Substitutions of conserved amino acids in the receptor-binding domain of the spike glycoprotein affect utilization of murine CEACAM1a by the murine coronavirus MHV-A59

Virology

Volumn 334, Issue 1, 2005, Pages 98-110

  Thackray, Larissa B ^a,b   Turner, Brian C ^a,c   Holmes, Kathryn V ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

CEACAM1a; Host range; Murine coronavirus; Mutations; Receptor binding domain; Receptor specificity; Spike glycoprotein

Indexed keywords

AMINO ACID; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; GLYCOPROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CORONAVIRUS; GENE TARGETING; HYDROPHOBICITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BINDING; RNA RECOMBINATION; VIRUS STRAIN; WILD TYPE;

EID: 14644404228     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2005.01.016     Document Type: Article

References (62)

1. G.J. Babcock, D.J. Esshaki, W.D. Thomas, and D.M. Ambrosino Amino acids 270 to 510 of the severe acute respiratory syndrome coronavirus spike protein are required for interaction with receptor J. Virol. 78 2004 4552 4560
2. R.S. Baric, E. Sullivan, L. Hensley, B. Yount, and W. Chen Persistent infection promotes cross-species transmissibility of mouse hepatitis virus J. Virol. 73 1999 638 649
3. A.A. Bogan, and K.S. Thorn Anatomy of hot spots in protein interfaces J. Mol. Biol. 280 1998 1 9
4. A. Bonavia, B.D. Zelus, D.E. Wentworth, P.J. Talbot, and K.V. Holmes Identification of a receptor-binding domain of the spike glycoprotein of human coronavirus HCoV-229E J. Virol. 77 2003 2530 2538
5. M.P. Bos, D. Hogan, and R.J. Belland Homologue scanning mutagenesis reveals CD66 receptor residues required for neisserial Opa protein binding J. Exp. Med. 190 1999 331 340
6. B.J. Bosch, R. van der Zee, C.A.M. de Haan, and P.J.M. Rottier The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex J. Virol. 77 2003 8801 8811
7. J.J. Breslin, I. Mork, M.K. Smith, L.K. Vogel, E.M. Hemmila, A. Bonavia, P.J. Talbot, H. Sjostrom, O. Noren, and K.V. Holmes Human coronavirus 229E: receptor binding domain and neutralization by soluble receptor at 37 degrees C J. Virol. 77 2003 4435 4438
8. A. Carfi, S.H. Willis, J.C. Whitbeck, C. Krummenacher, G.H. Cohen, R.J. Eisenberg, and D.C. Wiley Herpes simplex virus glycoprotein D bound to the human receptor HveA Mol. Cell 8 2001 169 179
9. S.R. Compton, C.B. Stephensen, S.W. Snyder, D.G. Weismiller, and K.V. Holmes Coronavirus species specificity-Murine coronavirus binds to a mouse-specific epitope on its carcinoembryonic antigen-related receptor glycoprotein J. Virol. 66 1992 7420 7428
10. S.A. Connolly, D.J. Landsburg, A. Carfi, D.C. Wiley, G.H. Cohen, and R.J. Eisenberg Structure-based mutagenesis of herpes simplex virus glycoprotein D defines three critical regions at the gD-HveA/HVEM binding interface J. Virol. 77 2003 8127 8140
11. J. Das Sarma, E. Scheen, S.H. Seo, M. Koval, and S.R. Weiss Enhanced green fluorescent protein expression may be used to monitor murine coronavirus spread in vitro and in the mouse central nervous system J. Neurovirol. 8 2002 381 391
12. R.A. Davey, Y. Zuo, and J.M. Cunningham Identification of a receptor-binding pocket on the envelope protein of friend murine leukemia virus J. Virol. 73 1999 3758 3763
13. B. Delmas, J. Gelfi, R. Lharidon, L.K. Vogel, H. Sjostrom, O. Noren, and H. Laude Aminopeptidase-N is a major receptor for the enteropathogenic coronavirus Tgev Nature 357 1992 417 420
