Deregulation of IGF-binding proteins -2 and -5 contributes to the development of endocrine resistant breast cancer in vitro

Oncotarget

Volumn 7, Issue 22, 2016, Pages 32129-32143

  Hawsawi, Yousef ^a,b,c   Humphries, Matthew P ^b   Wright, Alexander ^b   Berwick, Angelene ^b   Shires, Mike ^b   Al Kharobi, Hanaa ^a   El Gendy, Reem ^a   Jove, Maria ^a   Twelves, Chris ^a,b   Speirs, Valerie ^b   Beattie, James ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Breast cancer; Endocrine resistance; IGF

Indexed keywords

SMALL INTERFERING RNA; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C RECEPTOR; TAMOXIFEN; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; IGFBP-2 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; CANCER HORMONE THERAPY; CANCER RESISTANCE; CANCER SURVIVAL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROARRAY ANALYSIS; MOLECULAR IMAGING; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RETROSPECTIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; ADJUVANT CHEMOTHERAPY; BREAST TUMOR; CELL MOTION; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; KAPLAN MEIER METHOD; MCF-7 CELL LINE; METABOLISM; MORTALITY; PATHOLOGY; RISK ASSESSMENT; RISK FACTOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR; TREATMENT OUTCOME; TUMOR INVASION; TUMOR RECURRENCE;

ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CHEMOTHERAPY, ADJUVANT; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 2; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; KAPLAN-MEIER ESTIMATE; MCF-7 CELLS; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; RISK ASSESSMENT; RISK FACTORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TAMOXIFEN; TIME FACTORS; TRANSFECTION; TREATMENT OUTCOME;

EID: 84973557254     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8534     Document Type: Article

References (62)

