The Strategy of a Search for Viral Involvement in Human Cancer

  • F. Kingsley Sanders


The first suggestions that viruses could be concerned in the causation of neoplasia in birds were made over 60 years ago (Ellermann and Bang, 1908; Rous, 1911), to be followed, 20–30 years later, by compelling evidence (Bittner, 1942; Shope and Hurst, 1933; Gross, 1951) that viruses could similarly cause tumors in mammals. However, it is only recently that serious consideration has been given to the possibility that such a situation could also obtain in man. In principle, this has been because morphological, immunological, and biochemical, as well as biological, studies of animal model systems have established an association between viruses and neoplasms, particularly leukemias and sarcomas, in a whole range of mammalian species, extending from mice to primates (Dameshek and Dutcher, 1970), but similar studies have not so far led to the isolation and characterization of an authentic human cancer virus. This chapter represents an attempt to discover why this should be so, to decide what kind of evidence might be needed in the future to indicate viral involvement in the genesis of any one human tumor, and to see how current studies measure up to the criteria adopted.


Herpes Simplex Virus Type Herpes Virus Rous Sarcoma Virus Feline Leukemia Virus Tissue Culture Supernatant 
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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  1. Aaronson, S. A., Todaro, G. J., and Scolnick, E. M., 1971, Induction of murine C-type viruses from clonal lines of virus-free BALB/3T3 cells, Science 174: 157.PubMedCrossRefGoogle Scholar
  2. Allen, P. T., Newton, W. A., Jr., Georgiades, J., Maruyama, K., East, J. L., Bowen, J. M., and Dmochowski, L., 1973, Studies on transforming activities from human solid tumor cells following co-cultivation with human leukemic bone marrow cells, in: Proceedings of the Sixth Miles International Symposium on Molecular Biology, Baltimore.Google Scholar
  3. Andervont, H. P., (ed.), 1966, Suggestions for the classification of oncogenic RNA viruses, J. Natl. Cancer Inst. 37:395.Google Scholar
  4. Andrewes, C. H., 1967, The Natural History of Viruses, Weidenfeld and Nicolson, London. Axel, R., Gulati, N., and Spiegelman, S., 1973, Particles containing RIDP and virus-related RNA in human breast cancers, Proc. Natl. Acad. Sci. 69: 3133.Google Scholar
  5. Baltimore, D., 1970, Viral RNA-dependent DNA polymerase, Nature (Lond.) 226:1209. Baluda, M. A., 1972, Widespread presence in chickens of DNA complementary to the RNA genome of avian leukosis viruses, Proc. Natl. Acad. Sci. 69: 576.Google Scholar
  6. Becker, Y., and Weinberg, A., 1972, Molecular events in the biosynthesis of Epstein—Barr virus in Burkitt lymphoblasts, in: Oncogenesis and Herpesviruses, p. 326, International Agency for Research in Cancer, Lyon.Google Scholar
  7. Benveniste, R. E., and Todarok, G. J., 1973, Homology between type C-viruses of various species as determined by molecular hybridization, Proc. Natl. Acad. Sci. 70: 3316.PubMedCrossRefGoogle Scholar
  8. Biggs, P. M., 1968, Marek’s disease: Current state of knowledge, Curr. Topics Microbiol Immunol. 43: 93.Google Scholar
  9. Bittner, J. J., 1942, Hormones, susceptibility, and milk influence in cancer, Cancer Res. 2:710. Bittner, J. J., 1952, Transfer of the agent for mammary cancer in mice by the male, Cancer Res. 12: 387.Google Scholar
  10. Bolton, E. T., and McCarthy, B. J., 1962, A general method for the isolation of RNA complementary to DNA, Proc. Natl. Acad. Sci. 48: 1390.PubMedCrossRefGoogle Scholar
  11. Boyer, S., Porter, I. and Weilbacher, R., 1962, Electrophoretic heterogeneity of glucose-6phosphate dehydrogenase and its relationship to enzyme deficiency in man, Proc. Natl. Acad. Sci. 48:1868.Google Scholar
