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Estrogen action in the regulation of cell proliferation, cell survival, and tumorigenesis in the rat anterior pituitary gland

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Abstract

Estrogens act as important regulators of cell proliferation, cell survival, and differentiation in a variety of organ systems and tissues and have been implicated in the etiology of a variety of malignant cancers and benign tumors. The anterior pituitary gland of the rat provides an excellent model for the study of estrogen action in the regulation of cell proliferation and survival. Estrogens stimulate proliferation of the prolactin (PRL)-producing lactotroph and enhance lactotroph survival. Through these actions on lactotroph proliferation and survival, estrogens induce or contribute to the development of PRL-producing pituitary tumors in several rat strains. Data from our laboratory and others indicate that estrogen-induced pituitary growth is rat strain specific and segregates as a quantitative genetic trait in crosses between different rat strains. The purpose of this review is to summarize current know ledge pertaining to estrogen action in the regulation of cell proliferation, cell survival, and tumorigenesis in the anterior pituitary gland of the rat species, Rattus norvegicus, and to illustrate the advantages of the rat pituitary gland as a model for elucidating the mechanisms through which estrogens regulate these processes.

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References

  1. Spady, T. J., Pennington, K. L., McComb, R. D., and Shull, J. D. (1999), Endocrinology 140, 2828–2835.

    Article  PubMed  CAS  Google Scholar 

  2. Wiklund, J., Wertz, N., and Gorski, J., (1981), Endocrinology 109, 1700–1707.

    PubMed  CAS  Google Scholar 

  3. Wiklund, J., Rutledge, J., and Gorski, J., (1981), Endocrinology 109, 1708–1714.

    Article  PubMed  CAS  Google Scholar 

  4. Wiklund, J. A., and Gorsk, J., (1982), Endocrinology 111, 1140–1149.

    PubMed  CAS  Google Scholar 

  5. Shepel, L. A., and Gorski, J., (1990), Cancer Res. 50, 7920–7925.

    PubMed  CAS  Google Scholar 

  6. Wendell, D. L., Herman, A., and Gorski, J., (1996), Proc. Natl. Acad. Sci. USA, 93, 8112–8116.

    Article  PubMed  CAS  Google Scholar 

  7. Wendell, D. L., and Gorski, J., (1997), Mammal. Genome 8, 823–829.

    Article  CAS  Google Scholar 

  8. Burrow, G. N., Wortzman, G., Rewcastle, N. B., Holgate, R. C. and Kovasc, K., (1981), N. Engl. J. Med. 304, 156–158.

    Article  PubMed  CAS  Google Scholar 

  9. Annegers, J. F., Coulam, C. B., and Laws, E. R., Jr., (1982). In: Hormone secreting pituitary tumors. Givens, J. R., (ed.), Year Book Medical Publishers: Chicago, IL.

    Google Scholar 

  10. Miyai, K., Ichihara, K., Kondo, K., and Mori, S., (1986), Clin. Endocrinol., 25, 549–554.

    CAS  Google Scholar 

  11. Gooren, L. J. G., Assies, J., Asscheman, H., de Slegte, R., and van Kessel, H., (1988), J. Clin. Endocrinol. Metab. 66, 444–446.

    PubMed  CAS  Google Scholar 

  12. Kovasc, K., Stefaneanu, L., Ezzat, S., and Smyth, H. S., (1994). Arch. Pathol. Lab. Med. 118, 562–565.

    Google Scholar 

  13. Panteon, E., Loumaye, E., Maes, M., and Malvaux, P., (1988), J. Pediatr. 113, 337–339.

    Article  PubMed  CAS  Google Scholar 

  14. Baron, S. H., Sowers, J. R., and Feinberg, M., (1983), West. J. of Med., 138, 720–722.

    CAS  Google Scholar 

  15. Molitch, M. E., Elton, R. L., Blackwell, R. E., Caldwell, B., Chang, R. J., Jaffe, R., Joplin, G., Robbins, R. J., Tyson, J., and Thorner, M. O., Bromocriptine Study Group (1985) J. of Clin. Endocrinol. and Metab. 60, 698–705.

