The effect of estradiol on in vivo tumorigenesis is modulated by the human epidermal growth factor receptor 2/phosphatidylinositol 3-kinase/Akt1 pathway

Endocrinology

Volumn 148, Issue 3, 2007, Pages 1171-1180

  Lehnes, Kevin ^a   Winder, Abigail D ^a   Alfonso, Camille ^a   Kasid, Natasha ^a   Simoneaux, Michael ^a   Summe, Heather ^a   Morgan, Elisha ^a   Iann, Mary C ^a   Duncan, Jessica ^a   Eagan, Matthew ^a   Tavaluc, Raluca ^a   Evans Jr , Charles H ^a   Russell, Robert ^b   Wang, Antai ^c   Hu, Fengming ^c   Stoica, Adriana ^b,d  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c GEORGETOWN UNIVERSITY   (United States)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (2 BENZOTHIAZOLYL)THIOMETHYL 4 HYDROXY 3 METHOXYBENZYLIDENECYANOACETAMIDE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE RECEPTOR; PROTEIN KINASE B; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER INHIBITION; CARCINOGENESIS; CONTROLLED STUDY; CYTOMEGALOVIRUS; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NONHUMAN; NUDE MOUSE; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR VOLUME; XENOGRAFT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BENZOTHIAZOLES; CELL TRANSFORMATION, NEOPLASTIC; ESTRADIOL; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; OVARIECTOMY; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TYRPHOSTINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33847082588     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2006-1179     Document Type: Article

References (55)

