Sains Malaysiana 43(5)(2014): 689–695

Antioxidant and Antiproliferative Activities of Non-Edible Parts of Selected Tropical Fruits

(Aktiviti Antioksidan dan Antiproliferatif Bahagian Tidak Boleh Dimakan Buah-buahan Tropika Terpilih)

WARANGKANA CHUNGLOK*¹, TANYARATH UTAIPAN¹, NATHNARIN SOMCHIT¹,

MONTHON LERTCANAWANICHAKUL¹& YUTTANA SUDJAROEN²

¹School of Allied Health Sciences and Public Health, Walailak University, Nakhon Si Thammarat

Thailand

²Faculty of Science and Technology, Suan Sunandha Rajabhat University, Bangkok, Thailand

Diserahkan: 2 Februari 2013/Diterima: 26 Ogos 2013

ABSTRACT

It is of interest that seeds and pericarps of tropical fruits contain phytochemicals being the components of various biological activities for beneficial health effects. This study was aimed to evaluate antioxidant and anticancer activities of the methanolic extracts from seeds and pericarps of three selected tropical fruits including Rambutan (Nephelium lappaceum L.), Litchi (Litchi chinensis Sonn.) and Tamarind (Tamarindus indica L.). Total phenolic content was determined by using the Folin-Ciocalteu method. Antioxidant capacity was evaluated based on the ability of the fruit extracts to scavenge ABTS and DPPH radicals. MTT reduction assay and Annexin V-FITC/PI staining were carried out for cytotoxicity and apoptosis induction, respectively. Total phenolic contents of the seeds and pericarps of the tropical fruits ranged from 104.60 to 501.95 mg/g DW. All extracts were found to have significant antioxidant activities. Among them, tamarind seed extract contained the highest total phenolic contents and possessed the highest antioxidant capacities. Tamarind seed extract showed the highest cytotoxicity to human mouth carcinoma (CLS-354) cells and had no toxicity to PBMCs. Staining with annexin V-FITC/PI showed that this apoptosis occurred early in this cell type with 10.0% of the cells undergoing apoptosis. Tamarind seed extract might have potential anticancer activity which could be attributed, in part, to selectively inhibit the growth of CLS-354 cells and induce apoptosis. This research finding would be valuable information to identify major constituents of the extracts and mechanisms underlying anticancer activity which could be attributed to dietary health supplements or cancer chemoprevention from fruits.

Keywords: Antioxidant capacity; antiproliferation; non-edible parts; tropical fruits

ABSTRAK

Benih dan perikarpa buah-buahan tropika mengandungi fitokimia yang menjadi komponen pelbagai aktiviti biologi yang berfaedah kepada kesihatan. Kajian ini adalah bertujuan untuk menilai antioksidan dan aktiviti anti-kanser ekstrak metanolik daripada benih dan perikarpa 3 jenis buah-buahan tropika termasuk Rambutan (Nephelium lappaceum L.), Litchi (Litchi chinensis Sonn.) dan Asam (Tamarindus indica L.). Jumlah kandungan fenol ditentukan melalui kaedah Folin-Ciocalteu. Kapasiti antioksidan dinilai berdasarkan keupayaan ekstrak buah-buahan untuk menggarut ABTS dan radikal DPPH. Kesan pengurangan asai MTT dan pewarnaan Annexin V-FITC/PI masing-masing dijalankan untuk sitotoksisiti dan apoptosis aruhan. Jumlah kandungan fenol benih dan perikarpa buah-buahan tropika adalah daripada 104.60 ke 501.95 mg/g DW. Semua ekstrak didapati mengandungi aktiviti antioksidan bererti. Dalam kalangan mereka, ekstrak biji Asam mengandungi jumlah fenol tertinggi dan mempunyai keupayaan antioksidan tertinggi. Ekstrak biji Asam menunjukkan sitotoksisiti yang tertinggi untuk sel karsinoma mulut manusia (CLS-354) dan tidak mengandungi ketoksikan untuk PBMCs. Pewarnaan dengan annexin PI/V-FITC menunjukkan bahawa apoptosis berlaku awal dalam jenis sel ini dengan 10.0% daripada sel mengalami apoptosis. Ekstrak biji Asam mungkin mempunyai potensi aktiviti anti-kanser dengan sebahagiannya menghalang pertumbuhan sel CLS-354 dan mendorong apoptosis. Keputusan kajian ini akan menjadi maklumat penting untuk mengenal pasti juzuk utama ekstrak dan mekanisme yang mendasari aktiviti anti-kanser yang disebabkan oleh suplemen pemakanan kesihatan atau kanser kemocegahan daripada buah-buahan.

