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The Interface Between Adenovirus-Transformed Cells and Cellular Immune Response in the Challenged Host

  • A. M. LewisJr.
  • J. L. Cook
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 110)

Abstract

The discovery by Trentin et al. (1962) that human adenoviruses were capable of producing tumors when inoculated into hamsters created a major role for these agents in the field of viral oncology. As participants in this field, several of the adenovirus (Ad) serotypes are among the most thoroughly studied animal viruses. One of the primary objectives of the study of these agents as tumor viruses has been to elucidate the mechanisms that are associated with their capacity to convert normal cells to neoplastic cells that produce tumors in animals. In approaching this objective, theoretical and technical developments have focused current research on the structure, organization, and expression of the Ad genome, and much has been accomplished. The functional arrangement of the Ad2 genome has been determined and the DNA sequence structure of several Ad serotypes is far advanced. The processing of Ad RNA into cytoplasmic mRNA that is translated into viral proteins has provided new insights into the mechanisms of RNA transcription in eukaryotic organisms. The mode of replication of the Ad genomes is under intensive investigation. The regions of the viral genome that are associated with the conversion of normal cells to neoplastic cells have been located, and many of the proteins encoded by these genes have been identified and in some cases purified. For detailed discussions of these developments, we refer the reader to other chapters in this volume and to recent reviews by Flint (1980a, b), Persson and Philipson (1982), Challberg and Kelly (1982), and Doerfler (1982). In spite of these impressive accomplishments, the goal of defining the mechanism of Ad-induced carcinogenesis has remained elusive, and it is becoming increasingly apparent that the question of how viruses and neoplastic cells produce tumors in animals will most likely remain after understanding of the molecular mechanisms of cell transformation (as defined by the induction of immortality) in vitro has been reached. The complexities of the interactions between cells rendered neoplastic by adenoviruses and the cellular immune defenses of the potential animal host suggest that new concepts and approaches to the possible mechanism of viral carcinogenesis are needed.