1. Ikeda K, Inoue S 2004 Estrogen receptors and their downstream targets in cancer. Arch Histol Cytol 67:435-442
2. Marino M, Acconcia F, Ascenzi P 2005 Estrogen receptor signalling: bases for drug actions. Curr Drug Targets Immune Endocr Metabol Disord 5:305-314
3. Clarke R, Leonessa F, Welch JN, Skaar TC 2001 Cellular and molecular pharmacology of antiestrogens action and resistance. Pharmacol Rev 53:25-71
4. Jordan VC 2006 Pak up your breast tumor - and grow! J Natl Cancer Inst 98:657-659
5. Wakeling AE, Dukes M, Bowler J 1991 A potent specific pure antiestrogen with clinical potential. Cancer Res 51:3867-3873
6. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A, Press MF 1989 Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244:707-712
7. Thompson JE, Thompson CB 2004 Putting the rap on Akt. J Clin Oncol 22:4217-4226
8. Testa JR, Bellacosa A 2001 AKT plays a central role in tumorigenesis. Proc Natl Acad Sci USA 98:10983-10985
9. Press MF, Bernstein L, Thomas PA, Meisner LF, Zhou JY, Ma Y, Hung G, Robinson RA, Harris C, El-Naggar A, Slamon DJ, Phillips RN, Ross JS, Wolman SR, Flom KJ 1997 HER-2/neu gene amplification characterized by fluorescence in situ hybridization: poor prognosis in node-negative breast carcinomas. J Clin Oncol 15:2894-2904
10. Wright C, Angus B, Nicholson S, Sainsbury JR, Cairns J, Gullick WJ, Kelly P, Harris AL, Horne CH 1989 Expression of c-erbB-2 oncoprotein: a prognostic indicator in human breast cancer. Cancer Res 49:2087-2090
11. Liu W, Li J, Roth RA 1999 Heregulin regulation of Akt/protein kinase B in breast cancer cells. Biochem Biophys Res Commun 261:897-903
12. Di Giovanna MP 1999 Clinical significance of HER-2/neu overexpression - part I and II. In: De Vita Jr VT, Hellman S, Rosenberg SA, eds. Principles and practice of oncology. Cedar Knolls, NJ: Lippincott, Williams and Wilkins; part I; 1-10; part II; 1-14
13. Knowlden JM, Hutcheson IR, Jones HE, Madden T, Gee JM, Harper ME, Barrow D, Wakeling AE, Nicholson RI 2003 Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology 144:1032-1044
14. Sonoo H, Kurebayashi J 2000 Predictive factors for response to endocrine therapy in patients with recurrent breast cancer. Breast Cancer 7:297-301
15. Arteaga CL 2002 Overview of epidermal growth factor receptor biology and its role as a therapeutic target in human neoplasia. Semin Oncol 29(5 Suppl 14):3-9
16. Bunone G, Briand PA, Miksicek RJ, Picard D 1996 Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J 15:2174-2183
17. Kato S 2001 Estrogen receptor-mediated cross-talk with growth factor signaling pathways. Breast Cancer 8:3-9
18. Sun M, Wang G, Paciga JE, Feldman RI, Yuan ZQ, Ma XL, Shelley SA, Jove R, Tsichlis PN, Nicosia SV, Cheng JQ 2001 AKT1/PKBα kinase is frequently elevated in human cancers and its constitutive activation is required for oncogenic transformation in NIH3T3 cells. Am J Pathol 159:431-437
19. Kurokawa H, Lenferink AE, Simpson JF, Pisacane PI, Sliwkowski MX, Forbes JT, Arteaga CL 2000 Inhibition of HER2/neu (erbB-2) and mitogen-activated protein kinases enhances tamoxifen action against HER2-overexpressing, tamoxifen-resistant breast cancer cells. Cancer Res 60:5887-5894
20. Franke TF, Kaplan DR, Cantley LC, Toker A 1997 Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275:665-668
21. Hay N 2005 The Akt-mTOR tango and its relevance to cancer. Cancer Cell 8:179-183
22. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK 2000 Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541
23. Rai D, Frolova A, Frasor J, Carpenter AE, Katzenellenbogen BS 2005 Distinctive actions of membrane-targeted versus nuclear localized estrogen receptors in breast cancer cells. Mol Endocrinol 19:1606-1617
24. Martin MB, Franke TF, Stoica GE, Chambon P, Katzenellenbogen BS, Stoica BA, McLemore MS, Olivo SE, Stoica A 2000 A role for Akt in mediating the estrogenic functions of epidermal growth factor and insulin-like growth factor I. Endocrinology 141:4503-4511
25. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H 2001 Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor α: a new model for anti-estrogen resistance. J Biol Chem 276:9817-9824
26. Stoica GE, Franke TF, Moroni M, Mueller S, Morgan E, Iann MC, Winder AD, Reiter R, Wellstein A, Martin MB, Stoica A 2003 Effect of estradiol on estrogen receptor-α gene expression and activity can be modulated by the ErbB2/PI 3-K/Akt pathway. Oncogene 22:7998-8011
27. Berthois Y, Katzenellenbogen JA, Katzenellenbogen BS 1986 Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture. Proc Natl Acad Sci USA 83:2496-2500
28. Saceda M, Lippman ME, Chambon P, Lindsey RL, Ponglikitmongkol M, Puente M, Martin MB 1988 Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol Endocrinol 2:1157-1162
29. Ahmed NN, Franke TF, Bellacosa A, Datta K, Gonzalez-Portal ME, Taguchi T, Testa JR, Tsichlis PN 1993 The proteins encoded by c-akt and v-akt differ in post-translational modification, subcellular localization and oncogenic potential. Oncogene 8:1957-1963
30. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN 1995 The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736
31. Stoica A, Katzenellenbogen BS, Martin MB 2000 Activation of estrogen receptor-α by the heavy metal cadmium. Mol Endocrinol 14:545-553
