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Concepts of carcinogenesis

  • P. D. Lawley
Part of the Cancer Biology and Medicine book series (CABM, volume 1)

Abstract

Our present ideas about the biology of carcinogenesis owe much to the classic work of the late Leslie Foulds, the second volume of whose book Neoplastic Development 1 was published ten years ago. His principal theme was ‘the general concept of neoplasia as a sequential developmental process’. This led to the definition of three groups of lesions. Group A (non-neoplastic) is exemplified by ‘freckles and other familiar consequences of over-exposure of skin to sunlight’. Those of group B (often referred to as benign neoplasms) were defined as non-invasive, and are typified in experimental carcinogenesis by papillomas of mouse skin. Malignant tumours were designated as group C; they frequently constitute the sole manifestation of disease, in which case it is assumed that phase B has been ‘masked’. Lesions of group B do not inevitably lead to malignancy, and the various possibilities found experimentally are shown in Figure 1.1 which is taken from Foulds’ studies (mainly on development of mammary tumours in mice).

Keywords

Cold Spring Harbor Laboratory Mouse Skin Chemical Carcinogen Chinese Hamster Cell Ethyl Methanesulphonate 
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. 1.
    Vols. 1 and 2. (London: Academic Press)Google Scholar
  2. 2.
    Kennaway, E. L. and Hieger, I. (1930). Carcinogenic substances and their fluorescent Foulds, L. (1969,1975). Neoplastic Development. spectra. Br. Med. J., i, 1044Google Scholar
  3. 3.
    Rous, P. and Kidd, J. G. (1941). Conditional neoplasms and sub-threshold neoplastic states. A study of the tar tumours of rabbits.J. Exp. Med., 73, 365PubMedCrossRefGoogle Scholar
  4. 4.
    Berenblum, I. (1941). Co-carcinogenic action of croton resin. Cancer Res., 1,44Google Scholar
  5. 5.
    Mottram, J. C. (1945). Change from benign to malignant in chemically induced warts in mice. Br. J. Exp. Pathol., 26, 1Google Scholar
  6. 6.
    Friedewald, W. F. and Rous, P. (1944). Initiating and promoting elements in tumour production. Analysis of the effects of tar, benzpyrene and methylcholanthrene on rabbit skin. J Exp. Med., 80, 101PubMedCrossRefGoogle Scholar
  7. 7.
    Kaplan, H. S. (1972). Mouse leukaemia: interaction of multiple components in a complex oncogenic system. In Emmelot, P. and Bentvelzen, P. (eds.) RNA Viruses and Host Genome in Oncogenesis, pp. 143–154. (Amsterdam: North Holland)Google Scholar
  8. 8.
    Lilly, F. and Duran-Reynals, M. L. (1984). Genetics of susceptibility to murine lymphoma. In Bishop, M. J., Rowley, J. D. and Greaves, M. (eds.) Genes and Cancer, pp. 51–57. (New York: Alan R. Liss)Google Scholar
  9. 9.
    Huebner, R. J. and Todaro, G. J. (1969). Oncogenes of RNA tumour viruses as determinants of cancer. Proc. Natl Acad. Sci. USA, 64, 1087PubMedCrossRefGoogle Scholar
  10. 10.
    Cooper, G. M. (1982). Cellular transforming genes. Science, 218, 801CrossRefGoogle Scholar
  11. 11.
    Land, H., Parada, L. F. and Weinberg, R. A. (1983). Cellular oncogenes and multistage carcinogenesis. Science, 222, 771PubMedCrossRefGoogle Scholar
  12. 12.
    Reddy, E. P., Reynolds, R. K., Santos, E. and Barbacid, M. (1982). A point mutation is responsible for the acquisition of transforming properties by the T24 human bladder carcinoma oncogene.Nature, 300, 149PubMedCrossRefGoogle Scholar
  13. 13.
    Bashford, E. F. and Murray, J. A. (1906). On the occurrence of heterotypical mitoses in cancer. Proc. R. Soc., Ser. B, 77, 61CrossRefGoogle Scholar
  14. 14.
    Auerbach, C., Robson, J. M. and Carr, J. G. (1947). Chemical production of mutations. Science, 105, 243.PubMedCrossRefGoogle Scholar
  15. 15.
    Heston, W. E. (1950) Carcinogenic action of the mustards. J. Natl. Cancer Inst., 11, 415PubMedGoogle Scholar
  16. 16.
