Abstract
The receptors for the hemagglutinating encephalomyelitis virus (HEV, a porcine coronavirus) on chicken erythrocytes were analyzed and compared to the receptors for bovine coronavirus (BCV) and influenza C virus. Evidence was obtained that HEV requires the presence of N-acetyl-9-O-acetylneuraminic acid (Neu5,9Ac2) on the cell surface for agglutination of erythrocytes as has been previously shown for BCV and influenza C virus: (i) Incubation of red blood cells with sialate 9-O-acetylesterase, the receptor-destroying enzyme of influenza C virus, rendered the erythrocytes resistant against agglutination by each of the three viruses; (ii) Human erythrocytes which are resistant to agglutination by HEV acquire receptors for HEV after resialylation with Neu5,9Ac2. Sialylation of red blood cells with limiting amounts of sialic acid indicated that strain JHB/1/66 of influenza C virus requires less Neu5,9Ac2 for agglutination of erythrocytes than the two coronaviruses, both of which were found to be similar in their reactivity with Neu5,9Ac2-containing receptors.
Keywords: Bovine coronavirus, Hemagglutinating encephalomyelitis virus, receptor, Sialic acid, N-acetyl-9-O-acetylneuraminic acid
References
- Bingham R.W., Madge M.H., Tyrrell D.A.J. Haemagglutination by avian infectious bronchitis virus: a coronavirus. J. Gen. Virol. 1975;28:381–390. doi: 10.1099/0022-1317-28-3-381. [DOI] [PubMed] [Google Scholar]
- 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;61:185–189. doi: 10.1128/jvi.61.1.185-189.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carroll S.C., Higa H.H., Paulson J.C. Different cell surface receptor determinants of antigenically similar influenza virus hemagglutinins. J. Biol. Chem. 1981;256:8357–8363. [PubMed] [Google Scholar]
- Dea S., Garzon S., Tijssen P. Identification and location of the structural glycoproteins of a tissue culture-adapted turkey enteric coronavirus. Arch. Virol. 1989;106:221–237. doi: 10.1007/BF01313955. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gottschalk A., Bhargava A.S., Murty V.L.N. Submaxillary gland glycoproteins. In: Gottschalk A., editor. Glycoproteins, their Composition, Structure and Function. Elsevier; Amsterdam: 1972. pp. 810–829. [Google Scholar]
- Gross H.J., Bünsch A., Paulson J.C., Brossmer R. Activation and transfer of novel synthetic 9-substituted sialic acids. Eur. J. Biochem. 1987;168:595–602. doi: 10.1111/j.1432-1033.1987.tb13458.x. [DOI] [PubMed] [Google Scholar]
- Gross H.J., Kovac A., Watzlawick H., Rose U., Brossmer R. Interaction of N-acetyl-4-epi-D-neuraminic acid with key enzymes of sialic acid metabolism. Biochemistry. 1988;27:4279–4283. doi: 10.1021/bi00412a012. [DOI] [PubMed] [Google Scholar]
- Herrler G., Rott R., Klenk H.-D. Neuraminic acid is involved in the binding of influenza C virus to erythrocytes. Virology. 1985;141:144–147. doi: 10.1016/0042-6822(85)90190-4. [DOI] [PubMed] [Google Scholar]
- Herrler G., Geyer R., Müller H.-P., Stirm S., Klenk H.-D. Rat α1-macroglobulin inhibits hemagglutination by influenza C virus. Virus Res. 1985;2:183–192. doi: 10.1016/0168-1702(85)90248-5. [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. Eur. Mol. Biol. Organ. J. 1985;4:1503–1506. doi: 10.1002/j.1460-2075.1985.tb03809.x. [DOI] [PMC free article] [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;159:102–108. doi: 10.1016/0042-6822(87)90352-7. [DOI] [PubMed] [Google Scholar]
- Herrler G., Reuter G., Rott R., Klenk H.-D., Schauer R. N-acetyl-9-O-acetylneuraminic acid, the receptor determinant for influenza C virus, is a differentiation marker on chicken erythrocytes. Biol. Chem. Hoppe-Seyler. 1987;368:451–454. doi: 10.1515/bchm3.1987.368.1.451. [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;69:839–846. doi: 10.1099/0022-1317-69-4-839. [DOI] [PubMed] [Google Scholar]
- Holloway P.W. A simple procedure for removal of Triton X-100 from protein samples. Anal. Biochem. 1973;53:304–308. doi: 10.1016/0003-2697(73)90436-3. [DOI] [PubMed] [Google Scholar]