Keywords

Syrian Hamster Adenovirus Type Human Adenovirus Hybrid Cell Line Rodent Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Akagi T, Ogawa K (1972) Relationship among tumorigenicity, T antigen, and virus-specific transplantation antigen in adenovirus type 12 transformed and tumor cells. Gan 63: 307–312PubMedGoogle Scholar
  2. Allison AC, Berman LD, Levey RH (1967) Increased tumor induction by adenovirus type 12 in thymectomized mice and mice treated with anti-lymphocyte serum. Nature 215: 185–187PubMedCrossRefGoogle Scholar
  3. Ankerst J, Sjögren HO (1969) Cross-reacting TSTAs in adeno 7 and 12 tumors demonstrated by 51Cr-cytotoxicity and isograft rejection tests. Int J Cancer 4: 279–287PubMedCrossRefGoogle Scholar
  4. Ankerst J, Sjögren HO (1970) Cross-reacting tumor-specific transplantation of antigens in tumors induced by adenoviruses 3, 14, and 12. Cancer Res 30: 1499–1505PubMedGoogle Scholar
  5. Berman LD (1967) On the nature of transplantation immunity in the adenovirus tumor system. J Exp Med 125: 983–999PubMedCrossRefGoogle Scholar
  6. Billingham RE, Sawchuck GH, Silvers WK (1960) The induction of tolerance of skin homografts in Syrian hamsters. Transplant Bull 26: 446–449CrossRefGoogle Scholar
  7. Challberg MD, Kelly TJ Jr (1982) Eukaryotic DNA replication: viral and plasmid model systems. Ann Rev Biochem 51: 901–934PubMedCrossRefGoogle Scholar
  8. Collins JL, Patek PQ, Cohn M (1981) Tumorigenicity and lysis by natural killers. J Exp Med 153: 89–106PubMedCrossRefGoogle Scholar
  9. Cook JL, Lewis AM Jr (1979) Host response to adenovirus 2-transformed hamster embryo cells. Cancer Res 39: 1455–1461PubMedGoogle Scholar
  10. Cook JL, Kirkpatrick CH, Rabson AS, Lewis AM Jr (1979a) Rejection of adenovirus 2-transformed cell tumors and immune responsiveness in Syrian hamsters. Cancer Res 39: 4949–4955PubMedGoogle Scholar
  11. Cook JL, Lewis AM Jr, Kirkpatrick CH (1979b) Age-related and thymus-dependent rejection of adenovirus 2-transformed cell tumors in the Syrian hamster. Cancer Res 39: 3335–3340PubMedGoogle Scholar
  12. Cook JL, Hibbs JB Jr, Lewis AM Jr (1980) Resistance of simian virus 40-transformed hamster cells to the cytolytic effect of activated macrophages: a possible factor in species-specific viral oncogenicity. Proc Natl Acad Sci USA 77: 6773–6777PubMedCrossRefGoogle Scholar
  13. Cook JL, Hibbs JB Jr, Lewis AM Jr (1982) DNA virus-transformed hamster cell-host effector cell interactions: level of resistance to cytolysis correlated with tumorigenicity. Int J Cancer 30: 795–803PubMedCrossRefGoogle Scholar
  14. Cook JL, Hauser J, Patch C, Lewis AM Jr, Levine AS (1983) Adenovirus 2 early gene expression promotes susceptibility to effector cell lysis of hybrids formed between adenovirus 2 and simian virus 40 transformed hamster cells. Proc Natl Acad Sci USA 80: 5995–5999PubMedCrossRefGoogle Scholar
  15. Doerfler W (1982) Uptake, fixation, and expression of foreign DNA in mammalian cells: the organization of integrated adenovirus DNA sequencer. In: Graf T, Jaenisch R (eds) Tumor viruses, Neoplastic Transformations, and Differentiation. Springer, Berlin Heidelberg New York, pp 127–194 (Current topics in microbiology and immunology, vol 101 )CrossRefGoogle Scholar
  16. Eddy BE, Grubbs GE, Young RD (1964) Tumor immunity in hamsters infected with adenovirus 12 or simian virus 40. Proc Soc Exp Biol Med 117: 575–579PubMedGoogle Scholar
  17. Flint SJ (1980a) Structure and organization of adenoviruses. In: Tooze J (ed) Molecular biology of tumor viruses. Part 2, DNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 383–442Google Scholar
  18. Flint SJ (1980b) Transformation by adenoviruses. In: Tooze J (ed) Molecular biology of tumor viruses. Part 2, DNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 547–576Google Scholar
  19. Foulds L (1969) Neoplastic development. Academic, LondonGoogle Scholar
  20. Gallimore PH (1972) Tumour production in immunosuppressed rats with cells transformed in vitro by adenovirus type 2. J Gen Virol 16: 99–102PubMedCrossRefGoogle Scholar
  21. Gallimore PH, Paraskeva C (1980) A study to determine the reasons for differences in the tumorigenicity of rat cell lines transformed by adenovirus 2 and adenovirus 12. Cold Spring Harbor Symp Quant Biol 44: 703–713PubMedCrossRefGoogle Scholar
  22. Gallimore PH, McDougall JK, Chen LB (1977) In vitro traits of adenovirus-transformed cell lines and their relevance to tumorigenicity in nude mice. Cell 10: 669–678PubMedCrossRefGoogle Scholar
  23. Gilden RV, Kern J, Freeman AE, Martin CE, McAllister RM, Turner HC, Huebner RJ (1968) T and tumor antigens of adenovirus group C-infected and transformed cells. Nature 219: 517–518PubMedCrossRefGoogle Scholar
