Docosahexaenoic acid induces proteasome-dependent degradation of estrogen receptor α and inhibits the downstream signaling target in MCF-7 breast cancer cells

Journal of Nutritional Biochemistry

Volumn 21, Issue 6, 2010, Pages 512-517

  Lu, I Fen ^a   Hasio, Ann Che ^a   Hu, Meng Chun ^a   Yang, Feng Ming ^a   Su, Hui Min ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Arachidonic acid; Breast cancer; Cyclin D1; Docosahexaenoic acid; Estradiol; Estrogen receptor ; MAPK; Proteasome activity

Indexed keywords

ARACHIDONIC ACID; CYCLIN D1; DOCOSAHEXAENOIC ACID; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEASOME; ALBUMINOID;

ARTICLE; BREAST CANCER; CELL STIMULATION; CELL STRAIN MCF 7; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INHIBITION KINETICS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; BIOSYNTHESIS; BREAST TUMOR; CELL NUCLEUS; CELL SURVIVAL; DOSE RESPONSE; FEMALE; METABOLISM; TUMOR CELL LINE;

ALBUMINS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CELL SURVIVAL; CYCLIN D1; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 77952884757     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2009.02.009     Document Type: Article

References (51)

1. Parkin D.M., Pisani P., Ferlay J. Estimates of the worldwide incidence of 25 major cancers in 1990. Int J Cancer 1999, 806:827-841.
2. Glass A.G., Lacey J.V., Carreon J.D., Hoover R.N. Breast cancer incidence, 1980-2006: combined roles of menopausal hormone therapy, screening mammography, and estrogen receptor status. J Natl Cancer Inst 2007, 9915:1152-1161.
3. Walter P., Green S., Greene G., Krust A., Bornert J.M., Jeltsch J.M., et al. Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci USA 1985, 8223:7889-7893.
4. Mosselman S., Polman J., Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 1996, 3921:49-53.
5. Evans R.M. The steroid and thyroid hormone receptor superfamily. Science 1988, 2404854:889-895.
6. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr Rev 1999, 203:358-417.
7. Oesterreich S., Zhang P., Guler R.L., Sun X., Curran E.M., Welshons W.V., et al. Re-expression of estrogen receptor alpha in estrogen receptor alpha-negative MCF-7 cells restores both estrogen and insulin-like growth factor-mediated signaling and growth. Cancer Res 2001, 6115:5771-5777.
8. Roger P., Sahla M.E., Makela S., Gustafsson J.A., Baldet P., Rochefort H. Decreased expression of estrogen receptor beta protein in proliferative preinvasive mammary tumors. Cancer Res 2001, 616:2537-2541.
9. Paruthiyil S., Parmar H., Kerekatte V., Cunha G.R., Firestone G.L., Leitman D.C. Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Res 2004, 641:423-428.
10. Strom A., Hartman J., Foster J.S., Kietz S., Wimalasena J., Gustafsson J.A. Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc Natl Acad Sci USA 2004, 1016:1566-1571.
11. King W.J., Greene G.L. Monoclonal antibodies localize oestrogen receptor in the nuclei of target cells. Nature 1984, 3075953:745-747.
12. Welshons W.V., Lieberman M.E., Gorski J. Nuclear localization of unoccupied oestrogen receptors. Nature 1984, 3075953:747-749.
13. King W.J., DeSombre E.R., Jensen E.V., Greene G.L. Comparison of immunocytochemical and steroid-binding assays for estrogen receptor in human breast tumors. Cancer Res 1985, 451:293-304.
14. Razandi M., Oh P., Pedram A., Schnitzer J., Levin E.R. ERs associate with and regulate the production of caveolin: implications for signaling and cellular actions. Mol Endocrinol 2002, 161:100-115.
