Characterization of cellular furin content as a potential factor determining the susceptibility of cultured human and animal cells to coronavirus infectious bronchitis virus infection

Virology

Volumn 433, Issue 2, 2012, Pages 421-430

  Tay, Felicia P L ^a   Huang, Mei ^a   Wang, Li ^a   Yamada, Yoshiyuki ^a   Xiang Liu, Ding ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Coronavirus infectious bronchitis virus; Furin; Human and animal cell lines; Spike protein; Susceptibility

Indexed keywords

FURIN; SPIKE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; AVIAN INFECTIOUS BRONCHITIS VIRUS; CELL CULTURE; CELL STRAIN H1299; CELL STRAIN HEP3B; CELL STRAIN HEPG2; CELL STRAIN HUH7; CONTROLLED STUDY; CORONAVIRUS INFECTION; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; VERO CELL;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; CORONAVIRUS INFECTIONS; FURIN; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFECTIOUS BRONCHITIS VIRUS; MEMBRANE GLYCOPROTEINS; NUCLEOCAPSID PROTEINS; RNA, SMALL INTERFERING; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRAL MATRIX PROTEINS; VIRUS CULTIVATION;

ANIMALIA; AVIAN INFECTIOUS BRONCHITIS VIRUS; CORONAVIRUS;

EID: 84867215031     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.08.037     Document Type: Article

References (42)

