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Anti-metastasis Activity of Black Rice Anthocyanins Against Breast Cancer: Analyses Using an ErbB2 Positive Breast Cancer Cell Line and Tumoral Xenograft Model

  • Luo, Li-Ping (Department of Public Health, Chengdu Medical College) ;
  • Han, Bin (Department of Public Health, Chengdu Medical College) ;
  • Yu, Xiao-Ping (Department of Public Health, Chengdu Medical College) ;
  • Chen, Xiang-Yan (Department of Public Health, Chengdu Medical College) ;
  • Zhou, Jie (Department of Public Health, Chengdu Medical College) ;
  • Chen, Wei (Department of Public Health, Chengdu Medical College) ;
  • Zhu, Yan-Feng (Department of Public Health, Chengdu Medical College) ;
  • Peng, Xiao-Li (Department of Public Health, Chengdu Medical College) ;
  • Zou, Qiang (Department of Public Health, Chengdu Medical College) ;
  • Li, Sui-Yan (School of Life Science and Engineering, Southwest Jiaotong University)
  • Published : 2014.08.15

Abstract

Background: Increasing evidence from animal, epidemiological and clinical investigations suggest that dietary anthocyanins have potential to prevent chronic diseases, including cancers. It is also noteworthy that human epidermal growth factor receptor 2 (ErbB2) protein overexpression or ErbB2 gene amplification has been included as an indicator for metastasis and higher risk of recurrence for breast cancer. Materials and Methods: The present experiments investigated the anti-metastasis effects of black rice anthocyanins (BRACs) on ErbB2 positive breast cancer cells in vivo and in vitro. Results: Oral administration of BRACs (150 mg/kg/day) reduced transplanted tumor growth, inhibited pulmonary metastasis, and decreased lung tumor nodules in BALB/c nude mice bearing ErbB2 positive breast cancer cell MDA-MB-453 xenografts. The capacity for migration, adhesion, motility and invasion was also inhibited by BRACs in MDA-MB-453 cells in a concentration dependent manner, accompanied by decreased activity of a transfer promoting factor, urokinase-type plasminogen activator (u-PA). Conclusions: Together, our results indicated that BRACs possess anti-metastasis potential against ErbB2 positive human breast cancer cells in vivo and in vitro through inhibition of metastasis promoting molecules.