    Lawley, P. D. (1985). Carcinogenesis by alkylating agents. In Searle, C. E., (ed.)Chemical Carcinogens. 2nd Edn. ACS Monograph No. 182. Vol. I., pp. 326–484. (Washington: American Chemical Society)Google Scholar
  17. 17.
    Wada, S., Miyanishi, M., Nishimato, Y., Kambe, S. and Miller, R. W. (1968). Mustard gas as a cause of respiratory neoplasia in man. Lancet, i, 1611Google Scholar
  18. 18.
    Brookes, P. and Lawley, P. D. (1960). Reaction of mustard gas with nucleic acids in vitro and in vivo. Biochem. J., 77, 478Google Scholar
  19. 19.
    Lawley, P. D. and Brookes, P. (1961). Acidic dissociation of 7, 9-dialkylguanines and its possible relation to mutagenic properties of alkylating agents. Nature, 192, 1081PubMedCrossRefGoogle Scholar
  20. 20.
    Watson, J. D. and Crick, F. H. C. (1953). Genetical implications of the structure of DNA. Nature, 171, 1964Google Scholar
  21. 21.
    Loveless, A. (1969). Possible relevance of O6-alkylation of deoxyguanosine to mutagenicity of nitrosamines and nitrosamides. Nature, 223, 206PubMedCrossRefGoogle Scholar
  22. 22.
    Loveless, A. and Hampton, C. L. (1969). Inactivation and mutation of coliphage T2 by N-methyl- and N-ethyl-N-nitrosourea. Mutat. Res., 7, 1PubMedCrossRefGoogle Scholar
  23. 23.
    Lawley, P. D., Orr, J. D., Shah, S. A., Farmer, P. B. and Jarman, M. (1973). Reaction products from N-methyl-N-nitrosourea and DNA containing thymidine residues: synthesis and identification of a new methylation product O4-methylthymidine. Biochem. J., 135,193PubMedGoogle Scholar
  24. 24.
    Boyland, E. (1952). Different types of carcinogens and their mode of action: a review. Cancer Res ., 12, 77PubMedGoogle Scholar
  25. 25.
    Brookes, P. and Lawley, P. D. (1964). Evidence for binding of polynuclear aromatic hydrocarbons to nucleic acids of mouse skin: relation between carcinogenic power of hydrocarbons and their binding to DNA. Nature, 202, 781PubMedCrossRefGoogle Scholar
  26. 26.
    Sims, P., Grover, P. L., Swaisland, A., Pal, K. and Hewer, A. (1974). Metabolic activation of benzo(a)pyrene proceeds by a diol-epoxide. Nature, 252, 326PubMedCrossRefGoogle Scholar
  27. 27.
    Dipple, A., Moschel, R. C. and Bigger, C. A. H. (1985). Polynuclear aromatic hydrocarbons. In Searle, C. E. (ed.) Chemical Carcinogens. 2nd ed. ACS Monograph No. 182, Vol. I, pp. 42–163. (Washington: American Chemical Society)Google Scholar
  28. 28.
    Coulondre, C. and Miller, J. H. (1977). Genetic studies of the lac repressor. IV. Mutagenic specificity in the lacl gene of Escherichia coli. J. Mol. Biol, 117, 577Google Scholar
  29. 29.
    Eisenstadt, E., Warren, A. J., Porter, J., Atkins, D. and Miller, J. H. (1982). Carcinogenic epoxides of benzo(a)pyrene and cyclopenta(c, d)pyrene induce base substitutions. Proc. Natl. Acad. Sci. USA,79, 1945PubMedCrossRefGoogle Scholar
  30. 30.
    King, H. W. S. and Brookes, P. (1984). On the nature of the mutations induced by the diolepoxide of benzo(a)pyrene in mammalian cells. Carcinogenesis, 5, 965PubMedCrossRefGoogle Scholar
  31. 31.
    Marshall, C. J., Vousden, K. H. and Phillips, D. H. (1984). Activation of c-Ha-ras-1 proto-oncogene by in vitro modification with a chemical carcinogen, benzo(a)pyrene diolepoxide. Nature, 310, 568CrossRefGoogle Scholar
  32. 32.
    Santos, E., Martin-Zanca, D., Reddy, E. P., Pierotti, M. A., Delia Porta, G. and Barbacid, M. (1984). Malignant activation of a K-ras oncogene in lung carcinoma but not in normal tissue of the same patient. Science, 223, 661PubMedCrossRefGoogle Scholar
  33. 33.