    CAS  Google Scholar 

  16. Molitch, M. E., (1999), Endocrinol. Metab. Clin. North Am. 1, 143–169.

    Article  Google Scholar 

  17. Shimon, I., and Melmed, S., (1997), J. of Clin. Endocrinol. and Metab. 82, 1675–1681.

    Article  CAS  Google Scholar 

  18. Melmed, S. (1999), Endocrinol. Metab. Clin. North Am. 28, 1–12.

    Article  PubMed  CAS  Google Scholar 

  19. Moltich, M. E. (1999), Adv. Intern. Med. 44, 117–153.

    Google Scholar 

  20. Frawley, L. S., Boockfor, F. R., and Hoeffler, J. P. (1985). Endocrinology 116, 734–737.

    PubMed  CAS  Google Scholar 

  21. Hoeffler, J. P., Boockfor, F. R., and Frawley, L. S. (1985), Endocrinology 117, 187–195.

    PubMed  CAS  Google Scholar 

  22. Pasolli, H. A., Torres, A. I., and Aoki, A. (1994), Histochemistry 102, 287–296.

    Article  PubMed  CAS  Google Scholar 

  23. Lloyd, R. V. (1990), In: Pathology of tumours of the laboratory animal IARC Scientific: Lyon Cedex, France.

    Google Scholar 

  24. Dada, M. O., Campbell, G. T., and Blake, C. A. (1984), J. Endocrinol. 101, 87–94.

    PubMed  CAS  Google Scholar 

  25. Mitchner, N. A., Garlick, C., and Ben-Jonathan, N. (1998). Endocrinology 139, 3976–3983.

    Article  PubMed  CAS  Google Scholar 

  26. Scully, K. M., Gleiberman, A. S., Lindzey, J., Lubahn, D. B., Korach, K. S., and Rosenfeld, M. G. (1997), Mol. Endocrinol. 11, 674–681.

    Article  PubMed  CAS  Google Scholar 

  27. Maurer, R. A. (1982), J. of Biol. Chem. 257, 2133–2136.

    CAS  Google Scholar 

  28. Shull, J. D., and Gorski, J. (1984), Endocrinology 114, 1550–1557.

    PubMed  CAS  Google Scholar 

  29. Shull, J. D. and Gorski, J. (1984), Endocrinology 116, 2456–2462.

    Google Scholar 

  30. Shull, J. D. and Gorski, J. (1986), Vitam. and Horm. 43, 197–249.

    CAS  Google Scholar 

  31. Shull, J. D., Walent, J. H., and Gorski, J. (1987), J. of Steroid Biochem. 26, 451–456.

    Article  CAS  Google Scholar 

  32. Maurer, R. A. (1985), DNA 4, 1–9.

    PubMed  CAS  Google Scholar 

  33. Maurer, R. A. and Notides, A. C. (1987), Mol. and Cell. Biol. 7, 4247–4254.

    CAS  Google Scholar 

  34. Day, R. N., Koike, S., Sakai, M., Muramatsu, M., and Maurer, R. A. (1990), Mol. Endocrinol. 4, 1964–1971.

    PubMed  CAS  Google Scholar 

  35. Shull, J. D. and Gorski, J. (1989), Endocrinology 124, 279–285.

    PubMed  CAS  Google Scholar 

  36. Shull, J. D. and Gorski, J. (1990), Mol. Pharmacol. 37, 215–221.

    PubMed  CAS  Google Scholar 

  37. Shaw-Bruha, C. M., Happe, H. K., Murrin, L. C., Rodriguez-Sierra, J. F., and Shull, J. D. (1996), Brain Res. Bull. 40, 33–36.

    Article  PubMed  CAS  Google Scholar 

  38. Hammond, P. J., Smith, D. M., Akinsanya, K. O., Mufti, W. A., Wynick, D., and Bloom, S. R. (1996), J. Neuroendocrinol. 8, 457–464.

    Article  PubMed  CAS  Google Scholar 

  39. Wynick, D., Hammond, P. J., Akinsanya, K. O., and Bloom, S. R. (1993), Nature 364, 529–532.

    Article  PubMed  CAS  Google Scholar 

  40. Wynick, D., Small, C. J., Bacon, A., Holmes, F. E., Norman, M., Ormandy, C. J., Kilic, E., Kerr, N. C., Ghatei, M., Talamantes, F., Bloom, S. R., and Pachnis, V. (1998), Proc. Natl. Acad. Sci. USA 95, 12,671–12,676.

    Article  CAS  Google Scholar 

  41. Hyde, J. F., Moore, J. P., Jr., and Cai, A. (1998), Ann. N.Y. Acad. Sci. 863, 48–55.

    Article  PubMed  CAS  Google Scholar 

  42. Spady, T. J., Lemus-Wilson, A. M., Pennington, K. L., Blackwood, D. J., Paschall, T. M., Birt, D. F., McComb, R. D., and Shull, J. D. (1998), Mol. Carcinog. 23, 86–95.