1. Browne BC, Hochgrafe F, Wu J, Millar EK, Barraclough J, Stone A, McCloy RA, Lee CS, Roberts C, Ali NA, Boulghourjian A, Schmich F, Linding R, et al. Global characterization of signalling networks associated with tamoxifen resistance in breast cancer. FEBS J. 2013; 280:5237-5257.
2. Kleinberg DL, Ruan W. IGF-I, GH, and sex steroid effects in normal mammary gland development. J Mammary Gland Biol Neoplasia. 2008; 13:353-360.
3. 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.
4. 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.
5. 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.
6. Wiseman LR, Johnson MD, Wakeling AE, Lykkesfeldt AE, May FE, Westley BR. Type I IGF receptor and acquired tamoxifen resistance in oestrogen-responsive human breast cancer cells. Eur J Cancer. 1993; 29A:2256-2264.
7. Boylan M, van den Berg HW, Lynch M. The antiproliferative effect of suramin towards tamoxifen-sensitive and resistant human breast cancer cell lines in relation to expression of receptors for epidermal growth factor and insulin-like growth factor-I: growth stimulation in the presence of tamoxifen. Ann Oncol. 1998; 9:205-211.
8. Gualberto A, Pollak M. Emerging role of insulin-like growth factor receptor inhibitors in oncology: early clinical trial results and future directions. Oncogene. 2009; 28:3009-3021.
9. van den Berg HW, Claffie D, Boylan M, McKillen J, Lynch M, McKibben B. Expression of receptors for epidermal growth factor and insulin-like growth factor I by ZR-75-1 human breast cancer cell variants is inversely related: the effect of steroid hormones on insulin-like growth factor I receptor expression. Br J Cancer. 1996; 73:477-481.
10. Yee D, Favoni RE, Lippman ME, Powell DR. Identification of insulin-like growth factor binding proteins in breast cancer cells. Breast Cancer Res Treat. 1991; 18:3-10.
11. Yee D, Jackson JG, Kozelsky TW, Figueroa JA. Insulin-like growth factor binding protein 1 expression inhibits insulinlike growth factor I action in MCF-7 breast cancer cells. Cell Growth Differ. 1994; 5:73-77.
12. Chen JC, Shao ZM, Sheikh MS, Hussain A, LeRoith D, Roberts CT Jr, Fontana JA. Insulin-like growth factorbinding protein enhancement of insulin-like growth factor-I (IGF-I)-mediated DNA synthesis and IGF-I binding in a human breast carcinoma cell line. J Cell Physiol. 1994; 158:69-78.
13. McCaig C, Perks CM, Holly JM. Intrinsic actions of IGFBP-3 and IGFBP-5 on Hs578T breast cancer epithelial cells: inhibition or accentuation of attachment and survival is dependent upon the presence of fibronectin. J Cell Sci. 2002; 115:4293-4303.
14. McIntosh J, Dennison G, Holly JM, Jarrett C, Frankow A, Foulstone EJ, Winters ZE, Perks CM. IGFBP-3 can either inhibit or enhance EGF-mediated growth of breast epithelial cells dependent upon the presence of fibronectin. J Biol Chem. 2010; 285:38788-38800.
15. De Leon DD, Wilson DM, Bakker B, Lamsom G, Hintz RL, Rosenfeld RG. Characterization of insulin-like growth factor binding proteins from human breast cancer cells. Mol Endocrinol. 1989; 3:567-574.
16. Kim I, Manni A, Lynch J, Hammond JM. Identification and regulation of insulin-like growth factor binding proteins produced by hormone-dependent and -independent human breast cancer cell lines. Mol Cell Endocrinol. 1991; 78:71-78.
17. Perks CM, Bowen S, Gill ZP, Newcomb PV, Holly JM. Differential IGF-independent effects of insulin-like growth factor binding proteins (1-6) on apoptosis of breast epithelial cells. J Cell Biochem. 1999; 75:652-664.
18. Juncker-Jensen A, Lykkesfeldt AE, Worm J, Ralfkiaer U, Espelund U, Jepsen JS. Insulin-like growth factor binding protein 2 is a marker for antiestrogen resistant human breast cancer cell lines but is not a major growth regulator. Growth Horm IGF Res. 2006; 16:224-239.
19. Ahn BY, Elwi AN, Lee B, Trinh DL, Klimowicz AC, Yau A, Chan JA, Magliocco A, Kim SW. Genetic screen identifies insulin-like growth factor binding protein 5 as a modulator of tamoxifen resistance in breast cancer. Cancer Res. 2010; 70:3013-3019.
20. Hiscox S, Morgan L, Barrow D, Dutkowskil C, Wakeling A, Nicholson RI. Tamoxifen resistance in breast cancer cells is accompanied by an enhanced motile and invasive phenotype: inhibition by gefitinib ('Iressa', ZD1839). Clin Exp Metastasis. 2004; 21:201-212.
21. Perks CM, Vernon EG, Rosendahl AH, Tonge D, Holly JM. IGF-II, IGFBP-2 differentially regulate PTEN in human breast cancer cells. Oncogene. 2007; 26:5966-5972.
22. Pereira JJ, Meyer T, Docherty SE, Reid HH, Marshall J, Thompson EW, Rossjohn J, Price JT. Bimolecular interaction of insulin-like growth factor (IGF) binding protein-2 with alphavbeta3 negatively modulates IGF-Imediated migration and tumor growth. Cancer Res. 2004; 64:977-984.
