Abstract
In addition to the spike (S) glycoprotein that binds to carcinoembryonic antigen-related receptors on the host cell membrane, some strains of mouse coronavirus (mouse hepatitis virus [MHV]) express a hemagglutinin esterase (HE) glycoprotein with hemagglutinating and acetylesterase activity. Virions of strains that do not express HE, such as MHV-A59, can infect mouse fibroblasts in vitro, showing that the HE glycoprotein is not required for infection of these cells. The present work was done to study whether interaction of the HE glycoprotein with carbohydrate moieties could lead to virus entry and infection in the absence of interaction of the S glycoprotein with its receptor glycoprotein, MHVR. The DVIM strain of MHV expresses large amounts of HE glycoprotein, as shown by hemadsorption, acetylesterase activity, and immunoreactivity with antibodies directed against the HE glycoprotein of bovine coronavirus. A monoclonal anti-MHVR antibody, MAb-CC1, blocks binding of virus S glycoprotein to MHVR and blocks infection of MHV strains that do not express HE. MAb-CC1 also prevented MHV-DVIM infection of mouse DBT cells and primary mouse glial cell cultures. Although MDCK-I cells express O-acetylated sialic acid residues on their plasma membranes, these canine cells were resistant to infection with MHV-A59 and MHV-DVIM. Transfection of MDCK-I cells with MHVR cDNA made them susceptible to infection with MHV-A59 and MHV-DVIM. Thus, the HE glycoprotein of an MHV strain did not lead to infection of cultured murine neural cells or of nonmurine cells that express the carbohydrate ligand of the HE glycoprotein. Therefore, interaction of the spike glycoprotein of MHV with its carcinoembryonic antigen-related receptor glycoprotein is required for infectivity of MHV strains whether or not they express the HE glycoprotein.
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- Benjamins J. A., Callahan R. E., Montgomery I. N., Studzinski D. M., Dyer C. A. Production and characterization of high titer antibodies to galactocerebroside. J Neuroimmunol. 1987 Apr;14(3):325–338. doi: 10.1016/0165-5728(87)90019-1. [DOI] [PubMed] [Google Scholar]
- Dveksler G. S., Dieffenbach C. W., Cardellichio C. B., McCuaig K., Pensiero M. N., Jiang G. S., Beauchemin N., Holmes K. V. Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59. J Virol. 1993 Jan;67(1):1–8. doi: 10.1128/jvi.67.1.1-8.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Dyer C. A., Benjamins J. A. Redistribution and internalization of antibodies to galactocerebroside by oligodendroglia. J Neurosci. 1988 Mar;8(3):883–891. doi: 10.1523/JNEUROSCI.08-03-00883.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fuller A. O., Lee W. C. Herpes simplex virus type 1 entry through a cascade of virus-cell interactions requires different roles of gD and gH in penetration. J Virol. 1992 Aug;66(8):5002–5012. doi: 10.1128/jvi.66.8.5002-5012.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gallagher T. M., Buchmeier M. J., Perlman S. Cell receptor-independent infection by a neurotropic murine coronavirus. Virology. 1992 Nov;191(1):517–522. doi: 10.1016/0042-6822(92)90223-C. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
- Herrler G., Dürkop I., Becht H., Klenk H. D. The glycoprotein of influenza C virus is the haemagglutinin, esterase and fusion factor. J Gen Virol. 1988 Apr;69(Pt 4):839–846. doi: 10.1099/0022-1317-69-4-839. [DOI] [PubMed] [Google Scholar]
- Herrler G., Klenk H. D. The surface receptor is a major determinant of the cell tropism of influenza C virus. Virology. 1987 Jul;159(1):102–108. doi: 10.1016/0042-6822(87)90352-7. [DOI] [PubMed] [Google Scholar]
