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. 1994 Jun;96(3):395–402. doi: 10.1111/j.1365-2249.1994.tb06041.x

Adenovirus infection induces loss of HLA class I and CD3 antigens, but does not induce cell surface presentation of the La (SS-B) autoantigen.

R Peek 1, J R Westphal 1, G J Pruijn 1, A J Van der Kemp 1, W J Van Venrooij 1
PMCID: PMC1534570  PMID: 7516269

Abstract

Antibodies to the RNA polymerase III transcription termination factor La are frequently found in the serum of patients with various autoimmune diseases. The mechanisms by which autoimmune responses are evoked remain largely obscure, but the presentation of autoantigens on the cell surface during stress conditions has been reported as a possible factor. In this study we analysed the effects of adenovirus infection on the binding of anti-La antibodies to the surface of several human cell lines and on the levels of the membrane-expressed glycoproteins HLA class I, CD44 and the CD3 complex. In addition, we studied the relative amount and the intracellular distribution of the La protein as well as its association with the major species of non-coding virus-associated (VAI) RNA. While immunofluorescence patterns revealed a redistribution and possibly cell surface expression of the La protein during infection, this could not be confirmed by other techniques. In contrast, surface levels of HLA class I proteins and CD3 complex were severely affected. The data suggest that the subcellular distribution of the La protein is not detectably influenced by adenovirus infection.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abraham R. T., Karnitz L. M., Secrist J. P., Leibson P. J. Signal transduction through the T-cell antigen receptor. Trends Biochem Sci. 1992 Oct;17(10):434–438. doi: 10.1016/0968-0004(92)90015-2. [DOI] [PubMed] [Google Scholar]
  2. Akusjärvi G., Mathews M. B., Andersson P., Vennström B., Pettersson U. Structure of genes for virus-associated RNAI and RNAII of adenovirus type 2. Proc Natl Acad Sci U S A. 1980 May;77(5):2424–2428. doi: 10.1073/pnas.77.5.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alspaugh M. A., Talal N., Tan E. M. Differentiation and characterization of autoantibodies and their antigens in Sjögren's syndrome. Arthritis Rheum. 1976 Mar-Apr;19(2):216–222. doi: 10.1002/art.1780190214. [DOI] [PubMed] [Google Scholar]
  4. Baboonian C., Venables P. J., Booth J., Williams D. G., Roffe L. M., Maini R. N. Virus infection induces redistribution and membrane localization of the nuclear antigen La (SS-B): a possible mechanism for autoimmunity. Clin Exp Immunol. 1989 Dec;78(3):454–459. [PMC free article] [PubMed] [Google Scholar]
  5. Bachmann M., Chang S., Bernd A., Mayet W., Meyer zum Büschenfelde K. H., Müller W. E. Translocation of the nuclear autoantigen La to cell surface: assembly and disassembly with the extracellular matrix. Autoimmunity. 1991;9(2):99–107. doi: 10.3109/08916939109006745. [DOI] [PubMed] [Google Scholar]
  6. Bachmann M., Falke D., Preuhs J., Schröder H. C., Pfeifer K., Müller W. E. Occurrence of novel small RNAs with concomitant inhibition of host cellular U small nuclear RNA synthesis in Vero cells infected with herpes simplex virus type 1. J Gen Virol. 1986 Dec;67(Pt 12):2587–2594. doi: 10.1099/0022-1317-67-12-2587. [DOI] [PubMed] [Google Scholar]
  7. Boshkov L. K., Macen J. L., McFadden G. Virus-induced loss of class I MHC antigens from the surface of cells infected with myxoma virus and malignant rabbit fibroma virus. J Immunol. 1992 Feb 1;148(3):881–887. [PubMed] [Google Scholar]
