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. 1992 Dec;66(12):7420–7428. doi: 10.1128/jvi.66.12.7420-7428.1992

Coronavirus species specificity: murine coronavirus binds to a mouse-specific epitope on its carcinoembryonic antigen-related receptor glycoprotein.

S R Compton 1, C B Stephensen 1, S W Snyder 1, D G Weismiller 1, K V Holmes 1
PMCID: PMC240449  PMID: 1279203

Abstract

Like most coronaviruses, the coronavirus mouse hepatitis virus (MHV) exhibits strong species specificity, causing natural infection only in mice. MHV-A59 virions use as a receptor a 110- to 120-kDa glycoprotein (MHVR) in the carcinoembryonic antigen (CEA) family of glycoproteins (G. S. Dveksler, M. N. Pensiero, C. B. Cardellichio, R. K. Williams, G. S. Jiang, K. V. Holmes, and C. W. Dieffenbach, J. Virol. 65:6881-6891, 1991; and R. K. Williams, G. S. Jiang, and K. V. Holmes, Proc. Natl. Acad. Sci. USA 88:5533-5536, 1991). The role of virus-receptor interactions in determining the species specificity of MHV-A59 was examined by comparing the binding of virus and antireceptor antibodies to cell lines and intestinal brush border membranes (BBM) from many species. Polyclonal antireceptor antiserum (anti-MHVR) raised by immunization of SJL/J mice with BALB/c BBM recognized MHVR specifically in immunoblots of BALB/c BBM but not in BBM from adult SJL/J mice that are resistant to infection with MHV-A59, indicating a major difference in epitopes between MHVR and its SJL/J homolog which does not bind MHV (7). Anti-MHVR bound to plasma membranes of MHV-susceptible murine cell lines but not to membranes of human, cat, dog, monkey, or hamster cell lines. Cell lines from these species were resistant to MHV-A59 infection, and only the murine cell lines tested were susceptible. Pretreatment of murine fibroblasts with anti-MHVR prevented binding of radiolabeled virions to murine cells and prevented virus infection. Solid-phase virus-binding assays and virus overlay protein blot assays showed that MHV-A59 virions bound to MHVR on intestinal BBM from MHV-susceptible mouse strains but not to proteins on intestinal BBM from humans, cats, dogs, pigs, cows, rabbits, rats, cotton rats, or chickens. In immunoblots of BBM from these species, both polyclonal and monoclonal antireceptor antibodies that block MHV-A59 infection of murine cells recognized only the murine CEA-related glycoprotein and not homologous CEA-related glycoproteins of other species. These results suggest that MHV-A59 binds to a mouse-specific epitope of MHVR, and they support the hypothesis that the species specificity of MHV-A59 infection may be due to the specificity of the virus-receptor interaction.

