Polyphenol-rich strawberry extract (PRSE) shows in vitro and in vivo biological activity against invasive breast cancer cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Amatori, Stefano ^a,b   Mazzoni, Luca ^c   Alvarez Suarez, Josè Miguel ^c,d   Giampieri, Francesca ^b,c   Gasparrini, Massimiliano ^c   Forbes Hernandez, Tamara Yuliett ^c,e   Afrin, Sadia ^c   Errico Provenzano, Alfredo ^a   Persico, Giuseppe ^a   Mezzetti, Bruno ^c   Amici, Augusto ^f   Fanelli, Mirco ^a   Battino, Maurizio ^c,g  

^a UNIVERSITY OF URBINO   (Italy)

^b Fondazione Umberto Veronesi   (Italy)

^c UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^d UNIVERSIDAD DE LAS AMÉRICAS   (Ecuador)

^e Universidad Internacional Iberoamericana (UNINI)   (Mexico)

^f UNIVERSITY OF CAMERINO   (Italy)

^g Parque Científico y Tecnológico de Cantabria   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; PLANT EXTRACT; POLYPHENOL;

ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; CELL ADHESION; CELL CYCLE; CELL MOTION; CELL SURVIVAL; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; FRAGARIA; GENE EXPRESSION PROFILING; HUMAN; ISOLATION AND PURIFICATION; MOUSE; ORAL DRUG ADMINISTRATION; TREATMENT OUTCOME; TUMOR CELL LINE; XENOGRAFT;

ADMINISTRATION, ORAL; ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL ADHESION; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; DISEASE MODELS, ANIMAL; FRAGARIA; GENE EXPRESSION PROFILING; HETEROGRAFTS; HUMANS; MICE; NEOPLASM TRANSPLANTATION; PLANT EXTRACTS; POLYPHENOLS; TREATMENT OUTCOME;

EID: 84981156847     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep30917     Document Type: Article

References (66)