  8. Cooke A., Lydyard P. M. The role of T cells in autoimmune diseases. Pathol Res Pract. 1981 Apr;171(2):173–196. doi: 10.1016/S0344-0338(81)80036-2. [DOI] [PubMed] [Google Scholar]
  9. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  10. Furukawa F., Imamura S., Norris D. A. Stimulation of anti-RNP antibody binding to cultured keratinocytes by estradiol. Arch Dermatol Res. 1991;283(4):258–261. doi: 10.1007/BF01106112. [DOI] [PubMed] [Google Scholar]
  11. Furukawa F., Kashihara-Sawami M., Lyons M. B., Norris D. A. Binding of antibodies to the extractable nuclear antigens SS-A/Ro and SS-B/La is induced on the surface of human keratinocytes by ultraviolet light (UVL): implications for the pathogenesis of photosensitive cutaneous lupus. J Invest Dermatol. 1990 Jan;94(1):77–85. doi: 10.1111/1523-1747.ep12873930. [DOI] [PubMed] [Google Scholar]
  12. Furukawa F., Lyons M. B., Lee L. A., Coulter S. N., Norris D. A. Estradiol enhances binding to cultured human keratinocytes of antibodies specific for SS-A/Ro and SS-B/La. Another possible mechanism for estradiol influence of lupus erythematosus. J Immunol. 1988 Sep 1;141(5):1480–1488. [PubMed] [Google Scholar]
  13. Golan T. D., Elkon K. B., Gharavi A. E., Krueger J. G. Enhanced membrane binding of autoantibodies to cultured keratinocytes of systemic lupus erythematosus patients after ultraviolet B/ultraviolet A irradiation. J Clin Invest. 1992 Sep;90(3):1067–1076. doi: 10.1172/JCI115922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gottlieb E., Steitz J. A. The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO J. 1989 Mar;8(3):841–850. doi: 10.1002/j.1460-2075.1989.tb03445.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kohsaka H., Yamamoto K., Fujii H., Miura H., Miyasaka N., Nishioka K., Miyamoto T. Fine epitope mapping of the human SS-B/La protein. Identification of a distinct autoepitope homologous to a viral gag polyprotein. J Clin Invest. 1990 May;85(5):1566–1574. doi: 10.1172/JCI114606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. LeFeber W. P., Norris D. A., Ryan S. R., Huff J. C., Lee L. A., Kubo M., Boyce S. T., Kotzin B. L., Weston W. L. Ultraviolet light induces binding of antibodies to selected nuclear antigens on cultured human keratinocytes. J Clin Invest. 1984 Oct;74(4):1545–1551. doi: 10.1172/JCI111569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lerner M. R., Andrews N. C., Miller G., Steitz J. A. Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc Natl Acad Sci U S A. 1981 Feb;78(2):805–809. doi: 10.1073/pnas.78.2.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lerner M. R., Boyle J. A., Hardin J. A., Steitz J. A. Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus. Science. 1981 Jan 23;211(4480):400–402. doi: 10.1126/science.6164096. [DOI] [PubMed] [Google Scholar]
  19. Lukacher A. E., Braciale V. L., Braciale T. J. In vivo effector function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific. J Exp Med. 1984 Sep 1;160(3):814–826. doi: 10.1084/jem.160.3.814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maddison P. J., Skinner R. P., Vlachoyiannopoulos P., Brennand D. M., Hough D. Antibodies to nRNP, Sm, Ro(SSA) and La(SSB) detected by ELISA: their specificity and inter-relations in connective tissue disease sera. Clin Exp Immunol. 1985 Nov;62(2):337–345. [PMC free article] [PubMed] [Google Scholar]
  21. Mathews M. B. Genes for VA-RNA in adenovirus 2. Cell. 1975 Oct;6(2):223–229. doi: 10.1016/0092-8674(75)90013-6. [DOI] [PubMed] [Google Scholar]