  12. Boyland, E., 1963, The Biochemistry of Bladder Cancer,Charles C Thomas, Springfield, Ill.Google Scholar
  13. Boyse, E. A., Old, L. J. and Stockert, E., 1972, The relation of linkage group IX to leukemogenesis in the mouse, in: RNA Viruses and Host Genome in Oncogenesis (P. Emmelot and P. Bentvelsen,), p. 171, North-Holland, Amsterdam.Google Scholar
  14. Buonassisi, F., Sato, G., and Cohen, H. T., 1962, Hormone producing cultures of adrenal and pituitary tumor origin, Proc. Natl. Acad. Sci. 48:1184.Google Scholar
  15. Burkitt, D. C., 1962, Determining the climatic limitations of a children’s cancer common in Africa, Brit. Med. J. 27:1019.Google Scholar
  16. Burns, W., and Black, P., 1968, Analysis of simian virus 40—induced transformation of hamster kidney clones in vitro. V. Variability of virus recovery from cell clones inducible with mitomycin C and cell fusion, J. Virol. 2: 606.PubMedGoogle Scholar
  17. Butel, J. S., Tevethia, S. S., and Melnick, J. L., 1972, Oncogenesis and cell transformation by papova virus SV40: The role of the viral genome, Advan. Cancer Res. 15:1.Google Scholar
  18. Castro, J. E., and Hamilton, D. N., 1972, Human tumour xenografts, Brit. J. Surg. 59: 312.PubMedCrossRefGoogle Scholar
  19. Centifanto, Y. M., Drylie, D. M., and Deardourff, S. L., 1972, Herpes-virus type 2 in the male genitourinary tract, Science 178:318.Google Scholar
  20. Churchill, A. E., and Biggs, P. M., 1967, Agent of Marek’s disease in tissue culture, Nature (Lond.) 215: 528.CrossRefGoogle Scholar
  21. Cleaver, J. E., 1969, Xeroderma pigmentosum: A human disease in which an initial stage of DNA repair is defective, Proc. Natl. Acad. Sci. 63: 428.PubMedCrossRefGoogle Scholar
  22. Dameshek, W., and Dutcher, R. M., 1970, Proceedings of the Fourth International Symposium on Comparative Leukemia Research, Cherry Hill, N.Y., 1969, Karger, Basel and New York.Google Scholar
  23. Darai, G., and Munk, K., 1973, Human embryonic lung cells abortively infected with herpesvirus hominis type 2 show some properties of cell transformation, Nature (Lond.) 241:268.Google Scholar
  24. De Harven, E., 1968, Morphology of murine leukemic viruses, in: Experimental Leukemias ( M. Rich, ed.), p. 97, Appleton Cross, New York.Google Scholar
  25. Dmochowski, L., Seman, G., and Gallagher, H. S., 1969, Viruses as possible etiologic factors in human breast cancer, Cancer 24:1241.Google Scholar
  26. Doll, R., and Hill, A. B., 1952, A study of the aetiology of carcinoma of the lung, Brit. Med. J. 2:1271.Google Scholar
  27. Duff, R., and Rapp, F., 1971, Oncogenic transformation of hamster cells after exposure to herpes simplex virus type 2, Nature (Lund.) 233: 48.Google Scholar
  28. Eidson, C. S., Klever, S. H., and Anderson, D. P., 1972, Vaccination against Marek’s disease, in: Oncogenesis and Herpesviruses, p. 147, International Agency for Research in Cancer, Lyon.Google Scholar
  29. Eisinger, M., 1973, Human lymph nodes, in: Tissue Culture Methods and Applications ( P. F. Kruse and M. D. Patterson, eds.), p. 65, Academic Press, New York and London.Google Scholar
  30. Eisinger, M., Fox, S. M., De Harven, E., Biedler, J. L., and Sanders, F. K., 1971, Virus-like agents from patients with Hodgkin’s disease, Nature (Lond.) 233: 104.CrossRefGoogle Scholar
  31. Ellermann, V., and Bang, O., 1908, Experimentelle Leukemia bei Huhnern, Zentralbi. Bakteriol. Abt. I (Orig.) 46: 595.Google Scholar
  32. Epstein, M. A., and Achong, B. C., 1973, The EB virus, Am. Rev. Microbio. 27: 1624.Google Scholar
  33. Epstein, M. A., Achong, B. G., and Barr, Y. M., 1964, Virus particles in cultured lymphoblasts from Burkitt’s malignant lymphoma, Lancet 1: 702.PubMedCrossRefGoogle Scholar
