Constitutive activation of the Ras/mitogen-activated protein kinase signaling pathway promotes androgen hypersensitivity in LNCaP prostate cancer cells

Cancer Research

Volumn 63, Issue 8, 2003, Pages 1981-1989

  Bakin, Robert E ^a   Gioeli, Daniel ^a   Sikes, Robert A ^b   Bissonette, Eric A ^a   Weber, Michael J ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROSTATE SPECIFIC ANTIGEN; RAS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOCRINE EFFECT; CANCER GROWTH; CARCINOGENESIS; CARCINOMA CELL; CONTROLLED STUDY; HORMONE SENSITIVITY; MALE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANDROGEN ANTAGONISTS; ANDROGENS; ANILIDES; CELL DIVISION; ENZYME ACTIVATION; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS; RAS PROTEINS;

EID: 0037447330     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Djavan, B., Waldert, M., Seitz, C., and Marberger, M. Insulin-like growth factors and prostate cancer. World J. Urol., 19: 225-233, 2001.
2. Foster, B. A., Kaplan, P. J., and Greenberg, N. M. Peptide growth factors and prostate cancer: new models, new opportunities. Cancer Metastasis Rev., 17: 317-324, 1998.
3. Abrahamsson, P. A. Neuroendocrine cells in tumour growth of the prostate. Endocr. Relat. Cancer, 6: 503-519, 1999.
4. Russell, P. J., Bennett, S., and Stricker, P. Growth factor involvement in progression of prostate cancer. Clin. Chem., 44: 705-723, 1998.
5. Signoretti, S., Montironi, R., Manola, J., Altimari, A., Tam, C., Bubley, G., Balk, S., Thomas, G., Kaplan, I., Hlatky, L., Hahnfeldt, P., Kantoff, P., and Loda, M. Her-2-neu expression and progression toward androgen independence in human prostate cancer. J. Natl. Cancer Inst., 92: 1918-1925, 2000.
6. Ross, J. S., Nazeer, T., Church, K., Amato, C., Figge, H., Rifkin, M. D., and Fisher, H. A. Contribution of HER-2/neu oncogene expression to tumor grade and DNA content analysis in the prediction of prostatic carcinoma metastasis. Cancer (Phila.), 72: 3020-3028, 1993.
7. Osman, I., Scher, H. I., Drobnjak, M., Verbel, D., Morris, M., Agus, D., Ross, J. S., and Cordon-Cardo, C. HER-2/neu (p185neu) protein expression in the natural or treated history of prostate cancer. Clin. Cancer Res., 7: 2643-2647, 2001.
8. Sadasivan, R., Morgan, R., Jennings, S., Austenfeld, M., Van Veldhuizen, P., Stephens, R., and Noble, M. Overexpression of Her-2/neu may be an indicator of poor prognosis in prostate cancer. J. Urol., 150: 126-131, 1993.
9. Visakorpi, T., Kallioniemi, O. P., Koivula, T., Harvey, J., and Isola, J. Expression of epidermal growth factor receptor and ERBB2 (HER-2/Neu) oncoprotein in prostatic carcinomas. Mod. Pathol., 5: 643-648, 1992.
10. Kuhn, E. J., Kurnot, R. A., Sesterhenn, I. A., Chang, E. H., and Moul, J. W. Expression of the c-erbB-2 (HER-2/neu) oncoprotein in human prostatic carcinoma. J. Urol., 150: 1427-1433, 1993.
11. Zhau, H. E., Wan, D. S., Zhou, J., Miller, G. J., and von Eschenbach, A. C. Expression of c-erb B-2/neu proto-oncogene in human prostatic cancer tissues and cell lines. Mol. Carcinog., 5: 320-327, 1992.
12. Sherwood, E. R., Van Dongen, J. L., Wood, C. G., Liao, S., Kozlowski, J. M., and Lee, C. Epidermal growth factor receptor activation in androgen-independent but not androgen-stimulated growth of human prostatic carcinoma cells. Br. J. Cancer, 77: 855-861, 1998.
13. Craft, N., Shostak, Y., Carey, M., and Sawyers, C. L. A mechanism for hormone-independent prostate cancer through modulation of androgen receptor signaling by the HER-2/neu tyrosine kinase. Nat. Med., 5: 280-285, 1999.
14. Yeh, S., Lin, H. K., Kang, H. Y., Thin, T. H., Lin, M. F., and Chang, C. From HER2/Neu signal cascade to androgen receptor and its coactivators: a novel pathway by induction of androgen target genes through MAP kinase in prostate cancer cells. Proc. Natl. Acad. Sci. USA, 96: 5458-5463, 1999.
