Acquisition of cell-cell fusion activity by amino acid substitutions in spike protein determines the infectivity of a coronavirus in cultured cells

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Yamada, Yoshiyuki ^a   Liu, Xiao Bo ^b   Fang, Shou Guo ^a   Tay, Felicia P L ^a   Liu, Ding Xiang ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE; PHENYLALANINE; VIRUS SPIKE PROTEIN; MEMBRANE PROTEIN; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRUS ENVELOPE PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FUSION; CHICKEN; CONTROLLED STUDY; CORONAVIRUS; EMBRYO; KIDNEY CELL; MEMBRANE FUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; SYNCYTIUM; VERO CELL; VIRUS VIRULENCE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; ELECTROPORATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

ANIMALIA; AVES; AVIAN INFECTIOUS BRONCHITIS VIRUS; CORONAVIRUS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BLOTTING, WESTERN; CELL FUSION; CELLS, CULTURED; CORONAVIRUS; ELECTROPORATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL ENVELOPE PROTEINS;

EID: 67650547932     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006130     Document Type: Article

References (44)

1. Lai MM, Cavanagh D (1997) The molecular biology of coronaviruses. Adv Virus Res 48: 1-100.
2. Wege H, Siddell S, Ter Meulen V (1982) The biology and pathogenesis of coronavirus. Curr Top Microbiol Immunol 99: 165-200.
3. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, et al. (2003) Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302: 276-278.
4. Li W, Shi Z, Yu M, Ren W, Smith C, et al. (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310: 676-979.
5. Butler N, Pewe L, Trandem K, Perlman S (2006) Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology 347: 401-421.
6. Sanchez CM, Gebauer F, Sune C, Mendez A, Dopazo J, et al. (1992) Genetic evolution and tropism of transmissible gastroenteritis coronaviruses. Virology 190: 92-105.
7. Vijgen L, Keyaerts E, Lemey P, Moes E, Li S, et al. (2005) Circulation of genetically distinct contemporary human coronavirus OC43 strains. Virology 337: 85-92.
8. Alonso-Caplen FV, Matsuoka Y, Wilcox GE, Compans RW (1984) Replication and morphogenesis of avian coronavirus in Vero cells and their inhibition by momensin. Virus Res 1: 153-167.
9. Cavanagh D, Davis PJ, Pappin DJC, Binns MM, Boursnell MEG, et al. (1986) Coronavirus IBV: partial amino terminal sequencing of spike polypeptide S2 identifies the sequence Arg-Arg-Phe-Arg-Arg at the cleavage site of the spike precursor propolypeptide of IBV strains Beaudette and M41. Virus Res 4: 133-143.
10. Fang SG, Shen S, Tay FPL, Liu DX (2005) Selection of and recombination between minor variants lead to the adaptation of an avian coronavirus to primate cells. Biochem Biophys Res Commun 336: 417-423.
11. Shen S, Wen L, Liu DX (2003) Emergence of an avian coronavirus infectious bronchitis virus (IBV) mutant with a truncated 3b gene: functional characterization of the 3b gene in pathogenesis and replication. Virology 311: 16-27.
12. Shen S, Law YC, Liu DX (2004) 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 326: 288-298.
13. Youn S, Leibowitz JL, Collisson EW (2005) In vitro assembled, recombinant infectious bronchitis viruses demonstrate that the 5a open reading frame is not essential for replication. Virology 332: 206-215.
14. 2/M-phase in cells infected with the coronavirus infectious bronchitis virus promotes viral replication. Virology 365: 435-445.
15. Liu DX, Inglis SC (1992) Identification of two new polypeptides encoded by mRNA5 of the coronavirus infectious bronchitis virus. Virology 186: 342-347.
16. Fang SG, Chen B, Tay FPL, Liu DX (2007) 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 358: 136-147.
17. Tan YW, Fang SG, Fan H, Lescar J, Liu DX (2006) Amino acid residues critical for RNA-binding in the N-terminal domain of the nucleocapsid protein are essential determinants for the replication and infectivity of coronavirus in cultured cells. Nucleic Acids Res 34: 4816-4825.
18. Ng LF, Liu DX (2000) Further characterization of the coronavirus infectious bronchitis virus 3C-like proteinase and determination of a new cleavage site. Virology 272: 27-39.
19. Ng LF, Liu DX (2002) Membrane association and dimerization of a cysteinerich, 16-kDa polypeptide released from the C-terminal region of the coronavirus infectious bronchitis virus 1a polyprotein. J Virol 76: 6257-6267.
