Anthocyanin determination in blueberry extracts from various cultivars and their antiproliferative and apoptotic properties in B16-F10 metastatic murine melanoma cells

Phytochemistry

Volumn 95, Issue , 2013, Pages 436-444

  Bunea, Andrea ^a   Ruginǎ, Dumitriţa ^a   Sconţa, Zoriţa ^a   Pop, Raluca M ^a   Pintea, Adela ^a   Socaciu, Carmen ^a   Tǎbǎran, Flaviu ^a   Grootaert, Charlotte ^b   Struijs, Karin ^b   VanCamp, John ^b  

^a UNIVERSITY OF AGRICULTURAL SCIENCES AND VETERINARY MEDICINE   (Romania)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Anthocyanins; Apoptosis; Blueberry extracts; Cell culture

Indexed keywords

MURINAE; VACCINIUM;

ANTHOCYANIN; ANTINEOPLASTIC AGENT; ANTIOXIDANT; GLUCOSIDE; LACTATE DEHYDROGENASE; MALVIDIN 3 GLUCOSIDE; MALVIDIN-3-GLUCOSIDE; PLANT EXTRACT;

ANIMAL; APOPTOSIS; ARTICLE; BLUEBERRY; BLUEBERRY EXTRACTS; CELL CULTURE; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECT; EXPERIMENTAL MELANOMA; ISOLATION AND PURIFICATION; METABOLISM; MOUSE; PHYTOTHERAPY; SPECIES DIFFERENCE;

ANTHOCYANINS; APOPTOSIS; BLUEBERRY EXTRACTS; CELL CULTURE;

ANIMALS; ANTHOCYANINS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTIOXIDANTS; APOPTOSIS; BLUEBERRY PLANT; CELL PROLIFERATION; GLUCOSIDES; L-LACTATE DEHYDROGENASE; MELANOMA, EXPERIMENTAL; MICE; PHYTOTHERAPY; PLANT EXTRACTS; SPECIES SPECIFICITY;

EID: 84893731277     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2013.06.018     Document Type: Article

References (58)

