Sialic acids as receptor determinants for coronaviruses (original) (raw)

References

  1. 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 357, 417–20 (1992)
    Article CAS PubMed Google Scholar
  2. 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 357, 420–22 (1992)
    Article CAS PubMed Google Scholar
  3. 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. 70, 8669–74 (1996)
    CAS PubMed Google Scholar
  4. 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. 65, 6881–91 (1991)
    CAS PubMed Google Scholar
  5. 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 426, 450–54 (2003)
    CAS PubMed Google Scholar
  6. Wang, P., Chen, J., Zheng, A., Nie, Y., Shi, X., Wang, W., Wang, G., Luo, M., Liu, H., Tan, L., Song, X., Wang, Z., Yin, X., Qu, X., Wang, X., Qing, T., Ding, M., Deng, H.: Expression cloning of functional receptor used by SARS coronavirus. Biochem. Biophys. Res. Commun. 315, 439–44 (2004)
    CAS PubMed Google Scholar
  7. Vlasak, R., Luytjes, W., Spaan, W., Palese, P.: Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc. Natl Acad Sci USA 85, 4526–29 (1988)
    CAS PubMed Google Scholar
  8. Herrler, G., Rott, R., Klenk, H.D., Muller, H.P., Shukla, A.K., Schauer, R.: The receptor-destroying enzyme of influenza C virus is neuraminate-O-acetylesterase. EMBO J. 4, 1503–06 (1985)
    CAS PubMed Google Scholar
  9. Vlasak, R., Luytjes, W., Leider, J., Spaan, W., Palese, P.: The E3 protein of bovine coronavirus is a receptor-destroying enzyme with acetylesterase activity. J. Virol. 62, 4686–90 (1988)
    CAS PubMed Google Scholar
  10. Schultze, B., Wahn, K., Klenk, H.D., Herrler, G.: Isolated HE-protein from hemagglutinating encephalomyelitis virus and bovine coronavirus has receptor-destroying and receptor-binding activity. Virology. 180, 221–28 (1991)
    Article CAS PubMed Google Scholar
  11. Yokomori, K., La, Monica, N., Makino, S., Shieh, C.K., Lai, M.M.: Biosynthesis, structure, and biological activities of envelope protein gp65 of murine coronavirus. Virology. 173, 683–91 (1989)
    Article CAS PubMed Google Scholar
  12. Sugiyama, K., Kasai, M., Kato, S., Kasai, H., Hatakeyama, K.: Haemagglutinin-esterase protein (HE) of murine corona virus: DVIM (diarrhea virus of infant mice). Arch. Virol 143, 1523–34 (1998)
    Article CAS PubMed Google Scholar
  13. Klausegger, A., Strobl, B., Regl, G., Kaser, A., Luytjes, W., Vlasak, R.: Identification of a coronavirus hemagglutinin-esterase with a substrate specificity different from those of influenza C virus and bovine coronavirus. J. Virol. 73, 3737–43 (1999)
    CAS PubMed Google Scholar
  14. Regl, G., Kaser, A., Iwersen, M., Schmid, H., Kohla, G., Strobl B., Vilas U., Schauer, R., Vlasak, R.: The hemagglutinin-esterase of mouse hepatitis virus strain S is a sialate-4-O-acetylesterase. J. Virol. 73, 4721–27 (1999)
    CAS PubMed Google Scholar
  15. Smits, S.L., Gerwig, G.J., van Vliet, A.L., Lissenberg, A., Briza, P., Kamerling, J.P., Vlasak, R., de Groot, R.J.: Nidovirus sialate-O-acetylesterases: Evolution and substrate specificity of coronaviral and toroviral receptor-destroying enzymes. J. Biol. Chem. 280, 6933–41 (2005)
    Article CAS PubMed Google Scholar
  16. Strasser, P., Unger, U., Strobl, B., Vilas, U., Vlasak, R.: Recombinant viral sialate-O-acetylesterases. Glycoconj. J. 20, 551–61 (2004)
    CAS PubMed Google Scholar
  17. Wurzer, W.J., Obojes, K., Vlasak, R.: The sialate-4-O-acetylesterases of coronaviruses related to mouse hepatitis virus: A proposal to reorganize group 2 Coronaviridae. J. Gen. Virol. 83, 395–402 (2002)
    CAS PubMed Google Scholar
  18. Rinninger, A., Richet C., Pons, A., Kohla, G., Schauer, R., Bauer, H., Zanetta, J., Vlasak, R.: Localisation and distribution of O-acetylated N-acetylneuraminic acids, the endogenous substrates of the hemagglutinin-esterases of murine coronaviruses, in mouse tissue. Glycoconj. J. (2005)