    Article  PubMed  CAS  Google Scholar 

  43. Shull, J. D., Birt, D. F., McComb, R. D., Spady, T. J., Pennington, K. L., and Shaw-Bruha, C. M. (1998), Mol. Carcinog. 23, 96–105.

    Article  PubMed  CAS  Google Scholar 

  44. Gersten, B. E. and Baker, B. L. (1970), Am. J. Anat. 128, 1–19.

    Article  PubMed  CAS  Google Scholar 

  45. Davies, C., Jacobi, J., Lloyd, H. M., and Meares, J. D. (1974). J. Endocrinol. 61, 411–417.

    PubMed  CAS  Google Scholar 

  46. Lloyd, R. V. (1983), Am. J. Pathol. 113, 198–206.

    PubMed  CAS  Google Scholar 

  47. Lloyd, R. V., Schmidt, K., and Nath, V. (1985), Am. J. Pathol. 121, 486–495.

    PubMed  CAS  Google Scholar 

  48. Haggi, E. S., Torres, A. I., Maldonado, C. A., and Aoki, A. (1986), J. Endocrinol. 111, 367–373.

    Article  PubMed  CAS  Google Scholar 

  49. Takahashi, S., Okazaki, K., and Kawashima, S. (1984), Cell Tissue Res. 235, 497–502.

    Article  PubMed  CAS  Google Scholar 

  50. Hashi, A., Mazawa, S., Kato, J., and Arita, J. (1995), Endocrinology 136, 4665–4671.

    Article  PubMed  CAS  Google Scholar 

  51. Hashi, A., Mazawa, S., Chen, S. Y., Yamakawa, K., Kato, J., and Arita, J. (1996), Endocrinology 137, 3246–3252.

    Article  PubMed  CAS  Google Scholar 

  52. Takahashi, S. and Kawashima, S. (1982), ACTA Anat. 113, 211–217.

    Article  PubMed  CAS  Google Scholar 

  53. Drewett, N., Jacobi, J. M., Willgoss, D. A., and Lloyd, H. M. (1993), Neuroendocrinology 57, 89–95.

    PubMed  CAS  Google Scholar 

  54. Spady, T. J., Harvell, D. M. E., Lemus-Wilson, A., Strecker, T. E., Pennington, K. L., Vander Woude, E. A., Birt, D. F., McComb, R. D., and Shull, J. D. (1999), J. of Nutr. 129, 587S-590S.

