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Adenovirus DNA pp 343–366Cite as

Expression of Class I Major Histocompatibility Antigens in Adenovirus-Transformed Cells

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Part of the book series: Developments in Molecular Virology ((DMVI,volume 8))

Abstract

Human adenoviruses have been used extensively as a model for studies on the mechanism of oncogenic transformation. The interest in this group of viruses is due to the fact that they combine a number of unique features, that are not found in other viruses: (a) Oncogenic transformation by adenoviruses is the result of the activity of 2 or 3 distinct viral gene products, rather than by the action of a single viral protein, as in the case of SV40. This seemingly greater complexity of the transforming region of adenovirus is an advantage rather than a disadvantage. It should considerably simplify genetic and functional analysis of transformation as compared to the situation in SV40, where the transforming functions are all compressed into a single multifunctional protein (1). (b) Oncogenic transformation by adenoviruses can be considered to be a “multistep” process in which 2 or 3 genes are involved (2). This resembles the situation in spontaneous cancer in animals, which also requires the concerted activity of two, or possibly more, cellular oncogenes. Interestingly, a functional similarity has been established between the adenovirus E1A and E1B regions on one hand, which together constitute the viral transforming region, and the two cooperating cellular oncogenes myc and ras on the other (3,4). (c) The human adenoviruses can be divided into oncogenic and non-oncogenic serotypes (e.g. Ad 12, an oncogenic virus, and Ad2 or Ad5, both non-oncogenic viruses). Despite this difference in biological behavior, all human adenoviruses tested so far are capable of morphologically transforming cultured cells. The structural and organizational relatedness of the Ad5 and Ad 12 transforming regions implies that the difference in oncogenicity must be brought about by one or more subtle differences in gene function, and may enable us to dissociate oncogenicity, i.e. the ability to grow as a tumor in normal animals, from morphological transformation in vitro.

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References

  1. Tooze J: DNA Tumor Viruses. 2nd edition. Cold Spring Harbor Laboratory. 1981.

    Google Scholar 

  2. Van der Eb AJ, Van Ormondt H, Schrier PI, Lupker JH, Jochemsen H, DeLeys RJ, Maat J, Van Beveren, CP, Dijkema R, de Waard A: Structure and function of the transformed genes of human adenoviruses and SV40. Cold Spring Harbor Symp Quant Biol (44): 383–399, 1979.

    Google Scholar 

  3. Land H, Parada LF, Weinberg RA: Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature (304):596–602, 1979.

    Article  Google Scholar 

  4. Ruley HE: Adenovirus region 1A enables viral and cellular transforming genes to transform primary cells in cultures. Nature (304): 602–606, 1983.

    Article  PubMed  CAS  Google Scholar 

  5. Bernards R, Houweling A, Schrier PI, Bos JL, Van der Eb AJ: Characterization of cells transformed by Ad5/Adl2 hybrid early region 1 plasmids. Virology (120): 422–432, 1982.

    Article  PubMed  CAS  Google Scholar 

  6. Bernards R, Schrier PI, Houweling A, Bos JL, Van der Eb AJ, Zijlstra M, Melief CJM: Tumorigenicity of cells transformed by adenovirus type 12 by evasion of T-cell immunity. Nature (305): 776–779, 1983.

    Article  PubMed  CAS  Google Scholar 

  7. Eddy BE, Grubbs GE, Young RD: Tumor immunity in hamsters infected with adenovirus 12 or simian virus 40. Proc Soc Exp Biol Med (117): 575–579, 1964.

    PubMed  CAS  Google Scholar 

  8. Trentin JJ, Bryan E: Virus-induced transplantation immunity to human adenovirus type 12 tumors of the hamster and mouse. Proc Soc Exp Biol Med (121) 1216–1219, 1966.

    PubMed  CAS  Google Scholar 

  9. Sjögren HO, Minowada J, Ankerst J: Specific transplantation antigens of mouse sarcomas induced by adenovirus type 12. J Exp Med (25): 689–701, 1967.