15. Kahlert S., Nuedling S., van Eickels M., Vetter H., Meyer R., Grohe C. Estrogen receptor alpha rapidly activates the IGF-1 receptor pathway. J Biol Chem 2000, 27524:18447-18453.
16. Marquez D.C., Pietras R.J. Membrane-associated binding sites for estrogen contribute to growth regulation of human breast cancer cells. Oncogene 2001, 2039:5420-5430.
17. Pedram A., Razandi M., Levin E.R. Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 2006, 209:1996-2009.
18. Fan P., Wang J., Santen R.J., Yue W. Long-term treatment with tamoxifen facilitates translocation of estrogen receptor alpha out of the nucleus and enhances its interaction with EGFR in MCF-7 breast cancer cells. Cancer Res 2007, 673:1352-1360.
19. Stillwell W., Wassall S.R. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Physics Lipids 2003, 1261:1-27.
20. Schmitz G., Ecker J. The opposing effects of n-3 and n-6 fatty acids. Prog Lipid Res 2008, 472:147-155.
21. Bartsch H., Nair J., Owen R.W. Dietary polyunsaturated fatty acids and cancers of the breast and colorectum: emerging evidence for their role as risk modifiers. Carcinogenesis 1999, 2012:2209-2218.
22. Larsson S.C., Kumlin M., Ingelman-Sundberg M., Wolk A. Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 2004, 796:935-945.
23. Suzuki Y.J., Mizuno M., Packer L. Signal transduction for nuclear factor-kappa B activation. Proposed location of antioxidant-inhibitable step. J Immunol 1994, 15311:5008-5015.
24. Wang P.Y., Chen J.J., Su H.M. Docosahexaenoic acid supplementation of primary rat hippocampal neurons attenuates the neurotoxicity induced by aggregated amyloid beta protein42 and upregulates cytoskeletal protein expression. J Nutr Biochem 2009, [accepted].
25. Place R.F., Noonan E.J., Giardina C. HDAC inhibition prevents NF-kappa B activation by suppressing proteasome activity: down-regulation of proteasome subunit expression stabilizes I kappa B alpha. Biochem Pharmacol 2005, 703:394-406.
26. Butt A.J., McNeil C.M., Musgrove E.A., Sutherland R.L. Downstream targets of growth factor and oestrogen signalling and endocrine resistance: the potential roles of c-Myc, cyclin D1 and cyclin E. Endocr Relat Cancer 2005, 12(Suppl 1):S47-S59.
27. Dauvois S., Danielian P.S., White R., Parker M.G. Antiestrogen ICI 164,384 reduces cellular estrogen receptor content by increasing its turnover. Proc Natl Acad Sci USA 1992, 899:4037-4041.
28. Nawaz Z., Lonard D.M., Dennis A.P., Smith C.L., O'Malley B.W. Proteasome-dependent degradation of the human estrogen receptor. Proc Natl Acad Sci USA 1999, 965:1858-1862.
29. Alarid E.T., Bakopoulos N., Solodin N. Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol Endocrinol 1999, 139:1522-1534.
30. Calviello G., Resci F., Serini S., Piccioni E., Toesca A., Boninsegna A., et al. Docosahexaenoic acid induces proteasome-dependent degradation of beta-catenin, down-regulation of survivin and apoptosis in human colorectal cancer cells not expressing COX-2. Carcinogenesis 2007, 286:1202-1209.
31. Botolin D., Wang Y., Christian B., Jump D.B. Docosahexaneoic acid (22:6,n-3) regulates rat hepatocyte SREBP-1 nuclear abundance by Erk- and 26S proteasome-dependent pathways. J Lipid Res 2006, 471:181-192.
32. Qin C., Burghardt R., Smith R., Wormke M., Stewart J., Safe S. Peroxisome proliferator-activated receptor gamma agonists induce proteasome-dependent degradation of cyclin D1 and estrogen receptor alpha in MCF-7 breast cancer cells. Cancer Res 2003, 635:958-964.