  19. Air, G.M., Laver, W.G.: The neuraminidase of influenza virus. Proteins 6, 341–56 (1989)
    Article CAS PubMed Google Scholar
  20. Hofling, K., Brossmer, R., Klenk, H., Herrler, G.: Transfer of an esterase-resistant receptor analog to the surface of influenza C virions results in reduced infectivity due to aggregate formation. Virology. 218, 127–33 (1996)
    CAS PubMed Google Scholar
  21. Hofling, K., Klenk, H.D., Herrler, G.: Inactivation of inhibitors by the receptor-destroying enzyme of influenza C virus. J. Gen. Virol. 78(Pt 3), 567–70 (1997)
    PubMed Google Scholar
  22. Lin, X.Q., Chouljenko, V.N., Kousoulas, K.G., Storz, J.: Temperature-sensitive acetylesterase activity of haemagglutinin-esterase specified by respiratory bovine coronaviruses. J. Med. Microbiol. 49, 1119–27 (2000)
    CAS PubMed Google Scholar
  23. Storz, J., Zhang, X.M., Rott, R.: Comparison of hemagglutinating, receptor-destroying, and acetylesterase activities of avirulent and virulent bovine coronavirus strains. Arch. Virol. 125, 193-204 (1992)
    Article CAS PubMed Google Scholar
  24. Matrosovich, M.N., Matrosovich, T.Y., Gray, T., Roberts, N.A., Klenk, H.D.: Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J. Virol. 78, 12665–67 (2004)
    Article CAS PubMed Google Scholar
  25. Yokomori, K., Asanaka, M., Stohlman, S.A., Makino, S., Shubin, R.A., Gilmore, W., Weiner, L.P., Wang, F.I., Lai, M.M.: Neuropathogenicity of mouse hepatitis virus JHM isolates differing in hemagglutinin-esterase protein expression. J. Neurovirol. 1, 330–39 (1995)
    CAS PubMed Google Scholar
  26. Bingham, R.W., Madge, M.H., Tyrrell, D.A.: Haemagglutination by avian infectious bronchitis virus-a coronavirus. J. Gen. Virol. 28, 381–90 (1975)
    CAS PubMed Google Scholar
  27. Pokorny, J., Bruckova, M., Ryc, M.: Biophysical properties of coronavirus strain OC 43. Acta. Virol. 19, 137–42 (1975)
    CAS PubMed Google Scholar
  28. Herrler, G., Klenk, H.D.: The surface receptor is a major determinant of the cell tropism of influenza C virus. Virology. 159, 102–08 (1987)
    Article CAS PubMed Google Scholar
  29. Schultze, B., Herrler, G.: Bovine coronavirus uses N-acetyl-9-O-acetylneuraminic acid as a receptor determinant to initiate the infection of cultured cells. J. Gen. Virol. 73(Pt 4), 901–06 (1992)
    CAS PubMed Google Scholar
  30. Lin, X., O'Reilly, K.L., Storz, J.: Infection of polarized epithelial cells with enteric and respiratory tract bovine coronaviruses and release of virus progeny. Am. J. Vet. Res. 58, 1120–24 (1997)
    CAS PubMed Google Scholar
  31. Schultze, B., Zimmer, G., Herrler, G.: Virus entry into a polarized epithelial cell line (MDCK): Similarities and dissimilarities between influenza C virus and bovine coronavirus. J. Gen. Virol. 77(Pt 10), 2507–14 (1996)
    CAS PubMed Google Scholar
  32. Rossen, J.W., Bekker, C.P., Voorhout, W.F., Strous, G.J., van der, E.A., Rottier, P.J.: Entry and release of transmissible gastroenteritis coronavirus are restricted to apical surfaces of polarized epithelial cells. J. Virol. 68, 7966–73 (1994)
    CAS PubMed Google Scholar
  33. Rossen, J.W., Voorhout, W.F., Horzinek, M.C., van der, E.A., Strous, G.J., Rottier, P.J.: MHV-A59 enters polarized murine epithelial cells through the apical surface but is released basolaterally. Virology. 210, 54–66 (1995)
    Article CAS PubMed Google Scholar
  34. Wang, G., Deering, C., Macke, M., Shao, J., Burns, R., Blau, D.M., Holmes, K.V., Davidson, B.L., Perlman, S., McCray, P.B., Jr.: Human coronavirus 229E infects polarized airway epithelia from the apical surface. J. Virol. 74, 9234–39 (2000)