Keywords

References

  1. Adams LS, Kanaya N, Phung S, et al (2011). Whole blueberry powder modulates the growth and metastasis of MDAMB-231 triple negative breast tumors in nude mice. J Nutr, 141, 1805-12. https://doi.org/10.3945/jn.111.140178
  2. Adams LS, Phung S, Yee N, et al (2010). Blueberry phytochemicals inhibit growth and metastatic potential of MDA-MB-231 breast cancer cells through modulation of the phosphatidylinositol 3-kinase pathway. Cancer Res, 70, 3594-605. https://doi.org/10.1158/0008-5472.CAN-09-3565
  3. Aertgeerts K, Skene R, Yano J, et al (2011). Structural analysis of the mechanism of inhibition and allosteric activation of the kinase domain of HER2 protein. J Biol Chem, 286, 18756-65. https://doi.org/10.1074/jbc.M110.206193
  4. Aiyer HS, Gupta RC (2010). Berries and ellagic acid prevent estrogen-induced mammary tumorigenesis by modulating enzymes of estrogen metabolism. Cancer Prev Res, 3, 727-37. https://doi.org/10.1158/1940-6207.CAPR-09-0260
  5. Bernasconi B, Chiaravalli AM, Finzi G, et al (2012). Genetic heterogeneity in HER2 testing may influence therapy eligibility. Breast Cancer Res Treat, 133, 161-8. https://doi.org/10.1007/s10549-011-1744-3
  6. Berry DA, Cronin KA, Plevritis SK, et al (2005). Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med, 353, 1784-92. https://doi.org/10.1056/NEJMoa050518
  7. Bilal BH, Imtiaz AS, Mohammad A, et al (2008). A dietary anthocyanidin delphinidin induces apoptosis of human prostate cancer PC3 cells in vitro and in vivo: involvement of nuclear factor-kb signaling. Cancer Res, 68, 8564-72. https://doi.org/10.1158/0008-5472.CAN-08-2232
  8. Chang H, Yu B, Yu XP, et al (2010). Anti-cancer activities of an anthocyanin-rich extract from black rice against breast cancer cells in vitro and in vivo. Nutr cancer, 62, 1128-36. https://doi.org/10.1080/01635581.2010.494821
  9. Chen PN, Chu SC, Chiou HL, et al (2005). Cyanidin 3-glucoside and peonidin 3-glucoside inhibit tumor cell growth and induce apoptosis in vitro and suppress tumor growth in vivo. Nutr cancer, 53, 232-43. https://doi.org/10.1207/s15327914nc5302_12
  10. DeSantis C, Siegel R, Bandi P, Jemal A (2011). Breast cancer statistics, 2011. CA Cancer J Clin, 61, 409-18.
  11. Dreiseitel A, Oosterhius B, Vukman KV, et al (2009). Berry anthocyanins and anthocyanidins exhibit distinct affinities for the efflux transporters BCRP and MDR1. Br J Pharmacol, 158, 1942-50. https://doi.org/10.1111/j.1476-5381.2009.00495.x
  12. Faria A, Pestana D, Teixeira D, et al (2010). Blueberry anthocyanins and pyruvic acid adducts: Anti-cancer properties in breast cancer cell lines. Phytother Res, 24, 1862-9. https://doi.org/10.1002/ptr.3213
  13. Forester SC, Waterhouse AL (2010). Gut metabolites of anthocyanins, gallic acid, 3-O-methylgallic acid, and 2,4,6-trihydroxybenzaldehyde, inhibit cell proliferation of Caco-2 cells. J Agric Food Chem, 58, 5320-7. https://doi.org/10.1021/jf9040172
  14. Gerdes J, Lemke H, Baisch H, et al (1984). Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol, 133, 1710-5.
  15. Gretel M, Amelia P, Jorge OS (2013). Accurate breast cancer diagnosis through real-time PCR HER-2 gene quantification using immunohistochemically-identified biopsies. Oncol Lett, 5, 295-8.
  16. Gu J, Ahn-Jarvis JH, Riedl KM, et al (2014). Characterization of black raspberry functional food products for cancer prevention human clinical trials. J Agric Food Chem, 62, 3997-4006. https://doi.org/10.1021/jf404566p
  17. Gutierrez C, Schiff R (2011). HER 2: Biology, Detection, and Clinical Implications. Arch Pathol Lab Med, 135, 55-62.
  18. Gutierres JM, Carvalho FB, Schetinger MR, et al (2012). Protective effects of anthocyanins on the ectonucleotidase activity in the impairment of memory induced by scopolamine in adult rats. Life Sci, 91, 1221-8. https://doi.org/10.1016/j.lfs.2012.09.013
