Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1996 Aug;70(8):5495–5502. doi: 10.1128/jvi.70.8.5495-5502.1996

Lack of effect of mouse adenovirus type 1 infection on cell surface expression of major histocompatibility complex class I antigens.

S C Kring 1, K R Spindler 1
PMCID: PMC190507  PMID: 8764061

Abstract

It has been proposed that adenoviruses establish and maintain persistent infections by reducing the class I major histocompatibility complex-associated presentation of viral antigens to cytotoxic T lymphocytes, leading to ineffective cell-mediated immunity and impaired clearance of infected cells (W.S.M. Wold and L. R. Gooding, Virology 184:1-8, 1991). Early region 3 of human adenovirus types 2 and 5 encodes a 19-kDa glycoprotein that associates with the class I major histocompatibility complex (MHC) antigens in the endoplasmic reticulum and prevents their maturation and transport to the cell surface. Early region 1A of human adenovirus type 12 encodes a protein that inhibits class I MHC mRNA production at the transcriptional or posttranscriptional processing level. Unlike human adenovirus infections, however, mouse adenovirus type 1 (MAV-1) infection of a variety of cell types did not affect the surface expression of 10 different mouse class I MHC allotypes. MAV-1-infected cells also regenerated cell surface class I MHC antigens following proteolytic removal as efficiently as mock-infected cells. The ability of cells to present antigen to class I MHC (Kb)-ovalbumin-specific T-cell hybridoma cells was likewise unaltered by MAV-1 infection. Thus, the ability of MAV-1 to persist cannot be explained by the model of reduced class I MHC-associated antigen presentation proposed for human adenoviruses.

Full Text

The Full Text of this article is available as a PDF (268.3 KB).