    CAS PubMed Google Scholar
  35. King, B., Potts, B.J., Brian, D.A.: Bovine coronavirus hemagglutinin protein. Virus. Res. 2, 53–59 (1985)
    Article CAS PubMed Google Scholar
  36. Yoo, D., Graham, F.L., Prevec, L., Parker, M.D., Benko, M., Zamb T., Babiuk, L.A.: Synthesis and processing of the haemagglutinin-esterase glycoprotein of bovine coronavirus encoded in the E3 region of adenovirus. J. Gen. Virol. 73(Pt 10), 2591–600 (1992)
    CAS PubMed Google Scholar
  37. Schultze, B., Gross, H.J., Brossmer, R., Herrler, G.: The S protein of bovine coronavirus is a hemagglutinin recognizing 9-O-acetylated sialic acid as a receptor determinant. J. Virol. 65, 6232–37 (1991)
    CAS PubMed Google Scholar
  38. Laver, WG., Colman, P.M., Webster, R.G., Hinshaw, V.S., Air, G.M.: Influenza virus neuraminidase with hemagglutinin activity. Virology. 137, 314–23 (1984)
    Article CAS PubMed Google Scholar
  39. Hooper, B.E., Haelterman, E.O.: Lesions of the gastrointestinal tract of pigs infected with transmissible gastroenteritis. Can. J. Comp. Med. 33, 29–36 (1969)
    CAS PubMed Google Scholar
  40. Pensaert, M.B., Haelterman, E.O., Burnstein, T.: Transmissible gastroenteritis of swine: Virus-intestinal cell interactions. I. Immunofluorescence, histopathology and virus reproduction in the small intestine through the course of the infection. Arch. gesamte Virusforsch 31, 321–34 (1970)
    CAS PubMed Google Scholar
  41. Ballesteros, M.L., Sanchez, C.M., Enjuanes, L.: Two amino acid changes at the N-terminus of transmissible gastroenteritis coronavirus spike protein result in the loss of enteric tropism. Virology 227, 378–88 (1997)
    Article CAS PubMed Google Scholar
  42. Bernard, S., Laude, H.: Site-specific alteration of transmissible gastroenteritis virus spike protein results in markedly reduced pathogenicity. J. Gen. Virol. 76 (Pt 9), 2235–41 (1995)
    CAS PubMed Google Scholar
  43. Sanchez, C.M., Izeta, A., Sanchez-Morgado, J.M., Alonso, S., Sola, I., Balasch, M., Plana-Duran, J., Enjuanes, L.: Targeted recombination demonstrates that the spike gene of transmissible gastroenteritis coronavirus is a determinant of its enteric tropism and virulence. J. Virol. 73, 7607–18 (1999)
    CAS PubMed Google Scholar
  44. Krempl, C., Schultze, B., Laude, H., Herrler, G.: Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J. Virol. 71, 3285–87 (1997)
    CAS PubMed Google Scholar
  45. Pensaert, M.B., Callebaut, P., Vergote, J.: Isolation of a porcine respiratory, non-enteric coronavirus related to transmissible gastroenteritis. Vet. Q. 8, 257–61 (1986)
    CAS PubMed Google Scholar
  46. Rasschaert, D., Duarte, M., Laude, H.: Porcine respiratory coronavirus differs from transmissible gastroenteritis virus by a few genomic deletions. J. Gen. Virol. 71(Pt 11), 2599–607 (1990)
    CAS PubMed Google Scholar
  47. Sanchez, C.M., Gebauer, F., Sune, C., Mendez, A., Dopazo J., Enjuanes L.: Genetic evolution and tropism of transmissible gastroenteritis coronaviruses. Virology. 190, 92–105 (1992)
    CAS PubMed Google Scholar
  48. Wesley, R.D., Woods, R.D., Cheung, A.K.: Genetic analysis of porcine respiratory coronavirus, an attenuated variant of transmissible gastroenteritis virus. J. Virol 65, 3369–73 (1991)
    CAS PubMed Google Scholar
  49. Delmas, B., Gelfi, J., Sjostrom, H., Noren, O., Laude, H.: Further characterization of aminopeptidase-N as a receptor for coronaviruses. Adv. Exp. Med. Biol. 342, 293–98 (1993)
    CAS PubMed Google Scholar
  50. Godet, M., Grosclaude, J., Delmas, B., Laude, H.: Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J. Virol. 68, 8008–16 (1994)
    CAS PubMed Google Scholar
