Genetics of Susceptibility to Mouse Skin Tumor Promotion

  • John DiGiovanni

Abstract

The protocol used in most two-stage carcinogenesis studies in mouse skin was first described by Mottram1 and forms the basis of the operational criteria defining a promoter. Mottram elicited skin tumors by treating the backs of mice with a single subcarcinogenic dose of the polycyclic aromatic hydrocarbon (PAH) benzo(a)pyrene [B(a)P], followed by repeated applications of croton oil, obtained from the seeds of Crown tiglium. Subsequently, the most active tumor-promoting component of croton oil was identified as the phorbol diester, 12-O-tetradecanoyl-phorbol-13-acetate (TPA),2–5 and today it is the most frequently used promoter for mechanistic studies.

Keywords

Prostaglandin Psoriasis Streptomyces Pyrene Monophosphate 

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References

  1. 1.
    Mottram, J. C., 1944, A developing factor in experimental blastogenesis, J. Pathol. 56: 181–187.CrossRefGoogle Scholar
  2. 2.
    Van Duuren, B. L., 1969, Tumor-promoting agents in two-stage carcinogenesis, Prog. Exp. Tumor Res. 11: 31–68.PubMedGoogle Scholar
  3. 3.
    Van Duuren, B. L., and Orris, L., 1965, The tumor-enhancing principles of Croton tiglium L., Cancer Res. 25: 1871–1875.PubMedGoogle Scholar
  4. 4.
    Hecker, E., 1968, Cocarcinogenic principles from the seed oil of Croton tiglium and from other Euphorbiaceae, Cancer Res. 28: 2338–2349.PubMedGoogle Scholar
  5. 5.
    Hecker, E., 1971, Isolation and characterization of the cocarcinogenic principles from croton oil, in: Methods in Cancer Research, Vol. 6 ( H. Busch, ed.), pp. 439–484, Academic, New York.Google Scholar
  6. 6.
    Boutwell, R. K., 1964, Some biological aspects of skin carcinogenesis, Prog. Exp. Tumor Res. 4: 207–250.PubMedGoogle Scholar
  7. 7.
    Slaga, T. J., Fischer, S. M., Weeks, C. E., Nelson, K., Mamrack, M., and Klein-Szanto, A. J. P., 1982, Specificity and mechanism(s) of promoter inhibitors and multistage promotion, in: Carcinogenesis—A Comprehensive Survey, Cocarcinogenesis and Biological Effects of Tumor Promoters, Vol. 7 ( E. Hecker, W. Kunz, N. E. Fusenig, F. Marks, and H. W. Theilman, eds.), pp. 19–34, Raven, New York.Google Scholar
  8. 8.
    Slaga, T. J., 1983, Multistage skin carcinogenesis and specificity of inhibitors, in: Modulation and Mediation of Cancer by Vitamins ( F. L. Meyskens and K. N. Prasad, eds.), pp. 10–23, S. Karger AG, Basel.Google Scholar
  9. 9.
    Mufson, R. A., Fischer, S. M., Verma, A. K., Gleason, G. L., Slaga, T. J., and Boutwell, R. K., 1979, Effects of 12-O-tetradecanoylphorbol-13-acetate and mezerein on epidermal omithine decarboxylase activity, isoproterenol-stimulated levels of cyclic adenosine 3’:5’-monophosphate, and induction of mouse skin tumors in vivo, Cancer Res. 39: 4791–4795.PubMedGoogle Scholar
  10. 10.
    Slaga, T. J., Fischer, S. M., Nelson, K., and Gleason, G. L., 1980, Studies on the mechanism of skin tumor promotion: Evidence for several stages in promotion, Proc. Natl. Acad. Sci., USA 77: 3659–3663.CrossRefGoogle Scholar
  11. 11.
    Furstenberger, G., Berry, D. L., Sorg, B., and Marks, F., 1981, Skin tumor promotion by phorbol esters is a two-stage process, Proc. Natl. Acad. Sci. USA 78: 7722–7726.PubMedCrossRefGoogle Scholar
  12. 12.
    Fujiki, H., Mori, M., Nakayasu, M., Terada, M., Sugimura, T., and Moore, R. E., 1981, Indole alkaloids: Dihydroteleocidin B, teleocidin, and lyngbyatoxin A as members of a new class of tumor promoters, Proc. Natl. Acad. Sci. USA 78: 3872–3876.PubMedCrossRefGoogle Scholar
  13. 13.
    Fujiki, H., Suganuma, M., Matsukura, N., Sugimura, T., and Takayama, S., 1982, Teleocidin from Streptomyces is a potent promoter of mouse skin carcinogenesis, Carcinogenesis 3: 895–898.PubMedCrossRefGoogle Scholar
  14. 14.
    Suganuma, M., Fujiki, H., and Sugimura, T., 1982, Existence of an optimal dose of dihydroteleocidin B for skin tumor promotion, Gann 73: 531–533.PubMedGoogle Scholar
  15. 15.
    Cardellina, J. H. II, Marner, F.-J., and Moore, R. E., 1979, Seaweed dermatitis: Structure of lyngbyatoxin A, Science 204: 193–195.PubMedCrossRefGoogle Scholar
  16. 16.
    Sugimura, T., 1982, Potent tumor promoters other than phorbol ester and their significance, Gann 73: 499–507.PubMedGoogle Scholar
  17. 17.
    Fujiki, H., Suganuma, M., Nakayasu, M., Hoshino, H., Moore, R. E., and Sugimura, T., 1982, The third class of new tumor promoters, polyacetates (debromoaplysiatoxin and aplysiatoxin), can differentiate biological actions relevant to tumor promoters, Gann 73: 495–497.PubMedGoogle Scholar
  18. 18.
    Shimomura, K., Mullinix, M. G., Kakunaga, T., Fujiki, H., and Sugimura, T., 1983, Bromine residue at hydrophilic region influences biological activity of aplysiatoxin, a tumor promoter, Science 222: 1242–1244.PubMedCrossRefGoogle Scholar
  19. 19.
    Arffmann, E., and Glavind, J., 1971, Tumor-promoting activity of fatty acid methyl esters in mice, Experientia 27: 1465–1466.PubMedCrossRefGoogle Scholar
  20. 20.
    Bock, F. G., and Burns, R., 1963, Tumor-promoting properties of anthralin (1,8,9-Anthratriol), J. Natl. Cancer Inst. 30: 393–398.Google Scholar
  21. 21.
    Van Duuren, B. L., Witz, G., and Goldschmidt, B. M., 1978, Structure-activity relationships of tumor promoters and cocarcinogens and interaction of phorbol myristate acetate and related esters with plasma membranes, in: Carcinogenesis, Mechanisms of Tumor Promotion and Cocarcinogensis, Vol. 2 ( T. J. Slaga, A. Sivak, and R. K. Boutwell, eds.), pp. 491–507, Raven, New York.Google Scholar
  22. 22.
    DiGiovanni, J., and Boutwell, R. K., 1983, Tumor promoting activity of 1,8-dihydroxy-3-methyl-9anthrone (chrysarobin) in female SENCAR mice, Carcinogenesis 4: 281–284.PubMedCrossRefGoogle Scholar
  23. 23.
    Gwynn, R. H., and Salaman, M. H., 1953, Studies on co-carcinogenesis SH-reactors and other substances tested for co-carcinogenic action in mouse skin, Br. J. Cancer 7: 482–489.PubMedCrossRefGoogle Scholar
  24. 24.
    Wynder, E. L., and Hoffman, D., 1961, A study of tobacco carcinogenesis. VIII. The role of the acidic fractions as promoters, Cancer 14: 1306–1315.PubMedCrossRefGoogle Scholar
  25. 25.
    Bock, F. G., Swain, A. P., and Stedman, R. L., 1971, Composition studies on tobacco. XLIV. Tumor-promoting activity of subfractions of the weak acid fraction of cigarette smoke condensate, J. Natl. Cancer Inst. 47: 429–436.PubMedGoogle Scholar
  26. 26.
    Hecht, S. S., Thorne, R. L., Maronpot, R. R., and Hoffman, D., 1975, A study of tobacco carcinogenesis. XIII. Tumor-promoting subfractions of the weakly acidic fraction, J. Natl. Cancer Inst. 55:1329–1336.PubMedGoogle Scholar
  27. 27.
    Hecht, S. S., Carmella, S., and Hoffman, D., 1978, Chemical studies on tobacco smoke-LIV determination of hydroxybenzyl alcohols and hydroxyphenyl ethanols in tobacco and tobacco smoke, J. Anal. Toxicol. 2: 56–59.Google Scholar
  28. 28.
    Scribner, N. K., and Scribner, J. D., 1980, Separation of initiating and promoting effects of the skin carcinogen, 7-bromomethylbenz(a)anthracene, Carcinogenesis 1: 97–100.PubMedCrossRefGoogle Scholar
  29. 29.
    Slaga, T. J., Klein-Szanto, A. J. P., Triplett, L. L., Yotti, L. P., and Trosko, J. E., 1981, Skin tumor-promoting activity of benzoyl peroxide, a widely used free radical-generating compound, Science 213: 1023–1025.PubMedCrossRefGoogle Scholar
  30. 30.
    Hennings, H., Wenk, M. L., and Donahoe, R., 1982, Retinoic acid promotion of papilloma formation in mouse skin, Cancer Lett. 16: 1–5.PubMedCrossRefGoogle Scholar
  31. 31.
    Poland, A., Palen, D., and Glover, E., 1982, Tumor-promotion by TCDD in skin of HRS/J hairless mice, Nature (Lond.) 300: 271–273.CrossRefGoogle Scholar
  32. 32.
    Argyris, T. S., 1982, Epidermal tumor promotion by regeneration, in: Carcinogenesis—A Comprehensive Survey, Cocarcinogenesis and Biological Effects of Tumor Promoters, Vol. 7 ( E. Hecker, W. Kung, N. E. Fusenig, F. Marks, and H. W. Theilmann, eds.), pp. 43–48, Raven, New York.Google Scholar
  33. 33.
    Stenback, F., Garcia, H., and Shubik, P., 1974, Present status of the concept of promoting action of cocarcinogenesis in skin, in: The Physiopathology of Cancer, Biology and Biochemistry, Vol. 1 ( P. Shubik, ed.), pp. 155–225, S. Karger AG, Basel.Google Scholar
  34. 34.
    Scribner, J. D., and Suss, R., 1978, Tumor initiation and promotion, in: International Review of Experimental Pathology, Vol. 18 ( G. W. Richter and M. A. Epstein, eds.), pp. 137–198, Academic, New York.Google Scholar
  35. 35.
    Raick, A. N., 1973, Ultrastructural, histological, and biochemical alterations produced by 12–0tetradecanoylphorbol-13-acetate on mouse epidermis and their relevance to skin tumor promotion, Cancer Res. 33: 269–286.PubMedGoogle Scholar
  36. 36.
    Klein-Szanto, A. J. P., and Slaga, T. J., 1981, Numerical variation of dark cells in normal and chemically induced hyperplastic epidermis with age of animal and efficiency of tumor promoter, Cancer Res. 41: 4437–4440.PubMedGoogle Scholar
  37. 37.
    Klein-Szanto, A. J. P., Major, S. K., and Slaga, T. J., 1980, Induction of dark keratinocytes by 12–0tetradecanoylphorbol-13-acetate and mezerein as an indicator of tumor-promoting efficiency, Carcinogenesis 1:399–406.PubMedCrossRefGoogle Scholar
  38. 38.
    Raick, A. N., and Burdzy, K., 1973, Ultrastructural and biochemical changes induced in mouse epidermis by a hyperplastic agent, ethylphenylpropiolate, Cancer Res. 33: 2221–2230.PubMedGoogle Scholar
  39. 39.
    Slaga, T. J., Klein-Szanto, A. J. P., Fischer, S. M., Weeks, C. E., Nelson, K., and Major, S., 1980, Studies on mechanism of action of anti-tumor-promoting agents: Their specificity in two-stage promotion, Proc. Natl. Acad. Sci. USA 77: 2251–2254.PubMedCrossRefGoogle Scholar
  40. 40.
    Klein-Szanto, A. J. P., 1984, Morphological evaluation of tumor promoter effects on mammalian skin, in: Mechanisms of Tumor Promotion, Tumor Promotion and Skin Carcinogenesis, Vol. II ( T. J. Slaga, ed.), pp. 41–72, CRC Press, Boca Raton, Florida.Google Scholar
  41. 41.
    Parsons, D. F., Marko, M., Braun, S. J., and Wansor, K. J., 1983, Dark cells in normal, hyperplastic, and promoter-treated mouse epidermis studied by conventional and high-voltage electron microscopy, J. Invest. Dermatol. 81: 62–67.PubMedCrossRefGoogle Scholar
  42. 42.
    Glaso, M., Ree, K., Inversen, O. H., and Hovig, T., 1986, The influence of different fixatives and a tumor promoter, 12-O-tetradecanoylphorbol-13-acetate (TPA), on the induction of so-called dark cells in mouse epidermis, Virchows Arch. 50: 355–372.CrossRefGoogle Scholar
  43. 43.
    Murakami, Y., Hibino, T., Arai, M., and Kuroki, T., 1985, Appearance of dark keratinocytes following intracutaneous injection of cholera toxin in mouse skin, J. Invest. Dematol. 85: 115–117.CrossRefGoogle Scholar
  44. 44.
    Naito, M., Naito, Y., and DiGiovanni, J., 1987, Comparison of the histological changes in the skin of DBA/2 and C57BL/6 mice following exposure to various promoting agents, Carcinogenesis 8: 1807 1815.Google Scholar
  45. 45.
    Bach, H., and Goerttler, K., 1971, Morphologische Untersuchungen zur hyper-plasiogenen Wirkung des biologisch aktiven Phorbol esters A1, Virchows Arch. 8: 196–205.Google Scholar
  46. 46.
    Balmain, A., 1976, The synthesis of specific proteins in adult mouse epidermis during phases of proliferation and differentiation induced by the tumor promoter TPA, and in basal and differentiating layers of neonatal mouse epidermis, J. Invest. Dermatol. 67: 246–253.PubMedCrossRefGoogle Scholar
  47. 47.
    Raick, A. N., 1973, Late ultrastructural changes induced by 12-O-tetradecanoylphorbol-13-acetate in mouse epidermis and their reversal, Cancer Res. 33: 1096–1103.PubMedGoogle Scholar
  48. 48.
    Aldaz, C. M., Conti, C. J., Gimenez, I. B., Slaga, T. J., and Klein-Szanto, A. J. P., 1985, Cutaneous changes during prolonged application of I2-O-tetradecanoylphorbol-13-acetate on mouse skin and residual effects after cessation of treatment, Cancer Res. 45: 2753–2759.PubMedGoogle Scholar
  49. 49.
    Sisskin, E. E., Gray, T., and Barrett, J. C., 1982, Correlation between sensitivity to tumor promotion and sustained epidermal hyperplasia of mice and rats treated with 12-O-tetradecanoylphorbol-I3-acetate, Carcinogenesis 3:403–407.PubMedCrossRefGoogle Scholar
  50. 50.
    DiGiovanni, J., Slaga, T. J., and Boutwell, R. K., 1980, Comparison of the tumor-initiating activity of 7,12-dimethylbenz[a]anthracene and benzo[a]pyrene in female SENCAR and CD-1 mice, Carcinogenesis 1: 381–389.PubMedCrossRefGoogle Scholar
  51. 51.
    Paul, D., and Hecker, E., 1969, On the biochemical mechanism of tumorigenesis in mouse skin. II. Early effects on the biosynthesis of nucleic acids induced by initiating doses of DMBA and by promoting doses of phorbol-12,13-diester TPA, Z. Krebsforsch. 73: 149–163.PubMedCrossRefGoogle Scholar
  52. 52.
    Baird, W. M., Sedgwick, J. A., and Boutwell, R. K., 1971, Effects of phorbol and four diesters of phorbol on the incorporation of tritiated precursors into DNA, RNA and protein in mouse epidermis, Cancer Res. 31: 1434–1439.PubMedGoogle Scholar
  53. 53.
    Hennings, H., and Boutwell, R. K., 1970, Studies on the mechanism of skin tumor promotion, Cancer Res. 30: 312–320.PubMedGoogle Scholar
  54. 54.
    Suss, R., Kinzel, V., and Kreibich, G., 1971, Cocarcinogenic croton oil factor AI stimulates lipid synthesis in cell cultures, Experientia 27: 46–47.PubMedCrossRefGoogle Scholar
  55. 55.
    Rohrschneider, L. R., O’Brien, D. H., and Boutwell, R. K., 1972, The stimulation of phospholipid metabolism in mouse skin following phorbol ester treatment, Biochim. Biophys. Acta 280: 57–70.PubMedGoogle Scholar
  56. 56.
    Balmain, A., and Hecker, E., 1974, On the biochemical mechanism of tumorigenesis in mouse skin. VI. Early effects of growth-stimulating phorbol esters on phosphate transport and phospholipid synthesis in mouse epidermis, Biochim. Biophys. Acta 362: 457–468.PubMedCrossRefGoogle Scholar
  57. 57.
    Verma, A. K., Ashendel, C. L., and Boutwell, R. K., 1980, Inhibition by prostaglandin synthesis inhibitors of the induction of epidermal omithine decarboxylase activity, the accumulation of prostaglandins, and tumor promotion caused by 12-O-tetradecanoyl-phorbol-13-acetate, Cancer Res. 40: 308–315.PubMedGoogle Scholar
  58. 58.
    Furstenberger, G., and Marks, F., 1980, Early prostaglandin E synthesis is an obligatory event in the induction of cell proliferation in mouse epidermis in vivo by the phorbol ester TPA, Biochem. Biophys. Res. Commun. 92: 749–756.PubMedCrossRefGoogle Scholar
  59. 59.
    Marks, F., 1976, Epidermal growth control mechanisms, hyperplasia, and tumor promotion in the skin, Cancer Res. 36: 2636–2643.PubMedGoogle Scholar
  60. 60.
    Marks, F., Bertsch, S., Grimm, W., and Schweizer, J., 1978, Hyperplastic transformation and tumor promotion in mouse epidermis: Possible consequences of disturbances of endogenous mechanisms controlling proliferation and differentiation. Carcinogenesis, Mechanisms of Tumor Promotion and Cocarcinogenesis, Vol. 2 (T. J. Slaga, A. Sivak, and R. K. Boutwell, eds.), pp. 97–116, Raven, New York.Google Scholar
  61. 61.
    Marks, F., and Grimm, W., 1972, Diurnal fluctuation and ß-adrenergic elevation of cyclic AMP in mouse epidermis in vivo, Nature New Biol. 240: 178–179.PubMedGoogle Scholar
  62. 62.
    Grimm, W., and Marks, F., 1974, Effect of tumor-promoting phorbol esters on the normal and the isoproterenol-elevated level of adenosine 3’,5’-cyclic monophosphate in mouse epidermis in vivo, Cancer Res. 34: 3128–3134.PubMedGoogle Scholar
  63. 63.
    Verma, A. K., and Murray, A. W., 1974, The effect of benzo(a)pyrene on the basal and isoproterenolstimulated levels of cyclic adenosine 3’,5’-monophosphate in mouse epidermis, Cancer Res. 34: 3408–3413.PubMedGoogle Scholar
  64. 64.
    Mufson, R. A., Simsiman, R. C., and Boutwell, R. K., 1977, The effect of the phorbol ester tumor promoters on the basal and catecholamine-stimulated levels of cyclic adenosine 3’,5’-monophosphate in mouse skin and epidermis in vivo, Cancer Res. 37: 665–669.PubMedGoogle Scholar
  65. 65.
    Solanki, V., Rana, R. S., and Slaga, T. J., 1981, Diminution of mouse epidermal superoxide dismutase and catalase activities by tumor promoters, Carcinogenesis 2: 1141–1146.PubMedCrossRefGoogle Scholar
  66. 66.
    Colbum, N. H., Lau, S., and Head, R., 1975, Decrease of epidermal histidase activity by tumor-promoting phorbol esters, Cancer Res. 35: 3154–3159.Google Scholar
  67. 67.
    Schweizer, J., and Winter, H., 1982, Changes in regional keratin polypeptide patterns during phorbol ester-mediated reversible and permanently sustained hyperplasia of mouse epidermis, Cancer Res. 42: 1517–1529.PubMedGoogle Scholar
  68. 68.
    Nelson, K. G., and Slaga, T. J., 1982, Effect of inhibitors of tumor promotion on 12-O-tetradecanoylphorbol-13-acetate-induced keratin modification in mouse epidermis, Carcinogenesis 3: 1311–1315.PubMedCrossRefGoogle Scholar
  69. 69.
    Rainen, R., Simsiman, R. C., and Boutwell, R. K., 1973, Stimulation of the phosphorylation of mouse epidermal histones by tumor-promoting agents, Cancer Res. 33: 134–139.Google Scholar
  70. 70.
    Rainera, R., Simsiman, R. C., and Boutwell, R. K., 1978, Stimulation of the synthesis of the H1 and H3 histone fractions of mouse epidermis by 12-O-tetradecanoylphorbol-l3-acetate, Cancer Lett. 5: 277–284.CrossRefGoogle Scholar
  71. 71.
    Link, R., and Marks, F., 1981, Histone phosphorylation in phorbol ester stimulated and 3-adrenergically stimulated mouse epidermis in vivo and characterization of an epidermal protein phosphorylation system, Biochim. Biophys. Acta 675: 265–275.PubMedCrossRefGoogle Scholar
  72. 72.
    O’Brien, T. G., Simsiman, R. C., and Boutwell, R. K., 1975, Induction of the polyamine-biosynthetic enzymes in mouse epidermis by tumor-promoting agents, Cancer Res. 35: 1662–1670.PubMedGoogle Scholar
  73. 73.
    O’Brien, T. G., Simsiman, R. C., and Boutwell, R. K., 1975, Induction of the polyamine-biosynthetic enzymes in mouse epidermis and their specificity for tumor promotion. Cancer Res. 35: 2426–2433.PubMedGoogle Scholar
  74. 74.
    Ashendel, C. L., and Boutwell, R. K., 1981, Direct measurement of specific binding of highly lipophilic phorbol diester to mouse epidermal membranes using cold acetone, Biochem. Biophys. Res. Commun. 99: 435–449.CrossRefGoogle Scholar
  75. 75.
    Delclos, K. B., Nagle, D. S., and Blumberg, P. M., 1980, Specific binding of phorbol ester tumor promoters to mouse skin, Cell 19: 1025–1032.PubMedCrossRefGoogle Scholar
  76. 76.
    Driedger, P. E., and Blumberg, P. M., 1980, Specific binding of phorbol ester tumor promoters, Proc. Natl. Acad. Sci. USA 77: 5670–5671.CrossRefGoogle Scholar
  77. 77.
    Dunphy, W. G., Delclos, K. B., and Blumberg, P. M., 1980, Characterization of specific binding of [3H]-phorbol-12,13-dibutyrate and [3H]phorbol 12-myristate-13-acetate to mouse brain, Cancer Res. 40: 3635–3641.PubMedGoogle Scholar
  78. 78.
    Nagle, D. S., Jaken, S., Castagna, M., and Blumberg, P. M., 1981, Variation with embryonic development and regional localization of specific [3H]phorbol 12,13-dibutyrate binding to brain, Cancer Res. 41: 89–93.PubMedGoogle Scholar
  79. 79.
    Sando, J. J., Hilfiker, M. L., Piacentini, M. J., and Laufer, T. M., 1982, Identification of phorbol ester receptors in T-growth factor-producing and nonproducing EL4 mouse thymoma cells, Cancer Res. 42: 1676–1680.PubMedGoogle Scholar
  80. 80.
    Shoyab, M., and Todaro, G. J., 1980, Specific high affinity cell membrane receptors for biologically active phorbol and ingenol esters, Nature (Lond.) 288: 451–455.CrossRefGoogle Scholar
  81. 81.
    Solanki, V., and Slaga, T. J., 1981, Specific binding of phorbol ester tumor promoters to intact primary epidermal cells from SENCAR mice, Proc. Natl. Acad. Sci. USA 78: 2549–2553.PubMedCrossRefGoogle Scholar
  82. 82.
    Solanki, V., Slaga, T. J., Callahan, M., and Huberman, E., 1981, Down regulation of specific binding of [20–3H]phorbol-12,13-dibutyrate and phorbol ester-induced differentiation of human promyelocytic leukemia cells, Proc. Natl. Acad. Sci. USA 78: 1722–1725.PubMedCrossRefGoogle Scholar
  83. 83.
    Castagna, M., Takai, Y., Kaibuchi, K., Sano, K., Kikkawa, U., and Nishizuka, Y., 1982, Direct activation of calcium activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters, J. Biol. Chem. 257: 7847–7851.PubMedGoogle Scholar
  84. 84.
    Nishizuka, Y., 1983, Phospholipid degradation and signal translation for protein phosphorylation, Trends Biochem. Sci. 8: 13–16.CrossRefGoogle Scholar
  85. 85.
    Niedel, J. E., Kuhn, L. J., and Vandenbark, G. R., 1983, Phorbol diester receptor copurifies with protein kinase C, Proc. Natl. Acad. Sci. USA 80: 36–40.PubMedCrossRefGoogle Scholar
  86. 86.
    Leach, K. L., James, M. L., and Blumberg, P. M., 1983, Characterization of a specific phorbol ester aporeceptor in mouse brain cytosol, Proc. Natl. Acad. Sci. USA 80: 4208–4212.PubMedCrossRefGoogle Scholar
  87. 87.
    Ashendel, C. L., Staller, J. M., and Boutwell, R. K., 1983, Protein kinase activity associated with a phorbol ester receptor purified from mouse brain, Cancer Res. 43: 4333–4337.PubMedGoogle Scholar
  88. 88.
    Vandenbark, G. R., Kuhn, L. J., and Niedel, J. E., 1984, Possible mechanism of phorbol ester-induced maturation of human promyelocytic leukemia cells, J. Clin. Invest. 78: 448–457.CrossRefGoogle Scholar
  89. 89.
    Sharkey, N. A., Leach, K. L., and Blumberg, P. M., 1984, Competitive inhibition by diacyglycerol of specific phorbol ester binding, Proc. Natl. Acad. Sci. USA 81: 607–610.PubMedCrossRefGoogle Scholar
  90. 90.
    Mufson, R. A., 1984, The relationship of alterations in phospholipid metabolism to the mechanism of action of phorbol ester tumor promoters, in: Mechanisms of Tumor Promotion, Cellular Responses to Tumor Promoters, Vol. IV ( T. J. Slaga, ed.), pp. 109–117, CRC Press, Boca Raton, Florida.Google Scholar
  91. 91.
    Weinstein, I. B., 1983, Protein kinase, phospholipid and control of growth, Nature (Lond.) 302: 750.CrossRefGoogle Scholar
  92. 92.
    Jetten, A. M., Ganong, B. R., Vandenbark, G. R., Shirley, J. E., and Bell, R. M., 1985, Role protein kinase C in diacylglycerol-mediated induction of omithine decarboxylase and reduction of epidermal growth factor binding, Proc. Natl. Acad. Sci. USA 82: 1941–1945.PubMedCrossRefGoogle Scholar
  93. 93.
    Smart, R. C., Huang, M.-T., and Cooney, A. J., 1986, sn-1,2-Diacylglycerols mimic the effects of 12–0tetradecanoylphorbol- 13-acetate in vivo by inducing biochemical changes associated with tumor promotion in mouse epidermis, Carcinogenesis 7: 1865–1870.PubMedCrossRefGoogle Scholar
  94. 94.
    Verma, A. K., Pong, R.-C., and Erickson, D., 1986, Involvement of protein kinase C activation in omithine decarboxylase gene expression in primary culture of newborn mouse epidermal cells and in skin tumor promotion by 12-O-tetradecanoylphorbol-13-acetate, Cancer Res. 46: 6149–6155.PubMedGoogle Scholar
  95. 95.
    Ono, Y., Kurokawa, T., Kawahara, K., Nishimura, O., Marumoto, R., Igarashi, K., Sugina, Y., Kikkawa, U., Ogiba, K., and Nishizuka, Y., 1986, Cloning of rat brain protein kinase C complementary DNA, FEBS Lett. 203: 11 I - 115.Google Scholar
  96. 96.
    Knopf, J. L., Lee, M.-H., Sultzman, L. A., Keiz, R. W., Loomic, C. R., Hewick, R. M., and Bell, R. M., 1986, Cloning and expression of multiple protein kinase C cDNAs, Cell 46: 491–502.PubMedCrossRefGoogle Scholar
  97. 97.
    Coussens, L., Parker, P. J., Rhee, L., Yang-Feng, T. L., Chen, E., Waterfield, M. D., Franchke, V., and Ullrich, A., 1986, Multiple distinct forms of bovine and human protein kinase C suggest diversity in cellular signaling pathways, Science 233: 859–866.PubMedCrossRefGoogle Scholar
  98. 98.
    Huang, K. P., Nakabayashi, H., and Huang, F. L., 1986, Isozymic forms of rat brain Ca+2-activated and phospholipid-dependent protein kinase, Proc. Natl. Acad. Sci. USA 83: 8535–8539.PubMedCrossRefGoogle Scholar
  99. 99.
    Ohno, S., Kawasaki, H., Imajoh, S., Suzuki, K., Inagaki, M., Yikokura, H., Sakoh, T., and Hidaka, H., 1987, Tissue-specific expression of three distinct types of rabbit protein kinase C, Nature (Lond.) 325: 161–166.CrossRefGoogle Scholar
  100. 100.
    Housey, G. M., O’Brian, C. A., Johnson, M. D., Kirschmeier, P., and Weinstein, LB., 1987, Isolation of c-DNA clones encoding protein kinase C: Evidence for a protein kinase C-related gene family, Proc. Natl. Acad. Sci. USA 84: 1065–1069.PubMedCrossRefGoogle Scholar
  101. 101.
    Ono, Y., Kikkawa, Y., Ogita, K., Fujii, T., Kurokawa, T., Asaoka, Y., Sekiguchi, K., Ase, K., Igarashi, K., and Nishizuka, Y., 1987, Expression and properties of two types of protein kinase C: Alternative splicing from a single gene, Science 236: 1116–1120.PubMedCrossRefGoogle Scholar
  102. 102.
    Blumberg, P. M., Jeng, A. Y., Konig, B., Sharkey, N. A., Leach, K. L., and Jaken, S., 1985, Receptors and endogenous analogs for the phorbol ester tumor promoters, in: Carcinogenesis—A Comprehensive Survey, The Role of Chemicals and Radiation in the Etiology of Cancer, Vol. 10 ( E. Huberman and S. H. Barr, eds.), pp. 249–262, Raven, New York.Google Scholar
  103. 103.
    Shubik, P., 1950, Studies on the promoting phase in the stages of carcinogenesis in mice, rats, rabbits, and guinea pigs, Cancer Res. 10: 13–17.Google Scholar
  104. 104.
    Goerttler, K., Loehrke, H., Schweizer, J., and Hesse, B., 1982, in: Diterpene ester mediated two-stage carcinogenesis, in: Carcinogenesis—A Comprehensive Survey, Cocarcinogenesis and Biological Effects of Tumor Promoters, Volume 7 (E. Hecker, N. E. Fusenig, W. Kunz, F. Marks, and H. W. Thielmann, eds.), pp. 75–83, Raven, New York.Google Scholar
  105. 105.
    Goerttler, K., Loehrke, H., Schweizer, J., and Hesse, B., 1980, Positive two-stage carcinogenesis in female Sprague-Dawley rats using 7,12-dimethylbenz(a)anthracene (DMBA) as initiator and 12–0tetradecanoylphorbol- 13-acetate (TPA) as promoter, Results of a pilot study, Virchows Arch. 385: 18 1186.Google Scholar
  106. 106.
    Goerttler, K., Hecker, E., Loehrke, H., Seip, H., Hesse, B., and Schweizer, J., 1982, Effect of the tumor promoter 12-O-tetradecanoylphorbol-13 acetate and its nonpromoting analogue 4-O-methyl-TPA on dorsal dermal melanocytes of the Syrian golden hamster (Mesocricetus quratus), J. Cancer Res., Clin. Oncol. 103: 305–311.Google Scholar
  107. 107.
    Goerttler, K., Loehrke, H., Schweizer, J., and Hesse, B., 1980, Two-stage tumorigenesis of dermal melanocytes in the back of the Syrian golden hamster using systemic initiation with 7,12-dimethylbenz(a)anthracene and topical promotion with 12-O-tetradecanoylphorbol-13-acetate, Cancer Res. 40: 155–161.PubMedGoogle Scholar
  108. 108.
    Della Porta, G., Rappaport, H., Suffiotti, U., and Shubik, P., 1956, Induction of melanotic lesions during skin carcinogenesis in hamsters, Arch. Pathol. 61: 305–313.Google Scholar
  109. 109.
    Stenback, F., 1980, Skin carcinogenesis as a model system: Observations on species, strain, and tissue specificity to 7,12-dimethylbenz(a)anthracene with or without promotion with croton oil, Acta Pharmacol. Toxicol. 46: 89–97.CrossRefGoogle Scholar
  110. 110.
    Yuspa, S. H., Viguera, C., and Nims, R., 1979, Maintenance of human skin on nude mice for studies of chemical carcinogenesis, Cancer Lett. 6: 301–310.PubMedCrossRefGoogle Scholar
  111. 111.
    Krueger, G. G., and Shelby, J., 1981, Biology of human skin transplanted to the nude mouse. I. Response to agents which modify epidermal proliferation, J. Invest. Dermatol. 76: 506–510.PubMedCrossRefGoogle Scholar
  112. 112.
    Krueger, G. G., Chamberg, D. A., and Shelby, J., 1980, Epidermal proliferation by nude mouse skin, pig skin and pig skin grafts: Failure of nude mouse skin to respond to the tumor promoter, 12-O-tetradecanoylphorbol-13-acetate (TPA), J. Exp. Med. 152: 1329–1359.PubMedCrossRefGoogle Scholar
  113. 113.
    Stern, R. S., Parish, J. A., Bleuch, H. L., and Fitzpatrick, T. B., 1981, PUVA (psoralen and ultraviolet A) and squamous cell carcinoma in patients with psoriasis, J. Invest. Dermatol. 76: 311.Google Scholar
  114. 114.
    Schweizer, J., Loehrke, H., Edler, L., and Goerttler, K., 1987, Benzoyl peroxide promotes the formation of melanotic tumors in the skin of 7,12-dimethylbenz(a)-anthracene-initiated Syrian golden hamsters, Carcinogenesis 8: 479–482.PubMedCrossRefGoogle Scholar
  115. 115.
    Slaga, T. J., and Fischer, S. M., 1983, Strain differences and solvent effects in mouse skin carcinogenesis experiments using carcinogens, tumor initiators, and promoters, Prog. Exp. Tumor Res. 26: 85–109.PubMedGoogle Scholar
  116. 116.
    Reiners, J., Davidson, K., Nelson, K., Mamrack, M., and Slaga, T. J., 1983, Skin tumor promotion: A comparative study of several stocks and strains of mice, in: Organ and Species Specificity in Chemical Carcinogenesis ( R. Langenbach, S. Nesnow, and J. M. Rice, eds.), pp. 173–188, Plenum, New York.Google Scholar
  117. 117.
    Hennings, H., Devor, D., Wenk, M., Slaga, T. J., Farmer, B., Colbum, N., Bowden, G. T., Elgio, K., and Yuspa, S. H., 1981, Comparison of two-stage epidermal carcinogenesis initiated by 7,12-dimethylbenz(a)anthracene or N-methyl-N’-nitro-N-nitroso-guanidine in newborn and adult SENCAR and Balb/c mice, Cancer Res. 41: 773–779.PubMedGoogle Scholar
  118. 118.
    Reiners, J. J., Nesnow, S., and Slaga, T. J., 1984, Murine susceptibility to two-stage skin carcinogenesis is influenced by the agent used for promotion, Carcinogenesis 5: 301–307.PubMedCrossRefGoogle Scholar
  119. 119.
    DiGiovanni, J., Prichett, W. P., Decina, P. C., and Diamond, L., 1984, DBA/2 mice are as sensitive as SENCAR mice to skin tumor promotion by 12-O-tetradecanoylphorbol-13-acetate, Carcinogenesis 5: 1493–1498.PubMedCrossRefGoogle Scholar
  120. 120.
    Strickland, P. T., 1982, Tumor induction in SENCAR mice in response to ultraviolet radiation, Carcinogenesis 3: 1487–1489.PubMedCrossRefGoogle Scholar
  121. 121.
    DiGiovanni, J., Naito, M., and Chenicek, K. J., 1988, Genetic factors controlling susceptibility to skin tumor promotion in mice, in: Tumor Promoters: Biological Approaches for Mechanistic Studies and Assay Systems (C.J. Barrett, R. Langenbach, and E. Gilmore, eds.), Raven, New York (in press).Google Scholar
  122. 122.
    Fischer, S. M., O’Connell, J. F., Conti, C. J., Tacker, K. C., Fries, J. W., Patrick, K. E., Adams, L. M., and Slaga, T. J., 1987, Characterization of an inbred strain of the SENCAR mouse that is highly sensitive to phorbol esters, Carcinogenesis 8: 421–424.PubMedCrossRefGoogle Scholar
  123. 123.
    DiGiovanni, J., Kruszewski, F. H., and Chenicek, K. J., 1987, Studies on the skin tumor promoting actions of chrysarobin (1,8-dihydroxy-3-methyl-9-anthrone), in: Nongenotoxic Mechanisms of Carcinogenesis, Banbury Report 25 ( B. Butterworth, and T. J. Slaga, eds.), pp. 25–39, Cold Spring Harbor Press, Cold Spring Harbor, New York.Google Scholar
  124. 124.
    Naito, M., Chenicek, K. J., Naito, Y., and DiGiovanni, J., 1987, Susceptibility to phorbol ester skin tumor promotion in (C57BL/6 x DBA/2)FI mice is inherited as an incomplete dominant trait: evidence for multi-locus involvement, Carcinogenesis 9: 639–645.CrossRefGoogle Scholar
  125. 125.
    Drinkwater, N. R., and Ginsler, J. J., 1986, Genetic control of hepatocarcinogensis in C57BL/6 and C3H/H3J inbred mice, Carcinogenesis 7: 1701–1707.PubMedCrossRefGoogle Scholar
  126. 126.
    Gould, M. N., 1986, Inheritance and site of expression of genes controlling susceptibility to mammary cancer in an inbred rat model, Cancer Res. 46: 1199–1202.PubMedGoogle Scholar
  127. 127.
