Blueberry phytochemicals inhibit growth and metastatic potential of MDA-MB-231 breast cancer cells through modulation of the phosphatidylinositol 3-kinase pathway

Cancer Research

Volumn 70, Issue 9, 2010, Pages 3594-3605

  Adams, Lynn S ^a   Phung, Sheryl ^a   Yee, Natalie ^a   Seeram, Navindra P ^b   Li, Liya ^b   Chen, Shiuan ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BLUEBERRY EXTRACT; CASPASE 3; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN KINASE C; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UROKINASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST TUMOR; CANCER CELL; CELL ASSAY; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REPORTER GENE; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR VOLUME; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; BEVERAGES; BLUEBERRY PLANT; BREAST NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; FLAVONOIDS; FRUIT; HUMANS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; MICE, NUDE; PHENOLS; PLANT EXTRACTS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASE-1; UROKINASE-TYPE PLASMINOGEN ACTIVATOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77951703324     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-3565     Document Type: Article

References (49)

1. Reis-Filho JS, Tutt AN. Triple negative tumours: a critical review. Histopathology 2008;52:108-118
2. Cleator S, Heller W, Coombes RC. Triple-negative breast cancer: therapeutic options. Lancet Oncol 2007;8:235-244 (Pubitemid 46291713)
3. van de Rijn M, Perou CM, Tibshirani R, et al. Expression of cytokeratins 17 and 5 identifies a group of breast carcinomas with poor clinical outcome. Am J Pathol 2002;161:1991-1996 (Pubitemid 35434844)
4. +) phenotype of BRCA1-related breast cancer. Cancer Res 2004;64:830-835
5. Tsuda H, Takarabe T, Hasegawa F, Fukutomi T, Hirohashi S. Large, central acellular zones indicating myoepithelial tumor differentiation in high-grade invasive ductal carcinomas as markers of predisposition to lung and brain metastases. Am J Surg Pathol 2000;24: 197-202. (Pubitemid 30078708)
6. Folgueras AR, Pendas AM, Sanchez LM, Lopez-Otin C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol 2004;48:411-424
7. Sliva D, English D, Lyons D, Lloyd FP, Jr. Protein kinase C induces motility of breast cancers by upregulating secretion of urokinasetype plasminogen activator through activation of AP-1 and NF-κB. Biochem Biophys Res Commun 2002;290:552-557
8. Markus G. The relevance of plasminogen activators to neoplastic growth. A review of recent literature. Enzyme 1988;40:158-172
9. Look M, van Putten W, Duffy M, et al. Pooled analysis of prognostic impact of uPA and PAI-1 in breast cancer patients. Thromb Haemost 2003;90:538-548
10. Aguirre Ghiso JA, Alonso DF, Farias EF, Gomez DE, de Kier Joffe EB. Deregulation of the signaling pathways controlling urokinase production. Its relationship with the invasive phenotype. Eur J Biochem 1999;263:295-304.
11. Chazaud B, Ricoux R, Christov C, Plonquet A, Gherardi RK, Barlovatz-Meimon G. Promigratory effect of plasminogen activator inhibitor-1 on invasive breast cancer cell populations. Am J Pathol 2002;160:237-246 (Pubitemid 34052284)
12. Lijnen HR. Pleiotropic functions of plasminogen activator inhibitor-1. Thromb Haemost 2005;3:35-45. (Pubitemid 41647113)
13. Stetler-Stevenson WG. Tissue inhibitors of metalloproteinases in cell signaling: metalloproteinase-independent biological activities. Sci Signal 2008;1:re6.
14. Lee HS, Seo EY, Kang NE, Kim WK. [6]-Gingerol inhibits metastasis of MDA-MB-231 human breast cancer cells. J Nutr Biochem 2008; 19:313-319 (Pubitemid 351503763)