Selected References

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

  1. Andersson M., Päbo S., Nilsson T., Peterson P. A. Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance. Cell. 1985 Nov;43(1):215–222. doi: 10.1016/0092-8674(85)90026-1. [DOI] [PubMed] [Google Scholar]
  2. Ball A. O., Beard C. W., Redick S. D., Spindler K. R. Genome organization of mouse adenovirus type 1 early region 1: a novel transcription map. Virology. 1989 Jun;170(2):523–536. doi: 10.1016/0042-6822(89)90444-3. [DOI] [PubMed] [Google Scholar]
  3. Ball A. O., Williams M. E., Spindler K. R. Identification of mouse adenovirus type 1 early region 1: DNA sequence and a conserved transactivating function. J Virol. 1988 Nov;62(11):3947–3957. doi: 10.1128/jvi.62.11.3947-3957.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beard C. W., Ball A. O., Wooley E. H., Spindler K. R. Transcription mapping of mouse adenovirus type 1 early region 3. Virology. 1990 Mar;175(1):81–90. doi: 10.1016/0042-6822(90)90188-w. [DOI] [PubMed] [Google Scholar]
  5. Beard C. W., Spindler K. R. Characterization of an 11K protein produced by early region 3 of mouse adenovirus type 1. Virology. 1995 Apr 20;208(2):457–466. doi: 10.1006/viro.1995.1176. [DOI] [PubMed] [Google Scholar]
  6. Beersma M. F., Bijlmakers M. J., Ploegh H. L. Human cytomegalovirus down-regulates HLA class I expression by reducing the stability of class I H chains. J Immunol. 1993 Nov 1;151(9):4455–4464. [PubMed] [Google Scholar]
  7. Burgert H. G., Kvist S. An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell. 1985 Jul;41(3):987–997. doi: 10.1016/s0092-8674(85)80079-9. [DOI] [PubMed] [Google Scholar]
  8. Burgert H. G., Kvist S. The E3/19K protein of adenovirus type 2 binds to the domains of histocompatibility antigens required for CTL recognition. EMBO J. 1987 Jul;6(7):2019–2026. doi: 10.1002/j.1460-2075.1987.tb02466.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Burgert H. G., Maryanski J. L., Kvist S. "E3/19K" protein of adenovirus type 2 inhibits lysis of cytolytic T lymphocytes by blocking cell-surface expression of histocompatibility class I antigens. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1356–1360. doi: 10.1073/pnas.84.5.1356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cox J. H., Bennink J. R., Yewdell J. W. Retention of adenovirus E19 glycoprotein in the endoplasmic reticulum is essential to its ability to block antigen presentation. J Exp Med. 1991 Dec 1;174(6):1629–1637. doi: 10.1084/jem.174.6.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cox J. H., Buller R. M., Bennink J. R., Yewdell J. W., Karupiah G. Expression of adenovirus E3/19K protein does not alter mouse MHC class I-restricted responses to vaccinia virus. Virology. 1994 Nov 1;204(2):558–562. doi: 10.1006/viro.1994.1569. [DOI] [PubMed] [Google Scholar]
  12. Doherty P. C., Allan W., Eichelberger M., Carding S. R. Roles of alpha beta and gamma delta T cell subsets in viral immunity. Annu Rev Immunol. 1992;10:123–151. doi: 10.1146/annurev.iy.10.040192.001011. [DOI] [PubMed] [Google Scholar]
  13. Eager K. B., Williams J., Breiding D., Pan S., Knowles B., Appella E., Ricciardi R. P. Expression of histocompatibility antigens H-2K, -D, and -L is reduced in adenovirus-12-transformed mouse cells and is restored by interferon gamma. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5525–5529. doi: 10.1073/pnas.82.16.5525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gillis S., Ferm M. M., Ou W., Smith K. A. T cell growth factor: parameters of production and a quantitative microassay for activity. J Immunol. 1978 Jun;120(6):2027–2032. [PubMed] [Google Scholar]
  15. Ginsberg H. S., Lundholm-Beauchamp U., Horswood R. L., Pernis B., Wold W. S., Chanock R. M., Prince G. A. Role of early region 3 (E3) in pathogenesis of adenovirus disease. Proc Natl Acad Sci U S A. 1989 May;86(10):3823–3827. doi: 10.1073/pnas.86.10.3823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grunhaus A., Cho S., Horwitz M. S. Association of vaccinia virus-expressed adenovirus E3-19K glycoprotein with class I MHC and its effects on virulence in a murine pneumonia model. Virology. 1994 May 1;200(2):535–546. doi: 10.1006/viro.1994.1216. [DOI] [PubMed] [Google Scholar]
  17. HARTLEY J. W., ROWE W. P. A new mouse virus apparently related to the adenovirus group. Virology. 1960 Jul;11:645–647. doi: 10.1016/0042-6822(60)90109-4. [DOI] [PubMed] [Google Scholar]
  18. Heck F. C., Jr, Sheldon W. G., Gleiser C. A. Pathogenesis of experimentally produced mouse adenovirus infection in mice. Am J Vet Res. 1972 Apr;33(4):841–846. [PubMed] [Google Scholar]
  19. Hermiston T. W., Hellwig R., Hierholzer J. C., Wold W. S. Sequence and functional analysis of the human adenovirus type 7 E3-gp19K protein from 17 clinical isolates. Virology. 1993 Dec;197(2):593–600. doi: 10.1006/viro.1993.1633. [DOI] [PubMed] [Google Scholar]
  20. Inada T., Uetake H. Cell-mediated immunity assayed by 51Cr release test in mice infected with mouse adenovirus. Infect Immun. 1978 Apr;20(1):1–5. doi: 10.1128/iai.20.1.1-5.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jameson S. C., Bevan M. J. Dissection of major histocompatibility complex (MHC) and T cell receptor contact residues in a Kb-restricted ovalbumin peptide and an assessment of the predictive power of MHC-binding motifs. Eur J Immunol. 1992 Oct;22(10):2663–2667. doi: 10.1002/eji.1830221028. [DOI] [PubMed] [Google Scholar]
  22. Levine A. J. The adenovirus early proteins. Curr Top Microbiol Immunol. 1984;110:143–167. doi: 10.1007/978-3-642-46494-2_5. [DOI] [PubMed] [Google Scholar]
