ErbB3 recruitment of insulin receptor substrate 1 modulates insulin-like growth factor receptor signalling in oestrogen receptor-positive breast cancer cell lines

Breast Cancer Research

Volumn 13, Issue 5, 2011, Pages

  Knowlden, Janice M ^a   Gee, Julia M W ^a   Barrow, Denise ^a   Robertson, John F ^b   Ellis, Ian O ^b   Nicholson, Robert I ^a   Hutcheson, Iain R ^c  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b NOTTINGHAM CITY HOSPITAL   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Breast cancer; ErbB3; IRS 1IGF IR; Resistance

Indexed keywords

4 ANILINO 5 BROMO 2 [4 [2 HYDROXY 3 (N,N DIMETHYLAMINO)PROPOXY]ANILINO]PYRIMIDINE; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; ESTROGEN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; KI 67 ANTIGEN; NEU DIFFERENTIATION FACTOR; PROTEIN KINASE B; PYRIMIDINE DERIVATIVE; SOMATOMEDIN C RECEPTOR; SOMATOMEDIN RECEPTOR; UNCLASSIFIED DRUG; 4-AMINO-1-HYDROXYBUTYLIDENE-1,1-DIPHOSPHONATE; ALENDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; HEREGULIN BETA1; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL CULTURE; CELL STRAIN MCF 7; CONTROLLED STUDY; CORRELATION ANALYSIS; GENETIC ASSOCIATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; BREAST TUMOR; CELL PROLIFERATION; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DIPHOSPHONATES; FEMALE; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; NEUREGULIN-1; PHOSPHORYLATION; RECEPTOR, ERBB-3; RECEPTOR, IGF TYPE 1; RECEPTORS, ESTROGEN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 80053174807     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3018     Document Type: Article

References (52)