    CAS  Google Scholar 

  55. Spady, T. J. Pennington, K. L. McComb, R. D., Birt, D. F. and Shull, J. D. (1999), Mol. Carcinog., in press: 26.

  56. Léger, J. G., Montpetit, M. L., and Tenniswood, M. P. (1987). Biochem. Biophys. Res. Commun. 147, 196–203.

    Article  PubMed  Google Scholar 

  57. Buttyan, R., Zakeri, Z., Lockshin, R., and Wolgemuth, D. (1988), Mol. Endocrinol. 2, 650–657.

    PubMed  CAS  Google Scholar 

  58. Kyprianou, N., English, H. F., Davidson, N. E., and Isaacs, J. T. (1991), Cancer Res. 51, 162–166.

    PubMed  CAS  Google Scholar 

  59. McEuen, C. S., Selye, H., and Collip, J. B. (1936), Lancet 1, 775–776.

    Article  Google Scholar 

  60. Zondek, B. (1936), Lancet 1, 776–778.

    Article  Google Scholar 

  61. Clifton, K. H. and Meyer, R. K. (1956) The Anat. Rec. 125, 65–81.

    Article  CAS  Google Scholar 

  62. Cramer, W. and Horning, E. S. (1936), Lancet 1, 247–249.

    Article  Google Scholar 

  63. Bates, R. W., Clifton, K. H., and Anderson, E. (1956), Proc. Soc. Exper. Biol. Med. 93, 525–527.

    CAS  Google Scholar 

  64. Ueda, G., Otsuka, J., Mori, T., and Nagai, K. (1968), Wakayama Med. Rep. 13, 49–58.

    PubMed  CAS  Google Scholar 

  65. Furth, J., Ueda, G., and Clifton, K. H. (1973), Methods Cancer Res. 10, 201–277.

    Google Scholar 

  66. Welsch, C. W., Jenkins, T., Amenomori, Y., and Meites, J. (1971), Experientia 27, 1350–1352.

    Article  PubMed  CAS  Google Scholar 

  67. Phelps, C. and Hymer, W. C. (1983), Neuroendocrinology 37, 23–31.

    PubMed  CAS  Google Scholar 

  68. Piroli, G., Weisenberg, L. S., Grillo, C., and De Nicola, A. F. (1990), J. Natl. Cancer Inst. 82, 596–601.

    Article  PubMed  CAS  Google Scholar 

  69. Vrontakis, M. E., Thliveris, J. A., and Friesen, H. G. (1987). J. Endocrinol. 113, 383–388.

    PubMed  CAS  Google Scholar 

  70. Clifton, K. H. and Furth, J. (1961), Cancer Res. 21, 913–920.

    PubMed  CAS  Google Scholar 

  71. Festing, M. F. W. (1979). In The laboratory rat. Baker, D. E. J. (ed.), Academic, New York.

    Google Scholar 

  72. Lindsey, J. R. (1979). In The laboratory rat. Baker, D. E. J. (ed.) Academic Press: New York.

    Google Scholar 

  73. El-Azouzi, M., Hsu, D., Black, P. M., Jonesz, F., Hedley-Whyte, E. T., Klibanski, A. and Zervas, N. T. (1990), J. Neurosurg. 72, 273–281.

    PubMed  CAS  Google Scholar 

  74. Banerjee, S. K., De, A., and Sarkar, D. K. (1994), Cancer Lett. 87, 139–144.

    Article  PubMed  CAS  Google Scholar 

  75. Segaloff, A. and Dunning, W. F. (1945), Endocrinology 36, 238–240.

    CAS  Google Scholar 

  76. Furth, J., Clifton, K. H., Gadsden, E. L., and Buffett, R. F. (1956), Cancer Res. 16, 608–616.

    PubMed  Google Scholar 

  77. Kaplan, S. E. and De Nicola, A. F. (1976), J. Natl. Cancer Inst. 56, 37–42.

    PubMed  CAS  Google Scholar 

  78. Kalbermann, L. E., Machiavelli, G. A., DeNicola, A. F., Weissenberg, L. S., and Burdman, J. A. (1980), J. of Endocrinol. 87, 221–224.

    CAS  Google Scholar 

  79. Vouvier, C., Forget, H., Lagacé, G., Drews, R., Sinnett, D., Labuda, D., and Collu, R. (1991), Mol. Cell. Endocrinol. 78, 33–44.

