ZIZIPHUS JUJUBE (HÜNNAP) İÇ VE ÇEKİRDEK DOKULARINDAN FENOLİKLERİN IN VITRO SİNDİRİM SIRASINDA BAZI BİYOAKTİF ÖZELLİKLERİNDEKİ DEĞİŞİMİN ARAŞTIRILMASI

sindirim sırasında anjiyotensin-I dönüştürücü enzim (ADE) inhibisyon, α-amilaz inhibisyon ve antioksidan aktivitesi ile toplam fenolik madde (TFM) ve toplam monomerik antosiyanin miktarı (TMAM) üzerindeki değişiklikler incelenmiştir. In vitro sindirim sonrasında, çekirdek ve iç ekstraktlarındaki biyoerişilebilir fenolik fraksiyonlar sırasıyla %23.24±4.46 ve %9.43±0.24 olarak hesaplanmıştır. Ayrıca, çekirdek ekstraktlarında toplam monomerik antosiyaninlerin biyoerişilebilirliği (147.83±9.20%) iç ekstraktların toplam monomerik antosiyaninlerinin biyoerişilebilirliğinden (15.76±3.89%) daha yüksek bulunmuştur (P<0.05). In vitro sindirim sonrasında ekstraktların antioksidan aktivitesinde azalma meydana gelmiştir (P<0.05). Çekirdek ekstraktlarının sindirim öncesi ADE inhibisyon aktivitesi (%86.04±0.00), sindirim öncesi iç ekstraktın ADE inhibisyon aktivitesinden (%42.74±8.57) daha yüksektir (P<0.05). Çekirdek ve iç ekstraktların α-amilaz inhibisyon aktivitesi sırasıyla %49.18±0.35 ve %36.07±5.83 olarak belirlenmiştir. Çalışmanın sonuçlarına göre iç fraksiyonundan elde edilen ekstraktların ADE inhibisyon ve α-amilaz inhibisyon aktivitesi in vitro sindirimden sonra artmıştır.

Anahtar Kelimeler:

Ziziphus jujuba, antioksidan aktivite, ACE inhibisyon aktivite, α-amilaz inhibisyon aktivite, antosiyanin.

INVESTIGATION OF CHANGES IN SOME BIOACTIVE PROPERTIES OF PHENOLIC EXTRACTS FROM PULP AND SEED TISSUES OF ZIZIPHUS JUJUBA DURING IN VITRO DIGESTION

In this study, changes in angiotensin-I converting enzyme (ACE) inhibitory, α-amylase inhibitory and antioxidant activities, total phenolic content (TPC), total monomeric anthocyanin content (TMAC) of ultrasonic phenolic extracts from pulp and seed of Ziziphus jujuba were investigated during in vitro digestion. Bioaccessible fractions of phenolics in seed and pulp extracts were calculated as 23.24±4.46% and 9.43±0.24%, respectively. Moreover, bioaccessibility for TMAC in seed extracts (147.83±9.20%) was higher than pulp (15.76±3.89%) (P<0.05). A decrease in the antioxidant activity of the extracts occurred after in vitro digestion (P<0.05). The ACE inhibitory activity of undigested extracts from seed (86.04±0.00%) was higher than that of the undigested pulp extract (42.74±8.57%) (P<0.05). The α-amylase inhibitory activity of seed and pulp extracts was determined as 49.18±0.35% and 36.07±5.83%, respectively. The results of the study showed that ACE inhibitory activity and α-amylase inhibitory activity of the polyphenolics from pulp increased after in vitro digestion.

Keywords:

Ziziphus jujuba, antioxidant activity, ACE inhibitory activity, α-amylase inhibitory activity, anthocyanin.,

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Al-Azzawie, H. F., Alhamdani, M. S. S. (2006). Hypoglycemic and antioxidant effect of oleuropein in alloxan-diabetic rabbits. Life Sciences, 78(12), 1371-1377.
