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. 1998 Oct 6;46(1):157–170. doi: 10.1016/S0168-1702(96)01398-6

Expression and distribution of the receptors for coxsackievirus B3 during fetal development of the Balb/c mouse and of their brain cells in culture

Ruliang Xu 1,∗, Richard L Crowell 1
PMCID: PMC7133877  PMID: 9029788

Abstract

This study was designed mainly to determine the relationships between the expression and distribution of the cellular receptor proteins for coxsackievirus B3 (CVB3) and susceptibility of mouse brain cells during fetal development of Balb/c mice. Immunoblot analysis of fetal extracts demonstrated that the CVB3 receptor proteins were first expressed at day 14 of the fetal stage, and that maximal expression of the cellular receptor occurred at near term or newborn stage. Results also suggested that newborn mouse brain tissue expressed much larger quantities of viral receptor proteins, compared to other tissues. In vitro studies showed that both mouse neurons and astrocytes could be infected by two CVB3 strains, pantropic CVB3 Nancy strain (CVB3N) and myocardiotropic CVB3 Woodruff strain (CVB3W). CVB3N, however, replicated and grew to high titer in primary astrocyte cultures and in primary neuron cultures, whereas, primary astrocyte cultures were relatively resistant to CVB3W. Virus binding assays revealed that CVB3N bound faster and in greater amounts to mouse brain cells than CVBW. These two virus strains, however, were found to share the same receptor specificity by virus competition assays. The number of virus binding sites for CVB3 on newborn mouse brain cells was approximately 1.8 × 104 per cell. The data suggested that preferential expression of the cellular receptors on newborn mouse brain cells may be related to their high susceptibilities to CVB3 infection.

Keywords: Coxsackievirus B3, Cellular receptors, Astrocytes, Neurons, Newborn Balb/c mice, Immunoblot