  19. Hafeez BB, Siddiqui IA, Asim M, et al (2008). A dietary anthocyanidin delphinidin induces apoptosis of human prostate cancer PC3 cells in vitro and in vivo: involvement of nuclear factor-$\kappa{b}$ signaling. Cancer Res, 68, 8564-72. https://doi.org/10.1158/0008-5472.CAN-08-2232
  20. Han W, Lo HW (2012). Landscape of EGFR signaling network in human cancers: biology and therapeutic response in relation to receptor subcellular locations. Cancer Lett, 318, 124-34. https://doi.org/10.1016/j.canlet.2012.01.011
  21. Ho ML, Chen PN, Chu SC, et al (2010). Peonidin 3-glucoside inhibits lung cancer metastasis by downregulation of proteinases activities and MAPK pathway. Nutr cancer, 62, 505-16. https://doi.org/10.1080/01635580903441261
  22. Holliday DL, Speirs V (2011). Choosing the right cell line for breast cancer research. Breast Cancer Res, 13, 215. https://doi.org/10.1186/bcr2889
  23. Jemal A, Bray F, Center MM, et al (2011). Global cancer statistics. CA Cancer J Clin, 61, 69-90. https://doi.org/10.3322/caac.20107
  24. Joanna K (2014). Association between vegetable, fruit and carbohydrate intake and breast cancer risk in relation to physical activity. Asian Pac J Cancer Prev, 15, 4429-36. https://doi.org/10.7314/APJCP.2014.15.11.4429
  25. Kundu JK, Chun KS (2014). The promise of dried fruits in cancer chemoprevention. Asian Pac J Cancer Prev, 15, 3343-52. https://doi.org/10.7314/APJCP.2014.15.8.3343
  26. Stoner GD, Seeram NP (2011). Berries and cancer prevention, 1st edn. Springer publisher, New York.
  27. Li LY, Adams LS, Chen S, et al (2009). Eugenia jambolana Lam. Berry extract inhibits growth and induces apoptosis of human breast cancer but not non-tumorigenic breast cells. J Agric Food Chem, 57, 826-31. https://doi.org/10.1021/jf803407q
  28. Li Y, Sarkar FH (2002). Down-regulation of invasion and angiogenesis-related genes identified by cDNA microarray analysis of PC3 prostate cancer cells treated with genistein. Cancer Lett, 186, 157-64. https://doi.org/10.1016/S0304-3835(02)00349-X
  29. Ling WH, Wang LL, Ma J (2002). Supplementation of the black rice outer layer fraction to rabbits decreases atherosclerotic plaque formation and increases antioxidant status. J Nutr, 132, 20-6.
  30. Luigia L, Francesca P, Anna S, et al (2008). Autophagy inhibition enhances anthocyanin-induced apoptosis in hepatocellular carcinoma. Mol Cancer Ther, 7, 2476-85. https://doi.org/10.1158/1535-7163.MCT-08-0361
  31. Marczylo TH, Cooke D, Brown K, Steward WP, Gescher AJ (2009). Pharmacokinetics and metabolism of the putative cancer chemopreventive agent cyanidin-3-glucoside in mice. Cancer Chemother Pharmacol, 64, 1261-8. https://doi.org/10.1007/s00280-009-0996-7
  32. Muserref HS, Ammad AF, Muhammad ZQ, et al (2014). Anthocyanins: targeting of signaling networks in cancer cells. Asian Pac J Cancer Prev, 15, 2379-81. https://doi.org/10.7314/APJCP.2014.15.5.2379
  33. Nahta R, Shabaya S, Ozbay T, Rowe DL (2009). Personalizing HER2-targeted therapy in metastatic breast cancer beyond HER2 status: what we have learned from clinical specimens. Curr Pharmacogenomics Person Med, 7, 263-74. https://doi.org/10.2174/187569209790112337
  34. Neve RM, Chin K, Fridlyand J, et al (2006). A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell, 10, 515-27. https://doi.org/10.1016/j.ccr.2006.10.008
  35. Olson EM, Najita JS, Sohl J, et al (2013). Clinical outcomes and treatment practice patterns of patients with HER2-positive metastatic breast cancer in the post-trastuzumab era. Breast, 22, 525-31. https://doi.org/10.1016/j.breast.2012.12.006
  36. Pathmanathan N, Balleine RL (2013). Ki67 and proliferation in breast cancer. J Clin Pathol, 66, 512-6. https://doi.org/10.1136/jclinpath-2012-201085
