Skip to main content
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2002 Nov 13;33(3):181–190. doi: 10.1016/0165-5728(91)90105-G

Mouse hepatitis virus (MHV-4, JHM) blocks γ-interferon-induced major histocompatibility complex class II antigen expression on murine cerebral endothelial cells

Jeymohan Joseph 1,, Robert L Knobler 1, Fred D Lublin 1, MN Hart 2
PMCID: PMC7119494  PMID: 1651958

Abstract

The regulation of γ-interferon-induced major histocompatibility complex (MHC) class II antigen expression on mouse cerebral endothelial cells by the neurotropic mouse hepatitis virus (MHV-4, JHM) was studied in vitro. The results presented demonstrate that MHV-4 can selectively block γ-interferon-induced class II antigen expression on cerebral endothelial cells. The blocking effect of class II expression occurs in a strain-dependent manner, and is limited to virus-susceptible mouse strains. Virus replication is not required to obtain the blocking effect since UV-inactivated MHV-4 produces the same result. MHV-4 blocking of γ-interferon-induced class II antigen expression is observed at both the cell surface (flow cytometry) and transcriptional level (Norhtern analysis).

Keywords: MHV-4, Major histocompatibility complex class II antigen, Interferon-γ, Cerebral endothelial cell, Flow cytometry, Northern analysis

