Hsu L.Y., Chng H.H., Tai D., Leung B.P., and Melendez A.J. Expression profile of immune response genes in patients with Severe Acute Respiratory Syndrome. BMC Immunol. 6 (2005) 2
37. Rosenau C., Emery D., Kaboord B., and Qaranfleh M.W. Development of a high throughput plate-based chemiluminescent transcription factor assay. J. Biomol. Screen. 9 (2004) 334-342
38. Shao H., Lan D., Duan Z., Liu Z., Min J., Zhang L., Huang J., Su J., Chen S., and Xu A. Upregulation of mitochondrial gene expression in PBMC from convalescent SARS patients. J. Clin. Immunol. 26 (2006) 546-554
39. Song H.C., Seo M.Y., Stadler K., Yoo B.J., Choo Q.L., Coates S.R., Uematsu Y., Harada T., Greer C.E., Polo J.M., Pileri P., Eickmann M., Rappuoli R., Abrignani S., Houghton M., and Han J.H. Synthesis and characterization of a native, oligomeric form of recombinant severe acute respiratory syndrome coronavirus spike glycoprotein. J. Virol. 78 (2004) 10328-10335
40. Sui J., Li W., Murakami A., Tamin A., Matthews L.J., Wong S.K., Moore M.J., Tallarico A.S., Olurinde M., Choe H., Anderson L.J., Bellini W.J., Farzan M., and Marasco W.A. Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2536-2541
41. Thorp E.B., Boscarino J.A., Logan H.L., Goletz J.T., and Gallagher T.M. Palmitoylations on murine coronavirus spike proteins are essential for virion assembly and infectivity. J. Virol. 80 (2006) 1280-1289
42. 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 (2005) 7977-7985
43. Uematsu S., and Akria S. Toll-like receptors and type I interferons. J. Biol. Chem. 282 (2007) 15319-15324
44. Versteeg G.A., van de Nes P.S., Breedenbeek P.J., and Spaan W.J.M. The coronavirus spike protein induces endoplasmic reticulum stress and upregulation of intracellular chemokine mRNA concentrations. J. Virol. 8 (2007) 10981-10990
45. Walsh K.B., Lodoen M.B., Edwards R.A., Lanier L.L., and Lane T.E. Evidence for differential roles for NKG2D receptor signaling in innate host defense against coronavirus-induced neurological and liver disease. J. Virol. 82 (2008) 3021-3030
46. Wang W., Ye L., Ye L., Li B., Gao B., Zeng Y., Kong L., Fang X., Zheng H., Wu Z., and She Y. Up-regulation of IL-6 and TNF-α induced by SARS-coronavirus spike protein in murine macrophages via NF-κB pathway. Virus Res. 128 (2007) 1-8
47. Wolk D.M. WS-18. Basic Biostatistics for Clinical Microbiologists (2008), American Society for Microbiology General Meeting, Boston MA
48. Yeager C.L., Ashmun R.A., Williams R.K., Cardellichio C.B., Shapiro L.H., Look A.T., and Holmes K.V. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357 (1992) 420-422
49. 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 (2005) 5037-5043
50. Zhu H., Dinsdale D., Alnemri E.S., and Cohen G.M. Apoptosis in human monocytic THP.1 cells involves several distinct targets of N-tosyl-L-phenylalanyl chloromethyl ketone (TPCK). Cell Death Differ. 4 (1997) 590-599