Insulin-like growth factor binding protein-3 (IGFBP-3) plays a role in the anti-tumorigenic effects of 5-Aza-2'-deoxycytidine (AZA) in breast cancer cells

Experimental Cell Research

Volumn 319, Issue 14, 2013, Pages 2282-2295

  Zeng, Li ^a   Jarrett, Caroline ^a   Brown, Keith ^b   Gillespie, Kathleen M ^a   Holly, Jeff M P ^a   Perks, Claire M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b SCHOOL OF MEDICAL SCIENCES   (United Kingdom)

Author keywords

AZA; Breast cancer; Cell survival; IGFBP 3

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ESTROGEN RECEPTOR ALPHA; PROTEIN P53; SMALL INTERFERING RNA; SOMATOMEDIN BINDING PROTEIN 3;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CELL; BREAST EPITHELIUM; CANCER CELL; CELL COUNT; CELL GROWTH; CELL SURVIVAL; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DRUG EFFECT; EPITHELIUM CELL; GROWTH INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING;

EID: 84880709210     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.06.011     Document Type: Article

References (49)

1. Jemal A., Siegel R., Xu J., Ward E. Cancer Statistics, 2010. CA Cancer J. Clin. 2010, 61(2):133-134.
2. Shao W., Brown M. Advances in estrogen receptor biology: prospects for improvements in targeted breast cancer therapy. Breast Cancer Res. 2004, 6:39-52.
3. Yager J.D., Davidson N.E. Estrogen carcinogenesis in breast cancer. N. Engl. J. Med. 2006, 354:270-282.
4. Jones P.A., Baylin S.B. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 2002, 3:415-428.
5. Sharma D., Blum J., Yang X., Beaulieu N., Macleod A.R., Davidson N.E. Release of methyl CpG binding proteins and histone deacetylase 1 from the Estrogen receptor alpha (ER) promoter upon reactivation in ER-negative human breast cancer cells. Mol. Endocrinol. (Baltimore, M.) 2005, 19:1740-1751.
6. Wolf I., Bose S., Desmond J.C., Lin B.T., Williamson E.A., Karlan B.Y., Koeffler H.P. Unmasking of epigenetically silenced genes reveals DNA promoter methylation and reduced expression of PTCH in breast cancer. Breast Cancer Res. Treat. 2007, 105:139-155.
7. Yan L., Yang X., Davidson N.E. Role of DNA methylation and histone acetylation in steroid receptor expression in breast cancer. J. Mammary Gland Biol. Neoplasia 2001, 6:183-192.
8. Ottaviano Y.L., Issa J.P., Parl F.F., Smith H.S., Baylin S.B., Davidson N.E. Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res. 1994, 54:2552-2555.
9. Wei M., Xu J., Dignam J., Nanda R., Sveen L., Fackenthal J., Grushko T.A., Olopade O.I. Estrogen receptor alpha, BRCA1, and FANCF promoter methylation occur in distinct subsets of sporadic breast cancers. Breast Cancer Res. Treat. 2008, 111:113-120.
10. Ferguson A.T., Vertino P.M., Spitzner J.R., Baylin S.B., Muller M.T., Davidson N.E. Role of estrogen receptor gene demethylation and DNA methyltransferase. DNA adduct formation in 5-aza-2'deoxycytidine-induced cytotoxicity in human breast cancer cells. J. Biol. Chem. 1997, 272:32260-32266.
11. Kuo H.K., Griffith J.D., Kreuzer K.N. 5-Azacytidine induced methyltransferase-DNA adducts block DNA replication in vivo. Cancer Res. 2007, 67:8248-8254.
12. Jenkins P.J., Bustin S.A. Evidence for a link between IGF-I and cancer. Eur. J. Endocrinol. 2004, 151(Suppl 1):S17-22.
13. Perks C.M., Holly J.M. The insulin-like growth factor (IGF) family and breast cancer. Breast Dis. 2003, 18:45-60.
14. Ibanez de Caceres I., Dulaimi E., Hoffman A.M., Al-Saleem T., Uzzo R.G., Cairns P. Identification of novel target genes by an epigenetic reactivation screen of renal cancer. Cancer Res. 2006, 66:5021-5028.
15. Wiley A., Katsaros D., Chen H., Rigault de la Longrais I.A., Beeghly A., Puopolo M., Singal R., Zhang Y., Amoako A., Zelterman D., Yu H. Aberrant promoter methylation of multiple genes in malignant ovarian tumors and in ovarian tumors with low malignant potential. Cancer 2006, 107:299-308.