    Capon, D. J., Seeburg, P. H., Mrath, J. P., Hayflick, J. S., Edman, W., Levinson, A. D. and Goeddel, P. V. (1983). Activation of Ki-ras 2 gene in human colon and lung carcinogens by two different point mutations. Nature, 304, 507PubMedCrossRefGoogle Scholar
  34. 34.
    Yuasa, Y., Eva, A., Kraus, M. H., Strivastava, S. K., Needleman, S. W., Pierce, J. H., Rhim, J. S., Gol, R., Reddy, E. P., Tronick, S. R. and Aaronson, S. A. (1984). Ras-related oncogenes of human tumours. In Vande Woude, G. F., Levine, A. J., Topp, W. C. and Watson, J. D. (eds.) Cancer Cells. 2. Oncogenes and Viral Genes, pp. 433–439. (New York: Cold Spring Harbor Laboratory)Google Scholar
  35. 35.
    Taparowsky, E., Shimizu, K., Goldfarb, M. and Wigler, M. (1983). Structure and activation of human N-ras gene,Cell, 34, 581PubMedCrossRefGoogle Scholar
  36. 36.
    Bos, J. L., Toksoz, D., Marshall, C. J., Verlaan-de Vries, M., Veenernan, G. H., van der Eb, A., van Boom, J. H., Janssen, J. W. G. and Steenvoorden, A. C. M. (1985). Amino-acid substitution at codon-13 of the N-ras oncogene in human acute myeloid leukaemia.Nature, 315, 726PubMedCrossRefGoogle Scholar
  37. 37.
    Sukumar, S., Santos, E., Martin-Zanca, D., Arthur, A. V., Long, L. K. and Barbacid, M. (1984). Transformingras genes in human neoplasia and in chemically induced animal tumour systems. In Bishop, J. M., Rowley, J. D. and Greaves, M. (eds.) Genes and Cancer. pp. 353–371. (New York: Alan R. Liss)Google Scholar
  38. 38.
    Zarbl, H., Sukumar, S., Arthur, A. V., Martin-Zanca, D. and Barbacid, M. (1985). Direct mutagenesis of Ha-ras-1 oncogenes by.N-methyl-N-nitrosourea during initiation of mammary carcinogenesis in rats. Nature, 315, 382PubMedCrossRefGoogle Scholar
  39. 39.
    Guerrero, I., Villasante, A., Corces, V. and Pellicer, A. (1984). Activation of a c-K-ras oncogene by somatic mutation in mouse lymphomas induced by γ-radiation. Science, 225, 1159PubMedCrossRefGoogle Scholar
  40. 40.
    Vousden, K. H., Bos, J. L., Marshall, C. J. and Phillips, D. H. (1986). Mutations activating human c-Ha-ras-1 proto-oncogene (Hras1) induced by chemical carcinogens and depurination. Proc. Natl. Acad. Sci. USA, 83, 1222PubMedCrossRefGoogle Scholar
  41. 41.
    Wigler, M., Fasano, O., Taparowsky, E., Powers, S., Kataoka, T., Birenbaurn, D., Shimizu, K. and Goldford, M. (1984). Structure and activation of ras genes. In Vande Woude, G. F., Levine, A. J., Topp, W. C. and Watson, J. D. (eds.) Cancer Cells. 2. Oncogenes and Viral Genes , pp. 419–423. (New York: Cold Spring Harbor Laboratory)Google Scholar
  42. 42.
    Guerrero, I., Villasante, A., D’Eustachio, P. and Pellicer, A. (1984). Isolation, characterization and chromosome assignment of mouse N-ras gene from carcinogen- induced thymic lymphoma. Science, 225, 1041PubMedCrossRefGoogle Scholar
  43. 43.
    Friedrich, U. and Coffino, P. (1977). Mutagenesis in S49 mouse lymphoma cells: induction of resistance to ouabain, 6-thioguanine and dibutyryl cyclic AMP. Proc. Natl. Acad. Sci. USA, 74, 679PubMedCrossRefGoogle Scholar
  44. 44.
    Arlett, C. F., Turnbull, D., Harcourt, S. A., Lehmann, A. R. and Colella, C. M. (1975). Comparison of 8-azaguanine and ouabain-resistance systems for selection of induced mutant Chinese hamster cells. Mutat. Res., 33, 261.PubMedCrossRefGoogle Scholar
  45. 45.
