Elevated insulin-like growth factor 1 receptor signaling induces antiestrogen resistance through the MAPK/ERK and PI3K/Akt signaling routes

Breast Cancer Research

Volumn 13, Issue 3, 2011, Pages

  Zhang, Yinghui ^a   Moerkens, Marja ^a   Ramaiahgari, Sreenivasa ^a   de Bont, Hans ^a   Price, Leo ^a   Meerman, John ^a   van de Water, Bob ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; FULVESTRANT; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE B; SMALL INTERFERING RNA; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TAMOXIFEN; ANTIESTROGEN; DRUG DERIVATIVE; ESTRADIOL;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER RESISTANCE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PHENOTYPE; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; BREAST TUMOR; DRUG RESISTANCE; FEMALE; GENETICS; METABOLISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ESTRADIOL; ESTROGEN ANTAGONISTS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, IGF TYPE 1; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TAMOXIFEN;

EID: 84860390217     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2883     Document Type: Article

References (57)

1. Musgrove EA, Sutherland RL. Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 2009, 9:631-643. 10.1038/nrc2713, 19701242.
2. Zilli M, Grassadonia A, Tinari N, Di Giacobbe A, Gildetti S, Giampietro J, Natoli C, Iacobelli S. Molecular mechanisms of endocrine resistance and their implication in the therapy of breast cancer. Biochim Biophys Acta 2009, 1795:62-81.
3. Tonini G, Schiavon G, Fratto ME, Vincenzi B, Santini D. Hormono-biological therapy in metastatic breast cancer: preclinical evidence, clinical studies and future directions. Expert Opin Biol Ther 2008, 8:221-234. 10.1517/14712598.8.2.221, 18194078.
4. Riggins RB, Schrecengost RS, Guerrero MS, Bouton AH. Pathways to tamoxifen resistance. Cancer Lett 2007, 256:1-24. 10.1016/j.canlet.2007.03.016, 2533271, 17475399.
5. Frogne T, Benjaminsen RV, Sonne-Hansen K, Sorensen BS, Nexo E, Laenkholm AV, Rasmussen LM, Riese DJ, de Cremoux P, Stenvang J, Lykkesfeldt AE. Activation of ErbB3, EGFR and Erk is essential for growth of human breast cancer cell lines with acquired resistance to fulvestrant. Breast Cancer Res Treat 2009, 114:263-275. 10.1007/s10549-008-0011-8, 2764248, 18409071.
6. Arpino G, Wiechmann L, Osborne CK, Schiff R. Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance. Endocr Rev 2008, 29:217-233. 2528847, 18216219.
7. Dawood S, Cristofanilli M. Endocrine resistance in breast cancer: what really matters?. Ann Oncol 2007, 18:1289-1291. 10.1093/annonc/mdm359, 17693644.
8. Werner H, Bruchim I. The insulin-like growth factor-I receptor as an oncogene. Arch Physiol Biochem 2009, 115:58-71. 10.1080/13813450902783106, 19485702.
9. Surmacz E. Function of the IGF-I receptor in breast cancer. J Mammary Gland Biol Neoplasia 2000, 5:95-105. 10.1023/A:1009523501499, 10791772.
10. Sachdev D, Zhang X, Matise I, Gaillard-Kelly M, Yee D. The type I insulin-like growth factor receptor regulates cancer metastasis independently of primary tumor growth by promoting invasion and survival. Oncogene 2010, 29:251-262. 10.1038/onc.2009.316, 2843625, 19838209.
11. Klinakis A, Szabolcs M, Chen G, Xuan S, Hibshoosh H, Efstratiadis A. Igf1r as a therapeutic target in a mouse model of basal-like breast cancer. Proc Natl Acad Sci USA 2009, 106:2359-2364. 10.1073/pnas.0810221106, 2650161, 19174523.
12. Sachdev D, Hartell JS, Lee AV, Zhang X, Yee D. A dominant negative type I insulin-like growth factor receptor inhibits metastasis of human cancer cells. J Biol Chem 2004, 279:5017-5024.
13. Taunk NK, Goyal S, Moran MS, Yang Q, Parikh R, Haffty BG. Prognostic significance of IGF-1R expression in patients treated with breast-conserving surgery and radiation therapy. Radiother Oncol 2010, 96:204-208. 10.1016/j.radonc.2010.03.009, 20338651.