1. Sachdev D, Yee D. The IGF system and breast cancer. Endocr Rel Cancer 2001, 8:197-209.
2. 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.
3. 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, 19003523.
4. Surmacz E, Guvakova MA, Nolan MK, Nicosia RF, Sciacca L. Type I insulin-like growth factor receptor function in breast cancer. Breast Cancer Res Treat 1998, 47:255-267. 10.1023/A:1005907101686, 9516080.
5. Happerfield LC, Miles DW, Barnes DM, Thomsen LL, Smith P, Hanby A. The localization of the insulin-like growth factor receptor 1 (IGFR-1) in benign and malignant breast tissue. J Pathol 1997, 183:412-417. 10.1002/(SICI)1096-9896(199712)183:4<412::AID-PATH944>3.0.CO;2-4, 9496257.
6. Gee JM, Robertson JF, Gutteridge E, Ellis IO, Pinder SE, Rubini M, Nicholson RI. Epidermal growth factor receptor/HER2/insulin-like growth factor receptor signalling and oestrogen receptor activity in clinical breast cancer. Endocr Relat Cancer 2005, 12(Suppl 1):S99-S111.
7. Stewart AJ, Johnson MD, May FE, Westley BR. Role of insulin-like growth factors and the type I insulin-like growth factor receptor in the estrogen-stimulated proliferation of human breast cancer cells. J Biol Chem 1990, 265:21172-21178.
8. Lee AV, Jackson JG, Gooch JL, Hilsenbeck SG, Coronado-Heinsohn E, Osborne CK, Yee D. Enhancement of insulin-like growth factor signaling in human breast cancer: estrogen regulation of insulin receptor substrate-1 expression in vitro and in vivo. Mol Endocrinol 1999, 13:787-796. 10.1210/me.13.5.787, 10319328.
9. Hamelers IH, Steenbergh PH. Interactions between estrogen and insulin-like growth factor signaling pathways in human breast tumor cells. Endocr Relat Cancer 2003, 10:331-345. 10.1677/erc.0.0100331, 12790794.
10. Yee D, Lee AV. Crosstalk between the insulin-like growth factors and estrogens in breast cancer. J Mammary Gland Biol Neoplasia 2000, 5:107-115. 10.1023/A:1009575518338, 10791773.
11. Rocha RL, Hilsenbeck SG, Jackson JG, VanDenBerg CL, Weng C, Lee AV, Yee D. Insulin-like growth factor binding protein-3 and insulin receptor substrate-1 in breast cancer: correlation with clinical parameters and disease-free survival. Clin Cancer Res 1997, 3:103-109.
12. Turner BC, Haffty BG, Narayanan L, Yuan J, Havre PA, Gumbs AA, Kaplan L, Burgaud JL, Carter D, Baserga R, Glazer PM. Insulin-like growth factor-I receptor overexpression mediates cellular radioresistance and local breast cancer recurrence after lumpectomy and radiation. Cancer Res 1997, 57:3079-3083.
13. 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. 10.1038/onc.2009.172, 19581933.
14. Lee YH, White MF. Insulin receptor substrate proteins and diabetes. Arch Pharm Res 2004, 27:361-370. 10.1007/BF02980074, 15180298.
15. White MF. The insulin signalling system and the IRS proteins. Diabetologia 1997, 40(Suppl 2):S2-S17.
16. Lawlor MA, Alessi DR. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses?. J Cell Sci 2001, 114:2903-2910. 11686294, 11686294.
17. Nicholson KM, Anderson NG. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 2002, 14:381-395. 10.1016/S0898-6568(01)00271-6, 11882383.
18. Chang Q, Li Y, White MF, Fletcher JA, Xiao S. Constitutive activation of insulin receptor substrate 1 is a frequent event in human tumors: therapeutic implications. Cancer Res 2002, 62:6035-6038.
19. Dearth RK, Cui X, Kim HJ, Kuiatse I, Lawrence NA, Zhang X, Divisova J, Britton OL, Mohsin S, Allred DC, Hadsell DL, Lee AV. Mammary tumorigenesis and metastasis caused by overexpression of insulin receptor substrate (IRS)-1 or IRS-2. Mol Cell Biol 2006, 26:9302-9314. 10.1128/MCB.00260-06, 1698542, 17030631.
20. Koda M, Sulkowska M, Kanczuga-Koda L, Golaszewska J, Kisielewski W, Baltaziak M, Wincewicz A, Sulkowski S. Expression of the insulin receptor substrate 1 in primary tumors and lymph node metastases in breast cancer: correlations with Bcl-xL and Bax proteins. Neoplasma 2005, 52:361-363.
