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. 1986 Dec;83(24):9665–9669. doi: 10.1073/pnas.83.24.9665

Adenoviruses of subgenera B, C, D, and E modulate cell-surface expression of major histocompatibility complex class I antigens.

S Pääbo, T Nilsson, P A Peterson
PMCID: PMC387201  PMID: 3467330

Abstract

The immune defense against viral infections involves cytotoxic T lymphocytes that recognize viral products in the context of class I major histocompatibility complex (MHC) antigens. To evade such immune surveillance viruses may have evolved various strategies to manipulate the expression of class I antigens. Adenovirus 2 manufactures an early glycoprotein, E19, that binds to nascent class I antigens in the endoplasmic reticulum and impedes their transport to the cell surface. We now show that adenoviruses typical of all viral subgenera except the highly oncogenic subgenus A dramatically reduce the cell-surface expression of class I antigens. It has been shown that subgenus A viruses abolish class I antigen expression in transformed cells by reducing mRNA levels. Thus, all adenoviruses can modulate the cell-surface expression of class I antigens.

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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. Aterman K., Embil J., Easterbrook K. B., Haldane E. V., Crosby J. Liver necrosis, adenovirus type 2 and thymic dysplasia. Virchows Arch A Pathol Pathol Anat. 1973 Aug 9;360(2):155–171. doi: 10.1007/BF00543226. [DOI] [PubMed] [Google Scholar]
  3. Barnstable C. J., Bodmer W. F., Brown G., Galfre G., Milstein C., Williams A. F., Ziegler A. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell. 1978 May;14(1):9–20. doi: 10.1016/0092-8674(78)90296-9. [DOI] [PubMed] [Google Scholar]
  4. Bartok K., Garon C. F., Berry K. W., Fraser M. J., Rose J. A. Specific fragmentation of adenovirus heteroduplex DNA molecules with single-strand specific nucleases of Neurospora crassa. J Mol Biol. 1974 Aug 15;87(3):437–449. doi: 10.1016/0022-2836(74)90095-3. [DOI] [PubMed] [Google Scholar]
  5. Bello L. J., Ginsberg H. S. Inhibition of host protein synthesis in type 5 adenovirus-infected cells. J Virol. 1967 Oct;1(5):843–850. doi: 10.1128/jvi.1.5.843-850.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bergström L., Christensson I., Folkesson R., Stenström B., Terenius L. An ion exchange chromatography and radioimmunoassay procedure for measuring opioid peptides and substance P. Life Sci. 1983 Oct 17;33(16):1613–1619. doi: 10.1016/0024-3205(83)90703-8. [DOI] [PubMed] [Google Scholar]
  7. Bernards R., Schrier P. I., Houweling A., Bos J. L., van der Eb A. J., Zijlstra M., Melief C. J. Tumorigenicity of cells transformed by adenovirus type 12 by evasion of T-cell immunity. 1983 Oct 27-Nov 2Nature. 305(5937):776–779. doi: 10.1038/305776a0. [DOI] [PubMed] [Google Scholar]
  8. Blobel G., Dobberstein B. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol. 1975 Dec;67(3):835–851. doi: 10.1083/jcb.67.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Carmichael G. P., Jr, Zahradnik J. M., Moyer G. H., Porter D. D. Adenovirus hepatitis in an immunosuppressed adult patient. Am J Clin Pathol. 1979 Mar;71(3):352–355. doi: 10.1093/ajcp/71.3.352. [DOI] [PubMed] [Google Scholar]
  12. Chatterjee D., Maizel J. V., Jr Homology of adenoviral E3 glycoprotein with HLA-DR heavy chain. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6039–6043. doi: 10.1073/pnas.81.19.6039. [DOI] [PMC free article] [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. Fox J. P., Hall C. E., Cooney M. K. The Seattle Virus Watch. VII. Observations of adenovirus infections. Am J Epidemiol. 1977 Apr;105(4):362–386. doi: 10.1093/oxfordjournals.aje.a112394. [DOI] [PubMed] [Google Scholar]