1. Afaq, F., Saleem, M., Krueger, C.G., Reed, J.D., Mukhtar, H., 2005. Anthocyanin- and hydrolyzable tannin-rich pomegranate fruit extract modulates MAPK and NFkappaB pathways and inhibits skin tumorigenesis in CD-1 mice. Int. J. Cancer 113, 423-433. (Pubitemid 40038710)
2. Afaq, F., Syed, D.N., Malik, A., Hadi, N., Sarfaraz, S., Kweon, M.H., Khan, N., Zaid, M.A., Mukhtar, H., 2007. Delphinidin, an anthocyanidin in pigmented fruits and vegetables, protects human HaCaT keratinocytes and mouse skin against UVBmediated oxidative stress and apoptosis. J. Invest. Dermatol. 127, 222-232. (Pubitemid 46005682)
3. Apak, R., Guclu, K., Demirata, B., Ozyurek, M., Celik, S.E., Bektasoglu, B., Berker, K.I., Ozyurt, D., 2007. Comparative evaluation of various total antioxidant capacity assays applied to phenolic compounds with the CUPRAC assay. Molecules 12, 1496-1547.
4. Arnao, M.B., Cano, A., Alcolea, J.F., Acosta, M., 2001. Estimation of free radicalquenching activity of leaf pigment extracts. Phytochem. Anal. 12, 138-143.
5. Bowen-Forbes, C.S., Zhang, Y., Nair, M.G., 2010. Anthocyanin content, antioxidant, anti-inflammatory and anticancer properties of blackberry and raspberry fruits. J. Food Compos. Anal. 23, 554-560.
6. Castrejón, A.D.R., Eichholz, I., Rohn, S., Kroh, L.W., Huyskens-Keil, S., 2008. Phenolic profile and antioxidant activity of highbush blueberry (Vaccinium corymbosum L.) during fruit maturation and ripening. Food Chem. 109, 564-572.
7. Chen, P.N., Chu, S.C., Chiou, H.L., Chiang, C.L., Yang, S.F., Hsieh, Y.S., 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, 232-243.
8. Cuevas-Rodriguez, E.O., Yousef, G.G., Garcia-Saucedo, P.A., Lopez-Medina, J., Paredes-Lopez, O., Lila, M.A., 2010. Characterization of anthocyanins and proanthocyanidins in wild and domesticated Mexican blackberries (Rubus spp.). J. Agric. Food Chem. 58, 7458-7464.
9. Elisia, I., Hu, C., Popovich, D.G., Kitts, D.D., 2007. Antioxidant assessment of an anthocyanin-enriched blackberry extract. Food Chem. 101, 1052-1058.
10. Ehlenfeldt, M.K., Prior, R.L., 2001. Oxygen radical absorbance capacity (ORAC) and phenolic and anthocyanin concentrations in fruit and leaf tissues of highbush blueberry. J. Agric. Food Chem. 49, 2222-2227. (Pubitemid 32843236)
11. Espin, J.C., Garcia-Conesa, M.T., Tomas-Barberan, F.A., 2007. Nutraceuticals: facts and fiction. Phytochemistry 68, 2986-3008. (Pubitemid 350180953)
12. Feng, R., Ni, H.M., Wang, S.Y., Tourkova, I.L., Shurin, M.R., Harada, H., Yin, X.M., 2007. Cyanidin-3-rutinoside, a natural polyphenol antioxidant, selectively kills leukemic cells by induction of oxidative stress. J. Biol. Chem. 282, 13468-13476. (Pubitemid 47100551)
13. Gao, L., Mazza, G., 1994a. Quantitation and distribution of simple and acylated anthocyanins and other phenolics in blueberries. J. Food Sci. 59, 1057-1059.
14. Gao, L., Mazza, G., 1994b. Quantitation and distribution of simple and acylated anthocyanins and other phenolics in blueberries. J. Food Sci. 59, 1057-1059.
15. Garzón, G.A., Narváez, C.E., Riedl, K.M., Schwartz, S.J., 2010. Chemical composition, anthocyanins, non-anthocyanin phenolics and antioxidant activity of wild bilberry (Vaccinium meridionale Swartz) from Colombia. Food Chem. 122, 980-986.
16. Gavrilova, V., Kajdzanoska, M., Gjamovski, V., Stefova, M., 2011. Separation, characterization and quantification of phenolic compounds in blueberries and red and black currants by HPLC-DAD-ESI-MSn. J. Agric. Food Chem. 59, 4009-4018.
17. Giovanelli, G., Buratti, S., 2009. Comparison of polyphenolic composition and antioxidant activity of wild Italian blueberries and some cultivated varieties. Food Chem. 112, 903-908.
18. Grace, M.H., Ribnicky, D.M., Kuhn, P., Poulev, A., Logendra, S., Yousef, G.G., Raskin, I., Lila, M.A., 2009. Hypoglycemic activity of a novel anthocyanin-rich formulation from lowbush blueberry, Vaccinium angustifolium Aiton. Phytomedicine 16, 406-415.
19. Guerra, M.C., Galvano, F., Bonsi, L., Speroni, E., Costa, S., Renzulli, C., Cervellati, R., 2005. Cyanidin-3-O-beta-glucopyranoside, a natural free-radical scavenger against aflatoxin B1- and ochratoxin A-induced cell damage in a human hepatoma cell line (Hep G2) and a human colonic adenocarcinoma cell line (CaCo-2). Br. J. Nutr. 94, 211-220. (Pubitemid 41357792)