Adefegha, S. A., Oyeleye, S. I., Oboh, G. (2015). Distribution of phenolic contents, antidiabetic potentials, antihypertensive properties, and antioxidative effects of soursop (Annona muricata L.) fruit parts in vitro. Biochemistry Research International, 2015.
Ahn, C. B., Jeon, Y. J., Kim, Y. T., Je, J. Y. (2012). Angiotensin I converting enzyme (ACE) inhibitory peptides from salmon byproduct protein hydrolysate by Alcalase hydrolysis. Process Biochemistry, 47(12), 2240-2245.
Angerhofer, C. K., Maes, D., Giacomoni, P. U. (2009). The use of natural compounds and botanicals in the development of anti-aging skin care products. In Skin Aging Handbook (pp. 205-263). William Andrew Publishing. https://doi.org/10.1016/B978-0-8155-1584-5.50014-4
AOAC Official Method 2005.02 Total Monomeric Anthocyanin Pigment Content of Fruit Juices, Beverages, Natural Colorants, and Wines pH Differential Method First Action 2005.
AOAC international 2006. AOAC International Guidelines for Laboratories Performing Microbiological and Chemical Analyses of Food and Pharmaceuticals: An Aid to Interpretation of ISO/IEC 17025: 2005.
Apak, R., Güçlü, K., Özyürek, M., Karademir, S. E. (2004). Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. Journal of Agricultural and Food Chemistry, 52(26), 7970-7981. https://doi.org/10.1021/jf048741x
Benammar, C., Baghdad, C., Belarbi, M., Subramaniam, S., Hichami, A., Khan, N. A. (2014). Antidiabetic and antioxidant activities of Zizyphus lotus L aqueous extracts in Wistar rats. Journal of Nutrition Food Sciences, 8(004), 1-6.
Castañeda-Ovando, A., de Lourdes Pacheco-Hernández, M., Páez-Hernández, M. E., Rodríguez, J. A., Galán-Vidal, C. A. (2009). Chemical studies of anthocyanins: A review. Food Chemistry, 113(4), 859-871. https://doi.org/ 10.1016/j.foodchem.2008.09.001
Chel-Guerrero, L. D., Sauri-Duch, E., Fragoso-Serrano, M. C., Pérez-Flores, L. J., Gómez-Olivares, J. L., Salinas-Arreortua, N., ... Mendoza-Espinoza, J. A. (2018). Phytochemical profile, toxicity, and pharmacological potential of peels from four species of tropical fruits. Journal of Medicinal Food, 21(7), 734-743.
Choi, S. H., Ahn, J. B., Kim, H. J., Im, N. K., Kozukue, N., Levin, C. E., Friedman, M. (2012). Changes in free amino acid, protein, and flavonoid content in jujube (Ziziphus jujube) fruit during eight stages of growth and antioxidative and cancer cell inhibitory effects by extracts. Journal of Agricultural and Food Chemistry, 60(41), 10245-10255. https://doi.org/10.1021/ jf302848u
Daskaya-Dikmen, C., Yucetepe, A., Karbancioglu-Guler, F., Daskaya, H., Ozcelik, B. (2017). Angiotensin-I-converting enzyme (ACE)-inhibitory peptides from plants. Nutrients, 9(4), 316. https://doi.org/10.3390/nu9040316
de la Fuente, B., López-García, G., Máñez, V., Alegría, A., Barberá, R., Cilla, A. (2019). Evaluation of the bioaccessibility of antioxidant bioactive compounds and minerals of four genotypes of Brassicaceae microgreens. Foods, 8(7), 250. https://doi.org/10.3390/ foods8070250
Erşan, S., Üstündağ, Ö. G., Carle, R., Schweiggert, R. M. (2017). Determination of pistachio (Pistacia vera L.) hull (exo-and mesocarp) phenolics by HPLC-DAD-ESI/MSn and UHPLC-DAD-ELSD after ultrasound-assisted extraction. Journal of Food Composition and Analysis, 62, 103-114.