  51. Schultze, B., Krempl, C., Ballesteros, M.L., Shaw, L., Schauer, R., Enjuanes, L., Herrler, G.: Transmissible gastroenteritis coronavirus, but not the related porcine respiratory coronavirus, has a sialic acid (N-glycolylneuraminic acid) binding activity. J. Virol. 70, 5634–37 (1996)
    CAS PubMed Google Scholar
  52. Cox, E., Pensaert, M.B., Callebaut, P., Van Deun, K.: Intestinal replication of a porcine respiratory coronavirus closely related antigenically to the enteric transmissible gastroenteritis virus. Vet. Microbiol. 23, 237–43 (1990)
    Article CAS PubMed Google Scholar
  53. Noda, M., Yamashita, H., Koide, F., Kadoi, K., Omori, T., Asagi M., Inaba, Y.: Hemagglutination with transmissible gastroenteritis virus. Arch. Virol. 96, 109–15 (1987)
    Article CAS PubMed Google Scholar
  54. Noda, M., Koide, F., Asagi, M., Inaba, Y.: Physicochemical properties of transmissible gastroenteritis virus hemagglutinin. Arch. Virol. 99, 163–72 (1988)
    Article CAS PubMed Google Scholar
  55. Schultze, B., Enjuanes, L., Cavanagh, D., Herrler, G.: N-acetylneuraminic acid plays a critical role for the haemagglutinating activity of avian infectious bronchitis virus and porcine transmissible gastroenteritis virus. Adv. Exp. Med. Biol. 342, 305–10 (1993)
    CAS PubMed Google Scholar
  56. Krempl, C., Herrler, G.: Sialic acid binding activity of transmissible gastroenteritis coronavirus affects sedimentation behavior of virions and solubilized glycoproteins. J. Virol. 75, 844–49 (2001)
    Article CAS PubMed Google Scholar
  57. Schultze, B., Enjuanes, L., Herrler, G.: Analysis of the sialic acid-binding activity of the transmissible gastroenteritis virus. Adv. Exp. Med. Biol. 380, 367–70 (1995)
    CAS PubMed Google Scholar
  58. Krempl, C., Ballesteros, M.L., Enjuanes, L., Herrler G.: Isolation of hemagglutination-defective mutants for the analysis of the sialic acid binding activity of transmissible gastroenteritis virus. Adv. Exp. Med. Biol. 440, 563–68 (1998)
    CAS PubMed Google Scholar
  59. Krempl, C., Ballesteros, M.L., Zimmer, G., Enjuanes, L., Klenk, H.D., Herrler, G.: Characterization of the sialic acid binding activity of transmissible gastroenteritis coronavirus by analysis of haemagglutination-deficient mutants. J. Gen. Virol. 81, 489–96 (2000)
    CAS PubMed Google Scholar
  60. Ono, E., Abe, K., Nakazawa, M., Naiki, M.: Ganglioside epitope recognized by K99 fimbriae from enterotoxigenic Escherichia coli. Infect. Immun. 57, 907–11 (1989)
    CAS PubMed Google Scholar
  61. Teneberg, S., Willemsen, P., de Graaf, F.K., Karlsson, K.A.: Receptor-active glycolipids of epithelial cells of the small intestine of young and adult pigs in relation to susceptibility to infection with Escherichia coli K99. FEBS Lett. 263, 10–14 (1990)
    Article CAS PubMed Google Scholar
  62. Schwegmann, C., Zimmer, G., Yoshino, T., Enss, M., Herrler, G.: Comparison of the sialic acid binding activity of transmissible gastroenteritis coronavirus and E. coli K99. Virus. Res. 75, 69–73 (2001)
    Article CAS PubMed Google Scholar
  63. Schwegmann-Wessels, C., Zimmer, G., Laude, H., Enjuanes, L., Herrler G.: Binding of transmissible gastroenteritis coronavirus to cell surface sialoglycoproteins. J. Virol. 76, 6037–43 (2002)
    Article CAS PubMed Google Scholar
  64. Schwegmann-Wessels, C., Zimmer, G., Schroder, B., Breves, G., Herrler G.: Binding of transmissible gastroenteritis coronavirus to brush border membrane sialoglycoproteins. J. Virol. 77., 11846–48 (2003)
    Article CAS PubMed Google Scholar
  65. Schultze, B., Cavanagh, D., Herrler, G.: Neuraminidase treatment of avian infectious bronchitis coronavirus reveals a hemagglutinating activity that is dependent on sialic acid-containing receptors on erythrocytes. Virology. 189, 792–94 (1992)
    Article CAS PubMed Google Scholar

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