  34. Feldman, S. P., Schlom, J., and Spiegelman, S., 1973, Further evidence for oncornaviruses in human milk: The production of cores, Proc. Natl. Acad. Sci. 70:1976.Google Scholar
  35. Fialkow, P. J., Thomas, E. D., Bryant, J. I., and Neumann, P. E., 1971, Leukemic transformation of engrafted human bone marrow cells in vivo, Lancet 1: 251.PubMedCrossRefGoogle Scholar
  36. Fogel, M., and Sachs, L., 1970, Induction of virus synthesis in polyoma tranformed cells by ultraviolet light and mitomycin C, Virology 40:174.Google Scholar
  37. Frenkel, N., Roizmann, B., Cassai, Z., and Nahmias, A., 1972, A DNA fragment of herpes simplex 2 and its transcription in human cervical cancer tissue, Proc. Natl. Acad. Sci. 69: 3784.PubMedCrossRefGoogle Scholar
  38. Gallo, R. C., Yang, S. S., and Ting, R. C., 1970, RNA dependent DNA polymerase of human acute leukemia cells, Nature (Loud.) 228: 927.CrossRefGoogle Scholar
  39. Gallo, R. C., Miller, N. R., Saxinger, W. C., and Gillespie, D., 1973, Primate RNA tumor virus-like DNA synthesized endogenously by RNA-dependent DNA polymerase in virus-like particles from fresh human acute leukemic blood cells, Proc. Natl. Acad. Sci. 70: 3219.PubMedCrossRefGoogle Scholar
  40. Deering, G., Aoki, T., and Old, L. J., 1970, Shared viral antigen of mammalian leukemia viruses, Nature (Lond.) 226: 265.CrossRefGoogle Scholar
  41. Gelb, L. D., Kohne, D. E., and Martin, M. A., 1971, Quantitation of SV40 sequences in African green monkey, mouse and virus-transformed cell genomes, J. Mol. Biol. 57: 129.PubMedCrossRefGoogle Scholar
  42. Gerber, P., Virogenic hamster tumor cells: Induction of virus synthesis, Science 145: 833.Google Scholar
  43. Gerber, P., 1972, Activation of Epstein—Barr virus by 5-bromodeoxyuridine in “virus-free” human cells,Proc. Natl. Acad. Sci. 69: 83.CrossRefGoogle Scholar
  44. Gerber, P., Whang-Peng, J., and Monroe, J. H., 1969, Transformation and chromosome changes induced by Epstein—Barr virus in normal human leucocyte cultures, Proc. Natl. Acad. Sci. 63: 740.CrossRefGoogle Scholar
  45. Gillespie, D., and Spiegelman, S., 1965, A quantitative assay for DNA-RNA hybrids with DNA immobilized on a membrane, J. Mol. Biol. 12: 829.PubMedCrossRefGoogle Scholar
  46. Giraldo, G., Bethe, E., Coeur, P., Vogel, C. L., and Dhru, P. S., 1972, Kaposis sarcoma: A new model in the search for viruses associated with human malignancies, J. Natl. Cancer. Inst. 49: 1495PubMedGoogle Scholar
  47. Grand, C. G., 1947, Tissue culture studies of lymph nodes of Hodgkin’s disease, Cancer Res. 7: 49.PubMedGoogle Scholar
  48. Gross, L., 1951, “Spontaneous” leukemia developing in C3H mice following inoculation, in infancy, with A-K leukemic extracts, or AK embryos, Proc. Soc. Exp. Biol. Med. 103:509.Google Scholar
  49. Gross, L., 1970, Oncogenic Viruses, 2nd ed., Pergamon Press, New York and London. Hammond, E. C., 1968, Quantitative relation between cigarette smoking and death rates, Natl. Cancer Inst. Monogr. 28: 3.Google Scholar
  50. Hehlmann, R., Kufe, D., and Spiegelman, S., 1972a, RNA in human leukemic cells related to the RNA of a mouse leukemia virus, Proc. Natl. Acad. Sci. 69: 435.PubMedCrossRefGoogle Scholar
  51. Hehlmann, R., Kufe, D., and Spiegelman, S., 19726, Viral related RNA in Hodgkin’s disease and other human lymphomas, Proc. Natl. Acad. Sci. 69: 1727.Google Scholar
  52. Henle, G., and Henle, W., 1966, Immunofluorescence in cells derived from Burkitt’s lymphoma, J. Bacteriol. 91: 1248PubMedGoogle Scholar
  53. Henle, W., Diehl, V., Kohn, G., Zur Hausen, H., and Henle, G., 1967, Herpes-type virus and chromosome marker in normal leukocytes after growth with irradiated Burkitt cells, Science 157: 1064.PubMedCrossRefGoogle Scholar