Fernández, K., Labra, J. (2013). Simulated digestion of proanthocyanidins in grape skin and seed extracts and the effects of digestion on the angiotensin I-converting enzyme (ACE) inhibitory activity. Food Chemistry, 139(1-4), 196-202.
Ganachari, M. S., Kumar, S., Bhat, K. G. (2004). Effect of Ziziphus jujuba leaves extract on phagocytosis by human neutrophils. Journal of Natural Remedies, 47-51.
Gao, Q. H., Wu, C. S., Wang, M. (2013). The jujube (Ziziphus jujuba Mill.) fruit: a review of current knowledge of fruit composition and health benefits. Journal of Agricultural and Food Chemistry, 61(14), 3351-3363. https://doi.org/10.1021/jf4007032
Gao, Q. H., Wu, C. S., Yu, J. G., Wang, M., Ma, Y. J., Li, C. L. (2012). Textural characteristic, antioxidant activity, sugar, organic acid, and phenolic profiles of 10 promising jujube (Ziziphus jujuba Mill.) selections. Journal of Food Science, 77(11), C1218-C1225. https://doi.org/10.1111/ j.1750-3841.2012.02946.x
Ghosh, S., Ahire, M., Patil, S., Jabgunde, A., Bhat Dusane, M., Joshi, B. N., ... Chopade, B. A. (2012). Antidiabetic activity of Gnidia glauca and Dioscorea bulbifera: potent amylase and glucosidase inhibitors. Evidence-Based Complementary and Alternative Medicine, 2012. https://doi.org/ 10.1155/2012/929051
Goyal, R., Sharma, P. L., Singh, M. (2011). Possible attenuation of nitric oxide expression in anti-inflammatory effect of Ziziphus jujuba in rat. Journal of Natural Medicines, 65, 514-518. https://doi.org/10.1007/s11418-011-0531-0
Goulas, V., Hadjisolomou, A. (2019). Dynamic changes in targeted phenolic compounds and antioxidant potency of carob fruit (Ceratonia siliqua L.) products during in vitro digestion. LWT, 101, 269-275. https://doi.org/10.1016/ j.lwt.2018.11.003
Hamedi, S., Arian, A. A., Farzaei, M. H. (2015). Gastroprotective effect of aqueous stem bark extract of Ziziphus jujuba L. against HCl/ethanol-induced gastric mucosal injury in rats. Journal of Traditional Chinese Medicine, 35(6), 666-670.
Hemmati, M., Asghari, S., Zohoori, E., Karamian, M. (2015a). Hypoglycemic effects of three Iranian edible plants; jujube, barberry and saffron: Correlation with serum adiponectin level. Pakistan Journal of Pharmaceutical Sciences, 28(6), 2095-2099.
Hemmati, M., Zohoori, E., Mehrpour, O., Karamian, M., Asghari, S., Zarban, A., Nasouti, R. (2015b). Anti-atherogenic potential of jujube, saffron and barberry: anti-diabetic and antioxidant actions. EXCLI Journal, 14, 908. https://doi.org/10.17179/excli2015-232
Hoshyar, R., Mohaghegh, Z., Torabi, N., Abolghasemi, A. (2015). Antitumor activity of aqueous extract of Ziziphus jujube fruit in breast cancer: an in vitro and in vivo study. Asian Pacific Journal of Reproduction, 4(2), 116-122. https://doi.org/10.1016/S2305-0500(15)30007-5
Imamoglu, H. (2016). Total antioxidant capacity, phenolic compounds and sugar content of Turkey Ziziphus jujubes. Acta Scientiarum Polonorum Hortorum Cultus, 15(5), 93-108.