    Article  Google Scholar 

  10. Shiroki K, Shimojo H, Maeta Y, Hamada C: Tumor-specific transplantation and surface antigen in cellc transformed by the adenovirus 12 DNA fragments. Virology (99): 188–191, 1979.

    Article  PubMed  CAS  Google Scholar 

  11. Raska K, Morrongiello MP, Föhring B: Adenovirus type 12 tumor antigen. III. Tumorigenicity and immune response to syngeneic rat cells transformed with virions and isolated transforming fragment of adenovirus 12 DNA. Int J Cancer (26): 79–86, 1980.

    Article  PubMed  Google Scholar 

  12. Raska K, Dougherty J, Gallimore PH: Product of adenovirus type 2 early gene block El in transformed cells elicits cytolytic response in syngeneic rats. Virology (117): 530–535, 1982.

    Article  PubMed  Google Scholar 

  13. Schrier PI, Bernards R, Vaessen RTMJ, Houweling A, Van der Eb AJ: Expression of class I major histocompatibility antigens switched off by highly oncogenic adenovirus 12 in transformed rat cells. Nature (305): 771–775, 1983.

    Article  PubMed  CAS  Google Scholar 

  14. Van der Eb AJ, Bernards R, Schrier PI, Bos JL, Vaessen RTMJ, Jochemsen AG, Melief CJM: Altered expression of cellular gene in adenovirus-transformed cells, in: Van de Woude GF et al. (eds). Cancer Cells 2, Cold Spring Harbor Laboratory, 1984, pp 501–510.

    Google Scholar 

  15. Sood AK, Pereira D, Weissman SM: Isolation and partial nucleotide sequence of a cDNA clone for human histocompatibility antigen HLA-B by use of an oligodeoxynucleotide primer. Proc Natl Acad Sci USA (78): 616–620, 1981.

    Article  PubMed  CAS  Google Scholar 

  16. Van Ormondt H, Galibert F: Nucleotide sequences of adenovirus DNAs. Curr Topics Microbiol Immunol (110): 73–142, 1984.

    Google Scholar 

  17. Pettersson U, Virtanen A, Perricaudet M, Akusjärvi G: The messenger RNAs from the transforming region of human adenoviruses. Curr Topics Microbiol Immunol (109): 107–123, 1983.

    Article  CAS  Google Scholar 

  18. Bos JL, Jochemsen AG, Schrier PI, Van Ormondt H, Van der Eb AJ: Deletion mutants of region E1A of Adl2 El plasmids: effect of oncogenic transformation. Virology (129): 393–400, 1983.

    Article  PubMed  CAS  Google Scholar 

  19. Jochemsen AG, Bos JL, Van der Eb AJ: The first exon of region E1A genes of adenoviruses 5 and 12 encodes a separate functional protein domain. EMBO J (3): 2923–2927, 1984.

    PubMed  CAS  Google Scholar 

  20. Vaessen RTMJ, Bernards R, Oostra BA, Houweling A, Jochemsen AG, Bos JL, Van der Eb AJ: Expression of MHC genes in adenovirus:transformed cells. In: Bishop JM, Rowley JD and Greaves M (eds) Genes and Cancer. Alan R.Liss, Inc., New York 1984, pp 303–314.

    Google Scholar 

  21. Bernards R, Schrier PI, Bos JL, Van der Eb AJ: Role of adenovirus type 5 and 12 early region lb tumor antigens in oncogenic transformation. Virology (127): 45–53, 1983.

    Article  PubMed  CAS  Google Scholar 

  22. Mellow G, Föhring B, Dougherty T, Gallimore PH, Raska K: Tumorigenicity of adenovirus-transformed rat cells and expression of class I major histocompatibility antigens. Virology (134): 460–465, 1984.

    Article  PubMed  CAS  Google Scholar 

  23. Grosveld F, personal communication.

    Google Scholar 

  24. Yabe Y, Trentin JJ, Grant T: Cancer induction in hamsters by human type 12 adenovirus. Effect of age and of virus dose. Proc Soc Exp Biol Med (111): 343–344, 1982.

    Google Scholar 

  25. Kirschstein RL, Rabson AS, Peters EA: Oncogenic activity of adenovirus 12 in thymectonized BALB/c and C3H/HeN mice. Proc Soc Exp Biol Med (117): 198–200, 1964.