References

  1. Almond J.W. The attenuation of poliovirus neurovirulence. Ann. Rev. Microbiol. 1987;41:153–180. doi: 10.1146/annurev.mi.41.100187.001101. [DOI] [PubMed] [Google Scholar]
  2. Bergelson J.M., Mohanty J.G., Crowell R.L., St. John N.F., Lublin D.M., Finberg R.W. Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55) J. Virol. 1995;69:1903–1906. doi: 10.1128/jvi.69.3.1903-1906.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beatrice S.T., Katze M.G., Zajac B.A., Crowell R.L. Induction of neutralizing antibodies by the coxsackievirus B3 virion polypeptide, VP2. Virology. 1980;104:426–438. doi: 10.1016/0042-6822(80)90345-1. [DOI] [PubMed] [Google Scholar]
  4. Chapman N.M., Tu Z., Hufnagel G., Tracy S., Romero J.R., Barry W.H., Zhao L., Currey K. Determination of genetics and mechanism of coxsackievirus B3 cardiovirulence. Abstract of the 1995 American Society for Microbiology General Meeting; Washington, DC, 21–25 May, 1995; 1995. p. 583. [Google Scholar]
  5. Colonno R.J., Condra J.H., Mizutani S., Callahan P.L., Davies M.E., Murcko M.A. Vol. 85. 1988. Evidence for the direct involvement of the rhinovirus canyon in receptor binding; pp. 5449–5453. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crowell R.L. Specific cell-surface alteration by enteroviruses as reflected by viral-attachment interference. J. Bacteriol. 1966;91:198–204. doi: 10.1128/jb.91.1.198-204.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crowell R.L., Field A.K., Schleif W.A., Long W.L., Colonno R.J., Maploes J.E., Emini E.A. Monoclonal antibody that inhibits infection of HeLa and rhabdomyosarcoma cells by selected enteroviruses through receptor blockade. J. Virol. 1986;57:438–445. doi: 10.1128/jvi.57.2.438-445.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crowell R.L., Reagan K.J., Schultz M., Mapoles J.E., Grun J.B., Landau B.J. Cellular receptors as determinants of viral tropism. In: Fields B.N., Martin M.A., Kamely D., editors. Cold Spring Harbor Laboratory; Cold Spring Harbor, New York: 1985. pp. 147–164. (Genetically Altered Viruses and the Environment, Banbury Report 22). [Google Scholar]
  9. Dreyfus C.F., Black I.B. Multiple approaches to brain culture. In: Conn P.M., editor. Vol. 2. Academic Press; San Diego, CA: 1990. pp. 3–16. (Methods in Neurosciences). [Google Scholar]
  10. Grodums E.I., Dempster G. The age factor in experimental coxsackie B3 infection. Can. J. Microbiol. 1959;5:595–604. doi: 10.1139/m59-073. [DOI] [PubMed] [Google Scholar]
  11. Grodums E.I., Dempster G. Encephalitis in experimental coxsackie B-3 infection. Can. J. Microbiol. 1961;7:175–184. doi: 10.1139/m61-023. [DOI] [PubMed] [Google Scholar]
  12. Grun J.B., Schultz M., Finkelstein S.D., Crowell R.L., Landau B.J. Pathogenesis of acute myocardial necrosis in inbred mice infected with coxsackievirus B3. Microb. Pathogen. 1988;4:417–430. doi: 10.1016/0882-4010(88)90027-7. [DOI] [PubMed] [Google Scholar]
  13. Hsu K.-H.L., Crowell R.L. Characterization of a Yac-1 mouse cell receptor for group B coxsackieviruses. J. Virol. 1989;63:3105–3108. doi: 10.1128/jvi.63.7.3105-3108.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hsu K.-H.L., Paglini S., Alstein B., Crowell R.L. Identification of a second cellular receptor for a coxsackievirus B3 variant, CB3-RD. In: Brinton M.A., Heinz F.X., editors. New Aspects of Positive-Strand RNA Viruses. ASM Press; Washington DC: 1990. pp. 271–277. [Google Scholar]
  15. Hsu K.H., Lonberg-Holm K., Alstein B., Crowell R.L. A monoclonal antibody specific for the cellular receptor for the group B cov. J. Virol. 1988;62:1647–1652. doi: 10.1128/jvi.62.5.1647-1652.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Iwasaki T., Monma N., Satodate R., Kawana R., Kurata T. An immunofluorescent study of generalized coxsackie virus B3 infection in a newborn infant. Acta Pathol. Jpn. 1985;35:741–748. doi: 10.1111/j.1440-1827.1985.tb00615.x. [DOI] [PubMed] [Google Scholar]
  17. Kimelberg H.K., Norenberg M.D. Astrocytes. Sci. Am. 1989;260:66–72. doi: 10.1038/scientificamerican0489-66. [DOI] [PubMed] [Google Scholar]; Kimelberg H.K., Norenberg M.D. Astrocytes. Sci. Am. 1989;260:74. doi: 10.1038/scientificamerican0489-66. [DOI] [PubMed] [Google Scholar]; Kimelberg H.K., Norenberg M.D. Astrocytes. Sci. Am. 1989;260:76. doi: 10.1038/scientificamerican0489-66. [DOI] [PubMed] [Google Scholar]
  18. Koike S., Horie H., Ise I., Okitsu A., Yoshida M., Iizuka N., Takeuchi K., Takegami T., Nomoto A. The poliovirus receptor protein is produced both as membrane-bound and secreted forms. EMBO J. 1990;9:3217–3224. doi: 10.1002/j.1460-2075.1990.tb07520.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Krah D.L., Crowell R.L. A solid-phase assay of solubilized HeLa cell membrane receptors for binding group B coxsackieviruses and polioviruses. Virology. 1982;118:148–156. doi: 10.1016/0042-6822(82)90328-2. [DOI] [PubMed] [Google Scholar]
  20. Kunin C.M. Virus-tissue union and the pathogenesis of enterovirus infections. J. Immunol. 1962;88:556–569. [PubMed] [Google Scholar]
  21. Kunin C.M., Halmagyi N.E. The relative abundance of viral receptors: an explanation of the differential susceptibility of sucking and adult mice to coxsackie B1 infection. J. Clin. Invest. 1961;40:1055–1056. [Google Scholar]
  22. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.) 1970;227:680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Lavi E., Suzumura A., Hirayama M., Highkin M.K., Dambach D.M., Silberberg D.H., Weiss S.R. Coronavirus mouse hepatitis virus (MHV)-A59 causes a persistent productive infection in primary glial cell cultures. Microb. Pathogen. 1987;3:79–86. doi: 10.1016/0882-4010(87)90066-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lindberg A.M., Crowell R.L., Zell R., Kandolf R., Pettersson U. Mapping of the RD phenotype of the Nancy strain of coxsackievirus B3. Virus Res. 1992;24:187–196. doi: 10.1016/0168-1702(92)90006-u. [DOI] [PubMed] [Google Scholar]
  25. Lindberg A.M., Stalhandske P.O., Pettersson U. Genome of coxsackievirus B3. Virology. 1987;156:50–63. doi: 10.1016/0042-6822(87)90435-1. [DOI] [PubMed] [Google Scholar]
  26. Mapoles J.E., Krah D.L., Crowell R.L. Purification of a Hela cell receptor protein for the group B coxsackieviruses. J. Virol. 1985;55:560–566. doi: 10.1128/jvi.55.3.560-566.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McDermott P.J., Morgan H.E. Contraction modulates the capacity for protein synthesis during growth of neonatal heart cells in culture. Circ. Res. 1987;64:542–553. doi: 10.1161/01.res.64.3.542. [DOI] [PubMed] [Google Scholar]
  28. Melnick J.L. Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In: Fields B.N., Knipe D.M., editors. Virology. 2nd edn. Raven Press; New York: 1990. pp. 549–605. [Google Scholar]
  29. Minnich L.L., Ray C.G. Variable susceptibility of mice to group B coxsackievirus infections. J. Clin. Microbiol. 1980;11:73–75. doi: 10.1128/jcm.11.1.73-75.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pavesi G., Gemignani F., Macaluso G.M., Ventura P., Magnani G., Fiocchi A., Medici D., Marbini A., Mancia D. Acute sensory and autonomic neuropathy: possible association with coxsackie B virus infection. J. Neurol. Neurosurg. Psychiatry. 1992;55:613–615. doi: 10.1136/jnnp.55.7.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Reagan K.J., Goldberg B., Crowell R.L. Altered receptor specificity of coxsackievirus B3 after growth in rhabdomyosarcoma cells. J. Virol. 1984;49:635–640. doi: 10.1128/jvi.49.3.635-640.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schultz M., Crowell R.L. Eclipse of coxsackievirus infectivity: the restrictive event for a non-fusion myogenic cell line. J. Gen. Virol. 1983;64:1725–1734. doi: 10.1099/0022-1317-64-8-1725. [DOI] [PubMed] [Google Scholar]
  33. Xu R., Mohanty J.G., Crowell R.L. Receptor proteins on newborn Balb/c mouse brain cells for coxsackievirus B3 are immunologically distinct from those on HeLa cells. Virus Res. 1995;35:323–340. doi: 10.1016/0168-1702(94)00100-q. [DOI] [PubMed] [Google Scholar]
  34. Woodruff J.F. Viral myocarditis. A review. Am. J. Pathol. 1980;101:425–484. [PMC free article] [PubMed] [Google Scholar]

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