Indole-3-Carbinol disrupts Estrogen Receptor-alpha dependent expression of Insulin-like Growth Factor-1 Receptor and Insulin Receptor Substrate-1 and proliferation of human breast cancer cells

Molecular and Cellular Endocrinology

Volumn 363, Issue 1-2, 2012, Pages 74-84

  Marconett, Crystal N ^a   Singhal, Ankur K ^a   Sundar, Shyam N ^a   Firestone, Gary L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Estrogen receptor alpha; Hormone sensitive breast cancer; Indole 3 carbinol; Insulin Receptor Substrate 1; Insulin like Growth Factor 1 Receptor

Indexed keywords

3 INDOLEMETHANOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; INSULIN RECEPTOR SUBSTRATE 1; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR SP1;

ARTICLE; BREAST CANCER; CANCER INHIBITION; CELL CYCLE ARREST; CELL STRAIN MCF 7; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IGF1R GENE; IRS1 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN SYNTHESIS INHIBITION; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BASE SEQUENCE; BREAST NEOPLASMS; CELL PROLIFERATION; CONSERVED SEQUENCE; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INDOLES; INSULIN RECEPTOR SUBSTRATE PROTEINS; MCF-7 CELLS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION;

EID: 84866920429     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.07.008     Document Type: Article

References (53)