Kata kunci: Antipercambahan; bahagian yang tidak boleh dimakan; buah-buahan tropika; kapasiti antioksidan

RUJUKAN

Abeysinghe, D., Li, X., Sun, C., Zhang, W., Zhou, C. & Chen, K. 2007. Bioactive compounds and antioxidant capacities in different edible tissues of citrus fruit of four species. Food Chem. 104: 1338-1344.

Akhtar, S., Meeran, S.M., Katiyar, N. & Katiyar, S.K. 2009. Grape seed proanthocyanidins inhibit the growth of human non-small cell lung cancer xenografts by targeting insulin-like growth factor binding protein-3, tumor cell proliferation, and angiogenic factors. Clin. Cancer Res. 15: 821-831.

Al-Hazzani, A.A. & Alshatwi, A.A. 2011. Catechin hydrate inhibits proliferation and mediates apoptosis of SiHa human cervical cancer cells. Food Chem. Toxicol. 49: 3281-3286.

Cartmel, B. 2005. A randomized trial of an intervention to increase fruit and vegetable intake in curatively treated patients with early-stage head and neck cancer. Cancer Epidemiol. Biomarkers Prev. 14: 2848-2854.

De Stefani, E., Boffetta, P., Ronco, A.L., Correa, P., Oreggia, F., Deneo-Pellegrini, H., Mendilaharsu, M. & Leiva, J. 2005. Dietary patterns and risk of cancer of the oral cavity and pharynx in Uruguay. Nutr. Cancer. 51: 132-139.

Islami, F., Boffetta, P., Ren, J.S., Pedoeim, L., Khatib, D. & Kamangar, F. 2009. High-temperature beverages and foods and esophageal cancer risk-A systematic review. Int. J. Cancer 125: 491-524.

Jemal, A., Bray, F., Center, M.M., Ferlay, J., Ward, E. & Forman, D. 2011. Global cancer statistics. CA Cancer J. Clin. 61: 69-90.

Jiang, Z., Fletcher, N.M., Ali-Fehmi, R., Diamond, M.P., Abu- Soud, H.M., Munkarah, A.R. & Saed, G.M. 2011. Modulation of redox signaling promotes apoptosis in epithelial ovarian cancer cells. Gynecol. Oncol. 122: 418-423.

Ka¨hko¨nen, M.P., Hopia, A.I., Vuorela, H.J., Rauha, J.P., Pihlaja, K., Kujala, T.S. & Heinonen M. 1999. Antioxidant activity of plant extracts containing phenolic compounds. J. Agric. Food Chem. 47: 3954-3962.

Khanizadeh, S., Tsao, R., Rekika, D., Yang, R., Charles, M.T. & Vasantha Rupasinghe, H.P. 2008. Polyphenol composition and total antioxidant capacity of selected apple genotypes for processing. J. Food Compost. Anal. 21: 396-401.

Khonkarn, R., Okonogi, S., Ampasavate, C. & Anuchapreeda, S. 2010. Investigation of fruit peel extracts as sources for compounds with antioxidant and antiproliferative activities against human cell lines. Food Chem. Toxicol. 48: 2122-2129.

Ko, Y.C., Huang, Y.L., Lee, C.H., Chen, M.J., Lin, L.M. & Tsai, C.C. 1995. Betel quid chewing, cigarette smoking and alcohol consumption related to oral cancer in Taiwan. J. Oral Pathol. Med. 24: 450-453.

Kris-Etherton, P.M., Hecker, K.D., Bonanome, A., Coval, S.M., Binkoski, A.E., Hilpert, K.F., Griel, A.E. & Etherton, T.D. 2002. Bioactive compounds in foods: Their role in the prevention of cardiovascular disease and cancer. Am. J. Med. 113: 71-88.

Lopaczynski, W. & Zeisel, S.H. 2001. Antioxidants, programmed cell death, and cancer. Nutr. Res. 21: 295-307.