  54. Henle, G., Henle, W., and Diehl, V., 1968, Relation of Burkitt’s tumor-associated herpes-type virus to infectious mononucleosis, Proc. Natl. Acad. Sci. 59: 94.PubMedCrossRefGoogle Scholar
  55. Henle, G., Henle, W., Klein, G., Gunvèn, P., Clifford, P., Morrow, R. H., and Ziegler, J. L., 1971, Antibodies to early Epstein—Barr virus-induced antigens in Burkitt’s lymphoma, J. Natl. Cancer Inst. 46: 861.PubMedGoogle Scholar
  56. Higginson, J., 1967, Etiological factors in gastrointestinal cancer in man, in: Proceedings of the 9th International Cancer Congress, Tokyo, 1966, VICC Monogr. 10: 30.CrossRefGoogle Scholar
  57. Hirai, K., and Defendi, V., 1971, Homology between SV40 DNA and DNA of normal and SV-40 transformed Chinese hamster cells, Biochem. Biophys. Res. Commun. 42: 714.PubMedCrossRefGoogle Scholar
  58. Hirsch, M. S., Black, P. H., and Proffit, M. R., 1971, Immunosuppression and oncogenic virus infections, Fed. Proc. 30: 1852.Google Scholar
  59. Hirsch, M. S., Phillips, S. M., Solnik, C., Black, P. H., Schwartz, R. S., and Carpenter, C. B., 1972, Activation of leukemic viruses by graft-versus-host and mixed lymphocytic in vitro, Proc. Natl. Acad. Sci. 69: 1069.PubMedCrossRefGoogle Scholar
  60. Hirshaut, Y., Glade, P., Moses, H., Manaker, R., and Chesin, L., 1968, Association of herpes-like virus infection with infectious mononucleosis, Am. J. Med. 47: 520.CrossRefGoogle Scholar
  61. Hollinshead, A. C., and Tarro, G., 1973. Soluble membrane antigens of lip and cervical carcinomas: Reactivity with antibody for herpesvirus non-virion antigens, Science 179: 698.PubMedCrossRefGoogle Scholar
  62. Hoyer, B. H., McCarthy, B. J., and Bolton, E. T., 1964, A molecular approach in the systematics of higher organisms, Science 144: 959.CrossRefGoogle Scholar
  63. Hsiung, G. D., 1968, Latent virus infections in primate tissues with special reference to simian viruses, Bacteriol. Rev. 32: 185.PubMedGoogle Scholar
  64. Huebner, R. J., and Todaro, G. J., 1970, Oncogenesis of RNA tumor viruses as determinants of cancer, Proc. Natl. Acad. Sci. 64: 1087.CrossRefGoogle Scholar
  65. Hull, R. N., 1964, in: The Herpesvirus (A. S. Kaplan, ed.), p. 390, Academic Press, New York and London.Google Scholar
  66. Igel, H., Huebner, R., Turner, H., Kotin, P., and Falk, H., 1969, Mouse leukemia virus activation by chemical carcinogens, Science 160:1624. International Agency for Research in Cancer, 1972, Oncogenesis and Herpesviruses, Lyon.Google Scholar
  67. Jarrett, O., Laird, H., and Hay, D., 1969, Growth of feline leukemia virus in human cells, Nature (Lond.) 224: 1208.CrossRefGoogle Scholar
  68. Jarrett, W. F. H., Martin, W. B., Crichton, G. W., Dalton, R. G., and Stewart, M. F., 1964, Leukemia in the cat: Transmission experiments with leukemia (lymphosarcoma), Nature (Lond.) 202: 566.CrossRefGoogle Scholar
  69. Kaplan, H. S., 1967, On the natural history of the murine leukemias (presidential address), Cancer Res. 27: 1325.PubMedGoogle Scholar
  70. Klein, G., 1972, EBV-associated membrane antigens, in: Oncogenesis and Herpesviruses, p. 295, International Agency for Research in Cancer, Lyon.Google Scholar
  71. Klein, E., van Furth, R., Johansson, B., Ernberg, I., and Clifford, P., 1972, Immunoglobulin synthesis as cellular marker of malignant lymphoid cells, in: Oncogenesis and Herpesviruses, p. 253, International Agency for Research in Cancer, Lyon.Google Scholar
  72. Koprowski, H., Jensen, F., and Steplewski, Z., 1967, Activation of production of infectious tumor virus SV40 in heterokaryon cultures, Proc. Natl. Acad. Sci. 61: 42.Google Scholar
  73. Kufe, D., Hehlman, R., and Spiegelman, S., 1972, Human sarcomas contain RNA related to the RNA of a mouse leukemia virus, Science 175: 182.PubMedCrossRefGoogle Scholar