21. Dearth RK, Cui X, Kim HJ, Hadsell DL, Lee AV. Oncogenic transformation by the signaling adaptor proteins insulin receptor substrate (IRS)-1 and IRS-2. Cell Cycle 2007, 6:705-713. 10.4161/cc.6.6.4035, 17374994.
22. Nicholson RI, McClelland RA, Gee JMW, Manning DL, Cannon P, Robertson JF, Ellis IO, Blamey RW. Epidermal growth factor receptor expression in breast cancer: association with response to endocrine therapy. Breast Cancer Res Treat 1994, 29:117-125. 10.1007/BF00666187, 7912565.
23. Knowlden JM, Hutcheson IR, Jones HE, Madden T, Gee JM, Harper ME, Barrow D, Wakeling AE, Nicholson RI. Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology 2003, 144:1032-1044. 10.1210/en.2002-220620, 12586780.
24. 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.
25. Nicholson RI, Hutcheson IR, Hiscox SE, Knowlden JM, Giles M, Barrow D, Gee JM. Growth factor signalling and resistance to selective oestrogen receptor modulators and pure anti-oestrogens: the use of anti-growth factor therapies to treat or delay endocrine resistance in breast cancer. Endocr Relat Cancer 2005, 12(Suppl 1):S29-S36.
26. Fujioka T, Kim JH, Adachi H, Saito K, Tsujimoto M, Yokoyama S, Ui M. Further evidence for the involvement of insulin receptor substrates in epidermal growth factor-induced activation of phosphatidylinositol 3-kinase. Eur J Biochem 2001, 268:4158-4168. 10.1046/j.1432-1327.2001.02327.x, 11488908.
27. Fujioka T, Ui M. Involvement of insulin receptor substrates in epidermal growth factor induced activation of phosphatidylinositol 3-kinase in rat hepatocyte primary culture. Eur J Biochem 2001, 268:25-34. 10.1046/j.1432-1327.2001.01831.x, 11121098.
28. Jones RB, Gordus A, Krall JA, MacBeath G. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 2006, 439:168-174. 10.1038/nature04177, 16273093.
29. Knowlden JM, Jones HE, Barrow D, Gee JM, Nicholson RI, Hutcheson IR. Insulin receptor substrate-1 involvement in epidermal growth factor receptor and insulin-like growth factor receptor signalling: implication for gefitinib ('Iressa') response and resistance. Breast Cancer Res Treat 2007, 111:79-91.
30. Hutcheson IR, Knowlden JM, Hiscox SE, Barrow D, Gee JM, Robertson JF, Ellis IO, Nicholson RI. Heregulin β1 drives gefitinib-resistant growth and invasion in tamoxifen-resistant MCF-7 breast cancer cells. Breast Cancer Res 2007, 9:R50. 10.1186/bcr1754, 2206726, 17686159.
31. Prigent SA, Gullick WJ. Identification of c-erbB-3 binding sites for phosphatidylinositol 3'-kinase and SHC using an EGF receptor/c-erbB-3 chimera. EMBO J 1994, 13:2831-2841. 395164, 8026468.
32. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 2009, 9:463-475. 10.1038/nrc2656, 19536107.
33. Hamburger AW. The role of ErbB3 and its binding partners in breast cancer progression and resistance to hormone and tyrosine kinase directed therapies. J Mammary Gland Biol Neoplasia 2008, 13:225-233. 10.1007/s10911-008-9077-5, 18425425.
34. Lemoine NR, Barnes DM, Hollywood DP, Hughes CM, Smith P, Dublin E, Prigent SA, Gullick WJ, Hurst HC. Expression of the ERBB3 gene product in breast cancer. Br J Cancer 1992, 66:1116-1121. 10.1038/bjc.1992.420, 1978009, 1333787.
35. Naidu R, Yadav M, Nair S, Kutty MK. Expression of c-erbB3 protein in primary breast carcinomas. Br J Cancer 1998, 78:1385-1390. 10.1038/bjc.1998.689, 2063171, 9823984.
36. Travis A, Pinder SE, Robertson JF, Bell JA, Wencyk P, Gullick WJ, Nicholson RI, Poller DN, Blamey RW, Elston CW, Ellis IO. C-erbB3 in human breast carcinoma: expression and relation to prognosis and established prognostic indicators. Cancer 1996, 74:229-233.
37. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, Klapper L, Lavi S, Seger R, Ratzkin BJ, Sela M, Yarden Y. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J 1996, 15:2452-2467. 450177, 8665853.
38. Wiseman SM, Makretsov N, Nielsen TO, Gilks B, Yorida E, Cheang M, Turbin D, Gelmon K, Huntsman DG. Coexpression of the type 1 growth factor receptor family members HER-1, HER-2, and HER-3 has a synergistic negative prognostic effect on breast carcinoma survival. Cancer 2005, 103:1770-1777. 10.1002/cncr.20970, 15770691.