23. Soh CL, McNeil K, Owczarek CM, Hardy MP, Fabri LJ, Pearse M, Delaine CA, Forbes BE. Exogenous administration of protease-resistant, non-matrix-binding IGFBP-2 inhibits tumour growth in a murine model of breast cancer. British Journal of Cancer. 2014; 110: 2855-2864.
24. Schutt BS, Langkamp M, Rauschnabel U, Ranke MB, Elmlinger MW. Integrin-mediated action of insulin-like growth factor binding protein-2 in tumor cells. J Mol Endocrinol. 2004; 32:859-868.
25. Frommer KW, Reichenmiller K, Schutt BS, Hoeflich A, Ranke MB, Dodt G, Elmlinger MW. IGF-independent effects of IGFBP-2 on the human breast cancer cell line Hs578T. J Mol Endocrinol. 2006; 37:13-23.
26. Sureshbabu A, Okajima H, Yamanaka D, Tonner E, Shastri S, Maycock J, Szymanowska M, Shand J, Takahashi S, Beattie J, Allan G, Flint D. IGFBP5 induces cell adhesion, increases cell survival and inhibits cell migration in MCF-7 human breast cancer cells. J Cell Sci. 2012; 125:1693-1705.
27. Vijayan A, Guha D, Ameer F, Kaziri I, Mooney CC, Bennett L, Sureshbabu A, Tonner E, Beattie J, Allan GJ, Edwards J, Flint DJ. IGFBP-5 enhances epithelial cell adhesion and protects epithelial cells from TGFbeta1- induced mesenchymal invasion. Int J Biochem Cell Biol. 2013; 45:2774-2785.
28. Kricker JA, Towne CL, Firth SM, Herington AC, Upton Z. Structural and functional evidence for the interaction of insulin-like growth factors (IGFs) and IGF binding proteins with vitronectin. Endocrinology. 2003; 144:2807-2815.
29. Limer JL, Parkes AT, Speirs V. Differential response to phytoestrogens in endocrine sensitive and resistant breast cancer cells in vitro. Int J Cancer. 2006; 119:515-521.
30. Scott DJ, Parkes AT, Ponchel F, Cummings M, Poola I, Speirs V. Changes in expression of steroid receptors, their downstream target genes and their associated co-regulators during the sequential acquisition of tamoxifen resistance in vitro. Int J Oncol. 2007; 31:557-565.
31. Wong C, Chen S. The development, application and limitations of breast cancer cell lines to study tamoxifen and aromatase inhibitor resistance. J Steroid Biochem Mol Biol. 2012; 131:83-92.
32. Alam MW, Persson CU, Reinbothe S, Kazi JU, Ronnstrand L, Wigerup C, Ditzel HJ, Lykkesfeldt AE, Pahlman S, Jogi A. HIF2alpha contributes to antiestrogen resistance via positive bilateral crosstalk with EGFR in breast cancer cells. Oncotarget. 2016; 7:11238-11250. doi: 10.18632/oncotarget.7167.
33. Phuong NT, Kim SK, Im JH, Yang JW, Choi MC, Lim SC, Lee KY, Kim YM, Yoon JH, Kang KW. Induction of methionine adenosyltransferase 2A in tamoxifen-resistant breast cancer cells. Oncotarget. 2015; 7:13902-13916. doi: 10.18632/oncotarget.5298.
34. Perks CM, Holly JM. IGFBPs and breast cancer. Breast Dis. 2003; 17:91-104.
35. Busund LT, Richardsen E, Busund R, Ukkonen T, Bjornsen T, Busch C, Stalsberg H. Significant expression of IGFBP2 in breast cancer compared with benign lesions. J Clin Pathol. 2005; 58:361-366.
36. Elatiq F, Garrouste F, Remaclebonnet M, Sastre B, Pommier G. Alterations in Serum Levels of Insulin-Like Growth-Factors and Insulin-Like Growth-Factor-Binding Proteins in Patients with Colorectal-Cancer. International Journal of Cancer. 1994; 57:491-497.
37. Disis ML, Gad E, Herendeen DR, Lai VP, Park KH, Cecil DL, O'Meara MM, Treuting PM, Lubet RA. A multiantigen vaccine targeting neu, IGFBP-2, and IGF-IR prevents tumor progression in mice with preinvasive breast disease. Cancer Prev Res. 2013; 6:1273-1282.
38. Taylor KJ, Sims AH, Liang L, Faratian D, Muir M, Walker G, Kuske B, Dixon JM, Cameron DA, Harrison DJ, Langdon SP. Dynamic changes in gene expression in vivo predict prognosis of tamoxifen-treated patients with breast cancer. Breast Cancer Res. BCR. 2010; 12:R39.
39. Huynh H, Yang XF, Pollak M. A role for insulin-like growth factor binding protein 5 in the antiproliferative action of the antiestrogen ICI 182780. Cell Growth Differ. 1996; 7:1501-1506.
40. Yamashita H, Takahashi S, Ito Y, Yamashita T, Ando Y, Toyama T, Sugiura H, Yoshimoto N, Kobayashi S, Fujii Y, Iwase H. Predictors of response to exemestane as primary endocrine therapy in estrogen receptor-positive breast cancer. Cancer Sci. 2009; 100:2028-2033.
41. So AI, Levitt RJ, Eigl B, Fazli L, Muramaki M, Leung S, Cheang MC, Nielsen TO, Gleave M, Pollak M. Insulinlike growth factor binding protein-2 is a novel therapeutic target associated with breast cancer. Clin Cancer Res. 2008; 14:6944-6954.
42. Sehgal P, Kumar N, Praveen Kumar VR, Patil S, Bhattacharya A, Vijaya Kumar M, Mukherjee G, Kondaiah P. Regulation of protumorigenic pathways by insulin like growth factor binding protein2 and its association along with beta-catenin in breast cancer lymph node metastasis. Mol Cancer. 2013; 12:63.