    Article  Google Scholar 

  80. Arita, J., Kojima, Y., and Kimura, F. (1990), Neuroendocrinology 52, 249–255.

    PubMed  CAS  Google Scholar 

  81. Snyder, J., Wilfinger, W., and Hymer, W. C. (1976), Endocrinology 98, 25–32.

    PubMed  CAS  Google Scholar 

  82. Hymer, W. C. and Motter, K. A. (1988), Endocrinology 122, 2324–2338.

    PubMed  CAS  Google Scholar 

  83. Dunning, W. F., Curtis, M. R., and Segaloff, A. (1947), Cancer Res. 7, 511–521.

    CAS  Google Scholar 

  84. Morel, Y., Albaladejo, V., Bouvier, J., and Andre, J. (1982). Cancer Res. 42, 1492–1497.

    PubMed  CAS  Google Scholar 

  85. Borgundvaag, B. and George, S. R. (1988), Mol. and Cell. Endocrinol. 59, 35–45.

    Article  CAS  Google Scholar 

  86. Jin, L., Song, J., and Lloyd, R. V. (1989), Proc. Soc. Exp. Biol. Med. 192, 225–229.

    PubMed  CAS  Google Scholar 

  87. Minami, S. and Sarkar, D. K. (1997), Neurochem. Int. 30, 499–506.

    Article  PubMed  CAS  Google Scholar 

  88. Takechi, A., Uozumi, T., Kawamoto, K., Ito, A., Kurisu, K., and Sudo, K. (1994), Anticancer Res. 14, 157–162.

    PubMed  CAS  Google Scholar 

  89. Pastorcic, M., De A., Boyadjieva, N., Vale, W., and Sarkar, D. K. (1995), Cancer Res. 55, 4892–4898.

    PubMed  CAS  Google Scholar 

  90. Chun, T.-Y., Gregg, D., Sarkar, D. K., and Gorski, J. (1998). Proc. Natl. Acad. Sci. USA 95, 2325–2330.

    Article  PubMed  CAS  Google Scholar 

  91. Sarkar, D. K., Hee Kim, K., and Minami, S. (1992), Mol. Endocrinol. 6, 1825–1833.

    Article  PubMed  CAS  Google Scholar 

  92. Burns, G. and Sarkar, D. K. (1993), Endocrinology 133, 1444–1449.

    Article  PubMed  CAS  Google Scholar 

  93. De, A., Morgan, T. E., Speth, R. C., Boyadjieva, N., Sarkar, D. K. (1996), J. Endocrinol. 149, 19–27.

    Article  PubMed  CAS  Google Scholar 

  94. Kaplan, L. M., Gabriel, S. M., Koenig, J. I., Sunday, M. E., Spindel, E. R., Martin, J. B., and Chin, W. W. (1988), Proc. Natl. Acad. Sci. 85, 7408–7412.

    Article  PubMed  CAS  Google Scholar 

  95. Vrontakis, M. E., Yamamoto, T., Schroedter, I. C., Nagy, J. I., and Friesen, H. G. (1989), Neurosci. Lett. 100, 59–64.

    Article  PubMed  CAS  Google Scholar 

  96. Hsu, D. W., El-Azouzi, M., Black, P. M., Chin, W. W., Hedley-White, E. T., and Kaplan, L. M. (1990), Endocrinology 126, 3159–3167.

    PubMed  CAS  Google Scholar 

  97. O'Halloran, D. J., Jones, P. M., Steel, J. H., Gon, G., Giaid, A., Chatei, M. A., Polak, J. M., and Bloom, S. R. (1990), Endocrinology 127, 467–475.

    PubMed  Google Scholar 

  98. Gabriel, S. M., Koenig, J. I., and Kaplan, L. M. (1990), Neuroendocrinology 51, 168–173.

    PubMed  CAS  Google Scholar 

  99. Hemmer, A. and Hyde, J. F. (1992), Peptides 13, 1201–1206.

    Article  PubMed  CAS  Google Scholar 

  100. Vrontakis, M. E., Peden, L. M., Duckworth, M. L., Friesen, H. G. (1987), J. of Biol. Chem. 262, 16,755–16,758.

    CAS  Google Scholar 

  101. Wynick, D., Smith, D. M., Ghatei, M., Akinsanya, K., Bhogal, R., Purkiss, P., Byfield, P., Yanaihara, N., and Bloom, S. R. (1993), Proc. Natl. Acad. Sci. USA 90, 4231–4235.

    Article  PubMed  CAS  Google Scholar 

  102. Moore, K. E. (1987), Biol. of Reprod. 36, 47–58.

    Article  CAS  Google Scholar 

  103. Caron, M. G., Beaulieu, M., Raymond, V., Gagne, B., Drouin, J., Lefkowitz, R. J., and Labrie, F. (1978), J. of Biol. Chem. 253, 2244–2253.

    CAS  Google Scholar 

  104. Bouvier, C., Potier, M., Beauregard, G., Lafond, J., Amlaiky, N., Caron, M. G., and Collu, R. (1986), J. Neurochem. 47, 1653–1660.

    Article  PubMed  CAS  Google Scholar 

  105. Lin, C., McGonigle, P., and Molinoff, P. B. (1987), J. Pharmacol. Exp. Ther. 242, 950–956.

    PubMed  CAS  Google Scholar 

  106. Kukstas, L. A., Domec, C., Bascles, L., Bonnet, J., Verrier, D., Israel, J.-M., and Vincent, J.-D. (1991), Endocrinology 129, 1101–1103.

    Article  PubMed  CAS  Google Scholar 

  107. Maurer, R. A. (1981), Nature 294, 94–97.

    Article  PubMed  CAS  Google Scholar 

  108. Auricchio, F., Migliaccio, A., Castoria, G., Lastoria, S., and Schiavone, E. (1981), Biochem. Biophys. Res. Commun. 101, 1171–1178.

    Article  PubMed  CAS  Google Scholar 

  109. Fischberg, D. J., and Bancroft, C. (1995), Mol. Cell. Endocrinol. 111, 129–137.

    Article  PubMed  CAS  Google Scholar 

  110. McChesney, R., Sealfon, S. C., Tsutsumi, M., Dong, K. W., Roberts, J. L., and Bancroft, C. (1991) Mol. Cell. Endocrinol. 79, R1-R7.