1. Aravindaram, K., Yang, N.-S. Anti-inflammatory plant natural products for cancer therapy. Planta Med. 76, 1103-1117 (2010).
2. Johnsen, S. P. et al. Intake of fruit and vegetables and the risk of ischaemic stroke in a cohort of Danish men and women. Am. J. Clin. Nutr. 78, 57-64, 2003.
3. Vauzour, D., Vafeiadou, K., Rendeiro, C., Corona, G., Spencer, J. P. E. The inhibitory effects of berry-derived flavonoids against neurodegenerative processes. J. Berry Res. 1, 45-52 (2010).
4. Papathanasopoulos, A., Camilleri, M. Dietary fiber supplements: Effects in obesity and metabolic syndrome and relationship to gastrointestinal functions. Gastroenterology 138(1), 65-72 (2010).
5. Carter, P., Gray, L. J., Troughton, J., Khunti, K., Davies, M. J. Fruit and vegetable intake and incidence of type 2 diabetes mellitus: Systematic review and meta-analysis. BMJ 341, c4229 (2010).
6. Holt, E. M. et al. Fruit and vegetable consumption and its relation to markers of inflammation and oxidative stress in adolescents. J. Am. Diet. Assoc. 109(3), 414-421 (2009).
7. Kubota, M. et al. Anti-melanogenic compounds in Rubus croceacanthus. J. Berry Res. 4(3), 127-135 (2014).
8. Smith-Warner, S. A. et al. Fruits, vegetables and lung cancer: A pooled analysis of cohort studies. Int. J. Cancer 107, 1001-1011 (2003).
9. El Hasasna, H. et al. Rhus coriaria induces senescence and autophagic cell death in breast cancer cells through a mechanism involving p38 and ERK1/2 activation. Sci. Rep. 5, 13013 (2015).
10. Ariza, M. T. et al. Effects of harvest time on functional compounds and fruit antioxidant capacity in ten strawberry cultivars. J. Berry Res. 5(2), 71-80 (2015).
11. Tulipani, S. et al. Folate content in different strawberry genotypes and folate status in healthy subjects after strawberry consumption. Biofactors 34, 47-55 (2008).
12. Tulipani, S., Mezzetti, B., Battino, M. Impact of strawberries on human health: insight into marginally discussed bioactive compounds for the Mediterranean diet. Public Health Nutr. 12(9A), 1656-1662 (2009).
13. Giampieri, F. et al. The strawberry: Composition, nutritional quality, impact on human health. Nutrition 28, 9-19 (2012).
14. Giampieri, F. et al. The potential impact of strawberry on human health. Nat. Prod. Res. 27, 448-455 (2012).
15. Meyers, K. J., Watkins, C. B., Pritts, M. P., Liu, R. H. Antioxidant and antiproliferative activities of strawberries. J. Agric. Food Chem. 51, 6887-6892 (2003).
16. Olsson, M. E., Gustavsson, K.-E.,ersson, S., Nilsson, A., Duan, R.-D. Inhibition of cancer cell proliferation in vitro by fruit and berry extracts and correlations with antioxidant levels. J. Agric. Food Chem. 52, 7264-7271 (2004).
17. Liu, R. H. Potential synergy of phytochemicals in cancer prevention: mechanism of action. J. Nutr. 134, 3479S-3485S (2004).
18. Seeram, N. P. et al. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J. Nutr. Biochem. 16, 360-367 (2005).
19. Somasagara, R. R. et al. Extracts of Strawberry Fruits Induce Intrinsic Pathway of Apoptosis in Breast Cancer Cells and Inhibits Tumor Progression in Mice. PLoS One 7(10), e470212012 (2014).
20. Ferlay, J. et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136, E359-E386 (2015).
21. Clevers, H. The cancer stem cell: premises, promises and challenges. Nat. Med. 17(3), 313-319 (2011).
22. Montani, M. et al. The water soluble ruthenium(II) organometallic compound [Ru(p-cymene)(bis(3,5 dimethylpyrazol-1-yl) methane)Cl]Cl suppresses triple negative breast cancer growth by inhibiting tumor infiltration of regulatory T cells. Pharmacol Res. 107, 282-290 (2016).
23. Garulli, C. et al. Dorsomorphin reverses the mesenchymal phenotype of breast cancer initiating cells by inhibition of bone morphogenetic protein signaling. Cell Signal. 26(2), 352-362 (2014).
24. Bisaro, B. et al. p130Cas/Cyclooxygenase-2 axis in the control of mesenchymal plasticity of breast cancer cells. Breast Cancer Res. 14(5), R137 (2012).
25. Galiè, M. et al. Mammary carcinoma provides highly tumourigenic and invasive reactive stromal cells. Carcinogenesis 26, 1868-1878 (2005).
26. Galiè, M. et al. Mesenchymal stem cells share molecular signature with mesenchymal tumor cells and favor early tumor growth in syngeneic mice. Oncogene 27, 2542-2551 (2008).
27. Tulipani, S. et al. Ascorbate, not urate, modulates the plasma antioxidant capacity after strawberry intake. Food Chem. 117, 181-188 (2009).
28. Tulipani, S. et al. Antioxidants, phenolic compounds, nutritional quality of different strawberry genotypes. J. Agric. Food Chem. 56, 696-704 (2008).
29. Steeg, P. S. Tumor metastasis: mechanistic insights and clinical challenges. Nat. Med. 12, 895-904 (2006).
30. Capocasa, F., Scalzo, J., Mezzetti, B., Battino, M. Combining quality and antioxidant attributes in the strawberry: the role of genotype. Food Chem. 111, 872-878 (2008).
31. Tulipani, S. et al. Influence of environmental and genetic factors on health-related compounds in strawberry. Food Chem. 124, 906-913 (2011).
32. Lopes-da-Silva, F., de Pascual-Teresa, S., Rivas-Gonzalo, J. C., Santos-Buelga, C. Identification of anthocyanin pigments in strawberry (cv. Camarosa) by LC using DAD and ESI-MS detection. Eur. Food Res. Technol. 214, 248-253 (2002).
33. Yokoyama, T. et al. Serum vitamin C concentration was inversely associated with subsequent 20-year incidence of stroke in a Japanese rural community. The Shibata study. Stroke 31(10), 2287-2294 (2000).
34. Steinmetz, K. A., Potter, J. D. Vegetables, fruit, cancer prevention: a review. J. Am. Diet. Assoc. 96(10), 1027-1039 (1996).
35. Houston, D. K., Johnson, M. A. Does vitamin C intake protect against lead toxicity? Nutr. Rev. 58, 73-75 (2000).