43. Dean SJ, Perks CM, Holly JM, Bhoo-Pathy N, Looi LM, Mohammed NA, Mun KS, Teo SH, Koobotse MO, Yip CH, Rhodes A. Loss of PTEN expression is associated with IGFBP2 expression, younger age, and late stage in triplenegative breast cancer. Am J Clin Pathol 2014; 141:323-333.
44. Dokmanovic M, Shen Y, Bonacci TM, Hirsch DS, Wu WJ. Trastuzumab regulates IGFBP-2 and IGFBP-3 to mediate growth inhibition: implications for the development of predictive biomarkers for trastuzumab resistance. Mol Cancer Ther. 2011; 10:917-928.
45. Park KH, Gad E, Goodell V, Dang Y, Wild T, Higgins D, Fintak P, Childs J, Dela Rosa C, Disis ML. Insulinlike growth factor-binding protein-2 is a target for the immunomodulation of breast cancer. Cancer Res. 2008; 68:8400-8409.
46. Li X, Cao X, Li X, Zhang W, Feng Y. Expression level of insulin-like growth factor binding protein 5 mRNA is a prognostic factor for breast cancer. Cancer Sci. 2007; 98:1592-1596.
47. Hao X, Sun B, Hu L, Lahdesmaki H, Dunmire V, Feng Y, Zhang SW, Wang H, Wu C, Wang H, Fuller GN, Symmans WF, Shmulevich I, Zhang W. Differential gene and protein expression in primary breast malignancies and their lymph node metastases as revealed by combined cDNA microarray and tissue microarray analysis. Cancer. 2004; 100:1110-1122.
48. Wang H, Arun BK, Wang H, Fuller GN, Zhang W, Middleton LP, Sahin AA. IGFBP2 and IGFBP5 overexpression correlates with the lymph node metastasis in T1 breast carcinomas. Breast J. 2008; 14:261-267.
49. Punglia RS, Morrow M, Winer EP, Harris JR. Local therapy and survival in breast cancer. New England J Med. 2007; 356:2399-2405.
50. Plant HC, Kashyap AS, Manton KJ, Hollier BG, Hurst CP, Stein SR, Francis GD, Beadle GF, Upton Z, LeavesleyDI. Differential subcellular and extracellular localisations of proteins required for insulin-like growth factor- and extracellular matrix-induced signalling events in breast cancer progression. BMC Cancer. 2014; 14:627.
51. Leyh B, Dittmer A, Lange T, Martens JW, Dittmer J. Stromal cells promote anti-estrogen resistance of breast cancer cells through an insulin-like growth factor binding protein 5 (IGFBP5)/B-cell leukemia/lymphoma (Bcl-3) axis. Oncotarget. 2015; 6:39307-39328. doi: 10.18632/oncotarget.5624.
52. Limer JL, Parkes AT, Speirs V. Differential response to phytoestrogens in endocrine sensitive and resistant breast cancer cells in vitro. International Journal of Cancer. 2006; 119:515-521.
53. Scott DJ, Parkes AT, Ponchel F, Cummings M, Poola I, Speirs V. Changes in expression of steroid receptors, their downstream target genes and their associated co-regulators during the sequential acquisition of tamoxifen resistance in vitro. Int J Oncology. 2007; 31:557-565.
54. Bramani S, Song H, Beattie J, Tonner E, Flint DJ, Allan GJ. Amino acids within the extracellular matrix (ECM) binding region (201-218) of rat insulin-like growth factor binding protein (IGFBP)-5 are important determinants in binding IGF-I. J Mol Endocrinol. 1999; 23:117-123.
55. Fowlkes JL, Serra D. A rapid, non-radioactive method for the detection of insulin-like growth factor binding proteins by Western ligand blotting. Endocrinology. 1996; 137:5751-5754.
56. Maraqa L, Cummings M, Peter MB, Shaaban AM, Horgan K, Hanby AM, Speirs V. Carcinoembryonic antigen cell adhesion molecule 6 predicts breast cancer recurrence following adjuvant tamoxifen. Clin Cancer Res. 2008; 14:405-411.
57. Hamilton-Burke W, Coleman L, Cummings M, Green CA, Holliday DL, Horgan K, Maraqa L, Peter MB, Pollock S, Shaaban AM, Smith L, Speirs V. Phosphorylation of estrogen receptor beta at serine 105 is associated with good prognosis in breast cancer. Am J Pathol. 2010; 177:1079-1086.
58. Peter MB, Shaaban AM, Rajan SS, Maraqa L, Horgan K, Speirs V. Investigating and critically appraising the expression and potential role of androgen receptor in breast carcinoma. Horm Mol Biol Clin Invest 2011; 7:273-278.
59. Shaaban AM, Green AR, Karthik S, Alizadeh Y, Hughes TA, Harkins L, Ellis IO, Robertson JF, Paish EC, Saunders PT, Groome NP, Speirs V. Nuclear and cytoplasmic expression of ERbeta1, ERbeta2, and ERbeta5 identifies distinct prognostic outcome for breast cancer patients. Clini Cancer Res. 2008; 14:5228-5235.
60. Wong PP, Yeoh CC, Ahmad AS, Chelala C, Gillett C, Speirs V, Jones JL, Hurst HC. Identification of MAGEA antigens as causal players in the development of tamoxifenresistant breast cancer. Oncogene. 2014; 33:4579-4588.
61. Budczies J, Klauschen F, Sinn BV, Gyorffy B, Schmitt WD, Darb-Esfahani S, Denkert C. Cutoff Finder: A Comprehensive and Straightforward Web Application Enabling Rapid Biomarker Cutoff Optimization. Plos One. 2012; 7.
62. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat. 2010; 123:725-731.