  23. Lippincott-Schwartz J., Yuan L. C., Bonifacino J. S., Klausner R. D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell. 1989 Mar 10;56(5):801–813. doi: 10.1016/0092-8674(89)90685-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Livingstone A. M., Powis S. J., Diamond A. G., Butcher G. W., Howard J. C. A trans-acting major histocompatibility complex-linked gene whose alleles determine gain and loss changes in the antigenic structure of a classical class I molecule. J Exp Med. 1989 Sep 1;170(3):777–795. doi: 10.1084/jem.170.3.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nikolić-Zugić J., Carbone F. R. The effect of mutations in the MHC class I peptide binding groove on the cytotoxic T lymphocyte recognition of the Kb-restricted ovalbumin determinant. Eur J Immunol. 1990 Nov;20(11):2431–2437. doi: 10.1002/eji.1830201111. [DOI] [PubMed] [Google Scholar]
  26. Persson H., Jansson M., Philipson L. Synthesis and genomic site for an adenovirus type 2 early glycoprotein. J Mol Biol. 1980 Feb 5;136(4):375–394. doi: 10.1016/0022-2836(80)90396-4. [DOI] [PubMed] [Google Scholar]
  27. Pfizenmaier K., Pan S. H., Knowles B. B. Preferential H-2 association in cytotoxic T cell responses to SV40 tumor-associated specific antigens. J Immunol. 1980 Apr;124(4):1888–1891. [PubMed] [Google Scholar]
  28. Powis S. J., Deverson E. V., Coadwell W. J., Ciruela A., Huskisson N. S., Smith H., Butcher G. W., Howard J. C. Effect of polymorphism of an MHC-linked transporter on the peptides assembled in a class I molecule. Nature. 1992 May 21;357(6375):211–215. doi: 10.1038/357211a0. [DOI] [PubMed] [Google Scholar]
  29. Päbo S., Nilsson T., Peterson P. A. Adenoviruses of subgenera B, C, D, and E modulate cell-surface expression of major histocompatibility complex class I antigens. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9665–9669. doi: 10.1073/pnas.83.24.9665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ross S., Levine A. J. The genomic map position of the adenovirus type 2 glycoprotein. Virology. 1979 Dec;99(2):427–430. doi: 10.1016/0042-6822(79)90023-0. [DOI] [PubMed] [Google Scholar]
  31. Rotem-Yehudar R., Winograd S., Sela S., Coligan J. E., Ehrlich R. Downregulation of peptide transporter genes in cell lines transformed with the highly oncogenic adenovirus 12. J Exp Med. 1994 Aug 1;180(2):477–488. doi: 10.1084/jem.180.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Routes J. M., Cook J. L. Resistance of human cells to the adenovirus E3 effect on class I MHC antigen expression. Implications for antiviral immunity. J Immunol. 1990 Apr 1;144(7):2763–2770. [PubMed] [Google Scholar]
  33. Routes J. M., Metz B. A., Cook J. L. Endogenous expression of E1A in human cells enhances the effect of adenovirus E3 on class I major histocompatibility complex antigen expression. J Virol. 1993 Jun;67(6):3176–3181. doi: 10.1128/jvi.67.6.3176-3181.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rötzschke O., Falk K., Stevanović S., Jung G., Walden P., Rammensee H. G. Exact prediction of a natural T cell epitope. Eur J Immunol. 1991 Nov;21(11):2891–2894. doi: 10.1002/eji.1830211136. [DOI] [PubMed] [Google Scholar]
  35. Schrier P. I., Bernards R., Vaessen R. T., Houweling A., van der Eb A. J. Expression of class I major histocompatibility antigens switched off by highly oncogenic adenovirus 12 in transformed rat cells. 1983 Oct 27-Nov 2Nature. 305(5937):771–775. doi: 10.1038/305771a0. [DOI] [PubMed] [Google Scholar]
  36. Schwartz B. D., Nathenson S. G. Regeneration of transplantation antigens on mouse cells. Transplant Proc. 1971 Mar;3(1):180–182. [PubMed] [Google Scholar]
  37. Severinsson L., Martens I., Peterson P. A. Differential association between two human MHC class I antigens and an adenoviral glycoprotein. J Immunol. 1986 Aug 1;137(3):1003–1009. [PubMed] [Google Scholar]
  38. Shemesh J., Rotem-Yehudar R., Ehrlich R. Transcriptional and posttranscriptional regulation of class I major histocompatibility complex genes following transformation with human adenoviruses. J Virol. 1991 Oct;65(10):5544–5548. doi: 10.1128/jvi.65.10.5544-5548.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Storch T. G., Maizel J. V., Jr The early proteins of the nondefective Ad2-SV40 hybrid viruses: the 19K glycoprotein is coded by Ad2 early region 3. Virology. 1980 May;103(1):54–67. doi: 10.1016/0042-6822(80)90125-7. [DOI] [PubMed] [Google Scholar]
  40. Tanaka Y., Tevethia S. S. Differential effect of adenovirus 2 E3/19K glycoprotein on the expression of H-2Kb and H-2Db class I antigens and H-2Kb- and H-2Db-restricted SV40-specific CTL-mediated lysis. Virology. 1988 Aug;165(2):357–366. doi: 10.1016/0042-6822(88)90580-6. [DOI] [PubMed] [Google Scholar]
  41. Tarleton R. L., Kuhn R. E. Restoration of in vitro immune responses of spleen cells from mice infected with Trypanosoma cruzi by supernatants containing interleukin 2. J Immunol. 1984 Sep;133(3):1570–1575. [PubMed] [Google Scholar]
  42. Tarleton R. L. Trypanosoma cruzi-induced suppression of IL-2 production. I. Evidence for the presence of IL-2-producing cells. J Immunol. 1988 Apr 15;140(8):2763–2768. [PubMed] [Google Scholar]
  43. Townsend A., Ohlén C., Bastin J., Ljunggren H. G., Foster L., Kärre K. Association of class I major histocompatibility heavy and light chains induced by viral peptides. Nature. 1989 Aug 10;340(6233):443–448. doi: 10.1038/340443a0. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. York I. A., Roop C., Andrews D. W., Riddell S. R., Graham F. L., Johnson D. C. A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell. 1994 May 20;77(4):525–535. doi: 10.1016/0092-8674(94)90215-1. [DOI] [PubMed] [Google Scholar]
  46. del Val M., Hengel H., Häcker H., Hartlaub U., Ruppert T., Lucin P., Koszinowski U. H. Cytomegalovirus prevents antigen presentation by blocking the transport of peptide-loaded major histocompatibility complex class I molecules into the medial-Golgi compartment. J Exp Med. 1992 Sep 1;176(3):729–738. doi: 10.1084/jem.176.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. van der Veen J., Mes A. Experimental infection with mouse adenovirus in adult mice. Arch Gesamte Virusforsch. 1973;42(3):235–241. doi: 10.1007/BF01265648. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES