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Evidence for the Involvement of Genetic Differences and Mesenchymal Factors in the Progression of Oncogene-Induced Prostate Cancer in Reconstituted Mouse Prostate

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Molecular and Cellular Biology of Prostate Cancer

Abstract

Carcinogenesis is a multi-step process involving the accumulation of alterations within the cellular genome (reviewed in 1,2). These alterations can occur in protooncogenes converting them into activated oncogenes, and it has been suggested that the multi-step nature of carcinogenesis may partly reflect the consecutive activation of several dominantly acting oncogenes (3-7). It seems reasonable to presume that prostatic cancer follows this pattern. In support of this notion, oncogene activities have been reported to be present in human prostatic adenocarcinoma (8-10), in cell lines derived from cancerous prostatic tissues (11), and in Dunning R3327 rat prostatic adenocarcinomas (12,13). Recently, utilizing the mouse prostate reconstitution model system, it was demonstrated that activated ras or myc oncogenes singly were able to induce distinct dysplastic and hyperplastic lesions, respectively (14). The two oncogenes in combination induced rapidly growing, poorly differentiated malignant adenocarcinomas. Thus, the activation of the ras and myc oncogenes can induce a step-like progression of carcinogenesis in this experimental animal model.

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References

  1. Weinberg, R.A. The action of oncogenes in the cytoplasm and nucleus. Science 230:770–776, 1985.

    Article  PubMed  CAS  Google Scholar 

  2. Bishop, J.M. The molecular genetics of cancer. Science 235:305–310, 1987.

    Article  PubMed  CAS  Google Scholar 

  3. Houweling, A., van den Elsen, P.J. and van der Eb, A. Partial transformation of primary rat cells by the leftmost 4.5% fragment of adenovirus 5 DNA. Virology 105:537–550, 1980.

    Article  PubMed  CAS  Google Scholar 

  4. Rassoulzadegan, M., Cowie, A., Carr, A., Glaichenhaus, N., Kamen, R. and Cuzin, F. The roles of individual polyomavirus early proteins in oncogenic transformation. Nature 300:713–718, 1982.

    Article  PubMed  CAS  Google Scholar 

  5. Land, H., Parada, L.F. and Weinberg, R.A. Tumourigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304:596–602, 1983.

    Article  PubMed  CAS  Google Scholar 

  6. Ruley, H.E. Adenovirus early region IA enables viral and cellular transforming genes to transform primary cells in culture. Nature 304:602–606, 1983.

    Article  PubMed  CAS  Google Scholar 

  7. Newbold, R.F. and Overell, R.W. Fibroblast immortality is a prerequisite for transformation by EJ c-Ha-ras oncogene. Nature 304:648–651, 1983.

    Article  PubMed  CAS  Google Scholar 

  8. Buttyan, R., Sawczuk, I.S., Benson, M.C., Siegal, J.D. and Olsson, C.A. Enhanced expression of the c-myc proto-oncogene in high-grade human prostate cancers. The Prostate 11:327–337, 1987.

    Article  PubMed  CAS  Google Scholar 

  9. Fleming, W.H., Hamel, A., MacDonald, R., Framesey, E., Pettigrew, N.H., Johnston, B., Dodd, J.G. and Matusik, R.J. Expression of the c-myc protooncogene in human prostatic carcinoma and benign prostatic hyperplasia. Cancer Res. 46:1526–1531, 1986.

    Google Scholar 

  10. Peehl, D.M., Wehner, N. and Stamey, T.A. Activated Ki-ras oncogene in human prostatic adenocarcinoma. The Prostate 10:281–289, 1987.

    CAS  Google Scholar 

  11. Rijnders, A.W.M., van der Korput, J.A.G.M., van Steenbrugge, G.J., Romijn, J.C. and Trapman, J. Expression of cellular oncogenes in human prostatic carcinoma cell lines. Biochem. Biophys. Res. Commun. 132:548–554, 1985.

    Article  PubMed  CAS  Google Scholar 

  12. Cooke, D.B., Quarmby, V.E., Mickey, D.D., Isaacs, J.T. and French, F.S. Oncogene expression in prostate cancer: Dunning R3327 rat dorsal prostatic adenocarcinoma system. The Prostate 13:263–272, 1988.

    Article  PubMed  CAS  Google Scholar 

  13. Cooke, D.B., Quarmby, V.E., Petrusz, P., Mickey, D.D., Der, C.J., Isaacs, J.T. and French, F.S. Expression of ras proto-oncogenes in the Dunning R3327 rat prostatic adenocarcinoma system. The Prostate 13:273–287, 1988.

    Article  PubMed  CAS  Google Scholar 

  14. Thompson, T.C., Southgate, J., Kitchner, G. and Land, H. Multi-stage carcinogenesis induced by ras and myc oncogenes in a reconstituted organ. Cell 56:917–930

    Google Scholar 

  15. Epstein, J.I., Oesterling, J.E. and Walsh, P.C. The volume and anatomical location of residual tumor in radical prostatectomy specimens removed for stage A1 prostate cancer. J. Urol. 139:975–979. 1988.

    PubMed  CAS  Google Scholar 

  16. Mostofi, F.K. Precancerous lesions of the prostate. In: Carter, R.L. (ed.), Precancerous States. London: Oxford University Press. pp, 304–316, 1984.

    Google Scholar 

  17. Bostwick, D.G. and Brawer, M.K. Prostatic intra-epithelial neoplasia and early invasion in prostate cancer. Cancer 59:788–794, 1987.