- Kaye H.S., Dowdle W.R. Some characteristics of haemagglutination of certain strains of 'IBV-like' virus. J. Infect. Dis. 1969;120:576–581. doi: 10.1093/infdis/120.5.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- King B., Potts B.J., Brian D.A. Bovine coronavirus hemagglutinin protein. Virus Res. 1985;2:53–59. doi: 10.1016/0168-1702(85)90059-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kitame F., Nakamura K., Saito A., Sinohara H., Homma M. Isolation and characterization of influenza C virus inhibitor in rat serum. Virus Res. 1985;3:231–244. doi: 10.1016/0168-1702(85)90048-6. [DOI] [PubMed] [Google Scholar]
- Klenk H.-D., Rott R., Becht H. On the structure of the influenza virus envelope. Virology. 1972;47:579–591. doi: 10.1016/0042-6822(72)90547-8. [DOI] [PubMed] [Google Scholar]
- Luytjes W., Bredenbeek P.J., Noten A.F.H., Horzinek M.C., Spaan W.J.M. Sequence of mouse hepatitis virus A59 mRNA2: indications for RNA-recombination between coronaviruses and influenza C virus. Virology. 1988;166:415–422. doi: 10.1016/0042-6822(88)90512-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishimura H., Sugawara K., Kitame F., Nakamura K. Attachment of influenza C virus to human erythrocytes. J. Gen. Virol. 1988;69:2545–2553. doi: 10.1099/0022-1317-69-10-2545. [DOI] [PubMed] [Google Scholar]
- Noda M., Yamashita H., Koide F., Kadoi K., Omori T., Asagi M., Inaba Y. Hemag-glutination with transmissible gastroenteritis virus. Arch. Virol. 1987;96:109–115. doi: 10.1007/BF01310994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paulson J.C., Rogers G.N. Resialylated erythrocytes for assessment of the specificity of sialyloligosaccharide binding proteins. Methods Enzymol. 1987;138:162–168. doi: 10.1016/0076-6879(87)38013-9. [DOI] [PubMed] [Google Scholar]
- Pensaert M.B., Callebaut P.E. Characteristics of a coronavirus causing vomiting and wasting in pigs. Arch. Ges. Virusforsch. 1974;44:35–50. doi: 10.1007/BF01242179. [DOI] [PMC free article] [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;261:5947–5951. [PubMed] [Google Scholar]
- Sato K., Inaba Y., Kurogi H., Takahashi E., Satoda K., Omori T., Matumoto M. Haemagglutination by calf diarrhea coronavirus. Vet. Microbiol. 1977;2:83–87. [Google Scholar]
- Schauer R., Reuter G., Stoll S., Posadas del Rio F., Herrler G., Klenk H.-D. Isolation and characterization of sialate 9(4)-O-acetylesterase from influenza C virus. Biol. Chem. Hoppe-Seyler. 1988;369:1121–1130. doi: 10.1515/bchm3.1988.369.2.1121. [DOI] [PubMed] [Google Scholar]
- Shieh C.-K., Lee H.-J., Yokomori K., La Monica N., Makino S., Lai M.M.C. Identification of a new transcriptional initiation site and the corresponding functional gene 2b in the murine coronavirus RNA genome. J. Virol. 1989;63:3729–3736. doi: 10.1128/jvi.63.9.3729-3736.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shukla A.K., Schauer R. Fluorimetric determination of unsubstituted and 9(8)-O-acetylated sialic acids in erythrocyte membranes. Hoppe-Seyler's Z. Physiol. Chem. 1982;363:255–262. doi: 10.1515/bchm2.1982.363.1.255. [DOI] [PubMed] [Google Scholar]
- Sugiyama K., Amano Y. Hemagglutination and structural polypeptides of a new coronavirus associated with diarrhea in infant mice. Arch. Virol. 1980;66:95–105. doi: 10.1007/BF01314978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szepanski S., Klenk H.-D., Herrler G. Analysis of a mutant of influenza C virus with a change in the receptor specificity. In: Compans R.W., Helenius A., Oldstone M.B.A., editors. Cell Biology of Virus Entry, Replication, and Pathogenesis. Alan R. Liss, Inc; New York: 1989. pp. 125–134. [Google Scholar]
- Vlasak R., Luytjes W., Spaan W., Palese P. Vol. 85. 1988. Human and bovine coronaviruses recognize sialic acid containing receptors similar to those of influenza C viruses; pp. 4526–4529. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- The E3 protein of bovine coronavirus is a receptor-destroying enzyme with acetylesterase activityJ. Virol. 1988;62:4686–4690. doi: 10.1128/jvi.62.12.4686-4690.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]