14. Ouban A, Muraca P, Yeatman T, Coppola D. Expression and distribution of insulin-like growth factor-1 receptor in human carcinomas. Hum Pathol 2003, 34:803-808. 10.1016/S0046-8177(03)00291-0, 14506643.
15. Law JH, Habibi G, Hu K, Masoudi H, Wang MY, Stratford AL, Park E, Gee JM, Finlay P, Jones HE, Nicholson RI, Carboni J, Gottardis M, Pollak M, Dunn SE. Phosphorylated insulin-like growth factor-I/insulin receptor is present in all breast cancer subtypes and is related to poor survival. Cancer Res 2008, 68:10238-10246. 10.1158/0008-5472.CAN-08-2755, 19074892.
16. Fagan DH, Yee D. Crosstalk between IGF1R and estrogen receptor signaling in breast cancer. J Mammary Gland Biol Neoplasia 2008, 13:423-429. 10.1007/s10911-008-9098-0, 19003523.
17. Sisci D, Surmacz E. Crosstalk between IGF signaling and steroid hormone receptors in breast cancer. Curr Pharm Des 2007, 13:705-717. 10.2174/138161207780249182, 17346185.
18. Massarweh S, Osborne CK, Creighton CJ, Qin L, Tsimelzon A, Huang S, Weiss H, Rimawi M, Schiff R. Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Res 2008, 68:826-833. 10.1158/0008-5472.CAN-07-2707, 18245484.
19. Knowlden JM, Hutcheson IR, Barrow D, Gee JM, Nicholson RI. Insulin-like growth factor-I receptor signaling in tamoxifen-resistant breast cancer: a supporting role to the epidermal growth factor receptor. Endocrinology 2005, 146:4609-4618. 10.1210/en.2005-0247, 16037379.
20. Parisot JP, Hu XF, DeLuise M, Zalcberg JR. Altered expression of the IGF-1 receptor in a tamoxifen-resistant human breast cancer cell line. Br J Cancer 1999, 79:693-700. 10.1038/sj.bjc.6690112, 2362670, 10070856.
21. Song RX, Chen Y, Zhang Z, Bao Y, Yue W, Wang JP, Fan P, Santen RJ. Estrogen utilization of IGF-1-R and EGF-R to signal in breast cancer cells. J Steroid Biochem Mol Biol 2010, 118:219-230. 10.1016/j.jsbmb.2009.09.018, 2826506, 19815064.
22. Santen RJ, Fan P, Zhang Z, Bao Y, Song RX, Yue W. Estrogen signals via an extra-nuclear pathway involving IGF-1R and EGFR in tamoxifen-sensitive and -resistant breast cancer cells. Steroids 2009, 74:586-594. 10.1016/j.steroids.2008.11.020, 19138696.
23. Huang X, Gao L, Wang S, McManaman JL, Thor AD, Yang X, Esteva FJ, Liu B. Heterotrimerization of the growth factor receptors erbB2, erbB3, and insulin-like growth factor-I receptor in breast cancer cells resistant to herceptin. Cancer Res 2010, 70:1204-1214. 10.1158/0008-5472.CAN-09-3321, 20103628.
24. Romano G, Prisco M, Zanocco-Marani T, Peruzzi F, Valentinis B, Baserga R. Dissociation between resistance to apoptosis and the transformed phenotype in IGF-I receptor signaling. J Cell Biochem 1999, 72:294-310. 10.1002/(SICI)1097-4644(19990201)72:2<294::AID-JCB14>3.0.CO;2-0, 10022512.
25. Swift S, Lorens J, Achacoso P, Nolan GP. Rapid production of retroviruses for efficient gene delivery to mammalian cells using 293T cell-based systems. Curr Protoc Immunol 2001, Chapter 10:Unit 10.17C.
26. Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc 2006, 1:1112-1116. 10.1038/nprot.2006.179, 17406391.
27. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR. New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 1990, 82:1107-1112. 10.1093/jnci/82.13.1107, 2359136.