1. Belouzard S., Chu V.C., Whittaker G.R. Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(14):5871-5876.
2. Bosshart H., Humphrey J., Deignan E., Davidson J., Drazba J., Yuan L., Oorschot V., Peters P.J., Bonifacino J.S. The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system. J. Cell Biol. 1994, 126:1157-1172.
3. Butler N., Pewe L., Trandem K., Perlman S. Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology 2006, 347:401-421.
4. Cavanagh D. Coronavirus avian infectious bronchitis virus. Vet. Res. 2007, 38:281-297.
5. Chen H.Y., Guo A.Z., Peng B., Zhang M.F., Guo H.Y., Chen H.C. Infection of HeLa cells by avian infectious bronchitis virus is dependent on cell status. Avian Pathol. 2007, 36:269-274.
6. Chu V.C., McElroy L.J., Chu V., Bauman B.E., Whittaker G.R. The avian coronavirus infectious bronchitis virus undergoes direct low-pH-dependent fusion activation during entry into host cells. J. Virol. 2006, 80:3180-3188.
7. Coutelier J.P., Godfraind C., Dveksler G.S., Wysocka M., Cardellichio C.B., Noel H., Holmes K.V. B lymphocyte and macrophage expression of carcinoembryonic antigen-related adhesion molecules that serve as receptors for murine coronavirus. Eur. J. Immunol. 1994, 24:1383-1390.
8. Curtis B.M., Scharnowske S., Watson A.J. Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:8356-8360.
9. Delmas B., Gelfi J., L'Haridon R., Vogel L.K., Sjostrom H., Noren O., Laude H. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 1992, 357:417-420.
10. Dveksler G.S., Pensiero M.N., Cardellichio C.B., Williams R.K., Jiang G.S., Holmes K.V., Dieffenbach C.W. Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J. Virol. 1991, 65:6881-6891.
11. Fang S.G., Chen B., Tay F.P.L., Liu D.X. An arginine-to-proline mutation in a domain with undefined functions within the helicase protein (NSP13) is lethal to the coronavirus infectious bronchitis virus in cultured cells. Virology 2007, 358:136-147.
12. Fang S.G., Shen S., Tay F.P.L., Liu D.X. Selection of and recombination between minor variants lead to the adaptation of an avian coronavirus to primate cells. Biochem. Biophys. Res. Commun. 2005, 336(417-423).
13. Geijtenbeek T.B., Kwon D.S., Torensma R., van Vliet S.J., van Duijnhoven G.C., Middel J., Cornelissen I.L., Nottet H.S., KewalRamani V.N., Littman D.R., Figdor C.G., van Kooyk Y. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000, 100:587-597.
14. Godfraind C., Langreth S.G., Cardellichio C.B., Knobler R., Coutelier J.P., Dubois-Dalcq M., Holmes K.V. Tissue and cellular distribution of an adhesion molecule in the carcinoembryonic antigen family that serves as a receptor for mouse hepatitis virus. Lab. Invest. 1995, 73:615-627.
15. Gough R.E., Cox W.J., Winkler C.E., Sharp M.W., Spackman D. Isolation and identification of infectious bronchitis virus from pheasants. Vet. Rec. 1996, 138:208-209.
16. Guan Y., Zheng B.J., He Y.Q., Liu X.L., Zhuang Z.X., Cheung C.L., Luo S.W., Li P.H., Zhang L.J., Guan Y.J., Butt K.M., Wong K.L., Chan K.W., Lim W., Shortridge K.F., Yuen K.Y., Peiris J.S., Poon L.L. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 2003, 302:276-278.
17. Halary F., Amara A., Lortat-Jacob H., Messerle M., Delaunay T., Houlès C., Fieschi F., Arenzana-Seisdedos F., Moreau J.F., Déchanet-Merville J. Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity 2002, 17:653-664.
18. Hofmann H., Pyrc K., van der Hoek L., Geier M., Berkhout B., Pohlmann S. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7988-7993.
19. Jeffers S.A., Tusell S.M., Gillim-Ross L., Hemmila E.M., Achenbach J.E., Babcock G.J., Thomas W.D., Thackray L.B., Young M.D., Mason R.J., Ambrosino D.M., Wentworth D.E., Demartini J.C., Holmes K.V. CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:15748-15753.
20. Li F.Q., Xiao H., Tam J.P., Liu D.X. Sumoylation of the nucleocapsid protein of severe acute respiratory syndrome coronavirus. FEBS Lett. 2005, 579:2387-2396.
21. 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., Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003, 426:450-454.
22. Liu D.X., Tibbles K.W., Cavanagh D., Brown T.D.K., Brierley I. Identification, expression and processing of an 87K polypeptide encoded by ORF1a of the coronavirus infectious bronchitis virus. Virology 1995, 208:48-57.
23. Miguel B., Pharr G.T., Wang C. The role of feline aminopeptidase N as a receptor for infectious bronchitis virus. Arch. Virol. 2002, 147:2047-2056.
24. Molloy S.S., Thomas L., VanSlyke J.K., Stenberg P.E., Thomas G. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J. 1994, 13:18-33.
25. Otsuki K., Noro K., Yamamoto H., Tsubokura M. Studies on avian infectious bronchitis virus (IBV). II. Propagation of IBV in several cultured cells. Arch. Virol. 1979, 60:115-122.
26. Pohlmann S., Zhang J., Baribaud F., Chen Z., Leslie G.J., Lin G., Granelli-Piperno A., Doms R.W., Rice C.M., McKeating J.A. Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J. Virol. 2003, 77:4070-4080.
27. Shen H., Fang S.G., Chen B., Chen G., Tay F.P., Liu D.X. Towards construction of viral vectors based on avian coronavirus infectious bronchitis virus for gene delivery and vaccine development. J. Virol. Methods 2009, 160:48-56.
28. Shen S., Law Y.C., Liu D.X. A single amino acid mutation in the spike protein of coronavirus infectious bronchitis virus hampers its maturation and incorporation into virions at the nonpermissive temperature. Virology 2004, 326:288-298.
29. Shen S., Wen Z.L., Liu D.X. Emergence of a coronavirus infectious bronchitis virus mutant with a truncated 3b gene: functional characterization of the 3b protein in pathogenesis and replication. Virololgy 2003, 311:16-27.
30. Snijder B., Sacher R., Rämö P., Damm E.M., Liberali P., Pelkmans L. Population context determines cell-to-cell variability in endocytosis and virus infection. Nature 2009, 461:520-523.
31. Tassaneetrithep B., Burgess T.H., Granelli-Piperno A., Trumpfheller C., Finke J., Sun W., Eller M.A., Pattanapanyasat K., Sarasombath S., Birx D.L., Steinman R.M., Schlesinger S., Marovich M.A. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 2003, 197:823-829.
32. Tan Y.W., Hong W., Liu D.X. Binding of the 5'-untranslated region of coronavirus RNA to zinc finger CCHC-type and RNA binding motif 1 enhances viral replication and transcription. Nucleic Acids Res. 2012, 40:5065-5077.
33. Tresnan D.B., Levis R., Holmes K.V. Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J. Virol. 1996, 70:8669-8674.
34. Williams R.K., Jiang G.S., Holmes K.V. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:5533-5536.
35. Winter C., Schwegmann-Wessels C., Cavanagh D., Neumann U., Herrler G. Sialic acid is a receptor determinant for infection of cells by avian infectious bronchitis virus. J. Gen. Virol. 2006, 87:1209-1216.
36. Winter C., Herrler G., Neumann U. Infection of the tracheal epithelium by infectious bronchitis virus is sialic acid dependent. Microbes Infect. 2008, 10:367-373.
37. Xu L., Khadijah S., Fang S., Wang L., Tay F.P., Liu D.X. The cellular RNA helicase DDX1 interacts with coronavirus nonstructural protein 14 and enhances viral replication. J. Virol. 2010, 84:8571-8583.
38. Xu L.H., Huang M., Fang S.G., Liu D.X. Coronavirus infection induces DNA replication stress partly through interaction of its nonstructural protein 13 with the p125 subunit of DNA polymerase delta. J. Biol. Chem. 2011, 286:39546-39559.
39. Yamada Y., Liu D.X. Proteolytic activation of the spike protein at a novel RRRR/S motif is implicated in furin-dependent entry, syncytium formation, and infectivity of coronavirus infectious bronchitis virus in cultured cells. J. Virol. 2009, 83:8744-8758.
40. Yamada Y., Liu X.B., Fang S.G., Tay P.L., Liu D.X. Acquisition of cell-cell fusion activity by amino acid substitution in spike protein determines the infectivity of a coronavirus in cultured cells. PLoS ONE 2009, 4:e6130.
41. Yeager C.L., Ashmun R.A., Williams R.K., Cardellichio C.B., Shapiro L.H., Look A.T., Holmes K.V. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 1992, 357:420-422.
42. Zhang Y., Buckles E., Whittaker G.R. Expression of the C-type lectins DC-SIGN or L-SIGN alters host cell susceptibility for the avian coronavirus, infectious bronchitis virus. Vet. Microbiol. 2012, 157:285-293.