    Thacker, J., Stretch, A. and Stephens, M. A. (1977). Induction of thioguanine-resistant mutants of Chinese hamster cells by gamma-rays. Mutat. Res., 42, 313PubMedCrossRefGoogle Scholar
  46. 46.
    Yagi, T., Yarosh, D. B. and Day, R. S., III (1984). Comparison of repair of O 6- methylguanine produced by MNNG in mouse and human cells. Carcinogenesis, 5, 593PubMedCrossRefGoogle Scholar
  47. 47.
    Lawley, P. D. and Orr, D. J. (1970). Specific excision of methylation products from DNA of Escherichia coli treated with MNNG. Chem.-Biol. Interact., 2, 154PubMedCrossRefGoogle Scholar
  48. 48.
    Jeggo, P. (1979). Isolation and characterization of E. coli K-12 mutants unable to induce the adaptive response to simple alkylating agents. J. Bacteriol., 139, 783PubMedGoogle Scholar
  49. 49.
    Olsson, M. and Lindahl, T. (1980). Repair of alkylated DNA in E. coli: methyl group transfer from O 6-methylguanine to a protein cysteine residue.J Biol. Chem., 255, 10569Google Scholar
  50. 50.
    Craddock, V. M. and Henderson, A. R. (1984). Repair and replication of DNA in rat and mouse tissues in relation to cancer induction by -nitroso-N-alkylureas. Chem.-Biol. Interact., 52, 223PubMedCrossRefGoogle Scholar
  51. 51.
    Harris, G., Lawley, P. D. and Olsen, I. (1981). Mode of action of methylating carcinogens: comparative studies of murine and human cells. Carcinogenesis, 2, 403PubMedCrossRefGoogle Scholar
  52. 52.
    Medcalf, A. S. C. and Lawley, P. D. (1981). Time course of O 6-methylguanine removal from DNA of MNU-treated human fibroblasts. Nature, 289, 796PubMedCrossRefGoogle Scholar
  53. 53.
    Lawley, P. D., Harris, G., Phillips, E., Irving, W., Colaco, C. B., Lydyard, P. M. and Roitt, I. M. (1986). Repair of chemical carcinogen-induced damage in DNA of human lymphocytes and lymphoid cell lines — studies of the kinetics of removal of O 6-methyl- guanine and 3-methyladenine. Chem.-Biol. Interact, 57, 107PubMedCrossRefGoogle Scholar
  54. 54.
    Medcalf, A. S. C. and Wade, M. H. (1983). Comparison of mutagenicity of N-methyl-N- nitrosourea and -ethyl-N-nitrosourea in human diploid fibroblasts. Carcinogenesis, 4,115PubMedCrossRefGoogle Scholar
  55. 55.
    Balmain, A., Ramsden, M., Bowden, G. T. and Smith, J. (1984). Activation of mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature, 307, 658PubMedCrossRefGoogle Scholar
  56. 56.
    Bernstein, S. C. and Weinberg, R. A. (1985). Expression of the metastatic phenotype in cells transfected with human metastatic tumour DNA. Proc. Natl Acad. Sci. USA, 82, 1726PubMedCrossRefGoogle Scholar
  57. 57.
    Vousden, K. H. and Marshall, C. J. (1984). Three different activated ras genes in mouse tumours; evidence for oncogene activation during progression of a mouse lymphoma. EMBOJ., 3,913Google Scholar
  58. 58.
    Spandidos, D. A. and Kerr, I. B. (1984). Elevated expression of the human ras oncogene family in premalignant and malignant tumours of the colerectum. Br. J. Cancer, 49, 681PubMedCrossRefGoogle Scholar
  59. 59.
    Thor, A., Hand, P. H., Wunderlich, D., Curoso, A., Muraro, R. and Schlom, J. (1984). Monoclonal antibodies define differentialras gene expression in malignant and benign colonic disease. Nature, 311, 562PubMedCrossRefGoogle Scholar
  60. 60.
    Nordling, C. O. (1953). A new theory on the cancer-inducing mechanism. Br. J. Cancer, 7,68PubMedCrossRefGoogle Scholar
  61. 61.
    Burch, P. R. J. (1976). Biology of Cancer, A New Approach. (Lancaster: MTP)Google Scholar
  62. 62.