    Article  PubMed  CAS  Google Scholar 

  111. Lloyd, H. M., Meares, J. D., and Jacobi, J. (1975), Nature 255, 497–498.

    Article  PubMed  CAS  Google Scholar 

  112. Canonico, P. L., Valdenegro, C. A., and MacLeod, R. M. (1983). Endocrinology 113, 7–14.

    PubMed  CAS  Google Scholar 

  113. Day, R. N. and Hinkle, P. M. (1988), Endocrinology 122, 2165–2173.

    PubMed  CAS  Google Scholar 

  114. Gudelsky, G. A. (1981), Psychoneuroendocrinol 6, 3–16.

    Article  CAS  Google Scholar 

  115. Reymond, M. J. and Porter, J. C. (1985), Horm. Res. 22, 142–152.

    PubMed  CAS  Google Scholar 

  116. Cramer, O. M., Parker, C. R., Jr., and Porter, J. C. (1979). Endocrinology 104, 419–422.

    PubMed  CAS  Google Scholar 

  117. Pasqualini, C., Leviel, V., Guibert, B., Faucon-Biguet, N., and Kerdelhué, B. (1991), J. Neuroendocrinol. 3, 575–580.

    Article  CAS  PubMed  Google Scholar 

  118. Blum, M., McEwen, B. S., and Roberts, J. L. (1987), J. Biol. Chem. 262, 817–821.

    PubMed  CAS  Google Scholar 

  119. De Nicola, A. F., von Lawzewitsch, I., Kaplan, S. E., and Libertun, C. (1978), J. Natl. Cancer Inst. 61, 753–763.

    PubMed  Google Scholar 

  120. Elias, K. A. and Weiner, R. I. (1984), Proc. Natl. Acad. Sci. 81, 4549–4553.

    Article  PubMed  CAS  Google Scholar 

  121. Schechter, J., Ahmad, N., Elias, K., and Weiner, R. (1987). Am. J. Pathol. 179, 315–323.

    CAS  Google Scholar 

  122. Elias, K. A. and Weiner, R. I. (1987), Endocrinology 120, 617–621.

    PubMed  CAS  Google Scholar 

  123. Stepien, H., Grochal, M., Zielinski, K. W., Mucha, S., Kunert-Radek, J., Kulig, A., Stawowy, A. and Pisarek, H. (1996). J. Endocrinol. 150, 99–106.

    Article  PubMed  CAS  Google Scholar 

  124. Shull, J. D., Spady, T. J., Snyder, M. C., Johansson, S. L., and Pennington, K. L. (1997), Carcinogenesis 18, 1595–1601.

    Article  PubMed  CAS  Google Scholar 

  125. Dunning, W. F., Curtis, M. R., and Madsen, M. E. (1951), Acta-Unio Internationalis Contra Cancrum 7, 238–244.

    PubMed  CAS  Google Scholar 

  126. Dunning, W. F. and Curtis, M. R. (1952), Cancer Res. 12, 702–706.

    PubMed  CAS  Google Scholar 

  127. Dunning, W. F., Curtis, M. R., and Segaloff, A. (1953), Cancer Res. 13, 147–152.

    PubMed  CAS  Google Scholar 

  128. Holtzman, S., Stone, J. P., and Shellabarger, C. J. (1979). Cancer Res. 39, 779–784.

    PubMed  CAS  Google Scholar 

  129. Stone, J. P., Holtzman, S., and Shellabarger, C. J. (1979). Cancer Res. 39, 773–778.

    PubMed  CAS  Google Scholar 

  130. Lyle, S. F., Wright, K., and Collins, D. C. (1984), Cancer 53, 1473–1477.

    Article  PubMed  CAS  Google Scholar 

  131. Isaacs, J. T. (1986), Cancer Res. 46, 3958–3963.

    PubMed  CAS  Google Scholar 

  132. Isaacs, J. T. (1988), Cancer Res. 48, 2204–2213.

    PubMed  CAS  Google Scholar 

  133. Isaacs, J. T. (1991), Cancer Res. 51, 1591–1595.

    PubMed  CAS  Google Scholar 

  134. Hus, L.-C., Kennan, W. S., Shepel, L. A., Jacob, H. J., Szpirer, C., Szpirer, J., Lander, E. S., and Gould, M. N. (1994), Cancer Res. 54, 2765–2770.