20. He, J., Giusti, M.M., 2010. Anthocyanins: natural colorants with health-promoting properties. Annu. Rev. Food Sci. Technol. 1, 163-187.
21. He, J., Magnuson, B.A., Lala, G., Tian, Q., Schwartz, S.J., Giusti, M.M., 2006. Intact anthocyanins and metabolites in rat urine and plasma after 3 months of anthocyanin supplementation. Nutr. Cancer 54, 3-12. (Pubitemid 44141331)
22. Huang, D., Ou, B., Hampsch-Woodill, M., Flanagan, J.A., Prior, R.L., 2002. Highthroughput assay of oxygen radical absorbance capacity (ORAC) using a multichannel liquid handling system coupled with a microplate fluorescence reader in 96-well format. J. Agric. Food Chem. 50, 4437-4444. (Pubitemid 34823962)
23. Huang, H.P., Shih, Y.W., Chang, Y.C., Hung, C.N., Wang, C.J., 2008. Chemoinhibitory effect of mulberry anthocyanins on melanoma metastasis involved in the Ras/PI3K pathway. J. Agric. Food Chem. 56, 9286-9293.
24. Kader, F., Rovel, B., Girardin, M., Metche, M., 1996. Fractionation and identification of the phenolic compounds of highbush blueberries (Vaccinium corymbosum L.). Food Chem. 55, 35-40. (Pubitemid 126657402)
25. Katsube, N., Iwashita, K., Tsushida, T., Yamaki, K., Kobori, M., 2003. Induction of apoptosis in cancer cells by Bilberry (Vaccinium myrtillus) and the anthocyanins. J. Agric. Food Chem. 51, 68-75.
26. Kay, C.D., Mazza, G., Holub, B.J., Wang, J., 2004. Anthocyanin metabolites in human urine and serum. Br. J. Nutr. 91, 933-942. (Pubitemid 38931457)
27. Konczak, I., Zabaras, D., Dunstan, M., Aguas, P., 2010. Antioxidant capacity and hydrophilic phytochemicals in commercially grown native Australian fruits. Food Chem. 123, 1048-1054.
28. Kong, J.-M., Chia, L.-S., Goh, N.-K., Chia, T.-F., Brouillard, R., 2003. Analysis and biological activities of anthocyanins. Phytochemistry 64, 923-933. (Pubitemid 37295344)
29. Kraus, M., Kahle, K., Ridder, F., Schantz, M., Scheppach, W., Schreier, P., Richling, E., 2010. Colonic availability of bilberry anthocyanins in humans. In: Quian, M.R.A. (Ed.), Flavor and health benefits of small berries, vol. ACS Symposium Series. American Chemical Society, Washington DC, p. 18.
30. Latti, A.K., Kainulainen, P.S., Hayirlioglu-Ayaz, S., Ayaz, F.A., Riihinen, K.R., 2009. Characterization of anthocyanins in Caucasian blueberries (Vaccinium arctostaphylos L.) native to Turkey. J. Agric. Food Chem. 57, 5244-5249.
31. Lätti, A.K., Riihinen, K.R., Kainulainen, P.S., 2008. Analysis of anthocyanin variation in wild populations of bilberry (Vaccinium myrtillus L.) in Finland. J. Agric. Food Chem. 56, 190-196. (Pubitemid 351187572)
32. Liu, J., Zhang, W., Jing, H., Popovich, D.G., 2010. Bog bilberry (Vaccinium uliginosum L.) extract reduces cultured Hep-G2, Caco-2, and 3T3-L1 cell viability, affects cell cycle progression, and has variable effects on membrane permeability. J. Food Sci. 75, H103-H107.
33. Lohachoompol, V., Mulholland, M., Srzednicki, G., Craske, J., 2008. Determination of anthocyanins in various cultivars of highbush and rabbiteye blueberries. Food Chem. 111, 249-254.
34. Moyer, R.A., Hummer, K.E., Finn, C.E., Frei, B., Wrolstad, R.E., 2002. Anthocyanins, phenolics, and antioxidant capacity in diverse small fruits: vaccinium, rubus, and ribes. J. Agric. Food Chem. 50, 519-525. (Pubitemid 34106672)
35. Müller, D., Schantz, M., Richling, E., 2012. High performance liquid chromatography analysis of anthocyanins in bilberries (Vaccinium myrtillus L.), blueberries (Vaccinium corymbosum L.), and corresponding juices. J. Food Sci. 77, C340-C345.
36. Nicoué E.É., Savard, S., Belkacemi, K., 2007. Anthocyanins in wild blueberries of Quebec: extraction and identification. J. Agric. Food Chem. 55, 5626-5635. (Pubitemid 47092937)
37. Olsson, M.E., Gustavsson, K.E., Andersson, S., Nilsson, A., Duan, R.D., 2004. Inhibition of cancer cell proliferation in vitro by fruit and berry extracts and correlations with antioxidant levels. J. Agric. Food Chem. 52, 7264-7271.
38. Prior, R.L., Cao, G., Martin, A., Sofic, E., McEwen, J., O'Brien, C., Lischner, N., Ehlenfeldt, M., Kalt, W., Krewer, G., Mainland, C.M., 1998. Antioxidant capacity as influenced by total phenolic and anthocyanin content, maturity, and variety of vaccinium species. J. Agric. Food Chem. 46, 2686-2693. (Pubitemid 128488357)