28. Michalides R, Griekspoor A, Balkenende A, Verwoerd D, Janssen L, Jalink K, Floore A, Velds A, van't Veer L, Neefjes J. Tamoxifen resistance by a conformational arrest of the estrogen receptor α after PKA activation in breast cancer. Cancer Cell 2004, 5:597-605. 10.1016/j.ccr.2004.05.016, 15193262.
29. Lopaczynski W, Terry C, Nissley P. Autophosphorylation of the insulin-like growth factor I receptor cytoplasmic domain. Biochem Biophys Res Commun 2000, 279:955-960. 10.1006/bbrc.2000.4046, 11162456.
30. Shelton JG, Steelman LS, White ER, McCubrey JA. Synergy between PI3K/Akt and Raf/MEK/ERK pathways in IGF-1R mediated cell cycle progression and prevention of apoptosis in hematopoietic cells. Cell Cycle 2004, 3:372-379.
31. Vincent AM, Feldman EL. Control of cell survival by IGF signaling pathways. Growth Horm IGF Res 2002, 12:193-197. 10.1016/S1096-6374(02)00017-5, 12175651.
32. Sutherland RL, Green MD, Hall RE, Reddel RR, Taylor IW. Tamoxifen induces accumulation of MCF 7 human mammary carcinoma cells in the G0/G1 phase of the cell cycle. Eur J Cancer Clin Oncol 1983, 19:615-621. 10.1016/0277-5379(83)90177-3, 6683633.
33. Nicholson RI, Gee JMW, Francis AB, Manning DL, Wakeling AE, Katzenellenbogen BS. Observations arising from the use of pure antiestrogens on estrogen-responsive (Mcf-7) and estrogen growth-independent (K3) human breast-cancer cells. Endocr Relat Cancer 1995, 2:115-121.
34. Fan M, Yan PS, Hartman-Frey C, Chen L, Paik H, Oyer SL, Salisbury JD, Cheng AS, Li L, Abbosh PH, Huang TH, Nephew KP. Diverse gene expression and DNA methylation profiles correlate with differential adaptation of breast cancer cells to the antiestrogens tamoxifen and fulvestrant. Cancer Res 2006, 66:11954-11966. 10.1158/0008-5472.CAN-06-1666, 17178894.
35. Hall JM, Korach KS. Stromal cell-derived factor 1, a novel target of estrogen receptor action, mediates the mitogenic effects of estradiol in ovarian and breast cancer cells. Mol Endocrinol 2003, 17:792-803. 10.1210/me.2002-0438, 12586845.
36. Litzenburger BC, Kim HJ, Kuiatse I, Carboni JM, Attar RM, Gottardis MM, Fairchild CR, Lee AV. BMS-536924 reverses IGF-IR-induced transformation of mammary epithelial cells and causes growth inhibition and polarization of MCF7 cells. Clin Cancer Res 2009, 15:226-237. 10.1158/1078-0432.CCR-08-0801, 2819349, 19118050.
37. Duncia JV, Santella JB 3, Higley CA, Pitts WJ, Wityak J, Frietze WE, Rankin FW, Sun JH, Earl RA, Tabaka AC, Teleha CA, Blom KF, Favata MF, Manos EJ, Daulerio AJ, Stradley DA, Horiuchi K, Copeland RA, Scherle PA, Trzaskos JM, Magolda RL, Trainor GL, Wexler RR, Hobbs FW, Olson RE. MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg Med Chem Lett 1998, 8:2839-2844. 10.1016/S0960-894X(98)00522-8, 9873633.
38. Serra V, Markman B, Scaltriti M, Eichhorn PJ, Valero V, Guzman M, Botero ML, Llonch E, Atzori F, Di Cosimo S, Maira M, Garcia-Echeverria C, Parra JL, Arribas J, Baselga J. NVP-BEZ235, a dual PI3K/mTOR inhibitor, prevents PI3K signaling and inhibits the growth of cancer cells with activating PI3K mutations. Cancer Res 2008, 68:8022-8030. 10.1158/0008-5472.CAN-08-1385, 18829560.
39. Chitnis MM, Yuen JS, Protheroe AS, Pollak M, Macaulay VM. The type 1 insulin-like growth factor receptor pathway. Clin Cancer Res 2008, 14:6364-6370. 10.1158/1078-0432.CCR-07-4879, 18927274.