36. Sapei, L., Hwa, L. Study on the Kinetics of Vitamin C Degradation in Fresh Strawberry Juices. Procedia Chemistry 9, 62-68 (2014).
37. Giampieri, F. et al. An anthocyanin-rich strawberry extract protects against oxidative stress damage and improves mitochondrial functionality in human dermal fibroblasts exposed to an oxidizing agent. Food Funct. 5(8), 1939-1948 (2014).
38. Giampieri, F. et al. Polyphenol-Rich Strawberry Extract Protects Human Dermal Fibroblasts against Hydrogen Peroxide Oxidative Damage and Improves Mitochondrial Functionality. Molecules 19, 7798-7816 (2014).
39. Romandini, S. et al. Effects of an acute strawberry (Fragaria ?ananassa) consumption on the plasma antioxidant status of healthy subjects. J. Berry Res. 3, 169-179 (2013).
40. Alvarez-Suarez, J. M. et al. One-month strawberry-rich anthocyanin supplementation ameliorates cardiovascular risk, oxidative stress markers and platelet activation in humans. J. Nutr. Biochem. 25(3), 289-294 (2014).
41. Marchini, C. et al. Mesenchymal/stromal gene expression signature relates to basal-like breast cancers, identifies bone metastasis and predicts resistance to therapies. PLoS One 5(11), e14131 (2010).
42. Qin, L. et al. NCOA1 directly targets M-CSF1 expression to promote breast cancer metastasis. Cancer Res. 74(13), 3477-3488 (2014).
43. Zeng, G. F., Cai, S. X., Wu, G. J. Up-regulation of METCAM/MUC18 promotes motility, invasion, tumorigenesis of human breast cancer cells. BMC Cancer 11, 113 (2011).
44. Yuan, Z. Y. et al. Overexpression of ETV4 protein in triple-negative breast cancer is associated with a higher risk of distant metastasis. Onco. Targets Ther. 7, 1733-1742 (2014).
45. Loganathan, J. et al. The mushroom Ganoderma lucidum suppresses breast-to-lung cancer metastasis through the inhibition of proinvasive genes. Int. J. Oncol. 44(6), 2009-2015 (2014).
46. Zhao, J. et al. TIP30/CC3 expression in breast carcinoma: relation to metastasis, clinicopathologic parameters, P53 expression. Hum. Pathol. 38(2), 293-298 (2007).
47. Rose, A. A., Siegel, P. M. Osteoactivin/HGFIN: is it a tumor suppressor or mediator of metastasis in breast cancer? Breast Cancer Res. 9(6), 403 (2007).
48. Tholen, M. et al. Stress-resistant translation of Cathepsin L mRNA in breast cancer progression. J. Biol. Chem. 290(25), 15758-15769 (2015).
49. Okuyama Kishima, M. et al. Immunohistochemical expression of CXCR4 on breast cancer and its clinical significance. Anal. Cell Pathol. (Amst) 2015, 891020 (2015).
50. Carter, R. Z. et al. Tumour but not stromal expression of ? 3 integrin is essential, is required early, for spontaneous dissemination of bone-metastatic breast cancer. J. Pathol. 235(5), 760-772 (2015).
51. Bodey, B., Bodey, B. Jr., Siegel, S. E., Kaiser, H. E. Matrix metalloproteinases in neoplasm-induced extracellular remodeling in breast carcinomas. Anticancer Res. 21(3B), 2021-2028 (2001).
52. Re, R. et al. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26, 1231-1237 (1999).
53. Pellegrini, N., Re, R., Yang, M., Rice-Evans, C. A. Screening of dietary carotenoids and carotenoid-rich fruit extracts for antioxidant activities applying the 2,2?-azobis(3-ethylenebenzothiazoline-6-sulfonic) acid radical cation decolorization assay. Method Enzymol. 299, 379-389 (1999).
54. Deighton, N., Brennan, R., Finn, C., Davies, H. V. Antioxidant properties of domesticated and wild Rubus species. J. Sci. Food Agric. 80, 1307-1313 (2000).
55. Benzie, I. F. F., Strain, J. J. Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: The FRAP assay. Anal. Biochem. 239, 70-76 (1996).
56. Slinkard, K., Singleton, V. L. Total Phenol analysis: automation and comparision with manual methods. Am. J. Enol. Viticult. 28, 49-55 (1977).
57. Giusti, M. M., Wrolstad, R. E. Characterization and measurement of anthocyanins by UV-visible spectroscopy in Current Protocols Food Analytical Chemistry, F1.2.1-F1.2.13 (John Wiley & Sons, Inc 2001).
58. Jia, Z., Tang, M., Wu, J. The determination of flavonoid contents in mulberry and their scavenging effects on superoxides radicals. Food Chem. 64, 555-559 (1998).
59. Dewanto, V., Wu, X., Adom, K. K., Liu, R. H. Thermal processing enhances the nutritional values of tomatoes by increasing the total antioxidant activity. J. Agric. Food Chem. 50, 3010-3014 (2002).
60. Helsper, J. P. F. G. et al. Response of selected antioxidants and pigments in tissues of Rosa hybrida and Fuchsia hybrida to supplemental UV-A exposure. Physiol Plant. 117, 171-187 (2003).
61. Fanelli, M. et al. Loss of pericentromeric DNA methylation pattern in human glioblastoma is associated with altered DNA methyltransferases expression and involves the stem cell compartment. Oncogene 27(3), 358-365 (2008).
62. Puppo, F. et al. Cell-line specific chromatin acetylation at the Sox10-Pax3 enhancer site modulates the RET proto-oncogene expression. FEBS Lett. 523(1-3), 123-127 (2002).
63. Chou, T. C. Theoretical basis, experimental design, computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 58, 621-681 (2006).
64. Amatori, S. et al. Decitabine, differently from DNMT1 silencing, exerts its antiproliferative activity through p21 upregulation in malignant pleural mesothelioma (MPM) cells. Lung Cancer 66(2), 184-190 (2009).
65. Kalogris, C. et al. Sanguinarine suppresses basal-like breast cancer growth through dihydrofolate reductase inhibition. Biochem. Pharmacol. 90(3), 226-234 (2014).
66. Amatori, S. et al. Malten, a new synthetic molecule showing in vitro antiproliferative activity against tumour cells and induction of complex DNA structural alterations. Br. J. Cancer 103(2), 239-248 (2010).