    Google Scholar 

  135. Shepel, L. A., Lan, H., Haag, J. D., Brasic, G. M., Gheen, M. E., Simon, J. S., Hoff, P., Newton, M. A., and Gould, M. N. (1998), Genetics 149, 289–299.

    PubMed  CAS  Google Scholar 

  136. Spady, T. J., Harvell, D. M. E., Snyder, M. C., Pennington, K. L., McComb, R. D., and Shull, J. D. (1998), Cancer Lett. 124, 95–103.

    Article  PubMed  CAS  Google Scholar 

  137. Kim, U., Clifton, K. H., and Furth, J. (1960), J. Natl. Cancer. Inst. 24, 1031–1055.

    PubMed  CAS  Google Scholar 

  138. Ito, A., Moy, P., Kaunitz, H., Kortwright, K., Clarke, S., Furth, J., Meites, J. (1972), J. Natl. Cancer Inst. 49, 701–711.

    PubMed  CAS  Google Scholar 

  139. Prysor-Jones, R. A. and Jenkins, J. S. (1981), J. Endocrinol. 88, 463–469.

    PubMed  CAS  Google Scholar 

  140. Trouillas, J. and Girod, C. (1988), Path. Res. Pract. 183, 638–641.

    PubMed  CAS  Google Scholar 

  141. Nakagawa, K., Obara, T., and Tashiro, K. (1980), Endocrinology 106, 1033–1039.

    Article  PubMed  CAS  Google Scholar 

  142. Trei, C. S. (1983), J. of Pathol. 141, 29–40.

    Article  Google Scholar 

  143. Lloyd, R. V., Landefeld, T. D., Maslar, I., and Frohman, L. A. (1985), Amer. J. of Pathol. 118, 379–386.

    CAS  Google Scholar 

  144. Lloyd, R. V., and Landefeld, T. D. (1986). Am. J. Pathol. 125, 35–44.

    PubMed  CAS  Google Scholar 

  145. Lloyd, R. V., Schmidt, K., Coleman, K., and Wilson, B. S. (1986), Proc. Soc. Exp. Biol. Med. 181, 18–23.

    PubMed  CAS  Google Scholar 

  146. Lloyd, R. V., Coleman, K., Fields, K., and Nath, V. (1987). Cancer Res. 47, 1087–1092.

    PubMed  CAS  Google Scholar 

  147. Fujimoto, M., Yoshino, E., Hirakawa, K., Chihara, K., Ibata, Y. (1987), J. of Neuro-Oncol. 5, 151–159.

    Article  CAS  Google Scholar 

  148. Lloyd, R. V., Cano, M., and Landefeld, T. D. (1988), Am. J. Pathol. 133, 397–406.

    PubMed  CAS  Google Scholar 

  149. Arita, J., Kojima, Y., and Kimura, F. (1989), Endocrinology 124, 1998–2004.

    PubMed  CAS  Google Scholar 

  150. Brawer, J. R. and Sonnenschein, C. (1975), Am. J. of Anat. 144, 57–88.

    Article  CAS  Google Scholar 

  151. Trouillas, J., Girod, C., Claustrat, B., Joly-Pharaboz, M.-O., and Chevallier, P. (1990), Cancer Res. 50, 4081–4086.

    PubMed  CAS  Google Scholar 

  152. Tashjian, A. H. Jr., Yasumura, Y., Levine, L., Sato, G., Parker, M. L. (1968), Endocrinology 82, 342–352.

    PubMed  CAS  Google Scholar 

  153. Tashjian, A. H. Jr., Bancroft, F. C., and Levine, L. (1970), J. of Cell Biol. 47, 61–70.

    Article  CAS  Google Scholar 

  154. Shull, J. D. (1991). Endocrinology 129, 1644–1652.

    PubMed  CAS  Google Scholar 

  155. Shull, J. D., Beams, F. E.; Baldwin, T. M., Gilchrist, C. A., and Hrbek, M. J. (1992), Mol. Endocrinol. 6, 529–535.

    Article  PubMed  CAS  Google Scholar 

  156. Shull, J. D. and Pennington, K. L. (1993), J. Steroid Biochem. Mol. Biol. 44, 53–60.

    Article  PubMed  CAS  Google Scholar 

  157. Gilchrist, C. A., Park, J. H. Y., MacDonald, R. G., and Shull, J. D. (1995), Mol. and Cell. Endocrinol. 114, 147–156.