Jiang, J. G., Huang, X. J., Chen, J., Lin, Q. S. (2007). Comparison of the sedative and hypnotic effects of flavonoids, saponins, and polysaccharides extracted from Semen Ziziphus jujube. Natural Product Research, 21(4), 310-320. https://doi.org/10.1080/14786410701192827
Koh, J., Xu, Z., Wicker, L. (2020). Blueberry pectin and increased anthocyanins stability under in vitro digestion. Food Chemistry, 302, 125343. https://doi.org/10.1016/j.foodchem.2019.125343
Koley, T. K., Kaur, C., Nagal, S., Walia, S., Jaggi, S. (2016). Antioxidant activity and phenolic content in genotypes of Indian jujube (Zizyphus mauritiana Lamk.). Arabian Journal of Chemistry, 9, S1044-S1052.
Kumar, S., Ganachari, M. S., Nagoor, V. S. (2004). Anti-inflammatory activity of Ziziphus jujuba Lam leaves extract in rats. Journal of Natural Remedies, 183-185.
Kumar, S., Prahalathan, P., Raja, B. (2011). Antihypertensive and antioxidant potential of vanillic acid, a phenolic compound in L-NAME-induced hypertensive rats: a dose-dependence study. Redox Report, 16(5), 208-215. https://doi.org/10.1179/1351000211Y.0000000009
Kumaran, A., Karunakaran, R. J. (2006). Anti-oxidant activity of polyphenols from Phyllanthus debilis Klein ex Willd. Journal of Natural Remedies, 141-146.
Li, J. W., Ding, S. D., Ding, X. L. (2005). Comparison of antioxidant capacities of extracts from five cultivars of Chinese jujube. Process Biochemistry, 40(11), 3607-3613.
Li, J., Liu, Y., Fan, L., Ai, L., Shan, L. (2011). Antioxidant activities of polysaccharides from the fruiting bodies of Zizyphus Jujuba cv. Jinsixiaozao. Carbohydrate Polymers, 84(1), 390-394. https://doi.org/10.1016/j.carbpol.2010.11.051
Liu, Z., Dang, J., Wang, Q., Yu, M., Jiang, L., Mei, L., ... Tao, Y. (2013). Optimization of polysaccharides from Lycium ruthenicum fruit using RSM and its anti-oxidant activity. International Journal of Biological Macromolecules, 61, 127-134. https://doi.org/10.1016/j.ijbiomac.2013.06.042
Liu, X. X., Liu, H. M., Yan, Y. Y., Fan, L. Y., Yang, J. N., Wang, X. D., Qin, G. Y. (2020). Structural characterization and antioxidant activity of polysaccharides extracted from jujube using subcritical water. LWT, 117, 108645. https://doi.org/10.1016/j.lwt.2019.108645
López-Fernández-Sobrino, R., Soliz-Rueda, J. R., Margalef, M., Arola-Arnal, A., Suárez, M., Bravo, F. I., Muguerza, B. (2021). ACE Inhibitory and antihypertensive activities of wine lees and relationship among bioactivity and phenolic profile. Nutrients, 13(2), 679. https://doi.org/ 10.3390/nu13020679
Ma, Y., Yang, Y., Gao, J., Feng, J., Shang, Y., Wei, Z. (2020). Phenolics and antioxidant activity of bamboo leaves soup as affected by in vitro digestion. Food and Chemical Toxicology, 135, 110941. https://doi.org/10.1016/ j.fct.2019.110941
Marmouzi, I., Kharbach, M., El Jemli, M., Bouyahya, A., Cherrah, Y., Bouklouze, A., ... Faouzi, M. E. A. (2019). Antidiabetic, dermatoprotective, antioxidant and chemical functionalities in Zizyphus lotus leaves and fruits. Industrial Crops and Products, 132, 134-139. https://doi.org/10.1016/j.indcrop.2019.02.007
McDougall, G. J., Fyffe, S., Dobson, P., Stewart, D. (2005). Anthocyanins from red wine–their stability under simulated gastrointestinal digestion. Phytochemistry, 66(21), 2540-2548. https://doi.org/10.1016/j.phytochem.2005.09.003
Minekus, M., Alminger, M., Alvito, P., Ballance, S., Bohn, T. O. R. S. T. E. N., Bourlieu, C., ... Brodkorb, A. (2014). A standardised static in vitro digestion method suitable for food–an international consensus. Food Function, 5(6), 1113-1124. https://doi.org/10.1039/C3FO60702J