16. Perks C.M., Holly J.M. IGF binding proteins (IGFBPs) and regulation of breast cancer biology. J. Mammary Gland Biol. Neoplasia 2008, 13:455-469.
17. Renehan A.G., Harvie M., Howell A. Insulin-like growth factor (IGF)-I, IGF binding protein-3, and breast cancer risk: eight years on. Endocr. Relat. Cancer 2006, 13:273-278.
18. Clemmons D.R., Camacho-Hubner C., Coronado E., Osborne C.K. Insulin-like growth factor binding protein secretion by breast carcinoma cell lines: correlation with estrogen receptor status. Endocrinology 1990, 127:2679-2686.
19. Buckbinder L., Talbott R., Velasco-Miguel S., Takenaka I., Faha B., Seizinger B.R., Kley N. Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature 1995, 377:646-649.
20. Colston K.W., Perks C.M., Xie S.P., Holly J.M. Growth inhibition of both MCF-7 and Hs578T human breast cancer cell lines by vitamin D analogues is associated with increased expression of insulin-like growth factor binding protein-3. J. Mol. Endocrinol. 1998, 20:157-162.
21. McCaig C., Fowler C.A., Laurence N.J., Lai T., Savage P.B., Holly J.M., Perks C.M. Differential interactions between IGFBP-3 and transforming growth factor-beta (TGF-beta) in normal vs cancerous breast epithelial cells. Br. J. Cancer 2002, 86:1963-1969.
22. Hollowood A.D., Lai T., Perks C.M., Newcomb P.V., Alderson D., Holly J.M. IGFBP-3 prolongs the p53 response and enhances apoptosis following UV irradiation. Int. J. Cancer 2000, 88:336-341.
23. Campbell M.J., Woodside J.V., Secker-Walker J., Titcomb A., Leathem A.J. IGF status is altered by tamoxifen in patients with breast cancer. Mol. Pathol. 2001, 54:307-310.
24. Zeng L., Biernacka K.M., Holly J.M., Jarrett C., Morrison A.A., Morgan A., Winters Z.E., Foulstone E.J., Shield J.P., Perks C.M. Hyperglycaemia confers resistance to chemotherapy on breast cancer cells: the role of fatty acid synthase. Endocr. Relat. Cancer 2010, 17:539-551.
25. McIntosh J., Dennison G., Holly J.M., Jarrett C., Frankow A., Foulstone E.J., Winters Z.E., Perks C.M. 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.
26. Davies S.C., Holly J.M., Coulson V.J., Cotterill A.M., Abdulla A.F., Whittaker P.G., Chard T., Wass J.A. The presence of cation-dependent proteases for insulin-like growth factor binding proteins does not alter the size distribution of insulin-like growth factors in pregnancy. Clin. Endocrinol. (Oxford) 1991, 34:501-506.
27. Yateman M.E., Claffey D.C., Cwyfan Hughes S.C., Frost V.J., Wass J.A., Holly J.M. Cytokines modulate the sensitivity of human fibroblasts to stimulation with insulin-like growth factor-I (IGF-I) by altering endogenous IGF-binding protein production. J. Endocrinol. 1993, 137:151-159.
28. Burrows C., Holly J.M., Laurence N.J., Vernon E.G., Carter J.V., Clark M.A., McIntosh J., McCaig C., Winters Z.E., Perks C.M. Insulin-like growth factor binding protein 3 has opposing actions on malignant and nonmalignant breast epithelial cells that are each reversible and dependent upon cholesterol-stabilized integrin receptor complexes. Endocrinology 2006, 147:3484-3500.
29. Thomas F., Holly J.M., Persad R., Bahl A., Perks C.M. Fibronectin confers survival against chemotherapeutic agents but not against radiotherapy in DU145 prostate cancer cells: involvement of the insulin like growth factor-1 receptor. Prostate 2010, 70:856-865.
30. Xiong Z., Laird P.W. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res. 1997, 25:2532-2534.
31. Pryzbylkowski P., Obajimi O., Keen J.C. Trichostatin A and 5 Aza-2' deoxycytidine decrease estrogen receptor mRNA stability in ER positive MCF7 cells through modulation of HuR. Breast Cancer Res. Treat. 2008, 111:15-25.
