Phenolic Fractions from Muscadine Grape “Noble” Pomace can Inhibit Breast Cancer Cell MDA-MB-231 Better than those from European Grape “Cabernet Sauvignon” and Induce S-Phase Arrest and Apoptosis

Journal of Food Science

Volumn 82, Issue 5, 2017, Pages 1254-1263

  Luo, Jianming ^a,b   Wei, Zheng ^a,c   Zhang, Shengyu ^a   Peng, Xichun ^b   Huang, Yu ^c   Zhang, Yali ^a   Lu, Jiang ^c,d  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b JINAN UNIVERSITY   (China)

^c Agro products Quality Safety and Testing Technology Research Institute Guangxi Academy of Agricultural Science   (China)

^d SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

apoptosis; breast cancer cell; cell cycle; ellagic acid; muscadine grape pomace

Indexed keywords

ANTINEOPLASTIC AGENT; PHENOL DERIVATIVE; PLANT EXTRACT;

APOPTOSIS; BREAST TUMOR; CELL CYCLE CHECKPOINT; CHEMISTRY; DRUG EFFECTS; FEMALE; FRUIT; HUMAN; MASS SPECTROMETRY; VITIS;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BREAST NEOPLASMS; CELL CYCLE CHECKPOINTS; FEMALE; FRUIT; HUMANS; MASS SPECTROMETRY; PHENOLS; PLANT EXTRACTS; VITIS;

EID: 85016425754     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/1750-3841.13670     Document Type: Article

References (48)