- Herrler G., Rott R., Klenk H. D., Müller H. P., Shukla A. K., Schauer R. The receptor-destroying enzyme of influenza C virus is neuraminate-O-acetylesterase. EMBO J. 1985 Jun;4(6):1503–1506. doi: 10.1002/j.1460-2075.1985.tb03809.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hirano N., Fujiwara K., Hino S., Matumoto M. Replication and plaque formation of mouse hepatitis virus (MHV-2) in mouse cell line DBT culture. Arch Gesamte Virusforsch. 1974;44(3):298–302. doi: 10.1007/BF01240618. [DOI] [PubMed] [Google Scholar]
- Hogue B. G., Brian D. A. Structural proteins of human respiratory coronavirus OC43. Virus Res. 1986 Aug;5(2-3):131–144. doi: 10.1016/0168-1702(86)90013-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- King B., Brian D. A. Bovine coronavirus structural proteins. J Virol. 1982 May;42(2):700–707. doi: 10.1128/jvi.42.2.700-707.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kruse J., Mailhammer R., Wernecke H., Faissner A., Sommer I., Goridis C., Schachner M. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature. 1984 Sep 13;311(5982):153–155. doi: 10.1038/311153a0. [DOI] [PubMed] [Google Scholar]
- La Monica N., Banner L. R., Morris V. L., Lai M. M. Localization of extensive deletions in the structural genes of two neurotropic variants of murine coronavirus JHM. Virology. 1991 Jun;182(2):883–888. doi: 10.1016/0042-6822(91)90635-O. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Lai M. M. Coronavirus: organization, replication and expression of genome. Annu Rev Microbiol. 1990;44:303–333. doi: 10.1146/annurev.mi.44.100190.001511. [DOI] [PubMed] [Google Scholar]
- Lee V. M., Page C. D., Wu H. L., Schlaepfer W. W. Monoclonal antibodies to gel-excised glial filament protein and their reactivities with other intermediate filament proteins. J Neurochem. 1984 Jan;42(1):25–32. doi: 10.1111/j.1471-4159.1984.tb09692.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Makino S., Lai M. M. Evolution of the 5'-end of genomic RNA of murine coronaviruses during passages in vitro. Virology. 1989 Mar;169(1):227–232. doi: 10.1016/0042-6822(89)90060-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McClain D. S., Fuller A. O. Cell-specific kinetics and efficiency of herpes simplex virus type 1 entry are determined by two distinct phases of attachment. Virology. 1994 Feb;198(2):690–702. doi: 10.1006/viro.1994.1081. [DOI] [PubMed] [Google Scholar]
- 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]
- Pfleiderer M., Routledge E., Herrler G., Siddell S. G. High level transient expression of the murine coronavirus haemagglutinin-esterase. J Gen Virol. 1991 Jun;72(Pt 6):1309–1315. doi: 10.1099/0022-1317-72-6-1309. [DOI] [PubMed] [Google Scholar]
- Pfleiderer M., Routledge E., Siddell S. G. Functional analysis of the coronavirus MHV-JHM surface glycoproteins in vaccinia virus recombinants. Adv Exp Med Biol. 1990;276:21–31. doi: 10.1007/978-1-4684-5823-7_4. [DOI] [PubMed] [Google Scholar]
- Rogers G. N., Herrler G., Paulson J. C., Klenk H. D. Influenza C virus uses 9-O-acetyl-N-acetylneuraminic acid as a high affinity receptor determinant for attachment to cells. J Biol Chem. 1986 May 5;261(13):5947–5951. [PubMed] [Google Scholar]
- 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]
- 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. 1992 Apr;73(Pt 4):901–906. doi: 10.1099/0022-1317-73-4-901. [DOI] [PubMed] [Google Scholar]
- 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. 1991 Jan;180(1):221–228. doi: 10.1016/0042-6822(91)90026-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shieh C. K., Lee H. J., Yokomori K., La Monica N., Makino S., Lai M. M. Identification of a new transcriptional initiation site and the corresponding functional gene 2b in the murine coronavirus RNA genome. J Virol. 1989 Sep;63(9):3729–3736. doi: 10.1128/jvi.63.9.3729-3736.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shieh M. T., WuDunn D., Montgomery R. I., Esko J. D., Spear P. G. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol. 1992 Mar;116(5):1273–1281. doi: 10.1083/jcb.116.5.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siddell S. Coronavirus JHM: coding assignments of subgenomic mRNAs. J Gen Virol. 1983 Jan;64(Pt 1):113–125. doi: 10.1099/0022-1317-64-1-113. [DOI] [PubMed] [Google Scholar]