  74. Kufe, D., Magrath, V., Ziegler, V., and Spiegelman, S., 1973, Burkitt’s tumors contain particles encapsulating RIDP and high molecular weight virus-related RNA, Proc. Natl. Acad. Sci. 70: 737.PubMedCrossRefGoogle Scholar
  75. Kuff, E. L., Wivel, N. H., and Lueders, K. K., 1968, The extraction of intracisternal A-particles from a mouse plasma-cell tumor, Cancer Res. 28: 2137.PubMedGoogle Scholar
  76. Lemcke, R. M., 1971, Sizing small organisms, Nature (Lond.) 229: 492.CrossRefGoogle Scholar
  77. Levine, A. S., Oxman, M. N., Henry, P. H., Levin, M. J., Diamondopoulos, G. T., and Enders, J. F., 1970, Virus-specific deoxyribonucleic acid in simian virus 40–exposed hamster cells: Correlation with S and T antigens, J. Virol. 6: 199.PubMedGoogle Scholar
  78. Lowy, D. R., Rowe, W. P., Teich, N., and Hartley, J. W., 1971, Murine leukemia virus: High-frequency activation in vitro by 5-iodo-deoxyuridine and 5-bromo-deoxyuridine, Science 174: 155.PubMedCrossRefGoogle Scholar
  79. Lukes, R. F., and Butler, J. J., 1965, The pathology and nomenclature of Hodgkin’s disease, Cancer Res. 26:1063.Google Scholar
  80. Macpherson, I., and Montagnier, L., 1964, Agar suspension culture for the selective assay of cells transformed by polyoma virus, Virology 23: 29.CrossRefGoogle Scholar
  81. Markov, G. G., Bradrarova, I., Mintchera, A., Petrov, P., Shushkov, N., and Taner, R. G., 1969, Mycoplasma contamination of cell cultures: Interference with 32P labeling pattern of RNA, Exp. Cell. Res. 57: 374.PubMedCrossRefGoogle Scholar
  82. Melendez, L. V., Hunt, R. D., Daniel, M. D., Fraser, C. E. O., Barahana, H. H., Garcia, F. G., and King, N. W., 1972, Lymphoma viruses of monkeys; herpesvirus saimiri and herpesvirus ateles, the first oncogenic herpesviruses of primates—A review, in: Oncogenesis and Herpesvirus, p. 451, International Agency for Research in Cancer, Lyon.Google Scholar
  83. Miller, G., and Lipmann, M., 1973, Release of infectious Epstein–Barr virus by transformed marmoset leukocytes, Proc. Natl. Acad. Sci. 70: 190.PubMedCrossRefGoogle Scholar
  84. Miller, G., Shope, T., Lisco, H., Stitt, D., and Lipmann, M., 1972, Epstein–Barr virus: Transformation, cytopathic changes, and viral antigens in squirrel monkey and marmoset leukocytes, Proc. Natl. Acad. Sci. 69: 383.PubMedCrossRefGoogle Scholar
  85. Miller, J. M., and Olson, C., 1972, Precipitating antibody to an internal antigen of the C-type virus associated with bovine lymphosarcoma, J. Natl. Cancer Inst. 49:1459.Google Scholar
  86. Moore, D. H., Charney, J., Kramarsky, B., Lasfargues, E. Y., Sarkar, N. H., Brennan, M. J., Burrows, J. H., Surat, S. M., Paymaster, J. C., and Vaidya, A. B., 1971, Search for a human breast cancer virus, Nature (Land.) 229: 611.CrossRefGoogle Scholar
  87. Morton, D. L., and Malmgren, R. A., 1968, Human osteosarcomas: Immunological evidence suggesting an associated infectious agent, Science 162:-279.Google Scholar
  88. Murray, R. F., Hubbs, J., and Payne, B., 1971, Possible clonal origin of common warts (verruca vulgaria), Nature (Land.) 232: 50.CrossRefGoogle Scholar
  89. Nahmias, A. J., 1969, Association of genital herpesvirus with cervical cancer, Int. Virol. 1: 187.Google Scholar
  90. Nahmias, A. J., Naib, Z. M., and Josey, W. E., 1971, Herpesvirus hominis type 2 infection: Association with cervical cancer, and perinatal disease, Perspect. Virol. 7: 73.Google Scholar
  91. National Cancer Institute, 1966, Viruses of laboratory rodents, Natl. Cancer Inst. Monogr., No. 0.Google Scholar
  92. Ilsson, K., 1971, High frequency establishment of human immunoglobulin producing lymphoblastoid lines from normal and malignant lymphoid tissue and peripheral blood, Int. J. Cancer 8: 432.Google Scholar