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Selected References

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  1. Bang F. B., Warwick A. MOUSE MACROPHAGES AS HOST CELLS FOR THE MOUSE HEPATITIS VIRUS AND THE GENETIC BASIS OF THEIR SUSCEPTIBILITY. Proc Natl Acad Sci U S A. 1960 Aug;46(8):1065–1075. doi: 10.1073/pnas.46.8.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barnett T. R., Kretschmer A., Austen D. A., Goebel S. J., Hart J. T., Elting J. J., Kamarck M. E. Carcinoembryonic antigens: alternative splicing accounts for the multiple mRNAs that code for novel members of the carcinoembryonic antigen family. J Cell Biol. 1989 Feb;108(2):267–276. doi: 10.1083/jcb.108.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beauchemin N., Turbide C., Afar D., Bell J., Raymond M., Stanners C. P., Fuks A. A mouse analogue of the human carcinoembryonic antigen. Cancer Res. 1989 Apr 15;49(8):2017–2021. [PubMed] [Google Scholar]
  4. Bhatt P. N., Percy D. H., Jonas A. M. Characterization of the virus of sialodacryoadenitis of rats: a member of the coronavirus group. J Infect Dis. 1972 Aug;126(2):123–130. doi: 10.1093/infdis/126.2.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Binn L. N., Marchwicki R. H., Stephenson E. H. Establishment of a canine cell line: derivation, characterization, and viral spectrum. Am J Vet Res. 1980 Jun;41(6):855–860. [PubMed] [Google Scholar]
  6. Boyle J. F., Weismiller D. G., Holmes K. V. Genetic resistance to mouse hepatitis virus correlates with absence of virus-binding activity on target tissues. J Virol. 1987 Jan;61(1):185–189. doi: 10.1128/jvi.61.1.185-189.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  8. Delmas B., Gelfi J., L'Haridon R., Vogel L. K., Sjöström H., Norén O., Laude H. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature. 1992 Jun 4;357(6377):417–420. doi: 10.1038/357417a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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 Dec;65(12):6881–6891. doi: 10.1128/jvi.65.12.6881-6891.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. The major human rhinovirus receptor is ICAM-1. Cell. 1989 Mar 10;56(5):839–847. doi: 10.1016/0092-8674(89)90688-0. [DOI] [PubMed] [Google Scholar]
  11. Hinoda Y., Neumaier M., Hefta S. A., Drzeniek Z., Wagener C., Shively L., Hefta L. J., Shively J. E., Paxton R. J. Molecular cloning of a cDNA coding biliary glycoprotein I: primary structure of a glycoprotein immunologically crossreactive with carcinoembryonic antigen. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6959–6963. doi: 10.1073/pnas.85.18.6959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kessler M., Acuto O., Storelli C., Murer H., Müller M., Semenza G. A modified procedure for the rapid preparation of efficiently transporting vesicles from small intestinal brush border membranes. Their use in investigating some properties of D-glucose and choline transport systems. Biochim Biophys Acta. 1978 Jan 4;506(1):136–154. doi: 10.1016/0005-2736(78)90440-6. [DOI] [PubMed] [Google Scholar]
  13. King B., Potts B. J., Brian D. A. Bovine coronavirus hemagglutinin protein. Virus Res. 1985 Feb;2(1):53–59. doi: 10.1016/0168-1702(85)90059-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Knobler R. L., Tunison L. A., Oldstone M. B. Host genetic control of mouse hepatitis virus type 4 (JHM strain) replication. I. Restriction of virus amplification and spread in macrophages from resistant mice. J Gen Virol. 1984 Sep;65(Pt 9):1543–1548. doi: 10.1099/0022-1317-65-9-1543. [DOI] [PubMed] [Google Scholar]
  15. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  16. Lin S. H., Guidotti G. Cloning and expression of a cDNA coding for a rat liver plasma membrane ecto-ATPase. The primary structure of the ecto-ATPase is similar to that of the human biliary glycoprotein I. J Biol Chem. 1989 Aug 25;264(24):14408–14414. [PubMed] [Google Scholar]
  17. Luytjes W., Bredenbeek P. J., Noten A. F., Horzinek M. C., Spaan W. J. Sequence of mouse hepatitis virus A59 mRNA 2: indications for RNA recombination between coronaviruses and influenza C virus. Virology. 1988 Oct;166(2):415–422. doi: 10.1016/0042-6822(88)90512-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McIntosh K., Kapikian A. Z., Hardison K. A., Hartley J. W., Chanock R. M. Antigenic relationships among the coronaviruses of man and between human and animal coronaviruses. J Immunol. 1969 May;102(5):1109–1118. [PubMed] [Google Scholar]
  19. Mendelsohn C. L., Wimmer E., Racaniello V. R. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell. 1989 Mar 10;56(5):855–865. doi: 10.1016/0092-8674(89)90690-9. [DOI] [PubMed] [Google Scholar]
  20. Messer M., Dahlqvist A. A one-step ultramicro method for the assay of intestinal disaccharidases. Anal Biochem. 1966 Mar;14(3):376–392. doi: 10.1016/0003-2697(66)90280-6. [DOI] [PubMed] [Google Scholar]
  21. Morris V. L., Tieszer C., Mackinnon J., Percy D. Characterization of coronavirus JHM variants isolated from Wistar Furth rats with a viral-induced demyelinating disease. Virology. 1989 Mar;169(1):127–136. doi: 10.1016/0042-6822(89)90048-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Parker J. C., Cross S. S., Rowe W. P. Rat coronavirus (RCV): a prevalent, naturally occurring pneumotropic virus of rats. Arch Gesamte Virusforsch. 1970;31(3):293–302. doi: 10.1007/BF01253764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Percy D. H., Bond S. J., Paturzo F. X., Bhatt P. N. Duration of protection from reinfection following exposure to sialodacryoadenitis virus in Wistar rats. Lab Anim Sci. 1990 Mar;40(2):144–149. [PubMed] [Google Scholar]
  24. Percy D. H., Lynch J. A., Descôteaux J. P. Central nervous system lesions in suckling mice and rats inoculated intranasally with sialodacryoadenitis virus. Vet Pathol. 1986 Jan;23(1):42–49. doi: 10.1177/030098588602300107. [DOI] [PubMed] [Google Scholar]