40. Arpino G, De Angelis C, Giuliano M, Giordano A, Falato C, De Laurentiis M, De Placido S. Molecular mechanism and clinical implications of endocrine therapy resistance in breast cancer. Oncology 2009, 77(Suppl 1):23-37.
41. Yue W, Fan P, Wang J, Li Y, Santen RJ. Mechanisms of acquired resistance to endocrine therapy in hormone-dependent breast cancer cells. J Steroid Biochem Mol Biol 2007, 106:102-110. 10.1016/j.jsbmb.2007.05.008, 2147683, 17616457.
42. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, Weiss H, Schiff R. Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 2004, 96:926-935. 10.1093/jnci/djh166, 15199112.
43. Hurtado A, Holmes KA, Geistlinger TR, Hutcheson IR, Nicholson RI, Brown M, Jiang J, Howat WJ, Ali S, Carroll JS. Regulation of ERBB2 by oestrogen receptor-PAX2 determines response to tamoxifen. Nature 2008, 456:663-666. 10.1038/nature07483, 2920208, 19005469.
44. Green KA, Carroll JS. Oestrogen-receptor-mediated transcription and the influence of co-factors and chromatin state. Nat Rev Cancer 2007, 7:713-722. 10.1038/nrc2211, 17721435.
45. Varma H, Conrad SE. Antiestrogen ICI 182,780 decreases proliferation of insulin-like growth factor I (IGF-I)-treated MCF-7 cells without inhibiting IGF-I signaling. Cancer Res 2002, 62:3985-3991.
46. Johnston SR, Saccani-Jotti G, Smith IE, Salter J, Newby J, Coppen M, Ebbs SR, Dowsett M. Changes in estrogen receptor, progesterone receptor, and pS2 expression in tamoxifen-resistant human breast cancer. Cancer Res 1995, 55:3331-3338.
47. Surmacz E, Burgaud JL. Overexpression of insulin receptor substrate 1 (IRS-1) in the human breast cancer cell line MCF-7 induces loss of estrogen requirements for growth and transformation. Clin Cancer Res 1995, 1:1429-1436.
48. Guvakova MA, Surmacz E. Overexpressed IGF-I receptors reduce estrogen growth requirements, enhance survival, and promote E-cadherin-mediated cell-cell adhesion in human breast cancer cells. Exp Cell Res 1997, 231:149-162. 10.1006/excr.1996.3457, 9056422.
49. Bartucci M, Morelli C, Mauro L, Ando S, Surmacz E. Differential insulin-like growth factor I receptor signaling and function in estrogen receptor (ER)-positive MCF-7 and ER-negative MDA-MB-231 breast cancer cells. Cancer Res 2001, 61:6747-6754.
50. Osborne CK. Tamoxifen in the treatment of breast cancer. N Engl J Med 1998, 339:1609-1618. 10.1056/NEJM199811263392207, 9828250.
51. Hodges LC, Cook JD, Lobenhofer EK, Li L, Bennett L, Bushel PR, Aldaz CM, Afshari CA, Walker CL. Tamoxifen functions as a molecular agonist inducing cell cycle-associated genes in breast cancer cells. Mol Cancer Res 2003, 1:300-311.
52. Ghayad SE, Vendrell JA, Larbi SB, Dumontet C, Bieche I, Cohen PA. Endocrine resistance associated with activated ErbB system in breast cancer cells is reversed by inhibiting MAPK or PI3K/Akt signaling pathways. Int J Cancer 2010, 126:545-562. 10.1002/ijc.24750, 19609946.
53. Bender LM, Nahta R. Her2 cross talk and therapeutic resistance in breast cancer. Front Biosci 2008, 13:3906-3912. 2746389, 18508484.
54. Berstein LM. Molecular mechanisms of mutual effects of the pathological processes during combination of diabetes mellitus and cancer. Biochemistry (Mosc) 2003, 68:703-706.
55. Ignatov A, Ignatov T, Roessner A, Costa SD, Kalinski T. Role of GPR30 in the mechanisms of tamoxifen resistance in breast cancer MCF-7 cells. Breast Cancer Res Treat 2010, 123:87-96. 10.1007/s10549-009-0624-6, 19911269.
56. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
57. Wright GW, Simon RM. A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 2003, 19:2448-2455. 10.1093/bioinformatics/btg345, 14668230.