1. Burton LJ, Barnett P, Smith B, Arnold RS, Hudson T, Kundu K, Murthy N, Odero-Marah VA. 2014. Muscadine grape skin extract reverts snail-mediated epithelial mesenchymal transition via superoxide species in human prostate cancer cells. BMC Complem Altern Med 14:97–106.
2. Calabrese EJ. 2005. Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 138(3):379–411.
3. Casanova F, Quarti J, da Costa DC, Ramos CA, da Silva JL, Fialho E. 2012. Resveratrol chemosensitizes breast cancer cells to melphalan by cell cycle arrest. J Cell Biochem 113(8):2586–96.
4. Chang XZ, Li DQ, Hou YF, Wu J, Lu JS, Di GH, Jin W, Ou XL, Shen ZZ, Shao ZM. 2007. Identification of the functional role of peroxiredoxin 6 in the progression of breast cancer. Breast Cancer Res 9(6):R76.
5. Chien SY, Wu YC, Chung JG, Yang JS, Lu HF, Tsou MF, Wood WG, Kuo SJ, Chen DR. 2009. Quercetin-induced apoptosis acts through mitochondrial- and caspase-3-dependent pathways in human breast cancer MDA-MB-231 cells. Hum Exp Toxicol 28:493–503.
6. Cohen JJ. 1993. Apoptosis. Immonol Today 14:126–30.
7. Cohen JJ. 1999. Apoptosis: mechanisms of life and death in the immune system. J Allergy Clin Immunol 103:548–54.
8. Chou CC, Yang JS, Lu HF, Ip S, Lo C, Wu CC, Lin JP, Tang NY, Chung JG, Chou MJ, Teng YH, Chen DR. 2010. Quercetin-mediated cell cycle arrest and apoptosis involving activation of a caspase cascade through the mitochondrial pathway in human breast MCF-7 cells. Arch Pharm Res 33:1181–91.
9. de la Cerda-Carrasco A, López-Solís R, Nuñez-Kalasic H, Peña-Neira Á, Obreque-Slier E. 2014. Phenolic composition and antioxidant capacity of pomaces from four grape varieties (Vitis vinifera L.). J Sci Food Agric 95:1521–7.
10. García-Rivera D, Delgado R, Bougame N, Haegeman G, Berghe WV. 2011. Gallic acid indanone and mangiferin xanthone are strong determinants of immune- suppressive anti-tumour effects of Mangifera indica L. bark in MDA-MB231 breast cancer cells. Cancer Lett 305:21–31.
11. Halabe Bucay A. 2007. The biological significance of cancer: mitochondria as a cause of cancer and the inhibition of glycolysis with citrate as a cancer treatment. Med Hypotheses 69:826–8.
12. Hsu JD, Kao SH, Ou TT, Chen YJ, Li YJ, Wang CJ. 2011. Gallic acid induces G2/M phase arrest of breast cancer cell MCF-7 through stabilization of p27 (Kip1) attributed to disruption of p27 (Kip1)/Skp2 complex. J Agric Food Chem 59:1996–2003.
13. Huang Z, Wang B, Williams P, Pace RD. 2009. Identification of anthocyanins in muscadine grapes with HPLC-ESI-MS. LWT – Food Sci Technol 42:819–24.
14. Hudson TS, Hartle DK, Hursting SD, Nunez NP, Wang TT, Young HA, Arany P, Green JE. 2007. Identification of prostate cancer growth by muscadine grape skin extract and resveratrol through distinct mechanisms. Cancer Res 67:8396–405.
15. Kijima I, Phung S, Hur G, Kwok SL, Chen S. 2006. Grape seed extract is an aromatase inhibitor and a suppressor of aromatase expression. Cancer Res 66:5960–7.
16. Lacroix M, Leclercq G. 2004. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat 83:249–89.
17. Lee JH, Talcott ST. 2004. Fruit maturity and juice extraction influences ellagic acid derivatives and other antioxidant polyphenolics in musacadine grapes. J Agric Food Chem 52:361–6.
18. Lee JH, Johnson JV, Talcott ST. 2005. Identification of ellagic acid conjugates and other polyphenolics in muscadine grapes by HPLC-ESI-MS. J Agric Food Chem 53:6003–10.
19. Li Y, Liu JY, Liu XP, Xing KF, Wang Y, Li FY, Yao LB. 2006. Resveratrol-inducted cell inhibition of growth and apoptosis in MCF7 human breast cancer cells are associated with modulation of phosphorylated Akt and caspase-9. Appl Biochem Biotechnol 135(3):181–92.
20. Livak KJ, Schmitgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) methods. Methods 25(4):402–8
21. Lu Y, Zhang X, Zhang H, Lan J, Huang G, Varin E, Lincet H, Poulain L, Icard P. 2011. Citrate induces apoptotic cell death: a promising way to treat gastric carcinoma? Anticancer Res 31:797–805.
22. Mantena SK, Baliga MS, Katiyar SK. 2006. Grape seed proanthocyanidins induce apoptosis and inhibit metastasis of highly metastatic breast carcinoma cells. Carcinogenesis 27(8):1682–91.
23. Mertens-Talcott SU, Percival SS. 2005. Ellagic acid and quercetin interact synergistically with resveratrol in the induction of apoptosis and cause transient cell cycle arrest in human leukemia calls. Cancer Lett 218:141–51.
24. Mertens-Talcott SU, Lee JH, Percival SS, Talcott ST. 2006. Induction of cell death in Caco-2 human colon carcinoma cells by ellagic acid rich fractions from muscadine grapes (Vitis rotundifolia). J Agric Food Chem 54:5336–43.