  93. Nilsson, K., Klein, G., Henle, G., and Henle, W., 1972, The rôle of EBV in the establishment of lymphoblastoid cell lines from adult and foetal lymphoid tissue, in: Oncogenesis and Herpesviruses, p. 285, International Agency for Research in Cancer, Lyon.Google Scholar
  94. Niven, J. S. F., Armstrong, J. A., Andrewes, C. H., Pereira, H. G., and Valentine, R. C., 1961, Subcutaneous “growths” in monkeys produced by a pox virus, J. Pathol. Bacteriol. 81:1.Google Scholar
  95. Nowinski, R. C., Old, L. J., Sarkar, N. H., and Moore, D. H., 1970, Common properties of the oncogenic RNA viruses (oncornaviruses), Virology 42: 1152.PubMedCrossRefGoogle Scholar
  96. Nowinski, R. C., Old, L. J., O’Donnell, P. V., and Sanders, F. K., 1971, Serological identification of hamster oncornaviruses, Nature New Biol. 230: 282.PubMedGoogle Scholar
  97. Officer, J. E., Telson, N., Estes, J. D., Fontanilla, E., Rongey, R. W., and Gardner, M. B., 1973, Isolation of a neurotropic type C virus, Science 181: 945.Google Scholar
  98. Old, L. J., Boyse, E. A., Geering, G., and Oettgen, H. F., 1968, Serologic approaches to the study of cancer in animals and in man, Cancer Res. 28: 1288.Google Scholar
  99. Olson, C., Miller, L. D., Miller, J. M., and Hoss, H. E., 1972, Transmission of lymphosarcoma from cattle to sheep, J. Natl. Cancer Inst. 49:1463.Google Scholar
  100. Padgett, B. L., Walker, D. L., Zu Rhein, G. M., Eckroade, R. J., and Dessel, B. H., 1971, Cultivation of papova-like virus from human brain with progressive multifocal leukoencephalopathy, Lancet 1:1257.Google Scholar
  101. Pantelouris, E. M., 1971, Observations in the immunobiology of “nude” mice, Immunology 20: 247.PubMedGoogle Scholar
  102. Pantelouris, E. M., and Hair, J., 1970, Thymus dysgenesis in nude (nu/nu) mice, J. Embryol. Exp. Morphol. 24: 615.PubMedGoogle Scholar
  103. Payne, L. N., Pani, P. H., and Weiss, R., 1971, A dominant epistatic gene which inhibits cellular susceptibility to RSV (RA V-o), J. Gen. Virol. 13: 455.PubMedCrossRefGoogle Scholar
  104. Pontén, J., 1967, Spontaneous lymphoblastoid transformation of long-term cell cultures from human malignant lymphoma, Int. J. Cancer 2: 311.PubMedCrossRefGoogle Scholar
  105. Pott, P., 1775, Chirurgical Observations,London.Google Scholar
  106. Pulvertaft, R. J., 1965, A study of malignant tumors in Nigeria by short-term tissue culture, J. Clin. Pathol. 18: 261.Google Scholar
  107. Pulvertaft, R. J., 1967, Unpublished data quoted by Zur Hausen, H., Henle, W., Hummeler, K., Diehl, V., and Henle, G., Comparative study of cultured Burkitt tumor cells by immunofluorescence, autoradiography and electronmicroscopy, J. Virol. 1: 830.Google Scholar
  108. Rapp, F., Jui-Lies, H. L., and Jerkovsky, M., 1973, Transformation of mammalian cells by DNA-containing viruses following photodynamic inactivation. Virology 55: 339.PubMedCrossRefGoogle Scholar
  109. Reedman, B. M., and Klein, G., 1973, Cellular localization of an Epstein—Barr virus (EBV)—associated complement-fixing antigen in producer and non-producer lymphoblastoid cell lines, Int. J. Cancer 11: 499.PubMedCrossRefGoogle Scholar
  110. Roizman, B., and Spear, P., 1970, Herpesviruses: Current information on the composition and structure, in: Comparative Virology, p. 186, Academic Press, New York.Google Scholar
  111. Rotkin, I. D., 1973, A comparison review of key epidemiological studies in cervical cancer related to current search for transmissible agents, Cancer Res. 33:1353.Google Scholar
  112. Rottino, A., 1949a, In vitro studies of lymph nodes involved in Hodgkin’s disease. I. Liquefaction of culture medium, Arch. Pathol. (Chicago) 47: 317.Google Scholar