1. Aggarwal B.B., Ichikawa H. Molecular targets and anti-cancer potential of indole-3-carbinol and its derivatives. Cell Cycle 2005, 4:1201-1205.
2. Auborn K.J., Fan S., Rosen E.M., Goodwin L., Chandraskaren A., Williams D.E., Chen D., Carter T.H. Indole-3-carbinol is a negative regulator of estrogen. J. Nutr. 2003, 133:2470S-2475S.
3. Carboni J.M., Lee A.V., Hadsell D.L., Rowley B.R., Lee F.Y., Bol D.K., Camuso A.E., Gottardis M., Greer A.F., Ho C.P., Hurlburt W., Li A., Saulnier M., Velaparthi U., Wang C., Wen M.L., Westhouse R.A., Wittman M., Zimmermann K., Rupnow B.A., Wong T.W. Tumor development by transgenic expression of a constitutively active insulin-like growth factor I receptor. Cancer Res. 2005, 65:3781-3787.
4. Chitnis M.M., Yuen J.S., Protheroe A.S., Pollak M., Macaulay V.M. The type 1 insulin-like growth factor receptor pathway. Clin. Cancer Res. 2008, 14:6364-6370.
5. Clarke R.B., Howell A., Anderson E. Type I insulin-like growth factor receptor gene expression in normal human breast tissue treated with oestrogen and progesterone. Br. J. Cancer. 1997, 75:251-257.
6. Cover C.M., Hsieh S.J., Cram E.J., Hong C., Riby J.E., Bjeldanes L.F., Firestone G.L. Indole-3-carbinol and tamoxifen cooperate to arrest the cell cycle of MCF-7 human breast cancer cells. Cancer Res. 1999, 59:1244-1251.
7. Cram E.J., Liu B.D., Bjeldanes L.F., Firestone G.L. Indole-3-carbinol inhibits CDK6 expression in human MCF-7 breast cancer cells by disrupting Sp1 transcription factor interactions with a composite element in the CDK6 gene promoter. J. Biol. Chem. 2001, 276:22332-22340.
8. Cui X., Kim H.J., Kuiatse I., Kim H., Brown P.H., Lee A.V. Epidermal growth factor induces insulin receptor substrate-2 in breast cancer cells via c-Jun NH2-terminal kinase/activator protein-1 signaling to regulate cell migration. Cancer Res. 2006, 66:5304-5313.
9. Da Silva Xavier G., Qian Q., Cullen P.J., Rutter G.A. Distinct roles for insulin and insulin-like growth factor-1 receptors in pancreatic beta-cell glucose sensing revealed by RNA silencing. Biochem. J. 2004, 377:149-158.
10. Fagan D.H., Yee D. Crosstalk between IGF1R and estrogen receptor signaling in breast cancer. J. Mammary Gland Biol. Neoplasia. 2008, 13:423-429.
11. Firestone G.L., Sundar S.N. Minireview: modulation of hormone receptor signaling by dietary anticancer indoles. Mol. Endocrinol. 2009, 23:1940-1947.
12. Fry C.J., Farnham P.J. Context-dependent activation of transcription. J. Biol. Chem. 1999, 274:29583-29586.
13. Garcia-Echeverria C. Medicinal chemistry approaches to target the kinase activity of IGF-1R. IDrugs 2006, 9:415-419.
14. Goya M., Miyamoto S., Nagai K., Ohki Y., Nakamura K., Shitara K., Maeda H., Sangai T., Kodama K., Endoh Y., Ishii G., Hasebe T., Yonou H., Hatano T., Ogawa Y., Ochiai A. Growth inhibition of human prostate cancer cells in human adult bone implanted into nonobese diabetic/severe combined immunodeficient mice by a ligand-specific antibody to human insulin-like growth factors. Cancer Res. 2004, 64:6252-6258.
15. Happerfield L.C., Miles D.W., Barnes D.M., Thomsen L.L., 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.
16. Jones R.A., Campbell C.I., Gunther E.J., Chodosh L.A., Petrik J.J., Khokha R., Moorehead R.A. Transgenic overexpression of IGF-IR disrupts mammary ductal morphogenesis and induces tumor formation. Oncogene 2007, 26:1636-1644.
17. Jones R.A., Campbell C.I., Wood G.A., Petrik J.J., Moorehead R.A. Reversibility and recurrence of IGF-IR-induced mammary tumors. Oncogene 2009, 28:2152-2162.
18. Kang S.G., Brown A.L., Chung J.H. Oxygen tension regulates stability of insulin receptor substrate-1 (IRS-1) through caspase-mediated cleavage. J. Biol. Chem. 2006, 282(9):6090-6097.
19. Klinakis A., Szabolcs G., Chen G., Xuan S., Hibshoosh H., Efstratiadis A. IGF1R as a therapeutic target in a mouse model of basal-like breast cancer. Proc. Nat. Acad. Sci. 2009, 7:2359-2364.