20. Cavanagh D, Mawditt K, Welchman de B, Britton P, Gough RE (2002) Coronaviruses from pheasants (Phasianus colchicus) are genetically closely related to coronaviruses of domestic fowl (infectious bronchitis virus) and turkeys. Avian Pathol 31: 81-93.
21. Bosch BJ, van der Zee R, de Haan CAM, Rottier PJM (2003) The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J Virol 77: 8801-8811.
22. de Haan CAM, Li Z, te Lintelo E, Bosch BJ, Haijema BJ, Rottier PJM (2005) Murine coronavirus with an extended host range uses heparan sulfate as an entry receptor. J Virol 79: 14451-14456.
23. Dveksler GS, Pensiero MN, Cardellichio CB, Williams RK, Jiang GS, et al. (1991) Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J Virol 65: 6881-6891.
24. Tresnan DB, Levis R, Holmes KV (1996) Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J Virol 70: 8669-8674.
25. Tsai CW, Chang SC, Chang MF (1999) A 12-amino acid stretch in the hypervariable region of the spike protein S1 subunit is critical for cell fusion activity of mouse hepatitis virus. J Biol Chem 274: 26085-26090.
26. Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjostrom H, et al. (1992) Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV. Nature 357: 417-420.
27. Hofmann H, Pyrc K, van der Hoek L, Geier M, Berkhout B, et al. (2005) Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc Natl Acad Sci USA 102: 7988-7993.
28. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, et al. (2003) Angiotensinconverting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426: 450-454.
29. Williams RK, Jiang GS, Holmes KV (1991) Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc Natl Acad Sci USA 88: 5533-5536.
30. Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, et al. (1992) Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357: 420-422.
31. Winter C, Schwegmann-Wessels C, Cavanagh D, Neumann U, Herrler G (2006) Sialic acid is a receptor determinant for infection of cells by avian infectious bronchitis virus. J Gen Virol 87: 1209-1216.
32. Chen HY, Guo AZ, Peng B, Zhang MF, Guo HY, et al. (2007) Infection of HeLa cells by avian infectious bronchitis virus is dependent on cell status. Avian Pathol 36: 269-74.
33. Madu IG, Chu VC, Lee H, Regan AD, Bauman BE, et al. (2007) Heparan sulfate is a selective attachment factor for the avian coronavirus infectious bronchitis virus Beaudette. Avian Dis 51: 45-51.
34. Matsuyama S, Taguchi F (2002) Receptor-induced conformational changes of murine coronavirus spike protein. J Virol 76: 11819-11826.
35. Miura HS, Nakagaki K, Taguchi F (2004) N-terminal domain of the murine coronavirus receptor CEACAM1 is responsible for fusogenic activation and conformational changes of the spike protein. J Virol 78: 216-223.
36. Taguchi F, Ikeda T, Saeki K, Kubo H, Kikuchi T (1993) Fusogenic properties of uncleaved spike protein of murine coronavirus JHMV. Adv Exp Med Biol 342: 171-175.
37. Tsai JC, Zelus BD, Holmes KV, Weiss SR (2003) The N-terminal domain of the murine coronavirus spike glycoprotein determines the CEACAM1 receptor specificity of the virus strain. J Virol 77: 841-850.
38. Zelus BD, Schickli JH, Blau DM, Weiss SR, Holmes KV (2003) Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37°C either by soluble murine CEACAM1 receptors or by pH 8. J Virol 77: 830-840.
39. Xiao H, Xu LH, Yamada Y, Liu DX (2008) Coronavirus spike protein inhibits host cell translation by interaction with eIF3f. PloS ONE 3: e1494.
40. Xu Y, Liu Y, Lou Z, Qin L, Li X, et al. (2004) Structural basis for coronavirusmediated membrane fusion. Crystal structure of mouse hepatitis virus spike protein fusion core. J Biol Chem 279: 30514-30522.
41. Xu Y, Lou Z, Liu Y, Pang H, Tien P, et al. (2004) Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J Biol Chem 279: 49414-49419.
42. Trackray LB, Holmes KV (2004) Amino acid substitutions and an insertion in the spike glycoprotein extend the host range of the murine coronavirus MHVA59. Virology 324: 510-524.
43. Yamada YK, Takimoto K, Yabe M, Taguchi F (1997) Acquired fusion activity of a murine coronavirus MHV-2 variant with mutations in the proteolytic cleavage site and the signal sequence of the S protein. Virology 227: 215-219.
44. Winter C, Herrler G, Neumann U (2008) Infection of the tracheal epithelium by infectious bronchitis virus is sialic acid dependent. Microbes Infect 10: 367-373.