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. 1986 Dec;83(24):9684–9688. doi: 10.1073/pnas.83.24.9684

Tumorigenicity of hamster and mouse cells transformed by adenovirus types 2 and 5 is not influenced by the level of class I major histocompatibility antigens expressed on the cells.

H Haddada, A M Lewis Jr, J A Sogn, J E Coligan, J L Cook, T A Walker, A S Levine
PMCID: PMC387205  PMID: 3467332

Abstract

Inbred hamster and mouse cells transformed by the nononcogenic adenovirus (Ad) serotypes, Ad2 and Ad5, are nontumorigenic in syngeneic adult animals, while cells from these species transformed by the highly oncogenic Ad12 are tumorigenic in such rodents. By immunoprecipitation and flow cytometry, cells from four of six Ad2- and Ad5-transformed hamster and mouse lines expressed high levels of cell-surface class I major histocompatibility complex (MHC) antigens, while cells from two of these six lines expressed low levels of cell-surface class I MHC antigens. The levels of class I MHC proteins expressed by cells from these latter two lines were comparable to the levels of cell-surface class I MHC proteins expressed by cells from Ad12-transformed hamster and mouse lines. Moreover, an Ad2-transformed line that had become highly oncogenic after in vivo adaptation showed the same high level of MHC expression as the nononcogenic parent. The amounts of class I mRNA, analyzed by RNA blotting, were, in general, consistent with the levels of class I antigens expressed on the surfaces of these cells. These results indicate that there is no correlation between the tumorigenicity in immunocompetent syngeneic adult rodents of Ad2- and Ad5-transformed hamster and mouse cells and the level of class I MHC antigens expressed on the surfaces of these cells. Thus, the expression of different levels of class I MHC proteins does not seem to explain the differences in the oncogenicity between nononcogenic and highly oncogenic human Ad serotypes.

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Selected References

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

  1. Akagi K., Patch C. T., Cook J. L., Kato T., Lewis A. M., Jr, Levine A. S. The level of expression of adenovirus type 2 transforming genes governs sensitivity to nonspecific immune cytolysis and other phenotypic properties of adenovirus 2-simian virus 40-transformed cell hybrids. Mol Cell Biol. 1985 Aug;5(8):1870–1877. doi: 10.1128/mcb.5.8.1870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Coligan J. E., Kindt T. J., Uehara H., Martinko J., Nathenson S. G. Primary structure of a murine transplantation antigen. Nature. 1981 May 7;291(5810):35–39. doi: 10.1038/291035a0. [DOI] [PubMed] [Google Scholar]
  6. Cook J. L., Lewis A. M., Jr Host response to adenovirus 2-transformed hamster embryo cells. Cancer Res. 1979 May;39(5):1455–1461. [PubMed] [Google Scholar]
  7. Cook J. L., Walker T. A., Lewis A. M., Jr, Ruley H. E., Graham F. L., Pilder S. H. Expression of the adenovirus E1A oncogene during cell transformation is sufficient to induce susceptibility to lysis by host inflammatory cells. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6965–6969. doi: 10.1073/pnas.83.18.6965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Darden A. G., Streilein J. W. Syrian hamsters express two monomorphic class I major histocompatibility complex molecules. Immunogenetics. 1984;20(6):603–622. doi: 10.1007/BF00430319. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Evans G. A., Margulies D. H., Camerini-Otero R. D., Ozato K., Seidman J. G. Structure and expression of a mouse major histocompatibility antigen gene, H-2Ld. Proc Natl Acad Sci U S A. 1982 Mar;79(6):1994–1998. doi: 10.1073/pnas.79.6.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jochemsen A. G., Bos J. L., van der Eb A. J. The first exon of region E1a genes of adenoviruses 5 and 12 encodes a separate functional protein domain. EMBO J. 1984 Dec 1;3(12):2923–2927. doi: 10.1002/j.1460-2075.1984.tb02233.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  13. Lewis A. M., Jr, Cook J. L. A new role for DNA virus early proteins in viral carcinogenesis. Science. 1985 Jan 4;227(4682):15–20. doi: 10.1126/science.3843807. [DOI] [PubMed] [Google Scholar]
  14. Lewis A. M., Jr, Cook J. L. Spectrum of tumorigenic phenotypes among adenovirus 2-, adenovirus 12-, and simian virus 40-transformed Syrian hamster cells defined by host cellular immune-tumor cell interactions. Cancer Res. 1982 Mar;42(3):939–944. [PubMed] [Google Scholar]
  15. Lewis A. M., Jr, Cook J. L. The interface between adenovirus-transformed cells and cellular immune response in the challenged host. Curr Top Microbiol Immunol. 1984;110:1–22. doi: 10.1007/978-3-642-46494-2_1. [DOI] [PubMed] [Google Scholar]
  16. Long E. O., Gross N., Wake C. T., Mach J. P., Carrel S., Accolla R., Mach B. Translation and assembly of HLA-DR antigens in Xenopus oocytes injected with mRNA from a human B-cell line. EMBO J. 1982;1(5):649–654. doi: 10.1002/j.1460-2075.1982.tb01222.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ozato K., Evans G. A., Shykind B., Margulies D. H., Seidman J. G. Hybrid H-2 histocompatibility gene products assign domains recognized by alloreactive T cells. Proc Natl Acad Sci U S A. 1983 Apr;80(7):2040–2043. doi: 10.1073/pnas.80.7.2040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Raska K., Jr, Gallimore P. H. An inverse relation of the oncogenic potential of adenovirus-transformed cells and their sensitivity to killing by syngeneic natural killer cells. Virology. 1982 Nov;123(1):8–18. doi: 10.1016/0042-6822(82)90290-2. [DOI] [PubMed] [Google Scholar]
  19. Sawada Y., Föhring B., Shenk T. E., Raska K., Jr Tumorigenicity of adenovirus-transformed cells: region E1A of adenovirus 12 confers resistance to natural killer cells. Virology. 1985 Dec;147(2):413–421. doi: 10.1016/0042-6822(85)90143-6. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. TRENTIN J. J., YABE Y., TAYLOR G. The quest for human cancer viruses. Science. 1962 Sep 14;137(3533):835–841. doi: 10.1126/science.137.3533.835. [DOI] [PubMed] [Google Scholar]
  23. Tanaka K., Isselbacher K. J., Khoury G., Jay G. Reversal of oncogenesis by the expression of a major histocompatibility complex class I gene. Science. 1985 Apr 5;228(4695):26–30. doi: 10.1126/science.3975631. [DOI] [PubMed] [Google Scholar]
  24. Tanaka K., Isselbacher K. J., Khoury G., Jay G. Reversal of oncogenesis by the expression of a major histocompatibility complex class I gene. Science. 1985 Apr 5;228(4695):26–30. doi: 10.1126/science.3975631. [DOI] [PubMed] [Google Scholar]
  25. Vardimon L., Doerfler W. Patterns of integration of viral DNA in adenovirus type 2-transformed hamster cells. J Mol Biol. 1981 Apr 5;147(2):227–246. doi: 10.1016/0022-2836(81)90439-3. [DOI] [PubMed] [Google Scholar]
  26. Vasavada R., Eager K. B., Barbanti-Brodano G., Caputo A., Ricciardi R. P. Adenovirus type 12 early region 1A proteins repress class I HLA expression in transformed human cells. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5257–5261. doi: 10.1073/pnas.83.14.5257. [DOI] [PMC free article] [PubMed] [Google Scholar]

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