  24. Girardi AJ, Hilleman MR, Zwickey RE (1964) Tests in hamsters for oncogenic quality of ordinary viruses including adenovirus type 7. Proc Soc Exp Biol Med 115: 1141–1150PubMedGoogle Scholar
  25. Green M, Mackey JK, Wold WSM, Rigden P (1979) Thirty-one human adenovirus serotypes (Ad1-Ad31) from five groups ( A-E) based upon DNA genome homologies. Virology 93: 481–492Google Scholar
  26. Haller O, Orn A, Gidlund M, Wigzell H (1980) In vivo activity of murine NK cells. In: Herberman RB (ed) Natural cell-mediated immunity against tumors. Academic, New York, pp 1105–1116Google Scholar
  27. Harwood LMJ, Gallimore PH (1975) A study of the oncogenicity of adenovirus type 2 transformed rat embryo cells. Int J Cancer 16: 498–508PubMedCrossRefGoogle Scholar
  28. Henney CS (1981) Do natural killer cells function through recognition of glycoconjugates on target cell membranes? In: Saunders JP, Daniels JC, Serrou B, Rosenfeld C, Denney CB (eds) Fundamental mechanisms in human cancer immunology. Elsevier/North Holland, New York, pp 465–475Google Scholar
  29. Herberman R (1981) Overview of role of macrophages, natural killer cells, and antibody dependent cellular cytotoxicity as mediators of biological response modification. In: Chirigos MA, Mitchel M, Mastrangelo MJ, Krim M (eds) Mediation of cellular immunity in cancer by immune modifiers. Raven, New York, pp 261–267Google Scholar
  30. Herberman RB, Ortaldo JR (1981) Natural killer cells: their role in defenses against disease. Science 214: 24–30PubMedCrossRefGoogle Scholar
  31. Huebner RJ (1967) Adenovirus-directed tumor and T antigens. In: Pollard M (ed) Perspectives in virology, vol 5. Academic, New York, pp 147–166Google Scholar
  32. Huebner RJ, Rowe WP, Lane WT (1962) Oncogenic effects in hamsters of human adenovirus types 12 and 18. Proc Natl Acad Sci USA 48: 2051–2058PubMedCrossRefGoogle Scholar
  33. Huebner RJ, Lane WT, Welch AD, Calabresi P, McCollum RW, Prusoff WH (1963a) Inhibition by 5-iododeoxyuridine of the oncogenic effects of adenovirus type 12 in hamsters. Science 142: 488–490PubMedCrossRefGoogle Scholar
  34. Huebner RJ, Rowe WP, Turner HC, Lane WT (1963 b) Specific adenovirus complement-fixing antigens in virus-free hamster and rat tumors. Proc Natl Acad Sci USA 50:379–389 Adenovirus-Transformed Cells and Cellular Immune Response 21Google Scholar
  35. Kiessling R, Wigzell H (1979) An analysis of the murine NK cell as to structure, function, and biological relevance. Immunol Rev 44: 165–208PubMedCrossRefGoogle Scholar
  36. Kirschstein RL, Rabson AS, Peters EA (1964) Oncogenic activity of adenovirus 12 in thymectomized BALB/c and C3H/HeN mice. Proc Soc Exp Biol Med 117: 198–200PubMedGoogle Scholar
  37. Kvist D, Östberg L, Persson H, Philipson L, Peterson PA (1978) Molecular association between transplantation antigens and cell surface antigen in adenovirus-transformed cell line. Proc Natl Acad Sci USA 75: 5674–5678PubMedCrossRefGoogle Scholar
  38. Lewis AM Jr, Cook JL (1979) Association of tumor induction by ultraviolet light-inactivated adenovirus 2-simian virus 40 recombinants with a specific segment of simian virus 40 DNA. J Natl Cancer Inst 63: 695–705PubMedGoogle Scholar
  39. Lewis AM Jr, Cook JL (1980) Presence of allograft-rejection resistance in simian virus 40-transformed hamster cells and its possible role in tumor development. Proc Natl Acad Sci USA 77: 2886–2889PubMedCrossRefGoogle Scholar
  40. Lewis AM Jr, Cook JL (1982) 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: 939–944PubMedGoogle Scholar
  41. McAllister RM, MacPherson I (1968) Transformation of a hamster cell line by adenovirus 12. J Gen Virol 2: 99–106PubMedCrossRefGoogle Scholar
  42. McAllister RM, Nicolson MO, Reed G, Kern J, Gilden RV, Huebner RJ (1969) Transformation of rodent cells by adenovirus 19 and other group D adenoviruses. J Natl Cancer Inst 43: 917–922PubMedGoogle Scholar
  43. Patch C, Hauser J, Lewis AM Jr, Levine AS (1983) Adenovirus 2 early gene expression reduces the tumor-inducing capacity of hybrid cells formed from simian virus 40- and adenovirus 2-transformed hamster embryo cells. Cancer Res 43: 2571–2575PubMedGoogle Scholar
  44. Persson H, Philipson L (1982) Regulation of adenovirus gene expression. In: Cooper M et al. (eds) Current topies in microbiology and immunology, vol 97. Springer, Berlin Heidelberg New York, pp 157–203CrossRefGoogle Scholar
  45. Persson H, Kvist S, Ostberg L, Peterson PA, Philipson L (1980) Adenoviral early glycoprotein E3–19K and its association with transplantation antigens. Cold Spring Harbor Symp Quant Biol 45: 509–517CrossRefGoogle Scholar
  46. Persson H, Katze MG, Philipson L (1982) Purification of a native membrane-associated adenovirus tumor antigen. J Virol 42: 905–917PubMedGoogle Scholar