15. Pietras, R. J., Arboleda, J., Reese, D. M., Wongvipat, N., Pegram, M. D., Ramos, L., Gorman, C. M., Parker, M. G., Sliwkowski, M. X., and Slamon, D. J. HER-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells. Oncogene, 10: 2435-2446, 1995.
16. Liu, Y., el-Ashry, D., Chen, D., Ding, I. Y., and Kern, F. G. MCF-7 breast cancer cells overexpressing transfected c-erbB-2 have an in vitro growth advantage in estrogen-depleted conditions and reduced estrogen-dependence and tamoxifen-sensitivity in vivo. Breast Cancer Res. Treat., 34: 97-117, 1995.
17. George, D. J., Dionne, C. A., Jani, J., Angeles, T., Murakata, C., Lamb, J., and Isaacs, J. T. Sustained in vivo regression of Dunning H rat prostate cancers treated with combinations of androgen ablation and Trk tyrosine kinase inhibitors, CEP-751 (KT-6587) or CEP-701 (KT-5555). Cancer Res., 59: 2395-2401, 1999.
18. Agus, D. B., Scher, H. I., Higgins, B., Fox, W. D., Heller, G., Fazzari, M., Cordon-Cardo, C., and Golde, D. W. Response of prostate cancer to anti-Her-2/neu antibody in androgen-dependent and -independent human xenograft models. Cancer Res., 59: 4761-4764, 1999.
19. Melnyk, O., Zimmerman, M., Kim, K. J., and Shuman, M. Neutralizing anti-vascular endothelial growth factor antibody inhibits further growth of established prostate cancer and metastases in a pre-clinical model. J. Urol., 161: 960-963, 1999.
20. Smith, P. C., and Keller, E. T. Anti-interleukin-6 monoclonal antibody induces regression of human prostate cancer xenografts in nude mice. Prostate, 48: 47-53, 2001.
21. Scher, H. I., Sarkis, A., Reuter, V., Cohen, D., Netto, G., Petrylak, D., Lianes, P., Fuks, Z., Mendelsohn, J., and Cordon-Cardo, C. Changing pattern of expression of the epidermal growth factor receptor and transforming growth factor α in the progression of prostatic neoplasms. Clin. Cancer Res., 1: 545-550, 1995.
22. Marshall, C. J. Small GTPases and cell cycle regulation, Biochem. Soc. Trans., 27: 363-370, 1999.
23. Downward, J. Ras signalling and apoptosis. Curr. Opin. Genet. Dev., 8: 49-54, 1998.
24. Takai, Y., Kaibuchi, K., Sasaki, T., Tanaka, K., Shirataki, H., and Nakanishi, H. Rho small G protein and cytoskeletal control. Princess Takamatsu Symp., 24: 338-350, 1994.
25. Chavrier, P., and Goud, B. The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell Biol., 11: 466-475, 1999.
26. Katz, M. E., and McCormick, F. Signal transduction from multiple Ras effectors. Curr. Opin. Genet. Dev., 7: 75-79, 1997.
27. Carter, B. S., Epstein, J. I., and Isaacs, W. B. ras gene mutations in human prostate cancer. Cancer Res, 50: 6830-6832, 1990.
28. Gumerlock, P. H., Poonamallee, U. R., Meyers, F. J., and DeVere White, R. W. Activated ras alleles in human carcinoma of the prostate are rare. Cancer Res., 51: 1632-1637, 1991.
29. Moul, J. W., Friedrichs, P. A., Lance, R. S., Theune, S. M., and Chang, E. H. Infrequent RAS oncogene mutations in human prostate cancer. Prostate, 20: 327-338, 1992.
30. Hori, M., Inagawa, S., Shimazaki, J., and Itabashi, M. Overexpression of mitogen-activated protein kinase superfamily proteins unrelated to Ras and AF-1 of estrogen receptor α mutation in advanced stage human breast cancer. Pathol. Res. Pract., 196: 817-826, 2000.
31. Clark, G. J., and Der, C. J. Aberrant function of the Ras signal transduction pathway in human breast cancer. Breast Cancer Res. Treat., 35: 133-144, 1995.
32. Gioeli, D., Mandell, J. W., Petroni, G. R., Frierson, H. F., Jr., and Weber, M. J. Activation of mitogen-activated protein kinase associated with prostate cancer progression. Cancer Res., 59: 279-284, 1999.