  22. Mathews M. B., Shenk T. Adenovirus virus-associated RNA and translation control. J Virol. 1991 Nov;65(11):5657–5662. doi: 10.1128/jvi.65.11.5657-5662.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mattioli M., Reichlin M. Heterogeneity of RNA protein antigens reactive with sera of patients with systemic lupus erythematosus. Description of a cytoplasmic nonribosomal antigen. Arthritis Rheum. 1974 Jul-Aug;17(4):421–429. doi: 10.1002/art.1780170413. [DOI] [PubMed] [Google Scholar]
  24. Mellencamp M. W., O'Brien P. C., Stevenson J. R. Pseudorabies virus-induced suppression of major histocompatibility complex class I antigen expression. J Virol. 1991 Jun;65(6):3365–3368. doi: 10.1128/jvi.65.6.3365-3368.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Peek R., Pruijn G. J., van der Kemp A. J., van Venrooij W. J. Subcellular distribution of Ro ribonucleoprotein complexes and their constituents. J Cell Sci. 1993 Nov;106(Pt 3):929–935. doi: 10.1242/jcs.106.3.929. [DOI] [PubMed] [Google Scholar]
  26. Pizer L. I., Deng J. S., Stenberg R. M., Tan E. M. Characterization of a phosphoprotein associated with the SS-B/La nuclear antigen in adenovirus-infected and uninfected KB cells. Mol Cell Biol. 1983 Jul;3(7):1235–1245. doi: 10.1128/mcb.3.7.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rosa M. D., Gottlieb E., Lerner M. R., Steitz J. A. Striking similarities are exhibited by two small Epstein-Barr virus-encoded ribonucleic acids and the adenovirus-associated ribonucleic acids VAI and VAII. Mol Cell Biol. 1981 Sep;1(9):785–796. doi: 10.1128/mcb.1.9.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Scheppler J. A., Nicholson J. K., Swan D. C., Ahmed-Ansari A., McDougal J. S. Down-modulation of MHC-I in a CD4+ T cell line, CEM-E5, after HIV-1 infection. J Immunol. 1989 Nov 1;143(9):2858–2866. [PubMed] [Google Scholar]
  29. Scofield R. H., Harley J. B. Autoantigenicity of Ro/SSA antigen is related to a nucleocapsid protein of vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3343–3347. doi: 10.1073/pnas.88.8.3343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sharpe N. G., Isenberg D., Williams D. G., Latchman D. S. Elevation of the levels of SmB, B' and D proteins but not that of the La (SS-B) antigen during HSV infections. J Autoimmun. 1989 Oct;2(5):701–708. doi: 10.1016/s0896-8411(89)80008-3. [DOI] [PubMed] [Google Scholar]
  31. Smith P. R., Williams D. G., Venables P. J., Maini R. N. Monoclonal antibodies to the Sjögren's syndrome associated antigen SS-B (La). J Immunol Methods. 1985 Feb 28;77(1):63–76. doi: 10.1016/0022-1759(85)90184-x. [DOI] [PubMed] [Google Scholar]
  32. Spits H., Borst J., Tax W., Capel P. J., Terhorst C., de Vries J. E. Characteristics of a monoclonal antibody (WT-31) that recognizes a common epitope on the human T cell receptor for antigen. J Immunol. 1985 Sep;135(3):1922–1928. [PubMed] [Google Scholar]
  33. Stefano J. E. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3' termini of RNA polymerase III transcripts. Cell. 1984 Jan;36(1):145–154. doi: 10.1016/0092-8674(84)90083-7. [DOI] [PubMed] [Google Scholar]
  34. Wold W. S., Gooding L. R. Region E3 of adenovirus: a cassette of genes involved in host immunosurveillance and virus-cell interactions. Virology. 1991 Sep;184(1):1–8. doi: 10.1016/0042-6822(91)90815-s. [DOI] [PubMed] [Google Scholar]
  35. Zieve G. W., Sauterer R. A., Feeney R. J. Newly synthesized small nuclear RNAs appear transiently in the cytoplasm. J Mol Biol. 1988 Jan 20;199(2):259–267. doi: 10.1016/0022-2836(88)90312-9. [DOI] [PubMed] [Google Scholar]

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