    Article  PubMed  CAS  Google Scholar 

  18. Kovi, J., Mostofi, F.K., Heshmat, M.Y. and Enterline, J.P. Large acinar atypical hyperplasia and carcinoma of the prostate. Cancer 61:555–561, 1988.

    Article  PubMed  CAS  Google Scholar 

  19. McNeal, J.E. and Bostwick, D.G. Intraductal dysplasia: A premalignant lesion of the prostate. Hum. Pathol. 17:64–71, 1986.

    Article  PubMed  CAS  Google Scholar 

  20. McNeal, J.E., Price, H.M., Redwine, E.A., Freiha, F.S. and Stamey, R.A. Stage A versus stage B adenocarcinoma of the prostate: morphological comparison and biological significance. J. Urol. 139:61–65, 1988.

    PubMed  CAS  Google Scholar 

  21. Breslow, N., Chan, C.W., Dhom, G., Drury, R.A.B., Franks, L.M., Gellei, B., Lee, Y.S., Lundberg, S., Sparke, B., Sternby, N.H. and Tulinius, H. Latent carcinoma of the prostate at autopsy in seven areas. Int. J. Cancer 20:680–688, 1977.

    Article  PubMed  CAS  Google Scholar 

  22. Franks, L.M. Latent carcinoma of the prostate. J. Pathol. Bacteriol. 68:603–616, 1954.

    Article  PubMed  CAS  Google Scholar 

  23. Scardino, P.T. Early detection of prostate cancer. Urol. Clin. North Am. 16:635–655, 1989.

    PubMed  CAS  Google Scholar 

  24. Yatani, R., Chigusa, I., Akazaki, K., Stemmermann, G.N., Welsh, R.A and Correa, P. Geographic pathology of latent prostatic carcinoma. Int. J. Cancer 29:611–616, 1982.

    Article  PubMed  CAS  Google Scholar 

  25. Levine, E.G., King, R.A. and Bloomfield, C.D. The role of heredity in cancer. J. Clin. Oncol. 7:527–540, 1989.

    PubMed  CAS  Google Scholar 

  26. Siaga, T.J. and Fischer, S.M. Strain differences and solvent effects in mouse skin carcinogenesis experiments using carcinogens, tumor initiators and promoters. In: Homburger, F. (ed.), Progress in Experimental Tumor Research. New York: S. Karger Publishing Company, New York, 26: pp., 85–109, 1983.

    Google Scholar 

  27. Malkinson, A.M. The genetic basis of susceptibility to lung tumors in mice. Toxicology 54:241–271, 1989.

    Article  PubMed  CAS  Google Scholar 

  28. Cepko, C.L., Roberts, B.E. and Mulligan, R.C. Construction and application of a highly transmissible murine retrovirus shuttle vector. Cell 37:1053–1062, 1984.

    Article  PubMed  CAS  Google Scholar 

  29. Mann, R., Mulligan, R.C. and Baltimore, D. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell 33:153–159, 1983.

    Article  PubMed  CAS  Google Scholar 

  30. Cunha, G.R., Fujii, H., Neubauer, B.L., Shannon, J.M., Sawyer, L. and Reese, B.A. Epithelialmesenchymal interactions in prostatic development. 1. Morphological observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder. J. Cell Biol. 96:1662–1670, 1983.

    Article  PubMed  CAS  Google Scholar 

  31. Neubauer, B.L., Chung, L.W.K., McCormick, K.A., Taguchi, O., Thompson, T.C. and Cunha, G.R. Epithelial-mesenchymal interactions in prostatic development. 11. Biochemical observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder. J. Cell Biol. 96:1671–1676, 1983.

    Article  PubMed  CAS  Google Scholar 

  32. Thompson, T.C., Cunha, G.R., Shannon, J.M. and Chung, L.W.K. Androgen-induced biochemical responses in epithelium lacking androgen receptors: characterization of androgen receptors in the mesenchymal derivative of the urogenital sinus. J. Steroid Biochem. 25:627–634, 1986.

    Article  PubMed  CAS  Google Scholar 

  33. Rowlatt, C., Franks, L.M., Sheriff, M.U. and Chesterman, F.C. Naturally occurring tumors and other lesions of the digestive tract in untreated C57BL mice. J. Natl. Cancer Inst. 43:1353–1364, 1969.

    PubMed  CAS  Google Scholar 

  34. Price, J., Turner, D. and Cepko, C. Lineage analysis in the vertebrate nervous system by retrovirus mediated gene transfer. Proc. Natl. Acad. Sci. USA 84:156–160, 1987.

    Article  PubMed  CAS  Google Scholar 

  35. Rowe, W.P., Pugh, W.E. and Hartley, J.W. Plaque assay techniques for murine leukemia viruses. Virology 42:1136–1139, 1970.

    Article  PubMed  CAS  Google Scholar 

  36. Compere, S.J., Baldacci, P., Sharpe, A.H., Thompson, T., Land, H. and Jaenisch, R. The ras and myc oncogenes cooperate in tumor induction in many tissues when introduced into midgestation mouse embryos by retroviral vectors. Proc. Natl. Acad. Sci. USA 86:2224–2228, 1989.

    Article  PubMed  CAS  Google Scholar 

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Thompson, T.C. et al. (1991). Evidence for the Involvement of Genetic Differences and Mesenchymal Factors in the Progression of Oncogene-Induced Prostate Cancer in Reconstituted Mouse Prostate. In: Karr, J.P., Coffey, D.S., Smith, R.G., Tindall, D.J. (eds) Molecular and Cellular Biology of Prostate Cancer. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3704-5_37

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  • DOI: https://doi.org/10.1007/978-1-4615-3704-5_37

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6647-8

  • Online ISBN: 978-1-4615-3704-5

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