References

  1. Bailey O.T., Pappenheimer A.M., Cheever F.S. A murine virus (JHM) causing extensive destruction of myelin. Part 2: Pathology. J. Exp. Med. 1949;90:195–212. doi: 10.1084/jem.90.3.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ben-Nun A., Choi E., McInytre K.R., Leeman S.A., McKean D.J., Seidman J.G., Glimcher L.H. DNA-mediated transfer of major histocompatibility class II I-Ab and I-Abm12 genes into B lymphoma cells: molecular and functional analysis of introduced antigens. J. Immunol. 1985;135:1456–1464. [PubMed] [Google Scholar]
  3. Boyle J.F., Weissmiller D.G., Holmes K.V. Genetic resistance of 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]
  4. Collins T., Krensky A.M., Clayberger C., Fiers W., Gimbrone M.A., Burakoff S.J., Pober J.S. Human cytolytic T-lymphocyte interactions with vascular endothelium and fibroblasts: role of effectors and target molecules. J. Immunol. 1984;133:1878–1884. [PubMed] [Google Scholar]
  5. Crissman H.A., Steinkamp J.A. Rapid one step staining procedures for analysis of cellular DNA and protein by single and dual laser flow cytometry. Cytometry. 1982;3:84–90. doi: 10.1002/cyto.990030204. [DOI] [PubMed] [Google Scholar]
  6. Dropulic B., Masters C.L. Entry of neutotropic arboviruses into the central nervous system: an in vitro study using mouse brain endothelium. J. Infect. Dis. 1990;161:685–691. doi: 10.1093/infdis/161.4.685. [DOI] [PubMed] [Google Scholar]
  7. Hirschberg H. Presentation of viral antigens by human vascular endothelial cells in vitro. Hum. Immunol. 1981;2:235–241. doi: 10.1016/0198-8859(81)90015-x. [DOI] [PubMed] [Google Scholar]
  8. Johnson R.T. Pathophysiology and epidemiology of acute viral infections of the nervous system. Adv. Neurol. 1974;6:27–40. [PubMed] [Google Scholar]
  9. Johnson R.T. Raven Press; New York: 1982. Viral Infections of the Nervous System; p. 49. [Google Scholar]
  10. Johnson W.J., Kelley A., Connor J.C., Dalton B.J., Meunier P.C. Inhibition of interferon-γ-induced Ia antigen expression on synovial fibroblasts by IL-1. J. Immunol. 1989;143:1614–1618. [PubMed] [Google Scholar]
  11. Joseph J., Knobler R.L., D'Imperio C., Lublin F.D. Down-regulation of interferon-γ-induced class II expression on human glioma cells by recombinant interferon-β: effect of dosage treatment schedule. J. Neuroimmunol. 1988;20:39–44. doi: 10.1016/0165-5728(88)90112-9. [DOI] [PubMed] [Google Scholar]
  12. Joseph J., Knobler R.L., Lublin F.D., Hart M.N. Differential modulation of MHC class I antigen expression on mouse brain endothelial cells by MHV-4 infection. J. Neuroimmunol. 1989;22:241–253. doi: 10.1016/0165-5728(89)90022-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Knobler R.L., Haspel M.V., Oldstone M.B.A. Mouse hepatitis virus type 4 (JHM strain) induced fatal central nervous system disease. I. Genetic control and the murine neuron as the susceptible site of disease. J. Exp. Med. 1981;153:832–843. doi: 10.1084/jem.153.4.832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Knobler R.L., Tunison L.A., Lampert P.W., Oldstone M.B.A. Selected mutants of mouse hepatitis virus type 4 (JHM) induces different CNS diseases. Pathobiology of disease induced by wild type and mutants ts8 and ts15 in BALB/c and SJL mice. Am. J. Pathol. 1982;109:157–168. [PMC free article] [PubMed] [Google Scholar]
  15. Knobler R.L., Linthicum D.S., Cohn M. Host genetic regulation of acute MHV-4 viral encephalomyelitis and acute experimental autoimmune encephalomyelitis in (BALB / cKe × SJL / J) recombinant inbred mice. J. Neuroimmunol. 1985;8:15–28. doi: 10.1016/S0165-5728(85)80044-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Leeuwenberg J.F.M., Van Damme J., Meager T., Jeunhomme T.M.A.A., Buurman W.A. Effect of tumor necrosis factor on the interferon-γ-induced major histocompatibility complex class II antigen expression by human endothelial cells. Eur. J. Immunol. 1988;18:1469–1472. doi: 10.1002/eji.1830180925. [DOI] [PubMed] [Google Scholar]
  17. Maniatis T., Fritsch E.F., Sambrook J. Cold Spring Harbor Laboratory Press; Cold Spring Harbor, NY: 1982. Molecular Cloning, a Laboratory Manual. [Google Scholar]
  18. Mantovani A., Dejana E. Cytokines as communication signals between leukocytes and endothelial cells. Immunol. Today. 1989;10:370–375. doi: 10.1016/0167-5699(89)90270-3. [DOI] [PubMed] [Google Scholar]
  19. Massa P.T., Dorries R., ter Meulen V. Viral particles induce Ia antigen expression on astrocytes. Nature. 1986;320:543–546. doi: 10.1038/320543a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Massa P.T., Brinkmann R., ter Meulen V. Inducibility of Ia antigen on astrocytes is rat strain dependent. J. Exp. Med. 1987;166:259–264. doi: 10.1084/jem.166.1.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Maudsley D.J., Morris A.G. Regulation of interferon-γ-induced host cell MHC antigen expression by Kirsten MSV and MLV. I. Effects on class I antigen expression. Immunology. 1989;67:21–25. [PMC free article] [PubMed] [Google Scholar]
  22. Maudsley D.J., Morris A.G. Regulation of interferon-γ-induced host cell MHC expression by Kirsten MSV and MLV. II. Effects on class II antigen expression. Immunology. 1989;67:26–31. [PMC free article] [PubMed] [Google Scholar]
  23. McCarron R.M., Kempski O., Spatz M., McFarlin D.E. Presentation of myelin basic protein by murine cerebral vascular endothelial cells. J. Immunol. 1985;134:3100–3103. [PubMed] [Google Scholar]
  24. McCarron R.M., Spatz M., Kempski O., Hogan R.N., Muehl L., McFarlin D.E. Interaction between myelin basic protein-sensitexed T lymophocytes and murine cerebral vascular endothelial cells. J. Immunol. 1986;137:3428–3435. [PubMed] [Google Scholar]
  25. Pober J.S., Collins T., Gimbrone M.A., Libby P., Reiss C.S. Inducible expression of class II histocompatibility complex antigens and the immunogenicity of vascular endothelium. Transplantation. 1986;41:141–146. doi: 10.1097/00007890-198602000-00001. [DOI] [PubMed] [Google Scholar]
  26. Rupnick M.A., Carey A., Williams S.K. Phenotypic diversity in cultured cerebral microvascular endothelial cells. In vitro Cell Dev. Biol. 1988;24:435–444. doi: 10.1007/BF02628495. [DOI] [PubMed] [Google Scholar]
  27. Sahagun G., Moore S.A., Fabry Z., Schelper R.L., Hart M.N. Purification of murine endothelial cell cultures by flow cytometry using fluorescein-labeled Griffonia simplicifolia agglutinin. Am. J. Pathol. 1989;134:1227–1232. [PMC free article] [PubMed] [Google Scholar]
  28. Sasaki A., Levinson S.W., Ting J.P.Y. Differential suppression of interferon-induced Ia antigen expression on cultured rat astroglia and microglia by second messengers. J. Neuroimmunol. 1990;29:213–222. doi: 10.1016/0165-5728(90)90164-I. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Suzumura A., Lavi E., Weiss S.R., Silberberg D.H. Coronavirus infection induces H-2 antigen expression on oligodendrocytes and astrocytes. Science. 1986;232:991–993. doi: 10.1126/science.3010460. [DOI] [PubMed] [Google Scholar]
  30. Thomas H.C., Pignatelli M., Lever A.M.L. Homology between HBV-DNA and a sequence regulating the interferon induced antiviral system: possible mechanism of persistent infection. J. Med. Virol. 1986;19:63–69. doi: 10.1002/jmv.1890190110. [DOI] [PubMed] [Google Scholar]
  31. Voyta J.C., Netland P.A., Via D.P., Zetter B.R. Specific labeling of endothelial cells using fluorescent acetylated low density lipoproteins. J. Cell Biol. 1984;99:81A. doi: 10.1083/jcb.99.6.2034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wiley C.A., Schrier R.D., Nelson J.A., Lampert P.W., Oldstone M.B.A. Vol. 83. 1986. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients; pp. 7089–7093. (Proc. Natl. Acad. Sci. U.S.A.). [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wilhelmsen K.C., Leibowitz J.L., Bond C.W., Robb J.A. The replication of murine coronavirus in enucleared cells. Virology. 1981;110:225–230. doi: 10.1016/0042-6822(81)90027-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zurbriggen Z., Fujinami R.S. Theiler's virus infection in nude mice: viral RNA in vascular endothelial cells. J. Virol. 1988;62:3589–3596. doi: 10.1128/jvi.62.10.3589-3596.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Neuroimmunology are provided here courtesy of Elsevier

RESOURCES