    Platt, R. (1955). Clonal ageing and cancer. Lancet, i, 867CrossRefGoogle Scholar
  63. 63.
    Armitage, P. and Doll, R. (1957). A two-stage theory of carcinogenesis in relation to the age-distribution of human cancer. Br. J. Cancer, 11, 161PubMedCrossRefGoogle Scholar
  64. 64.
    Moolgavkar, S. H. and Knudson, A. G., Jr. (1981). Mutation and cancer: a model for human carcinogenesis. J. Natl Cancer Inst., 66, 1037PubMedGoogle Scholar
  65. 65.
    Vogel, F. and Motulsky, A. G. (1982). Human Genetics, Problems and Approaches. Chapter 5. (Berlin: Springer Verlag)Google Scholar
  66. 66.
    Baker, R. M., Brunette, D. M., Mankovitz, R., Thompson, L. H., Whitmore, G. F., Siminovitch, L. and Till, J. E. (1974). Ouabain-resistant mutants of mouse and hamster cells in culture. Cell, 1, 9CrossRefGoogle Scholar
  67. 67.
    Evans, H. J. (1984). Genetic damage and cancer. In Bishop, M. J., Rowley, J. D. and Greaves, M. (eds.) Genes and Cancer, pp. 3–18. (New York: Alan R. Liss)Google Scholar
  68. 68.
    Nowell, P. C. (1976). Clonal evolution of tumour cell subpopulations. Science, 194, 23PubMedCrossRefGoogle Scholar
  69. 69.
    Yamashina, K. and Heppner, G. H. (1985). Correlation of frequency of induced mutation and metastatic potential in tumor cell lines from a single mouse mammary tumor. Cancer Res., 45,4015PubMedGoogle Scholar
  70. 70.
    Albert, R. E. and Burns, F. J. (1977). Carcinogenic atmospheric pollutants and the nature of low level risks. In Hiatt, H. H., Watson, J. D. and Winsten, J. A. (eds.) Origins of Human Cancer, pp. 289–292. (New York: Cold Spring Harbor Laboratory)Google Scholar
  71. 71.
    Waynforth, H. B. and Magee, P. N. (1975). Effect of various doses and schedules of administration of MNU, with and without croton oil promotion, on skin papilloma production in Balb/c mice. Gann Monogr. Cancer Res., 17, 439Google Scholar
  72. 72.
    Peto, R., Gray, R., Brantom, P. and Grasso, P. (1984). Nitrosamine carcinogenesis in 5120 rodents: chronic administration of sixteen different concentrations of NDEA, NDMA and NPYR and NPIP in the water of 4440 inbred rats, with parallel studies on NDEA alone of the effect of age of starting (3, 6 or 20 weeks) and of species (rats, mice or hamsters). In O’Neill, I. K., Von Borstel, R. C., Miller, C. T., Long, J. and Bartsch, H. (eds.) N-nitroso compounds: occurrence, biological effects and relevance to human cancer. IARC Scientific Publication No. 57, (Lyon: International Agency for Research on Cancer)Google Scholar
  73. 73.
    Richardson, F. C., Dyroff, M. C., Boucheron, J. A. and Swenberg, J. A. (1985). Differential repair of o4-alkyl-thymidine following exposure to methylating and ethylating hepatocarcinogens. Carcinogenesis, 6, 625PubMedCrossRefGoogle Scholar
  74. 74.
    Herron, D. C. and Shank, R. C. (1980). Methylated purines in human liver DNA after probable dimethylnitrosamine poisoning. Cancer Res., 40, 3116PubMedGoogle Scholar
  75. 75.
    Umbenhauer, D., Wild, C. P., Montesano, R., Saffhill, R., Boyle, J. M., Huh, N., Kirstein, U., Thomale, J., Rajewsky, M. F. and Lu, S. H. (1985). O6-Methyldeoxyguanosine in oesophageal DNA among individuals at high risk of oesophageal cancer. Int. J. Cancer, 36, 661PubMedCrossRefGoogle Scholar
  76. 76.
    Frei, J. V., Swenson, D. H., Warren, W. and Lawley, P. D. (1978). Alkylation of DNA in vivo in various organs of C57BL mice by EMS, ENU and MNU: some applications of high pressure liquid chromatography. Biochem. J., 174, 1031PubMedGoogle Scholar
  77. 77.