20. Lee A.V., Schiff R., Cui X., Sachdev D., Yee D., Gilmore A.P., Streuli C.H., Oesterreich S., Hadsell D.L. New mechanisms of signal transduction inhibitor action: receptor tyrosine kinase down-regulation and blockade of signal transactivation. Clin. Cancer Res. 2003, 9:516S-523S.
21. Li S.L., Liang S.J., Guo N., Wu A.M., Fujita-Yamaguchi Y. Single-chain antibodies against human insulin-like growth factor I receptor: expression, purification, and effect on tumor growth. Cancer Immunol. Immunother. 2000, 49:243-252.
22. Liu W., Ye P., O'Kusky J.R., D'Ercole A.J. Type 1 insulin-like growth factor receptor signaling is essential for the development of the hippocampal formation and dentate gyrus. J. Neurosci. Res. 2009, 87:2821-2832.
23. Manson M.M., Farmer P.B., Gescher A., Steward W.P. Innovative agents in cancer prevention. Recent Results Cancer Res. 2005, 166:257-275.
24. Maor S., Mayer D., Yarden R.I., Lee A.V., Sarfstein R., Werner H., Papa M.Z. Estrogen receptor regulates insulin-like growth factor-I receptor gene expression in breast tumor cells: involvement of transcription factor Sp1. J. Endocrinol. 2006, 191:605-612.
25. Marconett C.N., Sundar S.N., Poindexter K.M., Stueve T.R., Bjeldanes L.F., Firestone G.L. Indole-3-carbinol triggers aryl hydrocarbon receptor-dependent estrogen receptor (ER)alpha protein degradation in breast cancer cells disrupting an ERalpha-GATA3 transcriptional cross-regulatory loop. Mol. Biol. Cell 2010, 21:1166-1177.
26. Marconett C.N., Sundar S.N., Tseng M., Tin A.S., Tran K.Q., Mahuron K.M., Bjeldanes L.F., Firestone G.L. Indole-3-carbinol downregulation of telomerase gene expression requires the inhibition of estrogen receptor-alpha and Sp1 transcription factor interactions within the hTERT promoter and mediates the G1 cell cycle arrest of human breast cancer cells. Carcinogenesis 2011, 32:1315-1323.
27. Marino M., Galluzzo P., Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr. Gen. 2006, 7:497-508.
28. Mauro L., Salerno M., Panno M.L., Bellizzi D., Sisci D., Miglietta A., Surmacz E., Ando S. Estradiol increases IRS-1 gene expression and insulin signaling in breast cancer cells. Biochem. Biophys. Res. Commun. 2001, 288:685-689.
29. Morelli C., Garofalo C., Sisci D., del Rincon S., Cascio S., Tu X., Vecchione A., Sauter E.R., Miller W.H., Surmacz E. Nuclear insulin receptor substrate 1 interacts with estrogen receptor alpha at ERE promoters. Oncogene 2004, 23:7517-7526.
30. Nagle J.A., Ma Z., Byrne M.A., White M.F., Shaw L.M. Involvement of insulin receptor substrate 2 in mammary tumor metastasis. Mol. Cell Biol. 2004, 24:9726-9735.
31. Osborne C.K., Schiff R. Mechanisms of endocrine resistance in breast cancer. Ann. Rev. Med. 2011, 62:233-247.
32. Parathath S.R., Mainwaring L.A., Fernandez-L A., Campbell D.O., Kenney A.M. Insulin receptor substrate 1 is an effector of sonic hedgehog mitogenic signaling in cerebellar neural precursors. Development 2008, 135:3291-3300.
33. Riedemann J., Macaulay V.M. IGF1R signaling and its inhibition. Endocr. Relat. Cancer 2006, 13(Suppl 1):S33-S43.
34. Ruiz-Alcaraz A.J., Liu H.K., Cuthbertson D.J., Mcmanus E.J., Akhtar S., Lipina C., Morris A.D., Petrie J.R., Hundal H.S., Sutherland C. A novel regulation of IRS1 (insulin receptor substrate-1) expression following short term insulin administration. Biochem. J. 2005, 392:345-352.
35. Ryan P.D., Goss P.E. The emerging role of the insulin-like growth factor pathway as a therapeutic target in cancer. Clin. Pharm. 2008, 13:16-24.
36. Sachdev D., Li S.L., Hartell J.S., Fujita-Yamaguchi Y., Miller J.S., Yee D. A chimeric humanized single-chain antibody against the type I insulin-like growth factor (IGF) receptor renders breast cancer cells refractory to the mitogenic effects of IGF-I. Cancer Res. 2003, 63:627-635.
37. Santen R., Cavalieri E., Rogan E., Russo J., Guttenplan J., Ingle J., Yue W. Estrogen mediation of breast tumor formation involves estrogen receptordependent, as well as independent, genotoxic effects. Ann. NY Acad. Sci. 2009, 1155:132-140.