    Malkinson, A. M., Nesbitt, M. N., and Skamene, E., 1985, Susceptibility to urethan-induced pulmonary adenomas between A/J and C57BL/6 mice: Use of AXB and BXA recombinant inbred lines indicating a three-locus genetic model, J. Natl. Cancer Inst. 75: 971–974.PubMedGoogle Scholar
  128. 128.
    Lerman, M. I., Hegamyer, G. A., and Colbum, N. H., 1986, Cloning and characterization of putative genes that specify sensitivity to neoplastic transformation by tumor promoters, Int. J. Cancer 37: 293–302.PubMedCrossRefGoogle Scholar
  129. 129.
    Raick, A. N., 1974, Cell differentiation and tumor-promoting action in skin carcinogenesis, Cancer Res. 34: 2915–2925.PubMedGoogle Scholar
  130. 130.
    Slaga, T. J., 1985, Mechanism involved in multistage skin tumorigenesis, in: Carcinogenesis: The Role of Chemicals and Radiation in the Etiology of Cancer, Vol. 10 ( E. Huberman and S. H. Barr, eds.), pp. 189–199, Raven, New York.Google Scholar
  131. 131.
    Chiba, M., Slaga, T. J., and Klein-Szanto, A. J. P., 1984, A morphometric study of dedifferentiated and involutional dark keratinocytes in 12-O-tetradecanoylphorbol-13-acetate-treated epidermis, Cancer Res. 44: 2711–2717.PubMedGoogle Scholar
  132. 132.
    Slaga, T. J., Fischer, S. M., Weeks, C. E., and Klein-Szanto, A. J. P., 1987, Cellular and biochemical mechanisms of mouse skin tumor promoters, in: Reviews in Biochemicals Toxicology, Vol. 3 ( E. Hodgson, E. Bend, and P. M. Philpot, eds.), pp. 231–281, Elsevier/North-Holland, New York.Google Scholar
  133. 133.
    Scribner, J. D., and Suss, R., 1978, Tumor initiation and promotion, Int. Rev. Pathol. 18: 137–198.Google Scholar
  134. 134.
    Lewis, J. G., and Adams, D. O., 1986, Correlation between inflammation in skin, the release of H2O2 by macrophages (m), and sensitivity to the promotion of skin tumors by phorbol esters (PE), Proc. Am. Assoc. Cancer Res. 27: 146.Google Scholar
  135. 135.
    Lewis, J. G., and Adams, 1986, Enhanced release of hydrogen peroxide and metabolites of arachidonic acid by macrophages from SENCAR mice following stimulation with phorbol esters, Cancer Res. 46: 5696–5700.PubMedGoogle Scholar
  136. 136.
    Wheldrake, J. F., Marshall, J., Ramli, J., and Murray, A. W., 1982, Skin carcinogenesis and promoter binding characteristics in different mouse strains, Carcinogenesis 3: 805–807.PubMedCrossRefGoogle Scholar
  137. 137.
    Blumberg, P. M., Delclos, K. B., and Jaken, S., 1983, Tissue and species specificity for phorbol ester receptors, in: Organ and Species Specificity in Chemical Carcinogenesis (R. Langenbach, S. Nesnow, and J. Rice, eds.), pp. 201–220, Plenum, New York.Google Scholar
  138. 138.
    Garte, S. J., Edinger, F., and Mufson, R. A., 1985, Phorbol ester activation of epidermal protein kinase C from tumor promotion sensitive and resistant mouse strains, Cancer Lett. 29: 215–221.PubMedCrossRefGoogle Scholar
  139. 139.
    Malkinson, A. M., Conway, K., Bartlett, S., Butley, M. S., and Conroy, C., 1984, Strain differences among inbred mice in protein kinase C activity, Biochem. Biophys. Res. Commun. 122: 492–498.PubMedCrossRefGoogle Scholar
  140. 140.
    Blumberg, B. M., Dunn, J. A., Jaken, S., Jeng, A. Y., Leach, K. L., Sharkey, N. A., and Yeh, E., 1984, Specific receptors for phorbol ester tumor promoters and their involvement in biological responses, in: Mechanisms of Tumor Promotion: Tumor Promotion and Carcinogenesis In Vitro, Vol. 3 ( T. J. Slaga, ed.), pp. 143–185, CRC Press, Boca Raton, Florida.Google Scholar
  141. 141.
    Homma, Y., Henning-Chubb, C. B., and Huberman, E., 1986, Translocation of protein kinase C in human leukemia cells susceptible or resistant to differentiation induced by phorbol-l2-myristate-13acetate, Proc. Natl. Acad. Sci. USA 83: 7316–7319.PubMedCrossRefGoogle Scholar
  142. 142.
    Kreibich, G., Suss, R., and Kinzel, V., 1974, On the biochemical mechanism of tumorigenesis in mouse skin. V. Studies of the metabolism of tumor promoting and non-promoting phorbol derivatives in vivo and in vitro, Z. Krebsforsch. 81: 135–149.CrossRefGoogle Scholar
  143. 143.
    Berry, D. L., Lieber, M. R., Fischer, S. M., and Slaga, T. J., 1977, Qualitative and quantitative separation of a series of phorbol ester tumor promoters by high-pressure liquid chromatography, Cancer Lett. 3: 125–132.PubMedCrossRefGoogle Scholar
  144. 144.
    Berry, D. L., Bracken, W. M., Fischer, S. M., Viaje, A., and Slaga, T. J., 1978, Metabolic conversion of 12-O-tetradecanoylphorbol-13-acetate in adult and newborn mouse skin and mouse liver microsomes, Cancer Res. 38: 2301–2306.PubMedGoogle Scholar
  145. 145.
    Barrett, J. C., Brown, M. T., and Sisskin, E. E., 1982, Deacylation of 12-O-[3H]-tetradecanoylphorbol-13-acetate and [3H]-phorbol-12,13-acetate in hamster skin and hamster cells in culture, Cancer Res. 42: 3098–3101.PubMedGoogle Scholar
  146. 146.
    Shoyab, M., Warren, R. C., and Todaro, G. J., 1982, Phorbol-12,13-diester 12-ester hydrolase may prevent tumor promotion by phorbol diesters in skin, Nature (Lond.) 295: 152–154.CrossRefGoogle Scholar
  147. 147.
    Segal, A., VanDuuren, B. L., and Mate, U., 1975, The identification of phorbolol myristate acetate as a new metabolite of phorbol myristate acetate in mouse skin, Cancer Res. 35: 2154–2159.PubMedGoogle Scholar
  148. 148.
    O’Brien, T. G., Saladik, D., Sina, J. F., and Mullin, J. M., 1982, Formation of a glucuronide conjugate of 12-O-tetradecanoylphorbol-13-acetate by LLC-Pk1 renal epithelial cells in culture, Carcinogenesis 3: 1165–1169.PubMedCrossRefGoogle Scholar
  149. 149.