    PubMed  CAS  Google Scholar 

  26. Yohn DS, Funk CA, Kalninus VI, Grace JT: Sex-related resistance in hamsters to adenovirus 12 oncogenesis. Influence of thymectomy at three weeks of age. J Natl Cancer Inst (35): 617–624, 1965.

    PubMed  CAS  Google Scholar 

  27. Yohn DS, Funk CA, Grace JTf Sex-related resistance in hamsters to adenovirus 12 oncogenesis. III. Influence of immunologic impairment by thymectomy or cortisone. J Immunol (100): 771–780, 1968.

    PubMed  CAS  Google Scholar 

  28. Allison AC, Berman LD, Levey RH: Increased tumor induction by adenovirus type 12 in thymectonized mice and mice treated with anti-lymphocyte serum. Nature (215): 185–187, 1967.

    Article  PubMed  CAS  Google Scholar 

  29. Harwood, LMJ, Gallimore PH: A study on the oncogenicity of adenovirus type 2-transformed rat embryo cells. Int J Cancer (16): 498–508, 1975.

    Article  PubMed  CAS  Google Scholar 

  30. Van den Elsen P, De Pater S, Houweling A, Van der Eb AJ: The relationship between region Ela and Elb of human adenoviruses in cell transformation. Gene (18): 175–185, 1982.

    Article  PubMed  Google Scholar 

  31. Gallimore PH, McDougall JK, Chen LB: In vitro traits of adenovirus-transformed cell lines and their relevance to tumorigenicity in nude mice. Cell (10): 669–678, 1977.

    Article  PubMed  CAS  Google Scholar 

  32. Cook JL, Lewis AM: Host response to adenovirus 2-transformed hamster embryo cells. Cancer Res (39): 1455–1461, 1979.

    PubMed  CAS  Google Scholar 

  33. Lewis AM, Cook JL: 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 (42): 939–944, 1982.

    PubMed  Google Scholar 

  34. Lewis AM, Cook JL: The interphase between adenovirus-transformed cells and cellular immune response in the challanged host. Curr Toppics Microbiol Immunol (110): 1–22, 1984.

    Google Scholar 

  35. Graham FL, Abrahams PJ, Mulder C, Heyneker HL, Warnaar SO, De Vries FAJ, Fiers W, Van der Eb AJ: Studies on in vitro transformation by DNA and DNA fragments of human adenoviruses and simian virus 40. Cold Spring Harbor Symp Quant Biol (39): 637–650, 1974.

    Google Scholar 

  36. Gallimore PH, Paraskeva C: A study to determine the reasons for difference in the tumorigenicity of rat cell lines transformed by adenovirus 2 and adenovirus 12. Cold Spring Harbor Symp Quant Biol (44):703–713, 1980.

    PubMed  Google Scholar 

  37. Yabe Y, Samper I, Bryan E, Taylor G, Trentin JJ: Oncogenic effect of human adenovirus type 12 in mice. Science (143): 46–47, 1964.

    Article  PubMed  CAS  Google Scholar 

  38. Zinkernagel RM, Doherty PC. Restriction of in vitro T cell-mediated cytotoxity in lymphocytic choriomeningitis within a syngeneic or semi-allogeneic system. Nature (248) 701–702, 1974.

    Article  PubMed  CAS  Google Scholar 

  39. Zinkernagel RM, Oldstone MB: Cells that express viral antigens but lack H-2 determinants are not lysed by immune thymus-derived lymphocytes but are lysed by other antiviral immune attack mechanisms. Proc Natl Acad Sci USA (73): 3666–3670, 1976.

    Article  PubMed  CAS  Google Scholar 

  40. Föhring B, Gallimore PH, Mellow GH, Raska K: Adenovirus type 12 specific cell surface antigen in transformed cells is a product of the Elb early region Virology (131): 463–472, 1983.

    Article  PubMed  Google Scholar 

  41. Tanaka K, Isselbacker KJ, Khoury G, Jay G: Reversal of oncogenesis by the expression of a MHC class I gene. Science in press, 1985.