  25. Percy D. H., Wojcinski Z. W., Schunk M. K. Sequential changes in the harderian and exorbital lacrimal glands in Wistar rats infected with sialodacryoadenitis virus. Vet Pathol. 1989 May;26(3):238–245. doi: 10.1177/030098588902600308. [DOI] [PubMed] [Google Scholar]
  26. Percy D., Bond S., MacInnes J. Replication of sialodacryoadenitis virus in mouse L-2 cells. Arch Virol. 1989;104(3-4):323–333. doi: 10.1007/BF01315553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. RUBINO A., ZIMBALATTI F., AURICCHIO S. INTESTINAL DISACCHARIDASE ACTIVITIES IN ADULT AND SUCKLING RATS. Biochim Biophys Acta. 1964 Nov 22;92:305–311. doi: 10.1016/0926-6569(64)90187-7. [DOI] [PubMed] [Google Scholar]
  28. Rudert F., Zimmermann W., Thompson J. A. Intra- and interspecies analyses of the carcinoembryonic antigen (CEA) gene family reveal independent evolution in primates and rodents. J Mol Evol. 1989 Aug;29(2):126–134. doi: 10.1007/BF02100111. [DOI] [PubMed] [Google Scholar]
  29. 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. 1991 Nov;65(11):6232–6237. doi: 10.1128/jvi.65.11.6232-6237.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shulman M., Wilde C. D., Köhler G. A better cell line for making hybridomas secreting specific antibodies. Nature. 1978 Nov 16;276(5685):269–270. doi: 10.1038/276269a0. [DOI] [PubMed] [Google Scholar]
  31. Smith A. L., Cardellichio C. B., Winograd D. F., de Souza M. S., Barthold S. W., Holmes K. V. Monoclonal antibody to the receptor for murine coronavirus MHV-A59 inhibits viral replication in vivo. J Infect Dis. 1991 Apr;163(4):879–882. doi: 10.1093/infdis/163.4.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith M. S., Click R. E., Plagemann P. G. Control of mouse hepatitis virus replication in macrophages by a recessive gene on chromosome 7. J Immunol. 1984 Jul;133(1):428–432. [PubMed] [Google Scholar]
  33. Sorensen O., Dugre R., Percy D., Dales S. In vivo and in vitro models of demyelinating disease: endogenous factors influencing demyelinating disease caused by mouse hepatitis virus in rats and mice. Infect Immun. 1982 Sep;37(3):1248–1260. doi: 10.1128/iai.37.3.1248-1260.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Spaan W., Cavanagh D., Horzinek M. C. Coronaviruses: structure and genome expression. J Gen Virol. 1988 Dec;69(Pt 12):2939–2952. doi: 10.1099/0022-1317-69-12-2939. [DOI] [PubMed] [Google Scholar]
  35. Staunton D. E., Merluzzi V. J., Rothlein R., Barton R., Marlin S. D., Springer T. A. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell. 1989 Mar 10;56(5):849–853. doi: 10.1016/0092-8674(89)90689-2. [DOI] [PubMed] [Google Scholar]
  36. Stohlman S. A., Frelinger J. A., Weiner L. P. Resistance to fatal central nervous system disease by mouse hepatitis virus, strain JHM. II. Adherent cell-mediated protection. J Immunol. 1980 Apr;124(4):1733–1739. [PubMed] [Google Scholar]
  37. Sturman L. S., Holmes K. V., Behnke J. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J Virol. 1980 Jan;33(1):449–462. doi: 10.1128/jvi.33.1.449-462.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sturman L. S., Takemoto K. K. Enhanced growth of a murine coronavirus in transformed mouse cells. Infect Immun. 1972 Oct;6(4):501–507. doi: 10.1128/iai.6.4.501-507.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Taguchi F., Siddell S. G., Wege H., ter Meulen V. Characterization of a variant virus selected in rat brains after infection by coronavirus mouse hepatitis virus JHM. J Virol. 1985 May;54(2):429–435. doi: 10.1128/jvi.54.2.429-435.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Thompson J. A., Mauch E. M., Chen F. S., Hinoda Y., Schrewe H., Berling B., Barnert S., von Kleist S., Shively J. E., Zimmermann W. Analysis of the size of the carcinoembryonic antigen (CEA) gene family: isolation and sequencing of N-terminal domain exons. Biochem Biophys Res Commun. 1989 Feb 15;158(3):996–1004. doi: 10.1016/0006-291x(89)92821-0. [DOI] [PubMed] [Google Scholar]
  41. Toofanian F., Hill F. W., Kidder D. E. The development of the intestinal disaccharidase activities in the fetal and newborn calf. Res Vet Sci. 1974 May;16(3):375–381. [PubMed] [Google Scholar]
  42. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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. 1988 Dec;62(12):4686–4690. doi: 10.1128/jvi.62.12.4686-4690.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Vogel S. N., Havell E. A., Spitalny G. L. Monoclonal antibody-mediated inhibition of interferon-gamma-induced macrophage antiviral resistance and surface antigen expression. J Immunol. 1986 Apr 15;136(8):2917–2923. [PubMed] [Google Scholar]
  45. Wege H., Siddell S., ter Meulen V. The biology and pathogenesis of coronaviruses. Curr Top Microbiol Immunol. 1982;99:165–200. doi: 10.1007/978-3-642-68528-6_5. [DOI] [PubMed] [Google Scholar]
  46. Wege H., Watanabe R., ter Meulen V. Coronavirus JHM infection of rats as a model for virus induced demyelinating encephalomyelitis. Prog Clin Biol Res. 1984;146:13–22. [PubMed] [Google Scholar]
  47. White J. M., Littman D. R. Viral receptors of the immunoglobulin superfamily. Cell. 1989 Mar 10;56(5):725–728. doi: 10.1016/0092-8674(89)90674-0. [DOI] [PubMed] [Google Scholar]
  48. 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 Jul 1;88(13):5533–5536. doi: 10.1073/pnas.88.13.5533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Williams R. K., Jiang G. S., Snyder S. W., Frana M. F., Holmes K. V. 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. 1990 Aug;64(8):3817–3823. doi: 10.1128/jvi.64.8.3817-3823.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. 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 Jun 4;357(6377):420–422. doi: 10.1038/357420a0. [DOI] [PMC free article] [PubMed] [Google Scholar]

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