    Article  CAS  Google Scholar 

  158. Pei, L. and Melmed, S. (1997), Mol. Endocrinol. 11, 433–441.

    Article  PubMed  CAS  Google Scholar 

  159. Zhang, X., Horwitz, G. A., Heaney, A. P., Nakashima, M., Prezant, T. R., Bronstein, M. D., and Medmed, S. (1999), J. of Clin. Endocrinol. and Metab. 84, 761–767.

    Article  CAS  Google Scholar 

  160. Prezant, T. R., Kadioglu, P., and Melmed, S. (1999), J. of Clin. Endocrinol. and Metab. 84, 1149–1152.

    Article  CAS  Google Scholar 

  161. Noble, R. L., Hochachka, B. C., and King, D. (1975), Cancer Res. 35, 766–780.

    PubMed  CAS  Google Scholar 

  162. Noble, R. L. and Cutts, J. H. (1959), Cancer Res. 19, 1125–1139.

    PubMed  CAS  Google Scholar 

  163. Cutts, J. H. and Noble, R. L. (1964), Cancer Res. 24, 1116–1123.

    PubMed  CAS  Google Scholar 

  164. Cutts, J. H. (1964), Cancer Res. 24, 1124–1130.

    CAS  Google Scholar 

  165. Noble, R. L. (1977), Cancer Res. 37, 82–94.

    PubMed  CAS  Google Scholar 

  166. De-Zhong, J. L., Pantazis, C. G., Hou, X., and Li, S. A. (1998), Carcinogenesis 19, 2173–2180.

    Article  Google Scholar 

  167. Xie, B., tsao, S. W., and Wong, Y. C. (1999), Carcinogenesis 20, 1069–1078.

    Article  PubMed  CAS  Google Scholar 

  168. Xie, B., Tsao, S. W., and Wong, Y. C. (1999), Carcinogenesis 20, 1597–1606.

    Article  PubMed  CAS  Google Scholar 

  169. Noble, R. L. (1975), Cancer Res. 37, 1929–1933.

    Google Scholar 

  170. Ho, S.-M., Leav, I., Merk, F. B., Yu, M., Kwan, P. W. L., and Ziar J. (1995), Lab. Invest. 73, 356–365.

    PubMed  CAS  Google Scholar 

  171. Lane, K. E., Leav, I., Ziar, J., Bridges, R. S., Rand, W. M., and Ho, S.-M. (1997), Carcinogenesis 18, 1505–1510.

    Article  PubMed  CAS  Google Scholar 

  172. Noble, R. L., McEuen, C. S., and Collip, J. B. (1940), Can. Med. Assoc. J. 42, 413–417.

    CAS  PubMed  Google Scholar 

  173. Noble, R. L. and Collip, J. B. (1941), Can. Med. Assoc. J. 44, 1–5.

    CAS  PubMed  Google Scholar 

  174. Blankenstein, M. A., Broerse, J. J., van Zwieten, M. J., and van cer Molen, H. J. (1984), Breast Cancer Res. Treat. 4, 137–141.

    Article  PubMed  CAS  Google Scholar 

  175. Hunter, D. J. and Willett, W. C. (1993), Epidemiol. Rev. 15, 110–132.

    PubMed  CAS  Google Scholar 

  176. Albanes, D. (1987) Nutr. Cancer 9, 199–217.

    Article  PubMed  CAS  Google Scholar 

  177. Weindruch, R., Albanes, D., and Kritchevsky, D. (1991). Hematol./Oncol. Clin. North Am. 5, 79–89.

    CAS  Google Scholar 

  178. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. (1992), J. of Cell Biol. 119, 493–501.

    Article  CAS  Google Scholar 

  179. Lloyd, R. V. and Mailloux, J. (1988), Am. J. Pathol. 133, 338–346.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, University of Nebraska Medical Center, Omaha, NE

    Thomas J. Spady &  James D. Shull

  2. Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE

    Rodney D. McComb &  James D. Shull

  3. Eppley Cancer Institute, University of Nebraska Medical Center, 986805 Nebraska Medical Center, Omaha, NE, 68198-6805

    Thomas J. Spady &  James D. Shull

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  1. Thomas J. Spady
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  2. Rodney D. McComb
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Spady, T.J., McComb, R.D. & Shull, J.D. Estrogen action in the regulation of cell proliferation, cell survival, and tumorigenesis in the rat anterior pituitary gland. Endocr 11, 217–233 (1999). https://doi.org/10.1385/ENDO:11:3:217

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