39. Prior, R.L., Lazarus, S.A., Cao, G., Muccitelli, H., Hammerstone, J.F., 2001. Identification of procyanidins and anthocyanins in blueberries and cranberries (Vaccinium Spp.) using high-performance liquid chromatography/mass spectrometry. J. Agric. Food Chem. 49, 1270-1276. (Pubitemid 32884947)
40. Prior, R.L., Wu, X., 2006. Anthocyanins: structural characteristics that result in unique metabolic patterns and biological activities. Free Radic. Res. 40, 1014-1028. (Pubitemid 44480542)
41. Reddivari, L., Vanamala, J., Chintharlapalli, S., Safe, S.H., Miller Jr., J.C., 2007. Anthocyanin fraction from potato extracts is cytotoxic to prostate cancer cells through activation of caspase-dependent and caspase-independent pathways. Carcinogenesis 28, 2227-2235. (Pubitemid 47543385)
42. Ribble, D., Goldstein, N.B., Norris, D.A., Shellman, Y.G., 2005. A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol. 5, 12.
43. Rodriguez-Mateos, A., Cifuentes-Gomez, T., Tabatabaee, S., Lecras, C., Spencer, J.P., 2012. Procyanidin, Anthocyanin, and Chlorogenic Acid Contents of Highbush and Lowbush Blueberries. J. Agric. Food Chem. 60, 5772-5778.
44. Ruginǎ, D., Sconţa, Z., Leopold, L., Pintea, A., Bunea, A., Socaciu, C., 2011. Antioxidant activities of chokeberry extracts and the cytotoxic action of their anthocyanin fraction on HeLa human cervical tumor cells. J. Med. Food 15, 700-706.
45. Sariburun, E., Sahin, S., Demir, C., Turkben, C., Uylaser, V., 2010. Phenolic content and antioxidant activity of raspberry and blackberry cultivars. J. Food Sci. 75, C328-C335.
46. Schantz, M., Mohn, C., Baum, M., Richling, E., 2010. Antioxidative efficiency of an anthocyanin rich bilberry extract in the human colon tumor cell lines Caco-2 and HT-29. J. Berry Res. 1, 25-33.
47. Seeram, N.P., Adams, L.S., Zhang, Y., Lee, R., Sand, D., Scheuller, H.S., Heber, D., 2006. 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. 54, 9329-9339. (Pubitemid 46086089)
48. Srivastava, A., Akoh, C.C., Fischer, J., Krewer, G., 2007. Effect of anthocyanin fractions from selected cultivars of Georgia-grown blueberries on apoptosis and phase II enzymes. J. Agric. Food Chem. 55, 3180-3185. (Pubitemid 46668332)
49. Triebel, S., Trieu, H.L., Richling, E., 2012. Modulation of inflammatory gene expression by a bilberry (Vaccinium myrtillus L.) extract and single anthocyanins considering their limited stability under cell culture conditions. J. Agric. Food Chem. 60, 8902-8910.
50. Vasco, C., Riihinen, K., Ruales, J., Kamal-Eldin, A., 2009. Chemical composition and phenolic compound profile of mortino (Vaccinium floribundum Kunth). J. Agric. Food Chem. 57, 8274-8281.
51. Wang, L.S., Hecht, S.S., Carmella, S.G., Yu, N., Larue, B., Henry, C., McIntyre, C., Rocha, C., Lechner, J.F., Stoner, G.D., 2009. Anthocyanins in black raspberries prevent esophageal tumors in rats. Cancer Prev. Res. (Phila.) 2, 84-93.
52. Wu, X., Beecher, G.R., Holden, J.M., Haytowitz, D.B., Gebhardt, S.E., Prior, R.L., 2006. Concentrations of anthocyanins in common foods in the United States and estimation of normal consumption. J. Agric. Food Chem. 54, 4069-4075. (Pubitemid 44030592)
53. Yi, W., Fischer, J., Krewer, G., Akoh, C.C., 2005. Phenolic compounds from blueberries can inhibit colon cancer cell proliferation and induce apoptosis. J. Agric. Food Chem. 53, 7320-7329. (Pubitemid 41375353)
54. You, Q., Wang, B., Chen, F., Huang, Z., Wang, X., Luo, P.G., 2011. Comparison of anthocyanins and phenolics in organically and conventionally grown blueberries in selected cultivars. Food Chem. 125, 201-208.
55. Yun, J.M., Afaq, F., Khan, N., Mukhtar, H., 2009. Delphinidin, an anthocyanidin in pigmented fruits and vegetables, induces apoptosis and cell cycle arrest in human colon cancer HCT116 cells. Mol. Carcinog. 48, 260-270.
56. Zafra-Stone, S., Yasmin, T., Bagchi, M., Chatterjee, A., Vinson, J.A., Bagchi, D., 2007. Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol. Nutr. Food Res. 51, 675-683. (Pubitemid 47083678)
57. Zhao, C., Giusti, M.M., Malik, M., Moyer, M.P., Magnuson, B.A., 2004. Effects of commercial anthocyanin-rich on colonic cancer and nontumorigenic colonic cell growth. J. Agric. Food Chem. 52, 6122-6128.
58. Zheng, W., Wang, S.Y., 2003. Oxygen radical absorbing capacity of phenolics in blueberries, cranberries, chokeberries, and lingonberries. J. Agric. Food Chem. 51, 502-509.