  37. Press MF, Finn RS, Cameron D, et al (2008). HER-2 gene amplification, HER-2 and epidermal growth factor receptor mRNA and protein expression, and Lapatinib efficacy in women with metastatic breast cancer. Clin Cancer Res, 14, 7861-70. https://doi.org/10.1158/1078-0432.CCR-08-1056
  38. Prior RL, Wu X, Gu L, et al (2008). Whole berries versus berry anthocyanins: interactions with dietary fat levels in the C57BL/6J mouse model of obesity. J Agric Food Chem, 56, 647-53. https://doi.org/10.1021/jf071993o
  39. Ratasark S, Teera C (2014). Purple rice extract supplemented diet reduces DMH induced aberrant crypt foci in the rat colon by inhibition of bacterial β-glucuronidase. Asian Pac J Cancer Prev, 15, 749-55. https://doi.org/10.7314/APJCP.2014.15.2.749
  40. Reeves PG, Nielsen FH, Fahey GCJ (1993). AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr, 23, 1939-51.
  41. Sahai E (2005). Mechanisms of cancer cell invasion. Curr Opin Genet Dev, 15, 87-96. https://doi.org/10.1016/j.gde.2004.12.002
  42. Schmalfeldt B, Prechtel D, Harting K, et al (2001). Increased expression of matrix metalloproteinases (MMP)-2, MMP-9, and the urokinase-type plasminogen activator is associated with progression from benign to advanced ovarian cancer. Clin Cancer Res, 7, 2396-404.
  43. Shim SH, Kim JM, Choi CY, Park KH (2012). Ginkgo biloba extract and bilberry anthocyanins improve visual function in patients with normal tension glaucoma. J Med Food, 15, 818-23. https://doi.org/10.1089/jmf.2012.2241
  44. Siegel R, Naishadham D, Jemal A (2012). Cancer statistics. CA Cancer J Clin, 62, 10-29. https://doi.org/10.3322/caac.20138
  45. Soule HD, Maloney TM, Wolman SR, et al (1990). Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res, 50, 6075-86.
  46. Stoner GD, Wang LS, Seguin C, et al (2010). Multiple berry types prevent N-nitrosomethylbenzylamine-induced esophageal cancer in rats. Pharm Res, 27, 1138-45. https://doi.org/10.1007/s11095-010-0102-1
  47. Thomasset S, Berry DP, Cai H, et al (2009). Pilot study of oral anthocyanins for colorectal cancer chemoprevention. Cancer Prev Res (Phila), 2, 625-33. https://doi.org/10.1158/1940-6207.CAPR-08-0201
  48. Tsuda T (2012). Dietary anthocyanin-rich plants: Biochemical basis and recent progress in health benefits studies. Mol Nutr Food Res, 56, 159-70. https://doi.org/10.1002/mnfr.201100526
  49. Van RM, Naidoo N, Landberg R (2013). Dietary flavonoids and the development of type 2 diabetes and cardiovascular diseases: review of recent findings. Curr Opin Lipidol, 24, 25-33. https://doi.org/10.1097/MOL.0b013e32835bcdff
  50. Vantyghem SA, Wilson SM, Postenka CO, et al (2005). Dietary genistein reduces metastasis in a postsurgical orthotopic breast cancer model. Cancer Res, 65, 3396-403.
  51. Wang Q, Han P, Zhang M, et al (2007). Supplementation of black rice pigment fraction improves antioxidant and antiinflammatory status in patients with coronary heart disease. Asia Pac J Clin Nutr, 16, 295-301.
  52. Wang YQ (2010). Breast cancer metastasis driven by ErbB2 and $14-3-3\xi$. Cell Adhes Migr, 4, 7-9. https://doi.org/10.4161/cam.4.1.10497
  53. Wedick NM, Pan A, Cassidy A, et al (2012). Dietary flavonoid intakes and risk of type 2 diabetes in US men and women. Am J Clin Nutr, 95, 925-33. https://doi.org/10.3945/ajcn.111.028894
  54. Xu M, Bower KA, Wang SY, et al (2010). Cyanidin-3-Glucoside inhibits ethanol-induced invasion of breast cancer cells overexpressing ErbB2. Mol Cancer, 9, 285. https://doi.org/10.1186/1476-4598-9-285
  55. Zeng YW, Yang JZ, Pu XY, et al (2013). Strategies of functional food for cancer prevention in human beings. Asian Pacific J Cancer Prev, 14, 1585-92. https://doi.org/10.7314/APJCP.2013.14.3.1585
  56. Zhang HT, Alan B, Wang Q (2007). ErbB receptors: from oncogenes to targeted cancer therapies. J Clin Invest, 117, 2051-8. https://doi.org/10.1172/JCI32278

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