Signal transducer and activator of transcription 5b, c-Src, and epidermal growth factor receptor signaling play integral roles in estrogen-stimulated proliferation of estrogen receptor-positive breast cancer cells

Molecular Endocrinology

Volumn 22, Issue 8, 2008, Pages 1781-1796

  Fox, Emily M ^a   Bernaciak, Teresa M ^b   Wen, Jie ^a   Weaver, Amanda M ^b   Shupnik, Margaret A ^a,c   Silva, Corinne M ^a,b,c  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ANTIESTROGEN; BROXURIDINE; CYCLIN D1; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; MESSENGER RNA; STAT5B PROTEIN; TAMOXIFEN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER RESISTANCE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MUTANT; ONCOGENE C MYC; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CELL COUNT; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN D1; DRUG RESISTANCE, NEOPLASM; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; HUMANS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TAMOXIFEN; TRANSCRIPTION, GENETIC;

EID: 48249132499     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2007-0419     Document Type: Article

References (64)

1. Herynk MH, Fuqua SA 2004 Estrogen receptor mutations in human disease. Endocr Rev 25:869-898
2. McGuire WL 1975 Endocrine therapy of breast cancer. Annu Rev Med 26:353-363
3. Nilsson S, Makela S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA 2001 Mechanisms of estrogen action. Physiol Rev 81:1535-1565
4. Foster JS, Henley DC, Ahamed S, Wimalasena J 2001 Estrogens and cell-cycle regulation in breast cancer. Trends Endocrinol Metab 12:320-327
5. Basu A, Rowan BG 2005 Genes related to estrogen action in reproduction and breast cancer. Front Biosci 10:2346-2372
6. Hall JM, Couse JF, Korach KS 2001 The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 276:36869-36872
7. Levin ER 2003 Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol Endocrinol 17:309-317
8. Clarke R, Liu MC, Bouker KB, Gu Z, Lee RY, Zhu Y, Skaar TC, Gomez B, O'Brien K, Wang Y, Hilakivi-Clarke LA 2003 Antiestrogen resistance in breast cancer and the role of estrogen receptor signaling. Oncogene 22: 7316-7339
9. Biscardi JS, Belsches AP, Parsons SJ 1998 Characterization of human epidermal growth factor receptor and c-Src interactions in human breast tumor cells. Mol Car-cinog 21:261-272
10. Belsches-Jablonski AP, Biscardi JS, Peavy DR, Tice DA, Romney DA, Parsons SJ 2001 Src family kinases and HER2 interactions in human breast cancer cell growth and survival. Oncogene 20:1465-1475
11. Tice DA, Biscardi JS, Nickles AL, Parsons SJ 1999 Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc Natl Acad Sci USA 96:1415-1420
12. 1101 is associated with modulation of receptor function. J Biol Chem 274:8335-8343
13. Riggins RB, Thomas KS, Ta HQ, Wen J, Davis RJ, Schuh NR, Donelan SS, Owen KA, Gibson MA, Shupnik MA, Silva CM, Parsons SJ, Clarke R, Bouton AH 2006 Physical and functional interactions between Cas and c-Src induce tamoxifen resistance of breast cancer cells through pathways involving epidermal growth factor receptor and signal transducer and activator of transcription 5b. Cancer Res 66:7007-7015
14. Kloth MT, Laughlin KK, Biscardi JS, Boerner JL, Parsons SJ, Silva CM 2003 STAT5b, a mediator of synergism between c-Src and the epidermal growth factor receptor. J Biol Chem 278:1671-1679
15. Yu H, Jove R 2004 The STATs of cancer - new molecular targets come of age. Nat Rev Cancer 4:97-105
16. Darnell Jr JE 1998 Studies of IFN-induced transcriptional activation uncover the Jak-Stat pathway. J Interferon Cytokine Res 18:549-554
17. Bowman T, Garcia R, Turkson J, Jove R 2000 STATs in oncogenesis. Oncogene 19:2474-2488
18. Liu X, Robinson GW, Gouilleux F, Groner B, Henning-hausen L 1995 Cloning and expression of STAT5 and an additional homologue (STAT5b) involved in prolactin signal transduction in mouse mammary tissue. Proc Natl Acad Sci USA 92:8831-8835
19. Silva CM, Lu H, Day RN 1996 Characterization and cloning of STAT5 from IM-9 cells and its activation by growth hormone. Mol Endocrinol 10:508-518
20. Lin JX, Mietz J, Modi WS, John S, Leonard WJ 1996 Cloning of human Stat5B. Reconstitution of interleukin-2-induced Stat5A and Stat5B DNA binding activity in COS-7 cells. J Biol Chem 271:10738-10744