Mohebbati, R., Rahimi, M., Bavarsad, K., Shafei, M. N. (2017). Long-term administration of Ziziphus jujuba extract attenuates cardiovascular responses in hypertensive rats induced by angiotensinii. Ancient Science of Life, 37(2), 68. https://doi.org/10.4103/asl.ASL_122_17
Mourya, P., Shukla, A., Rai, G., Lodhi, S. (2017). Hypoglycemic and hypolipidemic effects of ethanolic and aqueous extracts from Ziziphus oenoplia (L) Mill on alloxan-induced diabetic rats. Beni-Suef University Journal of Basic and Applied Sciences, 6(1), 1-9. https://doi.org/10.1016/ j.bjbas.2016.12.002
Naik, S. R., Bhagat, S., Shah, P. D., Tare, A. A., Ingawale, D., Wadekar, R. R. (2013). Evaluation of anti-allergic and anti-anaphylactic activity of ethanolic extract of Zizyphus jujuba fruits in rodents. Revista Brasileira de Farmacognosia, 23(5), 811-818. https://doi.org/10.1590/S0102-695X2013000500014
Ng, Z. X., See, A. N. (2019). Effect of in vitro digestion on the total polyphenol and flavonoid, antioxidant activity and carbohydrate hydrolyzing enzymes inhibitory potential of selected functional plant‐based foods. Journal of Food Processing and Preservation, 43(4), e13903. https://doi.org/10.1111/jfpp.13903
Nho, J. W., Hwang, I. G., Kim, H. Y., Lee, Y. R., Woo, K. S., Hwang, B. Y., ... Jeong, H. S. (2010). Free radical scavenging, angiotensin I-converting enzyme (ACE) inhibitory, and in vitro anticancer activities of ramie (Boehmeria nivea) leaves extracts. Food Science and Biotechnology, 19, 383-390. https://doi.org/10.1007/s10068-010-0054-6
Pérez-Vicente, A., Gil-Izquierdo, A., García-Viguera, C. (2002). In vitro gastrointestinal digestion study of pomegranate juice phenolic compounds, anthocyanins, and vitamin C. Journal of Agricultural and Food Chemistry, 50(8), 2308-2312. https://doi.org/10.1021/jf0113833
Puangkam, K., Muanghorm, W., Konsue, N. (2017). Stability of bioactive compounds and antioxidant activity of Thai cruciferous vegetables during in vitro digestion. Current Research in Nutrition and Food Science Journal, 5(2), 100-108. http://dx.doi.org/10.12944/CRNFSJ.5.2.06
Rawat, P., Singh, P. K., Kumar, V. (2016). Anti-hypertensive medicinal plants and their mode of action. Journal of Herbal Medicine, 6(3), 107-118. https://doi.org/10.1016/j.hermed.2016.06.001
Quesada, C., Bartolomé, B., Nieto, O., Gómez-Cordovés, C., Hernández, T., Estrella, I. (1996). Phenolic inhibitors of α-amylase and trypsin enzymes by extracts from pears, lentils, and cocoa. Journal of Food Protection, 59(2), 185-192. https://doi.org/10.4315/0362-028X-59.2.185
Sarmadi, B. H., Ismail, A. (2010). Antioxidative peptides from food proteins: A review. Peptides, 31(10), 1949-1956. https://doi.org/10.1016/ j.peptides.2010.06.020
Senevirathne, I. G. N. H., Abeysekera, W. K. S. M., Abeysekera, W. P. K. M., Jayanath, N. Y., Galbada Arachchige, S. P., Wijewardana, D. C. M. S. I. (2021). Antiamylase, antiglucosidase, and antiglycation properties of millets and sorghum from Sri Lanka. Evidence-Based Complementary and Alternative Medicine, 2021. https://doi.org/ 10.1155/2021/5834915
Şensu, E., Kasapoğlu, K. N., Gültekin-Özgüven, M., Demircan, E., Arslaner, A., Özçelik, B. (2021). Orange, red and purple barberries: Effect of in vitro digestion on antioxidants and ACE inhibitors. LWT, 140, 110820. https://doi.org/ 10.1016/j.lwt.2020.110820
Shi, Q., Zhang, Z., Su, J., Zhou, J., Li, X. (2018). Comparative analysis of pigments, phenolics, and antioxidant activity of Chinese jujube (Ziziphus jujuba Mill.) during fruit development. Molecules, 23(8), 1917. https://doi.org/10.3390/ molecules23081917
Shirdel, Z., Maadani, H., Mirbadalzadeh, R. (2009). Investigation into the hypoglycemic effect of hydroalcoholic extract of Ziziphus Jujuba Leaves on blood glucose and lipids in Alloxan-Induced diabetes in rats. Journal of Diabetes and Metabolic Disorders, 8, 2.