    Google Scholar 

  42. Raska K, 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 (123): 8–18, 1982.

    Article  PubMed  Google Scholar 

  43. Cook JL, Hibbs JB, Lewis AM: DNA virus-transformed hamster cell-host effector cell interactions: level of resistance to cytolysis correlated with tumorigenicity. Int J Cancer (30): 795–803, 1982.

    Article  PubMed  CAS  Google Scholar 

  44. Cook JL, Lewis AM: Differential NK cell and macrophage killing of hamster cells infected with non-oncogenic and oncogenic adenoviruses. Science (224): 612–614, 1984.

    Article  PubMed  CAS  Google Scholar 

  45. Sheil JM, Gallimore PH, Zimmer SG, Sopori ML. Susceptibility of adenovirus transformed rat cell lines to natural killer (NK) cells: direct correlation between NK resistance and in vivo tumourigenesis. J.Immunol (132): 1578–1582, 1984.

    PubMed  CAS  Google Scholar 

  46. Cook JL, Hauser J, Patch C, Lewis AM, Levine AS: Adenovirus 2 early gene expression promoter susceptibility to effector cell lysis of hybrids formed between adenovirus 2 and simian virus 40-transformed hamster cells. Proc Natl Acad Sci USA (80): 5995–5999, 1983.

    Article  PubMed  CAS  Google Scholar 

  47. Herberman RB, Holden HT: Natural cell-mediated immunity. Adv Cancer Res (27) 305–377, 1978.

    Article  PubMed  CAS  Google Scholar 

  48. Gooding LR: Characterization of a progressive tumor from CSH fibroblast transformed in vitro with SV40 virus. Immunoresistance in vivo correlates with phenotypic loss of H-2Kk J Immunol (129): 1306–1312, 1982.

    CAS  Google Scholar 

  49. Hui K, Grosveld F, Festenstein H: Rejection of transplantable AKR leukemia cells following MHC DNA-mediated cell transformation. Nature (311): 750–752, 1984.

    Article  PubMed  CAS  Google Scholar 

  50. Houweling A, Van den Elsen PJ, Van der Eb AJ: Partial transformation of primary rat cells by the leftmost 4.5% fragment of adenovirus 5 DNA. Virology (105) 537–550, 1980.

    Article  PubMed  CAS  Google Scholar 

  51. Van den Elsen PJ, Houweling A, Van der Eb AJ: Morphological transformation of human adenoviruses is determined to a large extent by gene products of region Ela. Virology (131): 242–246, 1983

    Article  PubMed  Google Scholar 

  52. Jones, N, Shenk T: Isolation of adenovirus type 5 hrt host range deletion mutants defective for transformation of rat embryo cells. Cell (17): 683–689, 1979.

    Article  PubMed  CAS  Google Scholar 

  53. Berk AJ, Lee F, Harrison T, Williams J, Sharp PA: Pre-early adenovirus 5 gene product regulate synthesis of early viral messenger RNAs. Cell (17): 935–944, 1979.

    Article  PubMed  CAS  Google Scholar 

  54. Nevins JR: Mechanism of activation of early viral transcription by the adenovirus E1A gene products. Cell (26): 213–220, 1981.

    Article  PubMed  CAS  Google Scholar 

  55. Ricciardi RP, Jones RL, Cepko CL, Sharp PA, Roberts BE: Expression of early adenovirus genes requires a viral-encoded acidic polypeptide. Proc Natl Acad Sci USA (78): 6121–6125, 1981.

    Article  PubMed  CAS  Google Scholar 

  56. Montell C, Fisher EF, Caruthers MH, Berk AJ: Resolving the functions of overlapping viral genes by site-specific mutagenesis at mRNA splice site. Nature (295): 380–384, 1982.

    Article  PubMed  CAS  Google Scholar 

  57. Carlock LR, Jones NC: Transformation-defective mutant of adenovirus type 5 containing a single altered Ela mRNA species. J Virol (40): 657–664, 1981.