21. Gouilleux F, Wakao H, Mundt M, Groner B 1994 Prolactin induces phosphorylation of Tyr694 of Stat5 (MGF), a prerequisite for DNA binding and induction of transcription. EMBO J 13:4361-4369
22. Kloth MT, Catling AD, Silva CM 2002 Novel activation of STAT5b in response to epidermal growth factor. J Biol Chem 277:8693-8701
23. Weaver AM, Silva CM 2006 Modulation of signal transducer and activator of transcription 5b activity in breast cancer cells by mutation of tyrosines within the transac-tivation domain. Mol Endocrinol 20:2392-2405
24. Moriggl R, Gouilleux-Gruart V, Jahne R, Berchtold S, Gartmann C, Liu X, Hennighausen L, Sotiropoulos A, Groner B, Gouilleux F 1996 Deletion of the carboxyl-terminal transactivation domain of MGF-Stat5 results in sustained DNA binding and a dominant negative pheno-type. Mol Cell Biol 16:5691-5700
25. Wang D, Stravopodis D, Teglund S, Kitazawa J, Ihle JN 1996 Naturally occurring dominant negative variants of State. Mol Cell Biol 16:6141-6148
26. Yu CL, Meyer DJ, Campbell GS, Larner AC, Carter-Su C, Schwartz J, Jove R 1995 Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269:81-83
27. Cao X, Tay A, Guy GR, Tan YH 1996 Activation and association of Stat3 with Src in v-Src-transformed cell lines. Mol Cell Biol 16:1595-1603
28. Chaturvedi P, Sharma S, Reddy EP 1997 Abrogation of interleukin-3 dependence of myeloid cells by the v-src oncogene requires SH2 and SH3 domains which specify activation of STATs. Mol Cell Biol 17:3295-3304
29. Bromberg JF, Horvath CM, Besser D, Lathem WW, Darnell Jr JE 1998 Stat3 activation is required for cellular transformation by v-src. Mol Cell Biol 18:2553-2558
30. Turkson J, Bowman T, Garcia R, Caldenhoven E, De Groot RP, Jove R 1998 Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol Cell Biol 18:2545-2552
31. Garcia R, Yu CL, Hudnall A, Catlett R, Nelson KL, Smithgall T, Fujita DJ, Ethier SP, Jove R 1997 Constitutive activation of Stat3 in fibroblasts transformed by diverse oncoproteins and in breast carcinoma cells. Cell Growth Differ 8:1267-1276
32. Garcia R, Bowman TL, Niu G, Yu H, Minton S, Muro-Cacho CA, Cox CE, Falcone R, Fairclough R, Parsons S, Laudano A, Gazit A, Levitzki A, Kraker A, Jove R 2001 Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20: 2499-2513
33. Yamashita H, Iwase H, Toyama T, Fujii Y 2003 Naturally occurring dominant-negative Stat5 suppresses transcriptional activity of estrogen receptors and induces apoptosis in T47D breast cancer cells. Oncogene 22: 1638-1652
34. Xi S, Zhang Q, Gooding WE, Smithgall TE, Grandis JR 2003 Constitutive activation of Stat5b contributes to carcinogenesis in vivo. Cancer Res 63:6763-6771
35. Sultan AS, Xie J, LeBaron MJ, Ealley EL, Nevalainen MT, Rui H 2005 STAT5 promotes homotypic adhesion and inhibits invasive characteristics of human breast cancer cells. Oncogene 24:746-760
36. Kazansky AV, Kabotyanski EB, Wyszomierski SL, Mancini MA, Rosen JM 1999 Differential effects of prolactin and src/abl kinases on the nuclear translocation of STAT5B and STAT5A. J Biol Chem 274: 22484-22492
37. Yamamoto T, Matsuda T, Junicho A, Kishi H, Saatcioglu F, Muraguchi A 2000 Cross-talk between signal transducer and activator of transcription 3 and estrogen receptor signaling. FEBS Lett 486:143-148
38. Bjornstrom L, Kilic E, Norman M, Parker MG, Sjoberg M 2001 Cross-talk between Stat5b and estrogen receptor-α and -β in mammary epithelial cells. J Mol Endocrinol 27:93-106
39. Faulds MH, Pettersson K, Gustafsson JA, Haldosen LA 2001 Cross-talk between ERs and signal transducer and activator of transcription 5 is E2 dependent and involves two functionally separate mechanisms. Mol Endocrinol 15:1929-1940
40. Wang Y, Cheng CH 2004 ERα and STAT5a cross-talk: interaction through C-terminal portions of the proteins decreases STAT5a phosphorylation, nuclear translocation and DNA-binding. FEBS Lett 572:238-244
41. Levitzki A, Gazit A 1995 Tyrosine kinase inhibition: an approach to drug development. Science 267: 1782-1788
42. Amorino GP, Deeble PD, Parsons SJ 2007 Neurotensin stimulates mitogenesis of prostate cancer cells through a novel c-Src/Stat5b pathway. Oncogene 26: 745-756
43. Fan P, Wang J, Santen RJ, Yue W 2007 Long-term treatment with tamoxifen facilitates translocation of estrogen receptor α out of the nucleus and enhances its interaction with EGFR in MCF-7 breast cancer cells. Cancer Res 67:1352-1360