  15. Garon C. F., Berry K. W., Hierholzer J. C., Rose J. A. Mapping of base sequence heterologies between genomes from different adenovirus serotypes. Virology. 1973 Aug;54(2):414–426. doi: 10.1016/0042-6822(73)90153-0. [DOI] [PubMed] [Google Scholar]
  16. Graham F. L., Smiley J., Russell W. C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977 Jul;36(1):59–74. doi: 10.1099/0022-1317-36-1-59. [DOI] [PubMed] [Google Scholar]
  17. Green M., Mackey J. K., Wold W. S., Rigden P. Thirty-one human adenovirus serotypes (Ad1-Ad31) form five groups (A-E) based upon DNA genome homologies. Virology. 1979 Mar;93(2):481–492. doi: 10.1016/0042-6822(79)90251-4. [DOI] [PubMed] [Google Scholar]
  18. Green M., Wold W. S. Human adenoviruses: growth, purification, and transfection assay. Methods Enzymol. 1979;58:425–435. doi: 10.1016/s0076-6879(79)58157-9. [DOI] [PubMed] [Google Scholar]
  19. Green M., Wold W. S., Mackey J. K., Rigden P. Analysis of human tonsil and cancer DNAs and RNAs for DNA sequences of group C (serotypes 1, 2, 5, and 6) human adenoviruses. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6606–6610. doi: 10.1073/pnas.76.12.6606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hayman M. J., Crumpton M. J. Isolation of glycoproteins from pig lymphocyte plasma membrane using Lens culinaris phytohemagglutinin. Biochem Biophys Res Commun. 1972 May 26;47(4):923–930. doi: 10.1016/0006-291x(72)90581-5. [DOI] [PubMed] [Google Scholar]
  21. Henson D., Mufson M. A. Myocarditis and pneumonitis with type 21 adenovirus infection. Association with fatal myocarditis and pneumonitis. Am J Dis Child. 1971 Apr;121(4):334–336. doi: 10.1001/archpedi.1971.02100150108015. [DOI] [PubMed] [Google Scholar]
  22. Jennings S. R., Rice P. L., Kloszewski E. D., Anderson R. W., Thompson D. L., Tevethia S. S. Effect of herpes simplex virus types 1 and 2 on surface expression of class I major histocompatibility complex antigens on infected cells. J Virol. 1985 Dec;56(3):757–766. doi: 10.1128/jvi.56.3.757-766.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kelly T. J., Jr, Lewis A. M., Jr Use of nondefective adenovirus-simian virus 40 hybrids for mapping the simian virus 40 genome. J Virol. 1973 Sep;12(3):643–652. doi: 10.1128/jvi.12.3.643-652.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kvist S., Ostberg L., Persson H., Philipson L., Peterson P. A. Molecular association between transplantation antigens and cell surface antigen in adenovirus-transformed cell line. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5674–5678. doi: 10.1073/pnas.75.11.5674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kämpe O., Bellgrau D., Hammerling U., Lind P., Päbo S., Severinsson L., Peterson P. A. Complex formation of class I transplantation antigens and a viral glycoprotein. J Biol Chem. 1983 Sep 10;258(17):10594–10598. [PubMed] [Google Scholar]
  26. Kärre K., Ljunggren H. G., Piontek G., Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature. 1986 Feb 20;319(6055):675–678. doi: 10.1038/319675a0. [DOI] [PubMed] [Google Scholar]