14. G.S. Dveksler, M.N. Pensiero, C.B. Cardellichio, R.K. Williams, G.S. Jiang, K.V. Holmes, and C.W. Dieffenbach Cloning of the mouse hepatitis-virus (Mhv) receptor-Expression in human and hamster-cell lines confers susceptibility to Mhv J. Virol. 65 1991 6881 6891
15. G.S. Dveksler, C.W. Dieffenbach, C.B. Cardellichio, K. Mccuaig, M.N. Pensiero, G.S. Jiang, N. Beauchemin, and K.V. Holmes Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59 J. Virol. 67 1993 1 8
16. G.S. Dveksler, M.N. Pensiero, C.W. Dieffenbach, C.B. Cardellichio, A.A. Basile, P.E. Elia, and K.V. Holmes Mouse hepatitis-virus strain-A59 and blocking antireceptor monoclonal-antibody bind to the N-terminal domain of cellular receptor Proc. Natl. Acad. Sci. U.S.A. 90 1993 1716 1720
17. S. Gagneten, O. Gout, M. Duboisdalcq, P. Rottier, J. Rossen, and K.V. Holmes Interaction of mouse hepatitis-virus (Mhv) spike glycoprotein with receptor glycoprotein Mhvr is required for infection with an Mhv strain that expresses the hemagglutinin-esterase glycoprotein J. Virol. 69 1995 889 895
18. S. Gagneten, C.A. Scanga, G.S. Dveksler, N. Beauchemin, D. Percy, and K.V. Holmes Attachment glycoproteins and receptor specificity of rat coronaviruses Lab. Anim. Sci. 46 1996 159 166
19. T.M. Gallagher A role for naturally occurring variation of the murine coronavirus spike protein in stabilizing association with the cellular receptor J. Virol. 71 1997 3129 3137
20. T.M. Gallagher, and M.J. Buchmeier Coronavirus spike proteins in viral entry and pathogenesis Virology 279 2001 371 374
21. E. Hemmila, C. Turbide, M. Olson, S. Jothy, K.V. Holmes, and N. Beauchemin Ceacam1a(-/-) mice are completely resistant to infection by murine coronavirus mouse hepatitis virus A59 J. Virol. 78 2004 10156 10165
22. H. Kubo, Y.K. Yamada, and F. Taguchi Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino-acids of the murine coronavirus spike protein J. Virol. 68 1994 5403 5410
23. L.L. Kuo, G.J. Godeke, M.J.B. Raamsman, P.S. Masters, and P.J.M. Rottier Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier J. Virol. 74 2000 1393 1406
24. P.D. Kwong, R. Wyatt, J. Robinson, R.W. Sweet, J. Sodroski, and W.A. Hendrickson Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody Nature 393 1998 648 659
25. M.M.C. Lai, and K.V. Holmes Coronaviridae and their replication D. Knipe 4th edition Fields Virol. vols. 1 and 2 2001 Lippincott Williams and Wilkins Philadelphia 1163 1185
26. I. Leparc-Goffart, S.T. Hingley, M.M. Chua, J. Phillips, E. Lavi, and S.R. Weiss Targeted recombination within the spike gene of murine coronavirus mouse hepatitis virus-A59: Q159 is a determinant of hepatotropism J. Virol. 72 1998 9628 9636
27. D.N. Lewicki, and T.M. Gallagher Quaternary structure of coronavirus spikes in complex with carcinoembryonic antigen-related cell adhesion molecule cellular receptors J. Biol. Chem. 277 2002 19727 19734
28. W. Li, M.J. Moore, N. Vasilieva, J. Sui, S.K. Wong, M.A. Berne, M. Somasundaran, J.L. Sullivan, K. Luzuriaga, T.C. Greenough, H. Choe, and M. Farzan Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus Nature 426 2003 450 454
29. S.W. Liu, G.F. Xiao, Y.B. Chen, Y.X. He, J.K. Niu, C.R. Escalante, H.B. Xiong, J. Farmar, A.K. Debnath, P. Tien, and S.B. Jiang Interaction between heptad repeat 1 and 2 regions in spike protein of SARS-associated coronavirus: implications for virus fusogenic mechanism and identification of fusion inhibitors Lancet 363 2004 938 947
30. S. Matsuyama, and F. Taguchi Impaired entry of soluble receptor-resistant mutants of mouse hepatitis virus into cells expressing MHVR2 receptor Virology 273 2000 80 89
31. S. Matsuyama, and F. Taguchi Receptor-induced conformational changes of murine coronavirus spike protein J. Virol. 76 2002 11819 11826
32. H.S. Miura, K. Nakagaki, and F. Taguchi N-terminal domain of the murine coronavirus receptor CEACAM1 is responsible for fusogenic activation and conformational changes of the spike protein J. Virol. 78 2004 216 223
33. E. Ontiveros, T.S. Kim, T.M. Gallagher, and S. Perlman Enhanced virulence mediated by the murine coronavirus, mouse hepatitis virus strain JHM, is associated with a glycine at residue 310 of the spike glycoprotein J. Virol. 77 2003 10260 10269
34. J.J. Phillips, M. Chua, S.H. Seo, and S.R. Weiss Multiple regions of the murine coronavirus spike glycoprotein influence neurovirulence J. Neurovirol. 7 2001 421 431
35. P.V. Rao, and T.M. Gallagher Intracellular complexes of viral spike and cellular receptor accumulate during cytopathic murine coronavirus infections J. Virol. 72 1998 3278 3288
36. P.V. Rao, S. Kumari, and T.M. Gallagher Identification of a contiguous 6-residue determinant in the MHV receptor that controls the level of virion binding to cells Virology 229 1997 336 348
37. K. Saeki, N. Ohtsuka, and F. Taguchi Identification of spike protein residues of murine coronavirus responsible for receptor-binding activity by use of soluble receptor-resistant mutants J. Virol. 71 1997 9024 9031
38. S.G. Sawicki, J.H. Lu, and K.V. Holmes Persistent infection of cultured-cells with mouse hepatitis-virus (Mhv) results from the epigenetic expression of the Mhv receptor J. Virol. 69 1995 5535 5543
39. J.H. Schickli, B.D. Zelus, D.E. Wentworth, S.G. Sawicki, and K.V. Holmes The murine coronavirus mouse hepatitis virus strain A59 from persistently infected murine cells exhibits an extended host range J. Virol. 71 1997 9499 9507
40. J.H. Schickli, L.B. Thackray, S.G. Sawicki, and K.V. Holmes The N-terminal region of the murine coronavirus spike glycoprotein is associated with the extended host range of viruses from persistently infected murine cells J. Virol. 78 2004 9073 9083
41. S. Shen, Y.C. Law, and D.X. Liu 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 2004 288 298
42. H. Suzuki, and F. Taguchi Analysis of receptor-binding site of murine coronavirus spike protein J. Virol. 70 1996 2632 2636
43. K.M. Tan, B.D. Zelus, R. Meijers, J.H. Liu, J.M. Bergelson, N. Duke, R. Zhang, A. Joachimiak, K.V. Holmes, and J.H. Wang Crystal structure of murine sCEACAM1a[1,4]: a coronavirus receptor in the CEA family EMBO J. 21 2002 2076 2086
44. L.B. Thackray, and K.V. Holmes Amino acid substitutions and an insertion in the spike glycoprotein extend the host range of the murine coronavirus MHV-A59 Virology 324 2004 510 524
45. B. Tripet, M.W. Howard, M. Jobling, R.K. Holmes, K.V. Holmes, and R.S. Hodges Structural characterization of the SARS-coronavirus spike S fusion protein core J. Biol. Chem. 279 2004 20836 20849
46. J.C. Tsai, B.D. Zelus, K.V. Holmes, and S.R. Weiss The N-terminal domain of the murine coronavirus spike glycoprotein determines the CEACAM1 receptor specificity of the virus strain J. Virol. 77 2003 841 850
47. M. Virji, D. Evans, A. Hadfield, F. Grunert, A.M. Teixeira, and S.M. Watt Critical determinants of host receptor targeting by Neisseria meningitides and Neisseria gonorrhoeae: identification of Opa adhesiotopes on the N-domain of CD66 molecules Mol. Microbiol. 34 1999 538 551