32. Yang X., Phillips D.L., Ferguson A.T., Nelson W.G., Herman J.G., Davidson N.E. Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells. Cancer Res. 2001, 61:7025-7029.
33. Sadikovic B., Al-Romaih K., Squire J.A., Zielenska M. Cause and consequences of genetic and epigenetic alterations in human cancer. Curr. Genomics 2008, 9:394-408.
34. Kalebic T. Epigenetic changes: potential therapeutic targets. Ann. N. Y. Acad. Sci. 2003, 983:278-285.
35. Mai A., Massa S., Rotili D., Cerbara I., Valente S., Pezzi R., Simeoni S., Ragno R. Histone deacetylation in epigenetics: an attractive target for anticancer therapy. Med. Res. Rev. 2005, 25:261-309.
36. Yoo C.B., Jones P.A. Epigenetic therapy of cancer: past, present and future. Nat. Rev. Drug Discovery 2006, 5:37-50.
37. Perks C., Holly J. Actions of IGFBP on epithelial cancer cells: potential for new therapeutic targets. Horm. Metab. Res. 2003, 35:828-835.
38. Gill Z.P., Perks C.M., Newcomb P.V., Holly J.M. Insulin-like growth factor-binding protein (IGFBP-3) predisposes breast cancer cells to programmed cell death in a non-IGF-dependent manner. J. Biol. Chem. 1997, 272:25602-25607.
39. Fowler C.A., Perks C.M., Newcomb P.V., Savage P.B., Farndon J.R., Holly J.M. Insulin-like growth factor binding protein-3 (IGFBP-3) potentiates paclitaxel-induced apoptosis in human breast cancer cells. Int. J. Cancer 2000, 88:448-453.
40. Christman J.K. 5-Azacytidine and 5-aza-2'-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 2002, 21:5483-5495.
41. Mirza S., Sharma G., Pandya P., Ralhan R. Demethylating agent 5-aza-2-deoxycytidine enhances susceptibility of breast cancer cells to anticancer agents. Mol. Cell. Biochem. 2010.
42. Gomyo Y., Sasaki J., Branch C., Roth J.A., Mukhopadhyay T. 5-aza-2'-deoxycytidine upregulates caspase-9 expression cooperating with p53-induced apoptosis in human lung cancer cells. Oncogene 2004, 23:6779-6787.
43. Hurtubise A., Momparler R.L. Effect of histone deacetylase inhibitor LAQ824 on antineoplastic action of 5-Aza-2'-deoxycytidine (decitabine) on human breast carcinoma cells. Cancer Chemother. Pharmacol. 2006, 58:618-625.
44. Suh Y.A., Kim J.H., Sung M.A., Boo H.J., Yun H.J., Lee S.H., Lee H.J., Min H.Y., Suh Y.G., Kim K.W., Lee H.Y. A novel antitumor activity of deguelin targeting the insulin-like growth factor (IGF) receptor pathway via up-regulation of IGF-binding protein-3 expression in breast cancer. Cancer Lett. 2013, 332:102-109.
45. Ricort J.M., Binoux M. Insulin-like growth factor (IGF) binding protein-3 inhibits type 1 IGF receptor activation independently of its IGF binding affinity. Endocrinology 2001, 142:108-113.
46. Anttila M.A., Kellokoski J.K., Moisio K.I., Mitchell P.J., Saarikoski S., Syrjanen K., Kosma V.M. Expression of transcription factor AP-2alpha predicts survival in epithelial ovarian cancer. Br. J. Cancer 2000, 82:1974-1983.
47. Orso F., Penna E., Cimino D., Astanina E., Maione F., Valdembri D., Giraudo E., Serini G., Sismondi P., De Bortoli M., Taverna D. AP-2alpha and AP-2gamma regulate tumor progression via specific genetic programs. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 2008, 22:2702-2714.
48. Douglas D.B., Akiyama Y., Carraway H., Belinsky S.A., Esteller M., Gabrielson E., Weitzman S., Williams T., Herman J.G., Baylin S.B. Hypermethylation of a small CpGuanine-rich region correlates with loss of activator protein-2alpha expression during progression of breast cancer. Cancer Res. 2004, 64:1611-1620.
49. Wajapeyee N., Raut C.G., Somasundaram K. Activator protein 2alpha status determines the chemosensitivity of cancer cells: implications in cancer chemotherapy. Cancer Res. 2005, 65:8628-8634.