39. Desbois-Mouthon C, Baron A, Blivet-Van Eggelpoël MJ, Fartoux L, Venot C, Bladt F, Housset C, Rosmorduc O. Insulin-like growth factor-1 receptor inhibition induces a resistance mechanism via the epidermal growth factor receptor/HER3/AKT signaling pathway: rational basis for cotargeting insulin-like growth factor-1 receptor and epidermal growth factor receptor in hepatocellular carcinoma. Clin Cancer Res 2009, 15:5445-5456. 10.1158/1078-0432.CCR-08-2980, 19706799.
40. Jones HE, Gee JMW, Barrow D, Tonge D, Holloway B, Nicholson RI. Inhibition of insulin receptor isoform-A signalling restores sensitivity to gefitinib in previously de novo resistant colon cancer cells. Br J Cancer 2006, 95:172-180. 10.1038/sj.bjc.6603237, 2360620, 16819546, 16819546.
41. Knowlden JM, Gee JM, Seery LT, Farrow L, Gullick WJ, Ellis IO, Blamey RW, Robertson JF, Nicholson R. c-erbB3 and c-erbB4 expression is a feature of the endocrine responsive phenotype in clinical breast cancer. Oncogene 1998, 17:1949-1957. 10.1038/sj.onc.1202107, 9788438.
42. Byron SA, Horwitz KB, Richer JK, Lange CA, Zhang X, Yee D. Insulin receptor substrates mediate distinct biological responses to insulin-like growth factor receptor activation in breast cancer cells. Br J Cancer 2006, 95:1220-1228. 10.1038/sj.bjc.6603354, 2360584, 17043687.
43. Mukohara T, Shimada H, Ogasawara N, Wanikawa R, Shimomura M, Nakatsura T, Ishii G, Park JO, Jänne PA, Saijo N, Minami H. Sensitivity of breast cancer cell lines to the novel insulin-like growth factor-1 receptor (IGF-IR) inhibitor NVP-AEW541 is dependent on the level of IRS-1 expression. Cancer Lett 2009, 282:14-24. 10.1016/j.canlet.2009.02.056, 19345478.
44. Jackson JG, White MF, Yee D. Insulin receptor substrate-1 is the predominant signaling molecule activated by insulin-like growth factor-I, insulin, and interleukin-4 in estrogen receptor-positive human breast cancer cells. J Biol Chem 1998, 273:9994-10003. 10.1074/jbc.273.16.9994, 9545345.
45. Alimandi M, Romano A, Curia MC, Muraro R, Fedi P, Aaronson SA, Di Fiore PP, Kraus MH. Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene 1995, 10:1813-1821.
46. Chakraborty AK, Liang K, DiGiovanna MP. Co-targeting insulin-like growth factor I receptor and HER2: dramatic effects of HER2 inhibitors on nonoverexpressing breast cancer. Cancer Res 2008, 68:1538-1545. 10.1158/0008-5472.CAN-07-5935, 18316619.
47. Haluska P, Carboni JM, Ten Eyck C, Attar RM, Hou X, Yu C, Sagar M, Wong TW, Gottardis MM, Erlichman CM. HER receptor signaling confers resistance to the insulin-like growth factor-I receptor inhibitor, BMS-536924. Mol Cancer Ther 2008, 7:2589-2598. 10.1158/1535-7163.MCT-08-0493, 2614316, 18765823.
48. Gijsen M, King P, Perera T, Parker PJ, Harris AL, Larijani B, Kong A. HER2 phosphorylation is maintained by a PKB negative feedback loop in response to anti-HER2 herceptin in breast cancer. PLoS Biol 2010, 8:e1000563. 10.1371/journal.pbio.1000563, 3006345, 21203579.
49. Dunn M, Sinha P, Campbell R, Blackburn E, Levinson N, Rampaul R, Bates T, Humphreys S, Gullick WJ. Co-expression of neuregulins 1, 2, 3 and 4 in human breast cancer. J Pathol 2004, 203:672-680. 10.1002/path.1561, 15141382.
50. Baserga R. The insulin receptor substrate-1: a biomarker for cancer?. Exp Cell Res 2009, 315:727-732. 10.1016/j.yexcr.2008.09.017, 18851963.
51. Lisztwan J, Pornon A, Chen B, Chen S, Evans DB. The aromatase inhibitor letrozole and inhibitors of insulin-like growth factor I receptor synergistically induce apoptosis in in vitro models of estrogen-dependent breast cancer. Breast Cancer Res 2008, 10:R56. 10.1186/bcr2113, 2575527, 18611244.
52. Ye JJ, Liang SJ, Guo N, Li SL, Wu AM, Giannini S, Sachdev D, Yee D, Brünner N, Ikle D, Fujita-Yamaguchi Y. Combined effects of tamoxifen and a chimeric humanized single chain antibody against the type I IGF receptor on breast tumor growth in vivo. Horm Metab Res 2003, 35:836-842.