48. J.H. Wang Protein recognition by cell surface receptors: physiological receptors versus virus interactions Trends Biochem. Sci. 27 2002 122 126
49. S.M. Watt, A.M. Teixeira, G.Q. Zhou, R. Doyonnas, Y. Zhang, F. Grunert, R.S. Blumberg, M. Kuroki, K.M. Skubitz, and P.A. Bates Homophilic adhesion of human CEACAM1 involves N-terminal domain interactions: structural analysis of the binding site Blood 98 2001 1469 1479
50. D.E. Wentworth, and K.V. Holmes Molecular determinants of species specificity in the coronavirus receptor aminopeptidase N (CD13): influence of N-linked glycosylation J. Virol. 75 2001 9741 9752
51. D.R. Wessner, P.C. Shick, J.H. Lu, C.B. Cardellichio, S.E. Gagneten, N. Beauchemin, K.V. Holmes, and G.S. Dveksler Mutational analysis of the virus and monoclonal antibody binding sites in MHVR, the cellular receptor of the murine coronavirus mouse hepatitis virus strain A59 J. Virol. 72 1998 1941 1948
52. R.K. Williams, G.S. Jiang, S.W. Snyder, M.F. Frana, and K.V. Holmes Purification of the 110-kilodalton glycoprotein receptor for mouse hepatitis-virus (Mhv)-A59 from mouse-liver and identification of a nonfunctional, homologous protein in Mhv-resistant Sjl/J mice J. Virol. 64 1990 3817 3823
53. S.K. Wong, W.H. Li, M.J. Moore, H. Choe, and M. Farzan A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2 J. Biol. Chem. 279 2004 3197 3201
54. H. Wu, D.G. Myszka, S.W. Tendian, C.G. Brouillette, R.W. Sweet, I.M. Chaiken, and W.A. Hendrickson Kinetic and structural analysis of mutant CD4 receptors that are defective in HIV gp120 binding Proc. Natl. Acad. Sci. U.S.A. 93 1996 15030 15035
55. X.D. Xiao, S. Chakraborti, A.S. Dimitrov, K. Gramatikoff, and D.S. Dimitrov The SARS-CoV S glycoprotein: expression and functional characterization Biochem. Biophys. Res. Commun. 312 2003 1159 1164
56. Y.H. Xu, Y.W. Liu, Z.Y. Lou, L. Qin, X. Li, Z.H. Bai, H. Pang, P. Tien, G.F. Gao, and Z. Rao Structural basis for coronavirus-mediated membrane fusion-Crystal structure of mouse hepatitis virus spike protein fusion core J. Biol. Chem. 279 2004 30514 30522
57. C.L. Yeager, R.A. Ashmun, R.K. Williams, C.B. Cardellichio, L.H. Shapiro, A.T. Look, and K.V. Holmes Human aminopeptidase-N is a receptor for human coronavirus-229e Nature 357 1992 420 422
58. K. Yokomori, and M.M.C. Lai Mouse hepatitis-virus utilizes 2 carcinoembryonic antigens as alternative receptors J. Virol. 66 1992 6194 6199
59. K. Yokomori, L.R. Banner, and M.M.C. Lai Heterogeneity of gene-expression of the hemagglutinin-esterase (He) protein of murine coronaviruses Virology 183 1991 647 657
60. B.D. Zelus, D.R. Wessner, R.K. Williams, M.N. Pensiero, F.T. Phibbs, M. deSouza, G.S. Dveksler, and K.V. Holmes Purified, soluble recombinant mouse hepatitis virus receptor, bgp1(b), and bgp2 murine coronavirus receptors differ in mouse hepatitis virus binding and neutralizing activities J. Virol. 72 1998 7237 7244
61. B.D. Zelus, J.H. Schickli, D.M. Blau, S.R. Weiss, and K.V. Holmes Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37 degrees C either by soluble murine CEACAM1 receptors or by pH 8 J. Virol. 77 2003 830 840
62. Y.M. Zhang, J.C. Rassa, M.E. deObaldia, L.M. Albritton, and S.R. Ross Identification of the receptor binding domain of the mouse mammary tumor virus envelope protein J. Virol. 77 2003 10468 10478