25. Monagas M, Gómez-Cordovés C, Bartolomé B, Laureano O, Ricardo da Silva JM. 2003. Monomeric, oligomeric and polymeric flavan-3-ol composition of wines and grapes from Vitis vinifera L. cv. Graciano, Tempranillo, and Cabernet Sauvignon. J Agric Food Chem 51:6475–81.
26. Nassiri-Asl M, Hosseinzadeh H. 2009. Review of the pharmacological effects of Vitis vinifera (grape) and its bioactive compounds. Phytother Res 23:1197–204.
27. Nesbitt WB, Carroll DE, Underwood VH. 1974. ‘Noble’ muscadine grape. Hortscience 9:247.
28. Obreque-Slier E, Peña-Neira A, López-Solís R, Zamora-Marín F, Ricardo da Silva JM, Laureano O. 2010. Comparative study of the phenolic composition of seeds and skins from Carménère and Cabernet sauvignon grape varieties (Vitis vinifera L) during ripening. J Agric Food Chem 58:3591–9.
29. Obreque-Slier E, López-Solís R, Castro-Ulloa L, Romero-Díaz C, Peña-Neira A. 2012. Phenoilc composition and physicochemical parameters of Carménère, Cabernet sauvignon, Merlot and Cabernet Franc grape seeds (Vitis vinifera L) during ripening. LWT – Food Sci Technol 48:134–41.
30. Obreque-Slier E, Peña-Neira A, López-Solís R, Cáceres-Mella A, Toledo-Araya H, López-Rivera A. 2013. Phenolic compositions of skins from four Carmenet grape varieties (Vitis vinifera L) during ripening. LWT – Food Sci Technol 54:404–13.
31. Phromnoi K, Yodkeeree S, Anuchapreeda S, Limtrakul P. 2009. Inhibition of MMP-3 activity and invasion of the MDA-MB-231 human invasive breast carcinoma cell line by bioflavonoids. Acta Pharmacol Sin 30:1169–76.
32. Rodríguez Montealegre R, Romero Peces R, Chacón Vozmediano JL, Martínez-Gascueña J, García-Romero R. 2006. Phenolic compounds in skins and seeds of ten Vitis vinifera varieties grown in a warm climate. J Food Compos Anal 19:687–93.
33. Rubio D, Garcia S, Paz MF, De la Cueva T, Lopez-Fernandez LA, Lloyd AC, Garcia-Castro J, Bernad A. 2008. Molecular characterization of spontaneous mesenchymal stem cell transformation. PLoS One 3(1):e1398.
34. Sánchez Y, Segura V, Marín-Béjar O, Athie A, Marchese FP, González J, Bujanda L, Guo S, Matheu A, Huarte M. 2014. Gnome-wide analysis of the human p53 transcriptional network unveils a lncRNA tumour suppressor signature. Nat Commun 5:5812.
35. Sandhu AK, Gu L. 2010. Antioxidant capacity, phenolic content, and profiling of phenolic compounds in the seeds, skin and pulp of Vitis rotundifolia (muscadine grapes) as determined by HPLC-DAD-ESI-MS. J Agric Food Chem 58:4681–92.
36. Sandhu AK, Gray DJ, Lu J, Gu L. 2011. Effects of exogenous abscisic acid on antioxidant capacities, anthocyanins, and flavonol contents of muscadine grape (Vitis rotundifolia) skins. Food Chem 123:982–8.
37. Singleton VL, Rossi JA. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticult 16:144–58.
38. Stewart BW, Wild CP. 2014. Cancer by organ site. In World cancer report 2014. WHO press, p 510.
39. Talcott ST, Lee JH. 2002. Ellagic acid and flavonoid antioxidant content of muscadine wine and juice. J Agric Food Chem 50:3186–92.
40. Vahidi R, Safi S, Farsinejad A, Panahi N. 2015. Citrate and celecoxib induce apoptosis and decrease necrosis in synergistic manner in canine mammary tumor cells. Cell Mol Biol 61:22–8.
41. Wang K, Zhu X, Zhang K, Zhu L, Zhou F. 2014. Investigation of gallic acid induced anticancer effect in human breast carcinoma MCF-7 cells. J Biochem Mol Toxicol 28:387–93.
42. Wang N, Wang ZY, Mo SL, Loo TY, Wang DM, Luo HB, Yang DP, Chen YL, Shen JG, Chen JP. 2012. Ellagic acid, a phenolic compound, exerts anti-angiogenesis effects via VEGFR-2 signaling pathway in breast cancer. Breast Cancer Res Treat 134(3):943–55.
43. Wang TA, Zhang XD, Guo XY, Xian SL, Lu YF. 2016. 3-Bromopyruvate and sodium citrate target glycolysis, suppress survivin, and induce mitochondrial-mediated apoptosis in gastric cancer cells and inhibit gastric orthotopic transplantation tumor growth. Oncol Rep 35:1287–96.
44. Xu CM, Zhang YL, Cao L, Lu J. 2010a. Phenolic compounds and antioxidant properties of different grape cultivars grown in China. Food Chem 119:1557–65.
45. Xu CM, Zhang YL, Wang J, Lu J. 2010b. Extraction, distribution and characterization of phenolic compounds and oil in grapeseeds, Food Chem 122:699–4.
46. Xue F, Zhao X, Yang Y, Zhao J, Cao Y, Hong C, Liu Y, Sun L, Huang M, Gu J. 2013. Responses of murine and human macrophages to leptospiral infection: a study using comparative array analysis. PLoS Negl Trop Dis 7(10):e2477.
47. Yi W, Fischer J, Akoh CC. 2005. Study of anticancer activities of muscadine grape phnolics in vitro. J Agric Food Chem 53:8804–12.
48. You Q, Chen F, Wang X, Sharp JL, You Y. 2012. Analysis of phenolic composition of Noble muscadine (Vitis rotundifolia) by HPLC-MS and the relationship to its antioxidant capacity. J Food Sci 77:C1115–23.