Toor, R. K., Savage, G. P. (2006). Changes in major antioxidant components of tomatoes during post-harvest storage. Food Chemistry, 99(4), 724-727. https://doi.org/10.1016/j.foodchem. 2005.08.049
Vinholes, J., Reis, S. F., Lemos, G., Barbieri, R. L., de Freitas, V., Franzon, R. C., Vizzotto, M. (2018). Effect of in vitro digestion on the functional properties of Psidium cattleianum Sabine (araçá), Butia odorata (Barb. Rodr.) Noblick (butiá) and Eugenia uniflora L.(pitanga) fruit extracts. Food Function, 9(12), 6380-6390.
Yu, Z., Yin, Y., Zhao, W., Liu, J., Chen, F. (2012). Anti-diabetic activity peptides from albumin against α-glucosidase and α-amylase. Food Chemistry, 135(3), 2078-2085. https://doi.org/ 10.1016/j.foodchem.2012.06.088
Wang, B. N., Liu, H. F., Zheng, J. B., Fan, M. T., Cao, W. (2011). Distribution of phenolic acids in different tissues of jujube and their antioxidant activity. Journal of Agricultural and Food Chemistry, 59(4), 1288-1292. https://doi.org/10.1021/ jf103982q
Wang, D., Zhao, Y., Jiao, Y., Yu, L., Yang, S., Yang, X. (2012). Antioxidative and hepatoprotective effects of the polysaccharides from Zizyphus jujube cv. Shaanbeitanzao. Carbohydrate Polymers, 88(4), 1453-1459. https://doi.org/10.1016/j.carbpol.2012.02.046
Wu, C. S., Gao, Q. H., Guo, X. D., Yu, J. G., Wang, M. (2012). Effect of ripening stage on physicochemical properties and antioxidant profiles of a promising table fruit ‘pear-jujube’(Zizyphus jujuba Mill.). Scientia Horticulturae, 148, 177-184. https://doi.org/10.1016/ j.scienta.2012.09.026
Zaidan, U. H., Zen, N. I. M., Amran, N. A., Shamsi, S., Abd Gani, S. S. (2019). Biochemical evaluation of phenolic compounds and steviol glycoside from Stevia rebaudiana extracts associated with in vitro antidiabetic potential. Biocatalysis and Agricultural Biotechnology, 18, 101049. https://doi.org/10.1016/j.bcab.2019.101049
Zhang, H., Jiang, L., Ye, S., Ye, Y., Ren, F. (2010). Systematic evaluation of antioxidant capacities of the ethanolic extract of different tissues of jujube (Ziziphus jujuba Mill.) from China. Food and Chemical Toxicology, 48(6), 1461-1465. https://doi.org/10.1016/j.fct.2010.03.011
Zhao, Y., Yang, X., Ren, D., Wang, D., Xuan, Y. (2014). Preventive effects of jujube polysaccharides on fructose-induced insulin resistance and dyslipidemia in mice. Food Function, 5(8), 1771-1778. https://doi.org/10.1039/ C3FO60707K