  47. Rabson AS, Kirschstein RL, Paul FJ (1964) Tumors produced by adenovirus 12 in mastomys and mice. J Natl Cancer Inst 32: 77–87PubMedGoogle Scholar
  48. Rask L, Lindblom JB, Peterson PA (1974) Subunit structure of H-2 alloantigens. Nature 249: 833–835PubMedCrossRefGoogle Scholar
  49. Raska K Jr, Gallimore PH (1982) An inverse relation of the oncogenic potential of adenovirus transformed cells and their sensitivity to killing by syngeneic natural killer cells. Virology 123: 8–18PubMedCrossRefGoogle Scholar
  50. Raska K Jr, Morrongiello MP, Fohring B (1980) 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 7 Cancer 26: 79–86CrossRefGoogle Scholar
  51. Raska K Jr, Dougherty J, Gallimore PH (1982) Product of adenovirus type 2 early gene block E1 in transformed cells elicits cytolytic response in syngeneic rats. Virology 117: 530–535PubMedCrossRefGoogle Scholar
  52. Sehgal PB, Frazer NW, Darnell JE (1979) Early Ad2-transcription units: only promoter-proximal RNA continues to be made in the presence of DRB. Virology 94: 185–191PubMedCrossRefGoogle Scholar
  53. Shiroki K, Shimojo H, Maeta Y, Hamada C (1979) Tumor-specific transplantation and surface antigen in cells transformed by the adenovirus 12 DNA fragments. Virology 99: 188–191PubMedCrossRefGoogle Scholar
  54. Signas C, Katze MG, Persson H, Philipson L (1982) An adenovirus glycoprotein binds heavy chains of class I transplantation antigens from man and mouse. Nature 299: 175–177PubMedCrossRefGoogle Scholar
  55. Silver J, Hood L (1974) Detergent-solubilized H-2 alloantigen is associated with a small molecular weight polypeptide. Nature 249: 764–765PubMedCrossRefGoogle Scholar
  56. Sjögren HO, Ankerst J (1969) Effect of BCG and allogeneic tumor cells on adenovirus type 12 tumorigenesis in mice. Nature 221: 863–864PubMedCrossRefGoogle Scholar
  57. Sjögren HO, Minowada J, Ankerst J (1967) Specific transplantation antigens of mouse sarcomas induced by adenovirus type 12. J Exp Med 125: 689–701PubMedCrossRefGoogle Scholar
  58. Tevethia SS (1980) Immunology of simian virus 40. In: Klein G (ed) Viral oncology. Raven, New York, pp 581–602Google Scholar
  59. Trentin JJ, Bryan E (1966) Virus-induced transplantation immunity to human adenovirus type 12 tumors of the hamster and mouse. Proc Soc Exp Biol Med 121: 1216–1219PubMedGoogle Scholar
  60. Trentin JJ, Yabe Y, Taylor G (1962) The quest for human cancer viruses. Science 137: 835–841PubMedCrossRefGoogle Scholar
  61. Trentin JJ, Van Hoosier GL Jr, Samper L (1968) The oncogenicity of human adenoviruses in hamsters. Proc Soc Exp Biol Med 127: 683–689PubMedGoogle Scholar
  62. Vitetta ES, Uhr JW, Boyse EA (1975) Association of a /32-microglobulin-like subunit with H-2 and TL alloantigens J Immunol 114: 252–254Google Scholar
  63. Wadell G (1979) Classification of human adenoviruses by SDS-polyacrylamide gel electrophoresis of structural polypeptides. Intervirology 11: 47–57PubMedCrossRefGoogle Scholar
  64. Wadell G, Hammarskjöld ML, Winberg G, Varsanyi TM, Sundell G (1980) Genetic variability of adenoviruses. Ann NY Acad Sci USA 354: 16–42CrossRefGoogle Scholar
  65. Wilson MC, Fraeser NW, Darnell JE (1979) Mapping of RNA initiation sites by high doses of UV irradiation: evidence for three independent promoters within the left 11% of the Ad2 genome. Virology 94: 175–184PubMedCrossRefGoogle Scholar
  66. Yabe Y, Trentin JJ, Grant T (1962) Cancer induction in hamsters by human type 12 adenovirus. Effect of age and of virus dose. Proc Soc Exp Biol Med 111: 343–344Google Scholar
  67. Yabe Y, Samper L, Grant T, Trentin JJ (1963) Cancer induction in hamsters by human type 12 adenovirus. Effect of route of injection. Proc Soc Exp Biol Med 113: 221–224Google Scholar
  68. Yabe Y, Samper L, Bryan E, Taylor G, Trentin J (1964) Oncogenic effect of human adenovirus type 12 in mice. Science 143: 46–47PubMedCrossRefGoogle Scholar
  69. Yohn DS, Funk CA, Kalnins VI, Grace JT Jr (1965) Sex-related resistance in hamsters to adenovirus-12 oncogenesis. Influence of thymectomy at three weeks of age. J Natl Cancer Inst 35: 617–624Google Scholar
  70. Yohn DS, Funk CA, Grace JT (1968) Sex-related resistance in hamsters to adenovirus 12 oncogenesis. III. Influence of immunologic impairment by thymectomy or cortisone. J Immunol 100: 771–780Google Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1984

Authors and Affiliations

  • A. M. LewisJr.
    • 1
  • J. L. Cook
    • 2
  1. 1.Laboratory of Molecular Microbiology, National Institute of Allergy and Infectious DiseasesNational Institutes of HealthBethesdaUSA
  2. 2.Department of MedicineNational Jewish Hospital and Research CenterDenverUSA

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