  27. Ljunggren H. G., Kärre K. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med. 1985 Dec 1;162(6):1745–1759. doi: 10.1084/jem.162.6.1745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Myerowitz R. L., Stalder H., Oxman M. N., Levin M. J., Moore M., Leith J. D., Gantz N. M., Hierholzer J. C., Hierholzer J. C. Fatal disseminated adenovirus infection in a renal transplant recipient. Am J Med. 1975 Oct;59(4):591–598. doi: 10.1016/0002-9343(75)90267-3. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Persson H., Signäs C., Philipson L. Purification and characterization of an early glycoprotein from adenovirus type 2-infected cells. J Virol. 1979 Mar;29(3):938–948. doi: 10.1128/jvi.29.3.938-948.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Päbo S., Weber F., Kämpe O., Schaffner W., Peterson P. A. Association between transplantation antigens and a viral membrane protein synthesized from a mammalian expression vector. Cell. 1983 Jun;33(2):445–453. doi: 10.1016/0092-8674(83)90426-9. [DOI] [PubMed] [Google Scholar]
  32. ROSEN L. A hemagglutination-inhibition technique for typing adenoviruses. Am J Hyg. 1960 Jan;71:120–128. doi: 10.1093/oxfordjournals.aje.a120085. [DOI] [PubMed] [Google Scholar]
  33. Rask L., Lindblom J. B., Peterson P. A. Structural and immunological similarities between HLA antigens from three loci. Eur J Immunol. 1976 Feb;6(2):93–100. doi: 10.1002/eji.1830060205. [DOI] [PubMed] [Google Scholar]
  34. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  35. Rosenthal A., Wright S., Quade K., Gallimore P., Cedar H., Grosveld F. Increased MHC H-2K gene transcription in cultured mouse embryo cells after adenovirus infection. Nature. 1985 Jun 13;315(6020):579–581. doi: 10.1038/315579a0. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Schneider C., Sutherland R., Newman R., Greaves M. Structural features of the cell surface receptor for transferrin that is recognized by the monoclonal antibody OKT9. J Biol Chem. 1982 Jul 25;257(14):8516–8522. [PubMed] [Google Scholar]
  38. 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]
  39. Sege K., Rask L., Peterson P. A. Role of beta2-microglobulin in the intracellular processing of HLA antigens. Biochemistry. 1981 Aug 4;20(16):4523–4530. doi: 10.1021/bi00519a003. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Severinsson L., Peterson P. A. Abrogation of cell surface expression of human class I transplantation antigens by an adenovirus protein in Xenopus laevis oocytes. J Cell Biol. 1985 Aug;101(2):540–547. doi: 10.1083/jcb.101.2.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shields A. F., Hackman R. C., Fife K. H., Corey L., Meyers J. D. Adenovirus infections in patients undergoing bone-marrow transplantation. N Engl J Med. 1985 Feb 28;312(9):529–533. doi: 10.1056/NEJM198502283120901. [DOI] [PubMed] [Google Scholar]
  43. Shinagawa M., Matsuda A., Ishiyama T., Goto H., Sato G. A rapid and simple method for preparation of adenovirus DNA from infected cells. Microbiol Immunol. 1983;27(9):817–822. doi: 10.1111/j.1348-0421.1983.tb00638.x. [DOI] [PubMed] [Google Scholar]
  44. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Tarentino A. L., Maley F. Purification and properties of an endo-beta-N-acetylglucosaminidase from Streptomyces griseus. J Biol Chem. 1974 Feb 10;249(3):811–817. [PubMed] [Google Scholar]
  47. Wold W. S., Cladaras C., Deutscher S. L., Kapoor Q. S. The 19-kDa glycoprotein coded by region E3 of adenovirus. Purification, characterization, and structural analysis. J Biol Chem. 1985 Feb 25;260(4):2424–2431. [PubMed] [Google Scholar]
  48. Zinkernagel R. M., Doherty P. C. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature. 1974 Apr 19;248(5450):701–702. doi: 10.1038/248701a0. [DOI] [PubMed] [Google Scholar]
  49. van Loon A. E., Rozijn T. H., de Jong J. C., Sussenbach J. S. Physicochemical properties of the DNAs of the fastidious adenovirus species 40 and 41. Virology. 1985 Jan 15;140(1):197–200. doi: 10.1016/0042-6822(85)90461-1. [DOI] [PubMed] [Google Scholar]

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