    Cerutti, P., 1985, Prooxidant states and tumor promotion, Science 227: 375–381.PubMedCrossRefGoogle Scholar
  150. 150.
    Fischer, S. M., Baldwin, J. K., and Adams, L. M., 1986, Effect of antipromoters and strain of mouse on tumor promoter-induced oxidants in murine epidermal cells, Carcinogenesis 7: 915–918.PubMedCrossRefGoogle Scholar
  151. 151.
    Yuspa, S. H., Spangler, E. F., Donahoe, R., Gensz, S., Ferguson, E., Wenk, M., and Hennings, H., 1982, Sensitivity to two-stage carcinogenesis of SENCAR mouse skin grafted to nude mice, Cancer Res. 42: 437–439.PubMedGoogle Scholar
  152. 152.
    Strickland, J. E., and Strickland, A. G., 1984, Host cell reactivation studies with epidermal cells of mice sensitive and resistant to carcinogenesis, Cancer Res. 44: 893–895.PubMedGoogle Scholar
  153. 153.
    Strickland, J. E., Jetten, A. M., Kawamura, H., and Yuspa, S. H., 1984, Interaction of epidermal growth factor with basal and differentiating epidermal cells of mice resistant and sensitive to carcinogenesis, Carcinogenesis 5: 735–740.PubMedCrossRefGoogle Scholar
  154. 154.
    Strickland, P. T., 1986, Abnormal wound healing in UV-irradiated skin of SENCAR mice, J. Invest. Dermatol. 86: 37–41.PubMedCrossRefGoogle Scholar
  155. 155.
    Weeks, C. E., and Slaga, T. J., 1979, Inhibition of phorbol ester induced polyamine accumulation in mouse epidermis by antiinflammatory steroids, Biochem. Biophys. Res. Commun. 91: 1488–1496.PubMedCrossRefGoogle Scholar
  156. 156.
    Slaga, T. J., 1984, Multistage skin tumor promotion and specificity of inhibition, in: Mechanisms of Tumor Promotion: Tumor Promotion and Skin Carcinogenesis, Vol. II ( T. J. Slaga, ed.), pp. 189–196, CRC Press, Boca Raton, Florida.Google Scholar
  157. 157.
    Fischer, S. M., Hardin, K., Klein-Szanto, A. J. P., and Slaga, T. J., 1985, Retinoyi-phorbol-acetate is a complete skin tumor promoter in SENCAR mice, Cancer Lett. 27: 323–327.PubMedCrossRefGoogle Scholar
  158. 158.
    Furstenberger, G., and Marks, F., 1983, Growth stimulation and tumor promotion in skin, J. Invest. Dermatol. 81: 157s - 161s.PubMedCrossRefGoogle Scholar
  159. 159.
    Hennings, H., and Yuspa, S. H., 1985, Two-stage promotion an altemative interpretation, J. Natl. Cancer Inst. 74: 735–740.PubMedGoogle Scholar
  160. 160.
    Argyris, T. S., 1983, Nature of the epidermal hyperplasia produced by mezerein, a weak tumor promoter, in initiated skin of mice, Cancer Res. 43: 1768–1773.PubMedGoogle Scholar
  161. 161.
    Ewing, M. W., Phillips, J., Slaga, T. J., and DiGiovanni, J., 1987, Influence of promoter dose, duration, and type on progression of papillomas to carcinomas in SENCAR mice, Proc. Am. Assoc. Cancer Res. 18: 173.Google Scholar
  162. 162.
    Boutwell, R. K., 1974, The function and mechanisms of promoters of carcinogenesis, Crit. Rev. Toxicol. 2: 419–443.CrossRefGoogle Scholar
  163. 163.
    Argyris, T. S., 1983, An analysis of the epidermal hyperplasia produced by acetic acid, a poor promoter, in the skin of female mice initiated with dimethylbenzanthracene, J. Invest. Dermatol. 80: 430–435.PubMedCrossRefGoogle Scholar
  164. 164.
    DiGiovanni, J., Decina, P. C., Prichett, W. P., Cantor, J., Aalfs, K. K., and Coombs, M. M., 1985, Mechanism of mouse skin tumor promotion by chrysarobin, Cancer Res. 45: 2584–2589.PubMedGoogle Scholar
  165. 165.
    Kruszewski, F. H., Naito, M., Naito, Y., and DiGiovanni, J., 1987, Histological alterations produced by the tumor promoting anthrone, chrysarobin, in SENCAR mouse skin, J. Invest. Dermatol. in press.Google Scholar
  166. 166.
    Klein-Szanto, A. J. P., and Slaga, T. J., 1982, Effects of peroxides on rodent skin: Epidermal hyperplasia and tumor promotion, J. Invest. Dermatol. 79: 30–34.PubMedCrossRefGoogle Scholar
  167. 167.
    Naito, M., Naito, Y., and DiGiovanni, J., 1987, Comparison of the histological changes in the skin of DBA/2 and C57BL/6 mice following exposure to various promoting agents, Carcinogenesis, in press.Google Scholar
  168. 168.
    Scribner, J. D., Scribner, N. K., McKnight, B., and Mottet, N. K., 1983, Evidence for a new model of tumor progression from carcinogenesis and tumor promotion studies with 7-bromomethylbenz(a)anthracene, Cancer Res. 43: 2034–2041.PubMedGoogle Scholar
  169. 169.
    Poland, A., Knutson, J., Glover, E., and Kende, A., 1983, Tumor promotion in the skin of hairless mice by halogenated aromatic hydrocarbons, in: Genes and Proteins in Oncogenesis ( I. B. Weinstein and J. H. Vogel, eds.), pp. 143–161, Academic Press, New York.Google Scholar
  170. 170.
    Colburn, N. H., 1985, Genes and membrane signals involved in neoplastic transformation, in: Carcinogenesis—A Comprehensive Survey, The Role of Chemicals and Radiation in the Etiology of Cancer, Volume 10 ( E. Huberman, and S. H. Barr, eds.), pp. 235–248, Raven Press, New York.Google Scholar
  171. 171.
    Colburn, N. H., Talmadge, C. B., and Gindhart, T. D., 1983, Transfer of sensitivity to tumor promoters by transfection of DNA from sensitive into insensitive mouse JB6 epidermal cells, Molec. Cell. Biol. 3: 1182–1186.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • John DiGiovanni
    • 1
  1. 1.Science Park, Research DivisionThe University of Texas System Cancer CenterSmithvilleUSA

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