15. Rose P, Huang Q, Ong CN, Whiteman M. Broccoli and watercress suppress matrix metalloproteinase-9 activity and invasiveness of human MDA-MB-231 breast cancer cells. Toxicol Appl Pharmacol 2005;209:105-113 (Pubitemid 41587401)
16. Ho YC, Yang SF, Peng CY, Chou MY, Chang YC. Epigallocatechin-3-gallate inhibits the invasion of human oral cancer cells and decreases the productions of matrix metalloproteinases and urokinase-plasminogen activator. J Oral Pathol Med 2007;36: 588-593
17. Bigelow RL, Cardelli JA. The green tea catechins, (-)-epigallocatechin-3- gallate (EGCG) and (-)-epicatechin-3-gallate (ECG), inhibit HGF/Met signaling in immortalized and tumorigenic breast epithelial cells. Oncogene 2006;25:1922-1930.
18. Lee WJ, Chen WK, Wang CJ, Lin WL, Tseng TH. Apigenin inhibits HGF-promoted invasive growth and metastasis involving blocking PI3K/Akt pathway and β4 integrin function in MDA-MB-231 breast cancer cells. Toxicol Appl Pharmacol 2008;226:178-191
19. Sliva D, Labarrere C, Slivova V, Sedlak M, Lloyd FP, Jr., Ho NW. Ganoderma lucidum suppresses motility of highly invasive breast and prostate cancer cells. Biochem Biophys Res Commun 2002; 298:603-612 (Pubitemid 35333701)
20. Jiang J, Grieb B, Thyagarajan A, Sliva D. Ganoderic acids suppress growth and invasive behavior of breast cancer cells by modulating AP-1 and NF-κB signaling. Int J Mol Med 2008;21: 577-584
21. Sliva D, Jedinak A, Kawasaki J, Harvey K, Slivova V. Phellinus linteus suppresses growth, angiogenesis and invasive behaviour of breast cancer cells through the inhibition of AKT signalling. Br J Cancer 2008;98:1348-1356 (Pubitemid 351543583)
22. Seeram NP, Adams LS, Zhang Y, et al. Blackberry, black raspberry, blueberry, cranberry, red raspberry, and strawberry extracts inhibit growth and stimulate apoptosis of human cancer cells in vitro. J Agric Food Chem 2006;54:9329-9339 (Pubitemid 46086089)
23. Seeram NP, Heber D. Impact of berry phytochemicals on human health: effects beyond antioxidation. In: Ho CT, Shahidi FS, editors. Lipid oxidation and antioxidants: chemistry, methodologies and health effects. Oxford: Oxford Press; 2006.
24. Seeram NP. Berry fruits: compositional elements, biochemical activities, and the impact of their intake on human health, performance, and disease. J Agric Food Chem 2008;56:627-629
25. Chen PN, Chu SC, Chiou HL, Kuo WH, Chiang CL, Hsieh YS. Mulberry anthocyanins, cyanidin 3-rutinoside and cyanidin 3-glucoside, exhibited an inhibitory effect on the migration and invasion of a human lung cancer cell line. Cancer Lett 2006;235: 248-259
26. Matchett MD, MacKinnon SL, Sweeney MI, Gottschall-Pass KT, Hurta RA. Inhibition of matrix metalloproteinase activity in DU145 human prostate cancer cells by flavonoids from lowbush blueberry (Vaccinium angustifolium): possible roles for protein kinase C and mitogen-activated protein-kinase-mediated events. J Nutr Biochem 2006;17:117-125
27. Wang LS, Hecht SS, Carmella SG, et al. Anthocyanins in black raspberries prevent esophageal tumors in rats. Cancer Prev Res 2009;2: 84-93.
28. Lechner JF, Reen RK, Dombkowski AA, et al. Effects of a black raspberry diet on gene expression in the rat esophagus. Nutr Cancer 2008;60 Suppl 1:61-69
29. Li J, Zhang D, Stoner GD, Huang C. Differential effects of black raspberry and strawberry extracts on BaPDE-induced activation of transcription factors and their target genes. Mol Carcinog 2008;47: 286-294 (Pubitemid 351500154)
30. Huang C, Zhang D, Li J, Tong Q, Stoner GD. Differential inhibition of UV-induced activation of NF κB and AP-1 by extracts from black raspberries, strawberries, and blueberries. Nutr Cancer 2007;58: 205-212 (Pubitemid 47328772)
31. Sharma M, Li L, Celver J, Killian C, Kovoor A, Seeram NP. Effects of fruit ellagitannin extracts, ellagic acid, and their colonic metabolite, urolithin A, on Wnt signaling. J Agric Food Chem 2009. Epub ahead of print. DOI: 10.1021/jf902857v.