44. Golubovskaya V, Beviglia L, Xu LH, Earp III HS, Craven R, Cance W 2002 Dual inhibition of focal adhesion kinase and epidermal growth factor receptor pathways cooperatively induces death receptor-mediated apoptosis in human breast cancer cells. J Biol Chem 277: 38978-38987
45. Smit LS, Meyer DJ, Billestrup N, Norstedt G, Schwartz J, Carter-Su C 1996 The role of the growth hormone (GH) receptor and JAK1 and JAK2 kinases in the activation of Stats 1, 3, and 5 by GH. Mol Endocrinol 10:519-533
46. Migliaccio A, Pagano M, Auricchio F 1993 Immediate and transient stimulation of protein tyrosine phosphorylation by estradiol in MCF-7 cells. Oncogene 8:2183-2191
47. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA 1996 Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-depen-dent T cell activation. J Biol Chem 271:695-701
48. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA, Klos KS, Li P, Monia BP, Nguyen NT, Hortobagyi GN, Hung MC, Yu D 2004 PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6:117-127
49. Silva CM, Shupnik MA 2007 Integration of steroid and growth factor pathways in breast cancer: focus on signal transducers and activators of transcription and their potential role in resistance. Mol Endocrinol 21: 1499-1512
50. Bjornstrom L, Sjoberg M 2002 Signal transducers and activators of transcription as downstream targets of non-genomic estrogen receptor actions. Mol Endocrinol 16: 2202-2214
51. Lange CA, Richer JK, Shen T, Horwitz KB 1998 Convergence of progesterone and epidermal growth factor signaling in breast cancer. Potentiation of mitogen-activated protein kinase pathways. J Biol Chem 273: 31308-31316
52. Richer JK, Lange CA, Manning NG, Owen G, Powell R, Horwitz KB 1998 Convergence of progesterone with growth factor and cytokine signaling in breast cancer. Progesterone receptors regulate signal transducers and activators of transcription expression and activity. J Biol Chem 273:31317-31326
53. Stocklin E, Wissler M, Gouilleux F, Groner B 1996 Functional interactions between Stat5 and the glucocorticoid receptor. Nature 383:726-728
54. Boerner JL, Gibson MA, Fox EM, Posner ED, Parsons SJ, Silva CM, Shupnik MA 2005 Estrogen negatively regulates epidermal growth factor (EGF)-mediated signal transducer and activator of transcription 5 signaling in human EGF family receptor-overexpressing breast cancer cells. Mol Endocrinol 19:2660-2670
55. Yamashita H, Nishio M, Fujii Y, Iwase H 2004 Dominant-negative Stat5 inhibits growth and induces apoptosis in T47D-derived tumors in nude mice. Cancer Sci 95: 662-665
56. Hitosugi T, Sasaki K, Sato M, Suzuki Y, Umezawa Y 2007 Epidermal growth factor directs sex-specific steroid signaling through Src activation. J Biol Chem 282: 10697-10706
57. Castoria G, Barone MV, Di Domenico MD, Bilancio A, Ametrano D, Migliaccio A, Auricchio F 1999 Non-tran-scriptional action of oestradiol and progestin triggers DNA synthesis. EMBO J 18:2500-2510
58. Shupnik MA 2004 Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene 23:7979-7989
59. Knowlden JM, Hutcheson IR, Jones HE, Madden T, Gee JM, Harper ME, Barrow D, Wakeling AE, Nicholson Rl 2003 Elevated levels of epidermal growth factor recep-tor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology 144:1032-1044
60. Brinkman A, van der Flier S, Kok EM, Dorssers LC 2000 BCAR1, a human homologue of the adapter protein p130Cas, and antiestrogen resistance in breast cancer cells. J Natl Cancer Inst 92:112-120
61. van der Flier S, Brinkman A, Look MP, Kok EM, Meijer-van Gelder ME, Klijn JG, Dorssers LC, Foekens JA 2000 Bcar1/p130Cas protein and primary breast cancer: prognosis and response to tamoxifen treatment. J Natl Cancer Inst 92:120-127
62. Chu I, Arnaout A, Loiseau S, Sun J, Seth A, McMahon C, Chun K, Hennessy B, Mills GB, Nawaz Z, Slingerland JM 2007 Src promotes estrogen-dependent estrogen receptor α proteolysis in human breast cancer. J Clin Invest 117: 2205-2215
63. Schreihofer DA, Resnick EM, Lin VY, Shupnik MA 2001 Ligand-independent activation of pituitary ER: dependence on PKA-stimulated pathways. Endocrinology 142: 3361-3368
64. Wood TJ, Sliva D, Lobie PE, Goullieux F, Mui AL, Groner B, Norstedt G, Haldosen LA 1997 Specificity of transcription enhancement via the STAT responsive element in the serine protease inhibitor 2.1 promoter. Mol Cell Endocrinol 130:69-81