Lotito, S.B. & Frei, B. 2006. Consumption of flavonoid-rich foods and increased plasma antioxidant capacity in humans: Cause, consequence, or epiphenomenon’. Free Radic. Biol. Med. 41: 1727-1746.

Miura, T., Chiba, M., Kasai, K., Nozaka, H., Nakamura, T., Shoji, T., Kanda, T., Ohtake, Y. & Sato, T. 2008. Apple procyanidins induce tumor cell apoptosis through mitochondrial pathway activation of caspase-3. Carcinogenesis 29: 585-593.

Nair, S., Li, W. & Kong, A.T. 2007. Natural dietary anti-cancer chemopreventive compounds: Redox-mediated differential signaling mechanisms in cytoprotection of normal cells versus cytotoxicity in tumor cells. Acta Pharmacol. Sin. 28: 459-472.

Okonogi, S., Duangrat, C., Anuchpreeda, S., Tachakittirungrod, S. & Chowwanapoonpohn, S. 2007. Comparison of antioxidant capacities and cytotoxicities of certain fruit peels. Food Chem. 103: 839-846.

Owuor, E.D. & Kong, A.T. 2002. Antioxidants and oxidants regulated signal transduction pathways. Biochem. Pharmacol. 62: 765-770.

Petti, S. 2009. Lifestyle risk factors for oral cancer. Oral Oncol. 45: 340-350.

Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M. & Rice-Evans, C. 1999. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26: 1231-1237.

Rupasinghe Vasantha, H.P. & Clegg, S. 2007. Total antioxidant capacity, total phenolic content, mineral elements, and histamine concentrations in wines of different fruit sources. J. Food Compost. Anal. 20: 133-137.

Singh, R.P., Murthy, C.K.N. & Jayaprakasha, G.K. 2002. Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vitro models. J. Agric. Food Chem. 50: 81-86.

Singleton, V.L., Orthofer, R. & Lamuela-Raventós, R.M. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 299: 152-178.

Sudjaroen, Y., Haubner, R., Wurtele, G., Hull, W.E., Erben, G., Spiegelhalder, B., Changbumrung, S., Bartsch, H. & Owen, R.W. 2005. Isolation and structure elucidation of phenolic antioxidants from Tamarind (Tamarindus indica L.) seeds and pericarp. Food Chem. Toxicol. 43: 1673-1682.

Sun, J., Chu, Y.F., Wu, X. & Liu, R.H. 2002. Antioxidant and antiproliferative activities of common fruits. J. Agric. Food Chem. 50: 7449-7454.

Surh, Y.J. 2003. Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 3: 768-780.

Thitilertdecha, N., Teerawutgulrag, A. & Rakariyatham, N. 2008. Antioxidant and antibacterial activities of Nephelium lappaceum L. extracts. LWT-Food Sci. Technol. 41: 2029- 2035.

Wang, X., Wei, Y., Yuan, S., Liu, G., Zhang, Y.L.J. & Wang, W. 2006a. Potential anticancer activity of litchi fruit pericarp extract against hepatocellular carcinoma in vitro and in vivo. Cancer Lett. 239: 144-150.

Wang, X., Yuan, S., Wang, J., Lin, P., Liu, G., Lu, Y., Zhang, J., Wang, W. & Wei, Y. 2006b. Anticancer activity of litchi fruit pericarp extract against human breast cancer in vitro and in vivo. Toxicol. Appl. Pharmacol. 215: 168-178.

Wang, Y., Zhang, H., Holmgren, A., Tian, W. & Zhong, L. 2008. Inhibitory effect of green tea extract and (-)-epigallocatechin- 3-gallate on mammalian thioredoxin reductase and HeLa cell viability. Oncol. Rep. 20: 1479-1487.

Warnakulasuriya, S. 2009. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol. 45: 309-316.

Xiao, H., Yang, C.S., Li, S., Jin, H., Ho, C.T. & Patel, T. 2009. Monodemethylated polymethoxyflavones from sweet orange (Citrus sinensis) peel inhibit growth of human lung cancer cells by apoptosis. Mol. Nutr. Food Res. 53: 398-406.

Zain, R.B. 2001. Cultural and dietary risk factors of oral cancer and precancer - a brief overview. Oral Oncol. 37: 205-210.

*Pengarang untuk surat-menyurat; email: cwarang@wu.ac.th