32. Adams LS, Phung S, Wu X, Ki L, Chen S. White button mushroom (Agaricus bisporus) exhibits antiproliferative and proapoptotic properties and inhibits prostate tumor growth in athymic mice. Nutr Cancer 2008;60:744-756
33. Seeram NP, Adams LS, Hardy ML, Heber D. Total cranberry extract versus its phytochemical constituents: antiproliferative and synergistic effects against human tumor cell lines. J Agric Food Chem 2004; 52:2512-2517
34. Aiyer HS, Srinivasan C, Gupta RC. Dietary berries and ellagic acid diminish estrogen-mediated mammary tumorigenesis in ACI rats. Nutr Cancer 2008;60:227-234 (Pubitemid 351454024)
35. Gordillo G, Fang H, Khanna S, Harper J, Phillips G, Sen CK. Oral administration of blueberry inhibits angiogenic tumor growth and enhances survival of mice with endothelial cell neoplasm. Antioxid Redox Signal 2009;11:47-58.
36. Stoner GD. Foodstuffs for preventing cancer: the preclinical and clinical development of berries. Cancer Prev Res 2009;2:187-194
37. Azios NG, Dharmawardhane SF. Resveratrol and estradiol exert disparate effects on cell migration, cell surface actin structures, and focal adhesion assembly in MDA-MB-231 human breast cancer cells. Neoplasia 2005;7:128-140
38. Kong D, Li Y, Wang Z, Banerjee S, Sarkar FH. Inhibition of angiogenesis and invasion by 3,3′-diindolylmethane is mediated by the nuclear factor-κB downstream target genes MMP-9 and uPA that regulated bioavailability of vascular endothelial growth factor in prostate cancer. Cancer Res 2007;67:3310-3319
39. Hung SH, Shen KH, Wu CH, Liu CL, Shih YW. α-Mangostin suppresses PC-3 human prostate carcinoma cell metastasis by inhibiting matrix metalloproteinase-2/9 and urokinase-plasminogen expression through the JNK signaling pathway. J Agric Food Chem 2009;57:1291-1298
40. Kwon GT, Cho HJ, Chung WY, Park KK, Moon A, Park JH. Isoliquiritigenin inhibits migration and invasion of prostate cancer cells: possible mediation by decreased JNK/AP-1 signaling. J Nutr Biochem 2009;20:663-676
41. Yoon SO, Shin S, Lee HJ, Chun HK, Chung AS. Isoginkgetin inhibits tumor cell invasion by regulating phosphatidylinositol 3-kinase/Akt-dependent matrix metalloproteinase-9 expression. Mol Cancer Ther 2006;5:2666-2675 (Pubitemid 44848993)
42. Dannemann N, Hart JR, Ueno L, Vogt PK. Phosphatidylinositol 4,5-bisphosphate (PIP(2))-specific AKT1 is oncogenic. Int J Cancer 2009. Epub ahead of print. DOI: 10.1002/ijc.25012.
43. Yamaguchi N, Ito T, Azuma S, et al. Constitutive activation of nuclear factor-κB is preferentially involved in the proliferation of basal-like subtype breast cancer cell lines. Cancer Sci 2009;100:1668-1674
44. Schneider BP, Winer EP, Foulkes WD, et al. Triple-negative breast cancer: risk factors to potential targets. Clin Cancer Res 2008;14: 8010-8018
45. Umemura S, Yoshida S, Ohta Y, Naito K, Osamura RY, Tokuda Y. Increased phosphorylation of Akt in triple-negative breast cancers. Cancer Sci 2007;98:1889-1892 (Pubitemid 350002194)
46. Aleskandarany MA, Rakha EA, Ahmed MA, et al. PIK3CA expression in invasive breast cancer: a biomarker of poor prognosis. Breast Cancer Res Treat 2009. Epub ahead of print. DOI: 10.1007/ s10549-009-0508-509
47. Lapidot T, Walker MD, Kanner J. Can apple antioxidants inhibit tumor cell proliferation? Generation of H(2)O(2) during interaction of phenolic compounds with cell culture media. J Agric Food Chem 2002;50: 3156-3160
48. Liu RH, Sun J. Antiproliferative activity of apples is not due to phenolic-induced hydrogen peroxide formation. J Agric Food Chem 2003;51:1718-1723
49. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008;22:659-661 (Pubitemid 351348146)