    PubMed  CAS  Google Scholar 

  58. Shenk T, Jones N, Colby W, Fowlkes D: Functional analysis of adenovirus type 5 host range deletion mutants defective for transformation of rat embryo cells. Cold Spring Harbor Symop Quant Biol (44): 367–375, 1979.

    Google Scholar 

  59. Katze MG, Persson H, Philipson L: Control of adenovirus early gene expression: a post-transcriptional control mediated by region Ela products. Mol Cell Biol (1): 807–813, 1981.

    PubMed  CAS  Google Scholar 

  60. Katze MG, Persson H, Johansson BM, Philipson L: Control of adenovirus gene expression: cellular gene products restrict expression of adenovirus host-range mutants in non-permissive cells. J Virol (46): 50–59, 1983.

    PubMed  CAS  Google Scholar 

  61. Gaynor RB, Berk AJ: Cis-acting induction of adenovirus transcription Cell (33): 683–693, 1983.

    Article  PubMed  CAS  Google Scholar 

  62. Nevins JR: Induction of the synthesis of a 70.000 dalton mammalian heat shock protein by the adenovirus E1A gene product. Cell (29): 913–919, 1982.

    Article  PubMed  CAS  Google Scholar 

  63. Kao HT, Nevins JR: Transcriptional activation and subsequent control of the human heat shock gene during adenovirus infection. Mol Cell Biol (3): 2058–2065, 1983.

    PubMed  CAS  Google Scholar 

  64. Stein R, Ziff EB: HeLa cell -tubilin gene transcription by adenovirus 5 in paralel with viral early genes by an E1A dependent mechanism. Mol Cell Biol (4): 2792–2801, 1984.

    PubMed  CAS  Google Scholar 

  65. Beltz GA, Flint SJ: Inhibition of HeLa cell protein synthesis during adenovirus infection: restriction of cellular messenger RNA sequences to the nucleus. J Mol Biol (131): 353–373, 1979.

    Article  PubMed  CAS  Google Scholar 

  66. Bos JL, Ten Wolde-Kraamwinkel HC: The Elb promoter of Ad 12 in mouse L tk cells is activated by adenovirus region Ela. EMBO J (2): 73–76, 1983.

    PubMed  CAS  Google Scholar 

  67. Green MR, Treisman R, Maniatis T: Transcriptional activation of cloned human -globin genes by viral intermediate-early gene products. Cell (35) 137–148, 1983.

    Article  PubMed  CAS  Google Scholar 

  68. Svenson C, Akusjärvi G: Adenovirus 2 early region E1A stimulates expression of both viral and cellular genes. EMBO J (3): 789–794, 1984.

    Google Scholar 

  69. Gaynor RB, Hillman D, Berk AJ: Adenovirus early region 1A protein activates transcription of a nonviral gene introduced into mammalian cells by infection or transfection. Proc Natl Acad Sci USA (81): 1193–1197, 1984.

    Article  PubMed  CAS  Google Scholar 

  70. Curtois G, Berk A: Adenovirus E1A protein activation of an integrated viral gene. Embo J (3): 1145–1149, 1984.

    PubMed  CAS  Google Scholar 

  71. Baker CC, Ziff EB: Promoters and heterogeneous 5’ termini of the messenger RNAs of adenovirus serotype 2. J Mol Biol (149) 189–221, 1983.

    Article  Google Scholar 

  72. Borelli E, Hen R, Chambon P: Adenovirus 2 E1A products repress enhancer-induced stimulation of transcription. Nature (312): 608–612, 1984.

    Article  Google Scholar 

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Authors and Affiliations

  1. Sylvius Laboratories, Univerity of Leiden, Leiden, The Netherlands

    A. J. van der Eb & B. A. Oostra

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  1. A. J. van der Eb
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  1. Institute of Genetics, University of Cologne, 5000, Cologne 41, Federal Republic of Germany

    Walter Doerfler

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© 1986 Martinus Nijhoff Publishing, Boston

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van der Eb, A.J., Oostra, B.A. (1986). Expression of Class I Major Histocompatibility Antigens in Adenovirus-Transformed Cells. In: Doerfler, W. (eds) Adenovirus DNA. Developments in Molecular Virology, vol 8. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2293-1_10

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