    Frei, J. V. (1980). MNU-induction of thymomas in AKR mice requires one or two “hits” only. Carcinogenesis, 1, 721PubMedCrossRefGoogle Scholar
  78. 78.
    Argyris, T. (1980). Tumor promotion by abrasion-induced epidermal hyperplasia in skin of mice. J. Invest. Dermatol., 75, 360PubMedCrossRefGoogle Scholar
  79. 79.
    Gwynn, R. H. and Salaman, M. H. (1953). Studies on co-carcinogens. SH-reactors tested for co-carcinogenic action on mouse skin. Br. J. Cancer, 7, 482PubMedCrossRefGoogle Scholar
  80. 80.
    Hunter, T. (1984). The epidermal growth factor receptor gene and its product.Nature, 311, 414PubMedCrossRefGoogle Scholar
  81. 81.
    Hill, M. J., Drasar, B. S., Aries, V., Crowder, J. S., Hawksworth, G. and Williams, R. E. O. (1971). Bacteria and aetiology of cancer of large bowel. Lancet, i, 95CrossRefGoogle Scholar
  82. 82.
    Committee on Diet, Nutrition and Cancer. Assembly of Life Sciences, National Research Council (1982). Diet, Nutrition and Cancer. Chapter 5. (Washington: National Academy Press)Google Scholar
  83. 83.
    Cox, P. J. (1979). Cyclophosphamide cystitis - identification of acrolein as the causative agent. Biochem. Pharmacol, 28, 2045PubMedCrossRefGoogle Scholar
  84. 84.
    Armstrong, B. K. (1977). Role of diet in human carcinogenesis with special reference to endometrial cancer. In Hiatt, H. H., Watson, J. D. and Winsten, J. A. (eds.) Origin of Human Cancer, pp. 557–565. (New York: Cold Spring Harbor Laboratory)Google Scholar
  85. 85.
    Committee on Diet, Nutrition and Cancer. Assembly of Life Sciences, National Research Council (1982). Diet, Nutrition and Cancer. Chapter 9. (Washington: National Academy Press)Google Scholar
  86. 86.
    Bollag, W. (1971). Therapy of chemically induced skin tumors of mice with vitamin A palmitate and vitamin A acid. Experientia, 27, 90PubMedCrossRefGoogle Scholar
  87. 87.
    Hill, D. L. and Grubbs, C. J. (1982). Retinoids as chemopreventive and anticancer agents in intact animals. Anticancer Res., 2, 111PubMedGoogle Scholar
  88. 88.
    Lower, G. U., Jr. and Kanarek, M. S. (1981). Retinoids, urinary bladder carcinogenesis, and chemoprevention: a review and synthesis. Mutat. Cancer, 3, 109Google Scholar
  89. 89.
    Yotti, L. P., Chang, C. C. and Trosko, J. E. (1979). Elimination of metabolic co-operation in Chinese hamster cells by a tumour promoter. Science, 206, 1089PubMedCrossRefGoogle Scholar
  90. 90.
    Newbold, R. F. (1982). Metabolic cooperation in tumour promotion and carcinogenesis. In Pitts, J. D. and Finbow, M. E. (eds.) Functional Integration of Cells in Animal Tissues: British Society for Cell Biology Symposium. No. 5, pp. 301–307. (Cambridge: Cambridge University Press)Google Scholar
  91. 91.
    Chang, C. -C., Trosko, J. E. and Warren, S. T. (1978). In vitro assay for tumor promoters and anti-promoters. J. Environ. Pathol. Toxicol., 2, 43PubMedGoogle Scholar
  92. 92.
    Berwald, Y. and Sachs, L. (1963). In vitro cell transformation with chemical carcinogens. Nature, 200, 1182PubMedCrossRefGoogle Scholar
  93. 93.
    Mishra, N., Dunkel, V. and Mehlman, M. (eds.) (1980). Mammalian Cell Transformation by Chemical Carcinogens. (Princeton Junction, NJ: Senate Press)Google Scholar
  94. 94.
    Newbold, R. F. and Overell, R. W. (1983). Fibroblast immortality is a prerequisite for transformation by EJ c-Ha-ras oncogene. Nature, 304, 648PubMedCrossRefGoogle Scholar
  95. 95.
    Tsutsui, T., Maizumi, H., Machlan, J. A. and Barrett, J. C. (1983). Aneuploidy induction and cell transformation by diethylstilbestrol: a possible chromosomal mechanism in carcinogenesis. Cancer Res., 43, 3814PubMedGoogle Scholar
  96. 96.