32. Osborne CK, Coronado-Heinsohn EB, Hilsenbeck SG, McCue BL, Wakeling AE, McClelland RA, Manning DL, Nicholson RI 1995 Comparison of the effects of a pure steroidal antiestrogen with those of tamoxifen in a model of human breast cancer. J Natl Cancer Inst 87:746-750
33. Brunner N, Svenstrup B, Spang-Thomsen M, Bennett P, Nielsen A, Nielsen J 1986 Serum steroid levels in intact and endocrine ablated BALB/c nude mice and their intact littermates. J Steroid Biochem 25:429-432
34. Brady H, Desai S, Gayo-Fung LM, Khammungkhune S, McKie JA, O'Leary E, Pascasio L, Sutherland MK, Anderson DW, Bhagwat SS, Stein B 2002 Effects of SP500263, a novel, potent antiestrogen, on breast cancer cells and in xenograft models. Cancer Res 62:1439-1442
35. Altomare DA, Testa JR 2005 Perturbations of the AKT signaling pathway in human cancer. Oncogene 24:7455-7464
36. Cuello M, Ettenberg SA, Clark AS, Keane MM, Posner RH, Nau MM, Dennis PA, Lipkowitz S 2001 Down-regulation of the erbB-2 receptor by trastuzumab (herceptin) enhances tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis in breast and ovarian cancer cell lines that overexpress erbB-2. Cancer Res 61:4892-4900
37. Kumar R, Hung MC 2005 Signaling intricacies take center stage in cancer cells. Cancer Res 65:2511-2515
38. Hutchinson JN, Muller WJ 2000 Transgenic mouse models of human breast cancer. Oncogene 19:6130-6137
39. Webster MA, Martin-Soudant N, Nepveu A, Cardiff RD, Muller WJ 1998 The induction of uterine leiomyomas and mammary tumors in transgenic mice expressing polyomavirus (PyV) large T (LT) antigen is associated with the ability of PyV LT antigen to form specific complexes with retinoblastoma and CUTL1 family members. Oncogene 16:1963-1972
40. Seibert K, Shafie SM, Triche TJ, Whang-Peng JJ, O'Brien SJ, Toney JH, Huff KK, Lippman ME 1983 Clonal variation of MCF-7 breast cancer cells in vitro and in athymic nude mice. Cancer Res 43:2223-2239
41. Kirkegaard T, Witton CJ, McGlynn LM, Tovey SM, Dunne B, Lyon A, Bartlett JM 2005 AKT activation predicts outcome in breast cancer patients treated with tamoxifen. J Pathol 207:139-146
42. Nakatani K, Thompson DA, Barthel A, Sakaue H, Liu W, Weigel RJ, Roth RA 1999 Up-regulation of Akt3 in estrogen receptor-deficient breast cancers and androgen-independent prostate cancer lines. J Biol Chem 274:21528-21532
43. Miwa W, Yasuda J, Murakami Y, Yashima K, Sugano K, Sekine T, Kono A, Egawa S, Yamaguchi K, Hayashizaki Y, Sekiya T 1996 Isolation of DNA sequences amplified at chromosome 19q13.1-q13.2 including the AKT2 locus in human pancreatic cancer. Biochem Biophys Res Commun 225:968-974
44. Sun M, Paciga JE, Feldman RI, Yuan Z, Coppola D, Lu YY, Shelley SA, Nicosia SV, Cheng JQ 2001 Phosphatidylinositol-3-OH kinase (PI3K)/AKT2, activated in breast cancer, regulates and is induced by estrogen receptor α (ERα) via interaction between ERα and PI3K. Cancer Res 61:5985-5991
45. Xia W, Chen JS, Zhou X, Sun PR, Lee DF, Liao Y, Zhou BP, Hung MC 2004 Phosphorylation/cytoplasmic localization of p21Cip1/WAF1 is associated with HER2/neu overexpression and provides a novel combination predictor for poor prognosis in breast cancer patients. Clin Cancer Res 10:3815-3824
46. Hutchinson J, Jin J, Cardiff RD, Woodgett JR, Muller WJ 2001 Activation of Akt (protein kinase B) in mammary epithelium provides a critical cell survival signal required for tumor progression. Mol Cell Biol 21:2203-2212
47. Pattengale PK, Stewart TA, Leder A, Sinn E, Muller W, Tepler I, Schmidt E, Leder P 1989 Animal models of human disease. Pathology and molecular biology of spontaneous neoplasms occurring in transgenic mice carrying and expressing activated cellular oncogenes. Am J Pathol 135:39-61
48. Zeng X, Xu H, Glazer RI 2002 Transformation of mammary epithelial cells by 3-phosphoinositide-dependent protein kinase-1 (PDK1) is associated with the induction of protein kinase Cα. Cancer Res 62:3538-3543
49. deGraffenried LA, Friedrichs WE, Russell DH, Donzis EJ, Middleton AK, Silva JM, Roth RA, Hidalgo M 2004 Inhibition of mTOR activity restores tamoxifen response in breast cancer cells with aberrant Akt Activity. Clin Cancer Res 10:8059-8067
50. Ackler S, Ahmad S, Tobias C, Johnson MD, Glazer RI 2002 Delayed mammary gland involution in MMTV-AKT1 transgenic mice. Oncogene 21:198-206
51. Schwertfeger KL, Richert MM, Anderson SM 2001 Mammary gland involution is delayed by activated Akt in transgenic mice. Mol Endocrinol 15:867-881
52. Ma N, Szmitko P, Brade A, Chu I, Lo A, Woodgett J, Klamut H, Liu FF 2004 Kinase-dead PKB gene therapy combined with hyperthermia for human breast cancer. Cancer Gene Ther 11:52-60
53. Jetzt A, Howe JA, Horn MT, Maxwell E, Yin Z, Johnson D, Kumar CC 2003 Adenoviral-mediated expression of a kinase-dead mutant of Akt induces apoptosis selectively in tumor cells and suppresses tumor growth in mice. Cancer Res 63:6697-6706
54. Beliakoff J, Bagatell R, Paine-Murrieta G, Taylor CW, Lykkesfeldt AE, Whitesell L 2003 Hormone-refractory breast cancer remains sensitive to the antitumor activity of heat shock protein 90 inhibitors. Clin Cancer Res 9:4961-4971
55. Yuan ZQ, Sun M, Feldman RI, Wang G, Ma X, Jiang C, Coppola D, Nicosia SV, Cheng JQ 2000 Frequent activation of AKT2 and induction of apoptosis by inhibition of phosphoinositide-3-OH kinase/Akt pathway in human ovarian cancer. Oncogene 19:2324-2330