33. Itoh T., Yamamoto K. Peroxisome proliferator activated receptor gamma and oxidized docosahexaenoic acids as new class of ligand. Naunyn Schmiedebergs Arch Pharmacol 2008, 3774-6:541-547.
34. Vigouroux S., Farout L., Clavel S., Briand Y., Briand M. Increased muscle proteasome activities in rats fed a polyunsaturated fatty acid supplemented diet. Int J Biochem Cell Biol 2003, 355:749-755.
35. Rivett A.J. Proteasomes: multicatalytic proteinase complexes. Biochem Journal. 1993, 291(Pt 1):1-10.
36. Goldberg A.L. Functions of the proteasome: the lysis at the end of the tunnel. Science 1995, 2685210:522-523.
37. Tamoxifen for early breast cancer: an overview of the randomised trials. Early Breast Cancer Trialists' Collaborative Group. Lancet 1998, 3519114:1451-1467.
38. Clarke R., Leonessa F., Welch J.N., Skaar T.C. Cellular and molecular pharmacology of antiestrogen action and resistance. Pharmacol Rev 2001, 531:25-71.
39. Santen R.J., Song R.X., Zhang Z., Yue W., Kumar R. Adaptive hypersensitivity to estrogen: mechanism for sequential responses to hormonal therapy in breast cancer. Clin Cancer Res 2004, 101(Pt 2):337S-345S.
40. Santen R.J., Song R.X., Zhang Z., Kumar R., Jeng M.H., Masamura A., et al. Long-term estradiol deprivation in breast cancer cells up-regulates growth factor signaling and enhances estrogen sensitivity. Endocr Relat Cancer 2005, 12(Suppl 1):S61-S73.
41. Wilcken N.R., Prall O.W., Musgrove E.A., Sutherland R.L. Inducible overexpression of cyclin D1 in breast cancer cells reverses the growth-inhibitory effects of antiestrogens. Clin Cancer Res 1997, 36:849-854.
42. Razandi M., Pedram A., Park S.T., Levin E.R. Proximal events in signaling by plasma membrane estrogen receptors. J Biol Chem 2003, 2784:2701-2712.
43. Zivadinovic D., Watson C.S. Membrane estrogen receptor-alpha levels predict estrogen-induced ERK1/2 activation in MCF-7 cells. Breast Cancer Res 2005, 71:R130-R144.
44. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001, 222:153-183.
45. Calviello G., Di Nicuolo F., Gragnoli S., Piccioni E., Serini S., Maggiano N., et al. n-3 PUFAs reduce VEGF expression in human colon cancer cells modulating the COX-2/PGE2 induced ERK-1 and -2 and HIF-1alpha induction pathway. Carcinogenesis 2004, 2512:2303-2310.
46. Khan N.A., Nishimura K., Aires V., Yamashita T., Oaxaca-Castillo D., Kashiwagi K., et al. Docosahexaenoic acid inhibits cancer cell growth via p27Kip1, CDK2, ERK1/ERK2, and retinoblastoma phosphorylation. J Lipid Res 2006, 4710:2306-2313.
47. Sun H., Berquin I.M., Owens R.T., O'Flaherty J.T., Edwards I.J. Peroxisome proliferator-activated receptor gamma-mediated up-regulation of syndecan-1 by n-3 fatty acids promotes apoptosis of human breast cancer cells. Cancer Res 2008, 688:2912-2919.
48. Schley P.D., Jijon H.B., Robinson L.E., Field C.J. Mechanisms of omega-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells. Breast Cancer Res Treat 2005, 922:187-195.
49. Schley P.D., Brindley D.N., Field C.J. (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells. J Nutr 2007, 1373:548-553.
50. Wu M., Harvey K.A., Ruzmetov N., Welch Z.R., Sech L., Jackson K., et al. Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway. Int J Cancer 2005, 1173:340-348.
51. Bernard-Gallon D.J., Vissac-Sabatier C., Antoine-Vincent D., Rio P.G., Maurizis J.C., Fustier P., et al. Differential effects of n-3 and n-6 polyunsaturated fatty acids on BRCA1 and BRCA2 gene expression in breast cell lines. Br J Nutr 2002, 874:281-289.