    Herbst, A. L. and Bern, H. A. (1981). Developmental effect of diethylstilbestrol in progeny. (New York: Thieme-Stratton, Inc.)Google Scholar
  97. 97.
    Foulds, L. (1975). Neoplastic Development. Vol. 2, Chapter 7. (London: Academic Press)Google Scholar
  98. 98.
    Sager, R. (1984). Resistance of human cells to oncogenic transformation. In Vande Woude, G. F., Levine, A. J., Topp, W. C. and Watson, J. P. (eds.) Cancer Cells. 2. Oncogenes and Viral Genes, pp. 487–500. (New York: Cold Spring Harbor Laboratory)Google Scholar
  99. 99.
    Burnet(Sir) M. F. (1970). Immunological Surveillance. (Oxford: Pergamon Press)Google Scholar
  100. 100.
    Thomas, L. (1959). Discussion. In Lawrence, H.S. (ed.) Cellular and Humoral Aspects of Hypersensitive States, p. 159. (London: Cassell)Google Scholar
  101. 101.
    Stutman, O. (1975). Immunodepression and malignancy. Adv. Cancer Res., 22, 261PubMedCrossRefGoogle Scholar
  102. 102.
    Hoover, R. (1977). Effects of drugs - immunosuppression. In Hiatt, H. H., Watson, J. D. and Winsten, J. A. (eds.) Origins of Human Cancer. Book A. Incidence of Cancer in Humans, pp. 369–379. (New York: Cold Spring Harbor Laboratory)Google Scholar
  103. 103.
    Penn, I. (1978). Tumours arising in organ transplant recipients.Adv. Cancer Res., 28, 32Google Scholar
  104. 104.
    Klein, G. and Klein, E. (1985). Evolution of tumours and the impact of molecular oncology. Nature, 315, 190PubMedCrossRefGoogle Scholar
  105. 105.
    Wallich, R., Bulbuc, N., Hammerling, G. J., Katzav, S., Segal, S. and Feldman, M. (1985). Abrogation of metastatic properties of tumour cells by de novo expression of H-2K antigens following H-2 gene transfection. Nature, 315, 301PubMedCrossRefGoogle Scholar
  106. 106.
    Hart, J. R. (1985). Molecular basis of tumour spread. Nature, 315, 274PubMedCrossRefGoogle Scholar
  107. 107.
    Hunter,T. (1984). Proteins of oncogenes. Sci. Am., 251, 60CrossRefGoogle Scholar
  108. 108.
    Doll, R. and Peto, R. (1981). Causes of cancer: Quantitative estimates of avoidable risks of cancer in the United States today. J. Natl. Cancer Inst., 66, 1192Google Scholar
  109. 109.
    German, J. (1979). Cancers in chromosome breakage syndromes. In Okada, S., Imamura, M., Terashima, T. and Yamaguchi, H. (eds.) Radiation Research. Proceedings 6th International Congress Radiation Research, pp. 496–505. (Tokyo: University of Tokyo Press)Google Scholar
  110. 110.
    Kraemer, K. H., Lee, M. M. and Scotto, J. (1982). Early onset of skin and oral cavity neoplasms in xeroderma pigmentosum. Lancet, i, 56CrossRefGoogle Scholar
  111. 111.
    Spriggs, A. I. (1984). Precancerous states of the cervix uteri. In Carter, R. L. (ed.) Precancerous States, pp. 317–355. (London: Oxford University Press)Google Scholar
  112. 112.
    Fischinger, P. J. and Dita, V. T., Jr. (1984). Governance of Science at the National Cancer Institute: Perceptions and opportunities in oncogene research. Cancer Res., 44,4693PubMedGoogle Scholar
  113. 113.
    Krontiris, T. G., Dimartino, N. A., Colb, M. and Parkinson, D. R. (1985). Unique allelic restriction fragments of the human Ha-ras locus in leukocyte and tumour DNAs of cancer patients. Nature, 313, 369PubMedCrossRefGoogle Scholar
  114. 114.
    Rowley, J. D. (1983). Chromosome changes in leukaemic cells as indicators of mutagenic exposure. In Rowley, J. D. and Ultmann, J. E. (eds.) Chromosomes and Cancer from Molecules to Man. Chapter 8. (New York: Academic PressGoogle Scholar

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  • P. D. Lawley

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