  113. Rottino, A., 19496, In vitro studies of lymph nodes involved in Hodgkin’s disease. II. Tissue culture studies; formation, behavior and significance of the multinucleated giant cell, Arch. Pathol. (Chicago) 47:328.Google Scholar
  114. Rous, P., 1911, A sarcoma of the fowl transmissible by an agent from the tumor cells, J. Exp. Med. 13: 397.PubMedCrossRefGoogle Scholar
  115. Sabin, A., 1965, Manifestations of latent viral genetic material in experimentally produced ancers and search for such manifestations in human cancers, Israel J. Med. Sci. 1: 93.PubMedGoogle Scholar
  116. Sabin, A. B., and Tarro, G., 1973, Herpes simplex and herpes genitalis viruses in etiology of ome human cancers, Proc. Natl. Acad. Sci. 70: 3225.CrossRefGoogle Scholar
  117. Sambrook, J., Westphal, H., Srinivasan, P. R., and Dulbecco, R., 1968, The integrated state of DNA in SV-40 transformed cells, Proc. Natl. Acad. Sci. 60:1288.Google Scholar
  118. Sanders, F. K., 1971, Problems in the study of oncogens in vitro, Med. Clin. North Am. 55: 653.Google Scholar
  119. Sanders, F. K., 1973, The presence of viruses in uninoculated tissue cultures: Sources and methods of detection, in: Contamination in Tissue Culture ( J. Fogh, ed.), p. 243, Academic Press, New York and London.Google Scholar
  120. Sarin, P. S., Abnell, J. and Gallo, R. C., 1973, in: International Symposium on Control of Transcription (A. Hollander, ed.), Plenum Press, New York.Google Scholar
  121. Sarngadhavan, M. G., Sarin, P. S., Reitz, M. S., and Gallo, R. C., 1972, Reverse transcriptase activity of human acute leukemic cells: Purification of the enzyme response to AMV 70S RNA and characterization of the DNA product, Nature New Biol., 240: 67.Google Scholar
  122. Schlom, J., and Spiegelman, S., 1971. Simultaneous detection of reverse transcriptase and igh molecular weight RNA unique to oncogenic RNA viruses, Science 174: 840.PubMedCrossRefGoogle Scholar
  123. Shope, R. E., and Hurst, E. W., 1933, Infectious papillomatosis of rabbits, J. Exp. Med. 58: 607.PubMedCrossRefGoogle Scholar
  124. Shope, T., DeChairo, D., and Miller, G., 1973, Malignant lymphoma in cottontop marmosets fter inoculation with Epstein—Barr virus, Proc. Natl. Acad. Sci. 70: 2487.PubMedCrossRefGoogle Scholar
  125. Sivak, A., and van Duuren, B., 1967, Phenotypic expression of transformation: Induction in cell culture by a phorbol ester, Science 157:1443.Google Scholar
  126. Spiegelman, S., Axel, R., and Schlom, J. 1972a, Virus-related RNA in human and mouse mammary tumors, J. Natl. Cancer Inst. 48:1205.Google Scholar
  127. Spiegelman, S., Schlom, J., Axel., R., and Kufe, D., 1972b, Molecular probing for a viral etiology of human cancer, University of Texas, M. D. Anderson Hospital and Tumor Institute, 25th Annual Symposium in Fundamental Cancer Research.Google Scholar
  128. Stephenson, J. R., and Aaronson, S. A., 1971, Murine sarcoma and leukemia viruses: Genetic differences determined by RNA—DNA hybridization, Virology 46: 480.PubMedCrossRefGoogle Scholar
  129. Stewart, J., and Ferguson-Smith, M., 1958, Klinefelter’s syndrome: Genetic studies, Lancet 2: 117.PubMedCrossRefGoogle Scholar
  130. Stewart, S. E., Kasmi, G., Jr., Draycott, C., and Ben, T., 1972, Activation of viruses in human tumors by 5-iododeoxyuridine and dimethyl sulfoxide, Science 175:198.Google Scholar
  131. Stoker, M., and Abel, P., 1962, Conditions affecting transformation by polyoma virus, Cold Spring Harbor Symp. Quant. Biol. 27: 375.PubMedCrossRefGoogle Scholar
  132. Tai, H. T., and O’Brien, R. L., 1969, Multiplicity of viral genomes in an SV-40 transformed hamster cell line, Virology 38: 698.PubMedCrossRefGoogle Scholar
  133. Temin, H., 1964, Homology between RNA from Rous sarcoma virus and DNA from Rous sarcoma virus-infected cells, Proc. Natl. Acad. Sci. 52: 323.PubMedCrossRefGoogle Scholar