33. Zecevic, M., Catling, A. D., Eblen, S. T., Renzi, L., Hittle, J. C., Yen, T. J., Gorbsky, G. J., and Weber, M. J. Active MAP kinase in mitosis: localization at kinetochores and association with the motor protein CENP-E. J. Cell Biol., 142: 1547-1558, 1998.
34. Rutter, C. M., and Elashoff, R. M. Analysis of longitudinal data: random coefficient regression modelling. Stat. Med., 13: 1211-1231, 1994.
35. Hoshino, R., Chatani, Y., Yamori, T., Tsuruo, T., Oka, H., Yoshida, O., Shimada, Y., Ari-i, S., Wada, H., Fujimoto, J., and Kohno, M. Constitutive activation of the 41-/43-kDa mitogen-activated protein kinase signaling pathway in human tumors. Oncogene, 18: 813-822, 1999.
36. Ito, Y., Sasaki, Y., Horimoto, M., Wada, S., Tanaka, Y., Kasahara, A., Ueki, T., Hirano, T., Yamamoto, H., Fujimoto, J., Okamoto, E., Hayashi, N., and Hori, M. Activation of mitogen-activated protein kinases/extracellular signal-regulated kinases in human hepatocellular carcinoma. Hepatology, 27: 951-958, 1998.
37. Oka, H., Chatani, Y., Hoshino, R., Ogawa, O., Kakehi, Y., Terachi, T., Okada, Y., Kawaichi, M., Kohno, M., and Yoshida, O. Constitutive activation of mitogen-activated protein (MAP) kinases in human renal cell carcinoma. Cancer Res., 55: 4182-4187, 1995.
38. Towatari, M., Iida, H., Tanimoto, M., Iwata, H., Hamaguchi, M., and Saito, H. Constitutive activation of mitogen-activated protein kinase pathway in acute leukemia cells. Leukemia (Baltimore), 11: 479-484, 1997.
39. McKillop, I. H., Schmidt, C. M., Cahill, P. A., and Sitzmann, J. V. Altered expression of mitogen-activated protein kinases in a rat model of experimental hepatocellular carcinoma. Hepatology, 26: 1484-1491, 1997.
40. Lin, T. H., Chen, Q., Howe, A., and Juliano, R. L. Cell anchorage permits efficient signal transduction between ras and its downstream kinases. J. Biol. Chem., 272: 8849-8852, 1997.
41. Wu, H. C., Hsieh, J. T., Gleave, M. E., Brown, N. M., Pathak, S., and Chung, L. W. Derivation of androgen-independent human LNCaP prostatic cancer cell sublines: role of bone stromal cells. Int. J. Cancer, 57: 406-412, 1994.
42. White, M. A., Nicolette, C., Minden, A., Polverino, A., Van Aelst, L., Karin, M., and Wigler, M. H. Multiple Ras functions can contribute to mammalian cell transformation. Cell, 80: 533-541, 1995.
43. Ramocki, M. B., White, M. A., Konieczny, S. F., and Taparowsky, E. J. A role for Ra1GDS and a novel Ras effector in the Ras-mediated inhibition of skeletal myogenesis. J. Biol. Chem., 273: 17696-17701, 1998.
44. White, M. A., Vale, T., Camonis, J. H., Schaefer, E., and Wigler, M. H. A role for the Ra1 guanine nucleotide dissociation stimulator in mediating Ras-induced transformation. J. Biol. Chem., 271: 16439-16442, 1996.
45. Miller, M. J., Rioux, L., Prendergast, G. V., Cannon, S., White, M. A., and Meinkoth, J. L. Differential effects of protein kinase A on Ras effector pathways. Mol. Cell. Biol., 18: 3718-3726, 1998.
46. Shao, J., Sheng, H., DuBois, R. N., and Beauchamp, R. D. Oncogenic Ras-mediated cell growth arrest and apoptosis are associated with increased ubiquitin-dependent cyclin D1 degradation. J. Biol. Chem., 275: 22916-22924, 2000.
47. Ravi, R. K., McMahon, M., Yangang, Z., Williams, J. R., Dillehay, L. E., Nelkin, B. D., and Mabry, M. Raf-1-induced cell cycle arrest in LNCaP human prostate cancer cells. J. Cell Biochem., 72: 458-469, 1999.
48. Chen, T., Cho, R. W., Stork, P. J. S., Weber, M. J. Elevation of cyclic adenosine 3′,5′-monophosphate potentiates activation of mitogen-activated protein kinase by growth factors in LNCaP prostate cancer cells. Cancer Res., 59: 213-218, 1999.
49. Srivastava, S. K., Yuasa, Y., Reynolds, S. H., and Aaronson, S. A. Effects of two major activating lesions on the structure and conformation of human ras oncogene products. Proc. Natl. Acad. Sci. USA, 82: 38-42, 1985.
50. Culig, Z., Hobisch, A., Cronauer, M. V., Radmayr, C., Trapman, J., Hittmair, A., Bartsch, G., and Klocker, H. Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-I, keratinocyte growth factor, and epidermal growth factor. Cancer Res., 54: 5474-5478, 1994.
51. Nazareth, L. V., and Weigel, N. L. Activation of the human androgen receptor through a protein kinase A signaling pathway. J. Biol. Chem., 271: 19900-19907, 1996.
52. Reinikainen, P., Palvimo, J. J., and Janne, O. A. Effects of mitogens on androgen receptor-mediated transactivation. Endocrinology, 137: 4351-4357, 1996.
53. Sadar, M. D. Androgen-independent induction of prostate-specific antigen gene expression via cross-talk between the androgen receptor and protein kinase A signal transduction pathways. J. Biol. Chem., 274: 7777-7783, 1999.
54. Ikonen, T., Palvimo, J. J., Kallio, P. J., Reinikainen, P., and Janne, O. A. Stimulation of androgen-regulated transactivation by modulators of protein phosphorylation. Endocrinology, 135: 1359-1366, 1994.
55. Debes, J. D., and Tindall, D. J. The role of androgens and the androgen receptor in prostate cancer. Cancer Lett., 187: 1-7, 2002.
56. Grossmann, M. E., Huang, H., and Tindall, D. J. Androgen receptor signaling in androgen-refractory prostate cancer. J. Natl. Cancer Inst., 93: 1687-1697., 2001.
57. Zegarra-Moro, O. L., Schmidt, L. J., Huang, H., and Tindall, D. J. Disruption of androgen receptor function inhibits proliferation of androgen-refractory prostate cancer cells. Cancer Res., 62: 1008-1013, 2002.
58. Klocker, H., Culig, Z., Kaspar, F., Hobisch, A., Eberle, J., Reissigl, A., and Bartsch, G. Androgen signal transduction and prostatic carcinoma. World J. Urol., 12: 99-103, 1994.
59. Eder, I. E., Hoffmann, J., Rogatsch, H., Schafer, G., Zopf, D., Bartsch, G., and Klocker, H. Inhibition of LNCaP prostate tumor growth in vivo by an antisense oligonucleotide directed against the human androgen receptor. Cancer Gene Ther., 9: 117-125, 2002.
60. Lannigan, D. A. Estrogen receptor phosphorylation. Steroids, 68: 1-9, 2003.
61. Gioeli, D., Ficarro, S. B., Kwiek, J. J., Aaronson, D., Hancock, M., Catling, A. D., White, F. M., Christian, R. E., Settlage, R. E., Shabanowitz, J., Hunt, D. F., and Weber, M. J. Androgen receptor phosphorylation. Regulation and identification of the phosphorylation sites. J. Biol. Chem., 277: 29304-29314, 2002.
62. Adachi, M., Takayanagi, R., Tomura, A., Imasaki, K., Kato, S., Goto, K., Yanase, T., Ikuyama, S., and Nawata, H. Androgen-insensitivity syndrome as a possible coactivator disease. N. Engl. J. Med., 343: 856-862, 2000.
63. Debes, J. D., Schmidt, L. J., Huang, H., and Tindall, D. J. P300 mediates androgen-independent transactivation of the androgen receptor by interleukin 6. Cancer Res., 62: 5632-5636, 2002.
64. Gregory, C. W., He, B., Johnson, R. T., Ford, O. H., Mohler, J. L., French, F. S., and Wilson, E. M. A mechanism for androgen receptor-mediated prostate cancer recurrence after androgen deprivation therapy. Cancer Res., 61: 4315-4319, 2001.
65. Li, P., Yu, X., Ge, K., Melamed, J., Roeder, R. G., and Wang, Z. Heterogeneous expression and functions of androgen receptor co-factors in primary prostate cancer. Am. J. Pathol., 161: 1467-1474, 2002.
66. Forti, G., Salerno, R., Moneti, G., Zoppi, S., Fiorelli, G., Marinoni, T., Natali, A., Costantini, A., Serio, M., Martini, L., and et al. Three-month treatment with a long-acting gonadotropin-releasing hormone agonist of patients with benign prostatic hyperplasia: effects on tissue androgen concentration, 5 α-reductase activity and androgen receptor content. J. Clin. Endocrinol. Metab., 68: 461-468, 1989.