38. Saville B., Wormke M., Wang F., Nguyen T., Enmark E., Kuiper G., Gustafsson J.A., Safe S. Ligand-, cell-, and estrogen receptor subtype (alpha/beta)-dependent activation at GC-rich (Sp1) promoter elements. J. Biol. Chem. 2000, 275:5379-5387.
39. Shekhar P.V., Chen M.L., Werdell J., Heppner G.H., Miller F.R., Christman J.K. Transcriptional activation of functional endogenous estrogen receptor gene expression in MCF10AT cells: a model for early breast cancer. Int. J. Oncol. 1998, 13:907-915.
40. Shibata H., Spencer T.E., Oñate S.A., Jenster G., Tsai S.Y., Tsai M.J., O'Malley B.W. Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action. Recent Prog. Horm. Res. 1997, 52:141-164.
41. Sisci D., Morelli C., Cascio S., Lanzino M., Garofalo C., Reiss K., Garcia M., Russo A., Ando S., Surmacz E. The estrogen receptor alpha: insulin receptor substrate 1 complex in breast cancer: structure-function relationships. Ann. Oncol. 2007, 18(Suppl. 6):vi81-vi85.
42. Stewart A.J., Johnson M.D., May F.E., Westley B.R. 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.
43. Strissel P.L., Ellmann S., Loprich E., Thiel F., Fasching P.A., Stiegler E., Hartmann A., Beckmann M.W., Strick R. Early aberrant insulin-like growth factor signaling in the progression to endometrial carcinoma is augmented by tamoxifen. Int. J. Cancer. 2008, 123:2871-2879.
44. Schultz-Norton J.R., Ziegler Y.S., Nardulli A.M. ERα-associated protein networks. Trends Endocrinol. Metab. 2011, 22:124-129.
45. Sundar S.N., Kerekatte V., Equinozio C.N., Doan V.B., Bjeldanes L.F., Firestone G.L. Indole-3-carbinol selectively uncouples expression and activity of estrogen receptor subtypes in human breast cancer cells. Mol. Endocrinol. 2006, 20:3070-3082.
46. Sundar S.N., Marconett C.N., Doan V.B., Willoughby J.A., Firestone G.L. Artemisinin selectively decreases functional levels of estrogen receptor-alpha and ablates estrogen-induced proliferation in human breast cancer cells. Carcinogenesis 2008, 29:252-2258.
47. Surmacz E., Bartucci M. Role of estrogen receptor alpha in modulating IGF-I receptor signaling and function in breast cancer. J. Exp. Clin. Cancer Res. 2004, 23:385-394.
48. Van den Berg C.L., Cox G.N., Stroh C.A., Hilsenbeck S.G., Weng C.N., McDermott M.J., Pratt D., Osborne C.K., Coronado-Heinsohn E.B., Yee D. Polyethylene glycol conjugated insulin-like growth factor binding protein-1 (IGFBP-1) inhibits growth of breast cancer in athymic mice. Eur. J. Cancer. 1997, 33:1108-1113.
49. Wang T.T., Milner M.J., Milner J.A., Kim Y.S. Estrogen receptor alpha as a target for indole-3-carbinol. J. Nutr. Biochem. 2006, 17:659-664.
50. Wang Y., Hailey J., Williams D., Lipari P., Malkowski M., Wang X., Xie L., Li G., Saha D., Ling W.L., Cannon-Carlson S., Greenberg R., Ramos R.A., Shields R., Presta L., Brams P., Bishop W.R., Pachter J.A. Inhibition of insulin-like growth factor-I receptor (IGF-IR) signaling and tumor cell growth by a fully human neutralizing anti-IGF-IR antibody. Mol. Cancer Ther. 2005, 4:1214-1221.
51. Werner H., Bruchim I. The insulin-like growth factor-I receptor as an oncogene. Arch. Physiol. Biochem. 2009, 115:58-71.
52. Wittman M., Carboni J., Attar R., Balasubramanian B., Balimane P., Brassil P., Beaulieu F., Chang C., Clarke W., Dell J., Eummer J., Frennesson D., Gottardis M., Greer A., Hansel S., Hurlburt W., Jacobson B., Krishnananthan S., Lee F.Y., Li A., Lin T.A., Liu P., Ouellet C., Sang X., Saulnier M.G., Stoffan K., Sun Y., Velaparthi U., Wong H., Yang Z., Zimmermann K., Zoeckler M., Vyas D. Discovery of a (1H-benzoimidazol-2-yl)-1H-pyridin-2-one (BMS-536924) inhibitor of insulin-like growth factor I receptor kinase with in vivo antitumor activity. J. Med. Chem. 2005, 48:5639-5643.
53. Zhou Q., Atadja P., Davidson N.E. Histone deacetylase inhibitor LBH589 reactivates silenced estrogen receptor alpha (ER) gene expression without loss of DNA hypermethylation. Cancer Biol. Ther. 2007, 6:64-69.