- Siddell S., Wege H., Ter Meulen V. The biology of coronaviruses. J Gen Virol. 1983 Apr;64(Pt 4):761–776. doi: 10.1099/0022-1317-64-4-761. [DOI] [PubMed] [Google Scholar]
- 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]
- Sommer I., Schachner M. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol. 1981 Apr 30;83(2):311–327. doi: 10.1016/0012-1606(81)90477-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Spear P. G., Shieh M. T., Herold B. C., WuDunn D., Koshy T. I. Heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus. Adv Exp Med Biol. 1992;313:341–353. doi: 10.1007/978-1-4899-2444-5_33. [DOI] [PubMed] [Google Scholar]
- 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]
- Sturman L. S., Holmes K. V. Characterization of coronavirus II. Glycoproteins of the viral envelope: tryptic peptide analysis. Virology. 1977 Apr;77(2):650–660. doi: 10.1016/0042-6822(77)90489-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugiyama K., Amano Y. Hemagglutination and structural polypeptides of a new coronavirus associated with diarrhea in infant mice. Arch Virol. 1980;66(2):95–105. doi: 10.1007/BF01314978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugiyama K., Amano Y. Morphological and biological properties of a new coronavirus associated with diarrhea in infant mice. Arch Virol. 1981;67(3):241–251. doi: 10.1007/BF01318134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugiyama K., Ishikawa R., Fukuhara N. Structural polypeptides of the murine coronavirus DVIM. Arch Virol. 1986;89(1-4):245–254. doi: 10.1007/BF01309893. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szepanski S., Gross H. J., Brossmer R., Klenk H. D., Herrler G. A single point mutation of the influenza C virus glycoprotein (HEF) changes the viral receptor-binding activity. Virology. 1992 May;188(1):85–92. doi: 10.1016/0042-6822(92)90737-A. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taguchi F., Massa P. T., ter Meulen V. Characterization of a variant virus isolated from neural cell culture after infection of mouse coronavirus JHMV. Virology. 1986 Nov;155(1):267–270. doi: 10.1016/0042-6822(86)90187-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Vlasak R., Krystal M., Nacht M., Palese P. The influenza C virus glycoprotein (HE) exhibits receptor-binding (hemagglutinin) and receptor-destroying (esterase) activities. Virology. 1987 Oct;160(2):419–425. doi: 10.1016/0042-6822(87)90013-4. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Yokomori K., Banner L. R., Lai M. M. Heterogeneity of gene expression of the hemagglutinin-esterase (HE) protein of murine coronaviruses. Virology. 1991 Aug;183(2):647–657. doi: 10.1016/0042-6822(91)90994-M. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang X. M., Kousoulas K. G., Storz J. The hemagglutinin/esterase gene of human coronavirus strain OC43: phylogenetic relationships to bovine and murine coronaviruses and influenza C virus. Virology. 1992 Jan;186(1):318–323. doi: 10.1016/0042-6822(92)90089-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang X. M., Kousoulas K. G., Storz J. The hemagglutinin/esterase glycoprotein of bovine coronaviruses: sequence and functional comparisons between virulent and avirulent strains. Virology. 1991 Dec;185(2):847–852. doi: 10.1016/0042-6822(91)90557-R. [DOI] [PMC free article] [PubMed] [Google Scholar]