  134. Temin, H. M., and Baltimore, D., 1972, RNA-directed DNA synthesis and RNA tumor viruses, Advan. Virus Res. 17:129.Google Scholar
  135. Temin, H. M., and Mizutani, S., 1970, RNA-dependent DNA polymerase in virions of Rous sarcoma virus, Nature (Land.) 226:1211.Google Scholar
  136. Theilen, G. H., Gould, D., Fowler, M., and Durgwatt, P. L., 1971, C-type virus in tumor tissue of woolly monkey (Lagothrix sp.) with fibrosarcoma, J. Natl. Cancer Inst. 47: 881.PubMedGoogle Scholar
  137. Todaro, G. J., and Gallo, R. C., 1973, Immunological relationship of DNA polymerase primate nd mouse leukemia virus reverse transcriptase, Nature (Lond.) 244: 206.CrossRefGoogle Scholar
  138. Todaro, G., and Martin, G., 1967, Increased susceptibility of Down’s syndrome fibroblasts to transformation by SV40, Proc. Soc. Exp. Biol. Med. 124: 1232.PubMedCrossRefGoogle Scholar
  139. Todaro, G. J., Aaronson, S. A., and Rands, E., 1971, Rapid detection of mycoplasma-infected cultures, Exp. Cell Res. 65: 256.PubMedCrossRefGoogle Scholar
  140. Tooze, J., ed., 1973, The Molecular Biology of Tumor Viruses, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.Google Scholar
  141. Van der Maaten, M. J., and Boothe, A. D., 1971, Isolation of a herpes-like virus from lymphosarcomatous cattle, Arch. Ges. Virusforsch. 37: 85.CrossRefGoogle Scholar
  142. Vianna, N. J., and Polan, A. K., 1973, Epidemiologic evidence for transmission of Hodgkin’s Disease, New Eng. J. Med. 289: 499.PubMedCrossRefGoogle Scholar
  143. Vianna, N. J., Greenwald, P., and Davies, J. N., 1971, Extended epidemic of Hodgkin’s disease in high school students, Lancet 1:1209.Google Scholar
  144. Vianna, N. J., Greenwald, P., Brady, J., and Davies, J. N., 1972, Hodgkin’s disease: Cases with features of a community outbreak, Ann. Int. Med. 77: 169.PubMedCrossRefGoogle Scholar
  145. Watkins, J., 1970, The effects of some metabolic inhibitors on the ability of SV40 virus in transformed cells to be detected by cell fusion. J. Cell Sci. 6: 721.PubMedGoogle Scholar
  146. Weiner, L. P., Herndon, R. M., Narayan, O., Johnson, R. T., Shah, K., Rubinstein, L. J., Presiosi, T. J., and Conley, F. K., 1972, Virus related to SV40 in patients with progressive multifocal leukoencephalopathy, New Engl. J. Med. 286: 385.PubMedCrossRefGoogle Scholar
  147. Weiss, R. A., Friis, R. R., Katz, E., and Vogt, P. K., 1971, Induction of avian tumor viruses in normal cells by physical and chemical carcinogens, Virology 46: 920.PubMedCrossRefGoogle Scholar
  148. Westphal, H., and Dulbecco, R., 1968, Viral DNA in polyoma and SV40 transformed cell lines, Proc. Natl. Acad. Sci. 59: 1158.PubMedCrossRefGoogle Scholar
  149. Westphal, H., and Kiehn, E. D., 1970, The in vitro product of SV40 DNA transcription and its specific hybridization with DNA of SV40 transformed cells, Cold Spring Harbor Symp. Quant. Biol. 35: 819.CrossRefGoogle Scholar
  150. Witter, R. L., 1972, Epidemiology of Marek’s disease—A review, in: Oncogenesis and Herpesviruses, p. 111, International Agency for Research in Cancer, Lyon.Google Scholar
  151. Wivel, N. A., Lueders, K. K., and Kuff, E. L., 1973, Structural organization of murine intracisternal particles, J. Virol. 11: 329.PubMedGoogle Scholar
  152. Zur Hausen, H., and Schulte-Holthausen, H., 1970, Presence of EB virus nucleic acid in a “virus-free” line of Burkitt tumor cells, Nature (Loud.) 227:245.Google Scholar

Copyright information

© Springer Science+Business Media New York 1975

Authors and Affiliations

  • F. Kingsley Sanders
    • 1
  1. 1.Sloan-Kettering Institute for Cancer ResearchWalker LaboratoryRyeUSA

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